Tadashi Fukami

All Publications

• Transcriptional Responses to Priority Effects in Nectar Yeast. Molecular ecology Chappell, C. R., Goddard, P. C., Golden, L. A., Hernandez, J., Ortiz Chavez, D., Hossine, M., Herrera Paredes, S., VanValkenburg, E., Nell, L. A., Fukami, T., Dhami, M. K. 2024: e17553

  Abstract

  Priority effects, where the order and timing of species arrival influence the assembly of ecological communities, have been observed in a variety of taxa and habitats. However, the genetic and molecular basis of priority effects remains unclear, hindering a better understanding of when priority effects will be strong. We sought to gain such an understanding for the nectar yeast Metschnikowia reukaufii commonly found in the nectar of our study plant, the hummingbird-pollinated Diplacus (Mimulus) aurantiacus. In this plant, M. reukaufii can experience strong priority effects when it reaches flowers after other nectar yeasts, such as M. rancensis. After inoculation into two contrasting types of synthetic nectar simulating early arrival of M. rancensis, we conducted whole-transcriptome sequencing of 108 strains of M. reukaufii. We found that several genes were differentially expressed in M. reukaufii strains when the nectar had been conditioned by growth of M. rancensis. Many of these genes were associated with amino acid metabolism, suggesting that M. reukaufii strains responded molecularly to the reduction in amino acid availability caused by M. rancensis. Furthermore, investigation of expression quantitative trait loci (eQTLs) revealed that genes involved in amino acid transport and resistance to antifungal compounds were enriched in some genetic variants of M. reukaufii. We also found that gene expression was associated with population growth rate, particularly when amino acids were limited. These results suggest that intraspecific genetic variation in the ability of nectar yeasts to respond to nutrient limitation and direct fungal competition underpins priority effects in this microbial system.

  View details for DOI 10.1111/mec.17553

  View details for PubMedID 39450887

• The development of ecological systems along paths of least resistance. Current biology : CB Deng, J., Cordero, O. X., Fukami, T., Levin, S. A., Pringle, R. M., Solé, R., Saavedra, S. 2024

  Abstract

  A long-standing question in biology is whether there are common principles that characterize the development of ecological systems (the appearance of a group of taxa), regardless of organismal diversity and environmental context.1,2,3,4,5,6,7,8,9,10,11 Classic ecological theory holds that these systems develop following a sequenced, orderly process that generally proceeds from fast-growing to slow-growing taxa and depends on life-history trade-offs.2,12,13 However, it is also possible that this developmental order is simply the path with the least environmental resistance for survival of the component species and hence favored by probability alone. Here, we use theory and data to show that the order from fast- to slow-growing taxa is the most likely developmental path for diverse systems when local taxon interactions self-organize in light of environmental resistance. First, we demonstrate theoretically that a sequenced development is more likely than a simultaneous one, at least until the number of iterations becomes so large as to be ecologically implausible. We then show that greater diversity of taxa and life histories improves the likelihood of a sequenced order from fast- to slow-growing taxa. Using data from bacterial and metazoan systems,14,15,16,17,18,19 we present empirical evidence that the developmental order of ecological systems moves along the paths of least environmental resistance. The capacity of simple principles to explain the trend in the developmental order of diverse ecological systems paves the way to an enhanced understanding of collective features of life.

  View details for DOI 10.1016/j.cub.2024.08.050

  View details for PubMedID 39332401

• Diversified farms bolster forest-bird populations despite ongoing declines in tropical forests. Proceedings of the National Academy of Sciences of the United States of America Hendershot, J. N., Echeverri, A., Frishkoff, L. O., Zook, J. R., Fukami, T., Daily, G. C. 2023; 120 (37): e2303937120

  Abstract

  While some agricultural landscapes can support wildlife in the short term, it is uncertain how well they can truly sustain wildlife populations. To compare population trends in different production systems, we sampled birds along 48 transects in mature forests, diversified farms, and intensive farms across Costa Rica from 2000 to 2017. To assess how land use influenced population trends in the 349 resident and 80 migratory species with sufficient data, we developed population models. We found, first, that 23% of species were stable in all three land use types, with the rest almost evenly split between increasing and decreasing populations. Second, in forest habitats, a slightly higher fraction was declining: 62% of the 164 species undergoing long-term population changes; nearly half of these declines occurred in forest-affiliated invertivores. Third, in diversified farms, 49% of the 230 species with population changes were declining, with 60% of these declines occurring in agriculture-affiliated species. In contrast, 51% of the species with population changes on diversified farms showed increases, primarily in forest-affiliated invertivores and frugivores. In intensive farms, 153 species showed population changes, also with similar proportions of species increasing (50%) and decreasing (50%). Declines were concentrated in agriculture-affiliated invertivores and forest-affiliated frugivores; increases occurred in many large, omnivorous species. Our findings paint a complex picture but clearly indicate that diversified farming helps sustain populations of diverse, forest-affiliated species. Despite not fully offsetting losses in forest habitats, diversified farming practices help sustain wildlife in a critical time, before possible transformation to nature-positive policies and practices.

  View details for DOI 10.1073/pnas.2303937120

  View details for PubMedID 37669369

• Phylogenomic analysis of the genus Rosenbergiella and description of Rosenbergiella gaditana sp. nov., Rosenbergiella metrosideri sp. nov., Rosenbergiella epipactidis subsp. epipactidis subsp. nov., Rosenbergiella epipactidis subsp. californiensis subsp. nov., Rosenbergiella epipactidis subsp. japonicus subsp. nov., Rosenbergiella nectarea subsp. nectarea subsp. nov. and Rosenbergiella nectarea subsp. apis subsp. nov., isolated from floral nectar and insects. International journal of systematic and evolutionary microbiology Álvarez-Pérez, S., de Vega, C., Vanoirbeek, K., Tsuji, K., Jacquemyn, H., Fukami, T., Michiels, C., Lievens, B. 2023; 73 (3)

  Abstract

  The genus Rosenbergiella is one of the most frequent bacterial inhabitants of flowers and a usual member of the insect microbiota worldwide. To date, there is only one publicly available Rosenbergiella genome, corresponding to the type strain of Rosenbergiella nectarea (8N4T), which precludes a detailed analysis of intra-genus phylogenetic relationships. In this study, we obtained draft genomes of the type strains of the other Rosenbergiella species validly published to date (R. australiborealis, R. collisarenosi and R. epipactidis) and 23 additional isolates of flower and insect origin. Isolate S61T, retrieved from the nectar of an Antirrhinum sp. flower collected in southern Spain, displayed low average nucleotide identity (ANI) and in silico DNA-DNA hybridization (isDDH) values when compared with other Rosenbergiella members (≤86.5 and ≤29.8 %, respectively). Similarly, isolate JB07T, which was obtained from the floral nectar of Metrosideros polymorpha plants in Hawaii (USA) had ≤95.7 % ANI and ≤64.1 % isDDH with other Rosenbergiella isolates. Therefore, our results support the description of two new Rosenbergiella species for which we propose the names Rosenbergiella gaditana sp. nov. (type strain: S61T=NCCB 100789T=DSM 111181T) and Rosenbergiella metrosideri sp. nov. (JB07T=NCCB 100888T=LMG 32616T). Additionally, some R. epipactidis and R. nectarea isolates showed isDDH values<79 % with other conspecific isolates, which suggests that these species include subspecies for which we propose the names Rosenbergiella epipactidis subsp. epipactidis subsp. nov. (S256T=CECT 8502T=LMG 27956T), Rosenbergiella epipactidis subsp. californiensis subsp. nov. (FR72T=NCCB 100898T=LMG 32786T), Rosenbergiella epipactidis subsp. japonicus subsp. nov. (K24T=NCCB 100924T=LMG 32785T), Rosenbergiella nectarea subsp. nectarea subsp. nov. (8N4T = DSM 24150T = LMG 26121T) and Rosenbergiella nectarea subsp. apis subsp. nov. (B1AT=NCCB 100810T= DSM 111763T), respectively. Finally, we present the first phylogenomic analysis of the genus Rosenbergiella and update the formal description of the species R. australiborealis, R. collisarenosi, R. epipactidis and R. nectarea based on new genomic and phenotypic information.

  View details for DOI 10.1099/ijsem.0.005777

  View details for PubMedID 36884370

• Harnessing island-ocean connections to maximize marine benefits of island conservation. Proceedings of the National Academy of Sciences of the United States of America Sandin, S. A., Becker, P. A., Becker, C., Brown, K., Erazo, N. G., Figuerola, C., Fisher, R. N., Friedlander, A. M., Fukami, T., Graham, N. A., Gruner, D. S., Holmes, N. D., Holthuijzen, W. A., Jones, H. P., Rios, M., Samaniego, A., Sechrest, W., Semmens, B. X., Thornton, H. E., Vega Thurber, R., Wails, C. N., Wolf, C. A., Zgliczynski, B. J. 2022; 119 (51): e2122354119

  Abstract

  Islands support unique plants, animals, and human societies found nowhere else on the Earth. Local and global stressors threaten the persistence of island ecosystems, with invasive species being among the most damaging, yet solvable, stressors. While the threat of invasive terrestrial mammals on island flora and fauna is well recognized, recent studies have begun to illustrate their extended and destructive impacts on adjacent marine environments. Eradication of invasive mammals and restoration of native biota are promising tools to address both island and ocean management goals. The magnitude of the marine benefits of island restoration, however, is unlikely to be consistent across the globe. We propose a list of six environmental characteristics most likely to affect the strength of land-sea linkages: precipitation, elevation, vegetation cover, soil hydrology, oceanographic productivity, and wave energy. Global databases allow for the calculation of comparable metrics describing each environmental character across islands. Such metrics can be used today to evaluate relative potential for coupled land-sea conservation efforts and, with sustained investment in monitoring on land and sea, can be used in the future to refine science-based planning tools for integrated land-sea management. As conservation practitioners work to address the effects of climate change, ocean stressors, and biodiversity crises, it is essential that we maximize returns from our management investments. Linking efforts on land, including eradication of island invasive mammals, with marine restoration and protection should offer multiplied benefits to achieve concurrent global conservation goals.

  View details for DOI 10.1073/pnas.2122354119

  View details for PubMedID 36508667

• Harnessing island-ocean connections to maximize marine benefits of island conservation PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Sandin, S. A., Becker, P. A., Becker, C., Brown, K., Erazo, N. G., Figuerola, C., Fisher, R. N., Friedlander, A. M., Fukami, T., Graham, N. J., Gruner, D. S., Holmes, N. D., Holthuijzen, W. A., Jones, H. P., Rios, M., Samaniego, A., Sechrest, W., Semmens, B. X., Thornton, H. E., Thurber, R., Wails, C. N., Wolf, C. A., Zgliczynski, B. J. 2022; 119 (51)

  View details for DOI 10.1073/pnas.2122354119/-/DCSupplemental

  View details for Web of Science ID 000944703500001

• Disease management during bloom affects the floral microbiome but not pollination in a mass-flowering crop JOURNAL OF APPLIED ECOLOGY Schaeffer, R. N., Crowder, D. W., Illan, J., Beck, J. J., Fukami, T., Williams, N. M., Vannette, R. L. 2022

  View details for DOI 10.1111/1365-2664.14320

  View details for Web of Science ID 000888253000001

• Wide-ranging consequences of priority effects governed by an overarching factor. eLife Chappell, C. R., Dhami, M. K., Bitter, M. C., Czech, L., Herrera Paredes, S., Barrie, F. B., Calderon, Y., Eritano, K., Golden, L., Hekmat-Scafe, D., Hsu, V., Kieschnick, C., Malladi, S., Rush, N., Fukami, T. 2022; 11

  Abstract

  Priority effects, where arrival order and initial relative abundance modulate local species interactions, can exert taxonomic, functional, and evolutionary influences on ecological communities by driving them to alternative states. It remains unclear if these wide-ranging consequences of priority effects can be explained systematically by a common underlying factor. Here, we identify such a factor in an empirical system. In a series of field and laboratory studies, we focus on how pH affects nectar-colonizing microbes and their interactions with plants and pollinators. In a field survey, we found that nectar microbial communities in a hummingbird-pollinated shrub, Diplacus (formerly Mimulus) aurantiacus, exhibited abundance patterns indicative of alternative stable states that emerge through domination by either bacteria or yeasts within individual flowers. In addition, nectar pH varied among D. aurantiacus flowers in a manner that is consistent with the existence of these alternative stable states. In laboratory experiments, Acinetobacter nectaris, the bacterium most commonly found in D. aurantiacus nectar, exerted a strongly negative priority effect against Metschnikowia reukaufii, the most common nectar-specialist yeast, by reducing nectar pH. This priority effect likely explains the mutually exclusive pattern of dominance found in the field survey. Furthermore, experimental evolution simulating hummingbird-assisted dispersal between flowers revealed that M. reukaufii could evolve rapidly to improve resistance against the priority effect if constantly exposed to A. nectaris-induced pH reduction. Finally, in a field experiment, we found that low nectar pH could reduce nectar consumption by hummingbirds, suggesting functional consequences of the pH-driven priority effect for plant reproduction. Taken together, these results show that it is possible to identify an overarching factor that governs the eco-evolutionary dynamics of priority effects across multiple levels of biological organization.

  View details for DOI 10.7554/eLife.79647

  View details for PubMedID 36300797

• Potential effects of nectar microbes on pollinator health. Philosophical transactions of the Royal Society of London. Series B, Biological sciences Martin, V. N., Schaeffer, R. N., Fukami, T. 2022; 377 (1853): 20210155

  Abstract

  Floral nectar is prone to colonization by nectar-adapted yeasts and bacteria via air-, rain-, and animal-mediated dispersal. Upon colonization, microbes can modify nectar chemical constituents that are plant-provisioned or impart their own through secretion of metabolic by-products or antibiotics into the nectar environment. Such modifications can have consequences for pollinator perception of nectar quality, as microbial metabolism can leave a distinct imprint on olfactory and gustatory cues that inform foraging decisions. Furthermore, direct interactions between pollinators and nectar microbes, as well as consumption of modified nectar, have the potential to affect pollinator health both positively and negatively. Here, we discuss and integrate recent findings from research on plant-microbe-pollinator interactions and their consequences for pollinator health. We then explore future avenues of research that could shed light on the myriad ways in which nectar microbes can affect pollinator health, including the taxonomic diversity of vertebrate and invertebrate pollinators that rely on this reward. This article is part of the theme issue 'Natural processes influencing pollinator health: from chemistry to landscapes'.

  View details for DOI 10.1098/rstb.2021.0155

  View details for PubMedID 35491594

• Higher Variability in Fungi Compared to Bacteria in the Foraging Honey Bee Gut. Microbial ecology Decker, L. E., San Juan, P. A., Warren, M. L., Duckworth, C. E., Gao, C., Fukami, T. 2022

  Abstract

  Along with bacteria, fungi can represent a significant component of animal- and plant-associated microbial communities. However, we have only begun to describe these fungi, much less examine their effects on most animals and plants. Bacteria associated with the honey bee, Apis mellifera, have been well characterized across different regions of the gut. The mid- and hindgut of foraging bees house a deterministic set of core species that affect host health, whereas the crop, or the honey stomach, harbors a more diverse set of bacteria that is highly variable in composition among individual bees. Whether this contrast between the two regions of the gut also applies to fungi remains unclear despite their potential influence on host health. In honey bees caught foraging at four sites across the San Francisco Peninsula of California, we found that fungi were less distinct in species composition between the crop and the mid- and hindgut than bacteria. Unlike bacteria, fungi varied substantially in species composition throughout the honey bee gut, and much of this variation could be predicted by the location where we collected the bees. These observations suggest that fungi may be transient passengers and unimportant as gut symbionts. However, our findings also indicate that honey bees could be vectors of infectious plant diseases as many of the fungi we found in the honey bee gut are recognized as plant pathogens.

  View details for DOI 10.1007/s00248-021-01922-5

  View details for PubMedID 34997310

• The effects of ecological selection on species diversity and trait distribution: predictions and an empirical test. Ecology DeMalach, N., Ke, P., Fukami, T. 2021: e03567

  Abstract

  Ecological selection is a major driver of community assembly. Selection is classified as stabilizing when species with intermediate trait values gain the highest reproductive success, whereas selection is considered directional when fitness is highest for species with extreme trait values. Previous studies have investigated the effects of different selection types on trait distribution, but the effects of selection on species diversity have remained unclear. Here, we propose a framework for inferring the type and strength of selection by studying species diversity and trait distribution together against null expectations. We use a simulation model to confirm our prediction that directional selection should lead to lower species diversity than stabilizing selection despite a similar effect on trait community-weighted variance. We apply the framework to a mesocosm system of annual plants to test whether differences in species diversity between two habitats that vary in productivity are related to differences in selection on seed mass. We show that, in both habitats, species diversity was lower than the null expectation, but that species diversity was lower in the more productive habitat. We attribute this difference to strong directional selection for large-seeded species in the productive habitat as indicated by trait community-weighted-mean being higher and community-weighted variance being lower than the null expectations. In the less productive habitat, we found that community-weighted variance was higher than expected by chance, suggesting that seed mass could be a driver of niche partitioning under such conditions. Altogether, our results suggest that viewing species diversity and trait distribution as interrelated patterns driven by the same process, ecological selection, is helpful in understanding community assembly.

  View details for DOI 10.1002/ecy.3567

  View details for PubMedID 34674221

• Untangling the complexity of priority effects in multispecies communities. Ecology letters Song, C., Fukami, T., Saavedra, S. 2021

  Abstract

  The history of species immigration can dictate how species interact in local communities, thereby causing historical contingency in community assembly. Since immigration history is rarely known, these historical influences, or priority effects, pose a major challenge in predicting community assembly. Here, we provide a graph-based, non-parametric, theoretical framework for understanding the predictability of community assembly as affected by priority effects. To develop this framework, we first show that the diversity of possible priority effects increases super-exponentially with the number of species. We then point out that, despite this diversity, the consequences of priority effects for multispecies communities can be classified into four basic types, each of which reduces community predictability: alternative stable states, alternative transient paths, compositional cycles and the lack of escapes from compositional cycles to stable states. Using a neural network, we show that this classification of priority effects enables accurate explanation of community predictability, particularly when each species immigrates repeatedly. We also demonstrate the empirical utility of our theoretical framework by applying it to two experimentally derived assembly graphs of algal and ciliate communities. Based on these analyses, we discuss how the framework proposed here can help guide experimental investigation of the predictability of history-dependent community assembly.

  View details for DOI 10.1111/ele.13870

  View details for PubMedID 34472694

• Successful management of invasive rats across a fragmented landscape ENVIRONMENTAL CONSERVATION Barney, S. K., Leopold, D. R., Francisco, K., Flaspohler, D. J., Fukami, T., Giardina, C. P., Gruner, D. S., Knowlton, J. L., Pitt, W. C., Wilson Rankin, E. E. 2021; 48 (3): 200-207

  View details for DOI 10.1017/S0376892921000205

  View details for Web of Science ID 000687642400010

• Alternative States in Plant Communities Driven by a Life-History Trade-Off and Demographic Stochasticity AMERICAN NATURALIST DeMalach, N., Shnerb, N., Fukami, T. 2021

  View details for DOI 10.1086/714418

  View details for Web of Science ID 000656575400003

• Dynamic plant-soil microbe interactions: the neglected effect of soil conditioning time. The New phytologist Ke, P., Zee, P. C., Fukami, T. 2021

  Abstract

  Plant-soil feedbacks (PSF) may change in strength over the life of plant individuals as plants continue to modify the soil microbial community. However, the temporal variation in PSF is rarely quantified and its impacts on plant communities remain unknown. Using a chronosequence reconstructed from annual aerial photos of a coastal dune ecosystem, we characterized >20-year changes in soil microbial communities associated with individuals of the four dominant perennial species, one legume and three non-legume. We quantified the effects of soil biota on conspecific and heterospecific seedling performance in a greenhouse experiment that preserved soil properties of these individual plants. We used a general individual-based model to explore the potential consequences of temporally varying PSF on plant community assembly. In all plant species, microbial communities changed with plant age. However, plant's response to the turnover in microbial composition depended on the transplanted seedling species: only the soil biota effect experienced by the non-legume species became increasingly negative with longer soil conditioning. Model simulations suggested that temporal changes in PSF could affect the transient dynamics of plant community assembly. These results suggest that temporal variation in PSF over the course of decades should be considered to understand how PSF structures plant communities.

  View details for DOI 10.1111/nph.17420

  View details for PubMedID 34105771

• Acinetobacter pollinis sp. nov., Acinetobacter baretiae sp. nov. and Acinetobacter rathckeae sp. nov., isolated from floral nectar and honey bees. International journal of systematic and evolutionary microbiology Alvarez-Perez, S., Baker, L. J., Morris, M. M., Tsuji, K., Sanchez, V. A., Fukami, T., Vannette, R. L., Lievens, B., Hendry, T. A. 2021; 71 (5)

  Abstract

  A detailed evaluation of eight bacterial isolates from floral nectar and animal visitors to flowers shows evidence that they represent three novel species in the genus Acinetobacter. Phylogenomic analysis shows the closest relatives of these new isolates are Acinetobacter apis, Acinetobacter boissieri and Acinetobacter nectaris, previously described species associated with floral nectar and bees, but high genome-wide sequence divergence defines these isolates as novel species. Pairwise comparisons of the average nucleotide identity of the new isolates compared to known species is extremely low (<83 %), thus confirming that these samples are representative of three novel Acinetobacter species, for which the names Acinetobacter pollinis sp. nov., Acinetobacter baretiae sp. nov. and Acinetobacter rathckeae sp. nov. are proposed. The respective type strains are SCC477T (=TSD-214T=LMG 31655T), B10AT (=TSD-213T=LMG 31702T) and EC24T (=TSD-215T=LMG 31703T=DSM 111781T).

  View details for DOI 10.1099/ijsem.0.004783

  View details for PubMedID 33970854

• Correction to: Nitrogen Assimilation Varies Among Clades of Nectar- and Insect-Associated Acinetobacters. Microbial ecology Alvarez-Perez, S., Tsuji, K., Donald, M., Van Assche, A., Vannette, R. L., Herrera, C. M., Jacquemyn, H., Fukami, T., Lievens, B. 2021

  View details for DOI 10.1007/s00248-021-01755-2

  View details for PubMedID 33864130

• Diversity of putative ericoid mycorrhizal fungi increases with soil age and progressive phosphorus limitation across a 4.1 million-year chronosequence. FEMS microbiology ecology Leopold, D. R., Peay, K. G., Vitousek, P. M., Fukami, T. 2021

  Abstract

  Ericaceous plants rely on ericoid mycorrhizal fungi for nutrient acquisition. However, the factors that affect the composition and structure of fungal communities associated with the roots of ericaceous plants remain largely unknown. Here, we use a 4.1-myr soil chronosequence in Hawaii to test the hypothesis that changes in nutrient availability with soil age determine the diversity and species composition of fungi associated with ericoid roots. We sampled roots of a native Hawaiian plant, Vaccinium calycinum, and used DNA metabarcoding to quantify changes in fungal diversity and community composition. We also used a fertilization experiment at the youngest and oldest sites to assess the importance of nutrient limitation. We found an increase in diversity and a clear pattern of species turnover across the chronosequence, driven largely by putative ericoid mycorrhizal fungi. Fertilization with nitrogen at the youngest site and phosphorus at the oldest site reduced fungal diversity, suggesting a direct role of nutrient limitation. Our results also reveal the presence of novel fungal species associated with Hawaiian Ericaceae and suggest a greater importance of phosphorus availability for communities of ericoid mycorrhizal fungi than is generally assumed.

  View details for DOI 10.1093/femsec/fiab016

  View details for PubMedID 33512432

• Nitrogen Assimilation Varies Among Clades of Nectar- and Insect-Associated Acinetobacters. Microbial ecology Alvarez-Perez, S., Tsuji, K., Donald, M., Van Assche, A., Vannette, R. L., Herrera, C. M., Jacquemyn, H., Fukami, T., Lievens, B. 2021

  Abstract

  Floral nectar is commonly colonized by yeasts and bacteria, whose growth largely depends on their capacity to assimilate nutrient resources, withstand high osmotic pressures, and cope with unbalanced carbon-to-nitrogen ratios. Although the basis of the ecological success of these microbes in the harsh environment of nectar is still poorly understood, it is reasonable to assume that they are efficient nitrogen scavengers that can consume a wide range of nitrogen sources in nectar. Furthermore, it can be hypothesized that phylogenetically closely related strains have more similar phenotypic characteristics than distant relatives. We tested these hypotheses by investigating the growth performance on different nitrogen-rich substrates of a collection of 82 acinetobacters isolated from nectar and honeybees, representing members of five species (Acinetobacter nectaris, A. boissieri, A. apis, and the recently described taxa A. bareti and A. pollinis). We also analyzed possible links between growth performance and phylogenetic affiliation of the isolates, while taking into account their geographical origin. Results demonstrated that the studied isolates could utilize a wide variety of nitrogen sources, including common metabolic by-products of yeasts (e.g., ammonium and urea), and that phylogenetic relatedness was associated with the variation in nitrogen assimilation among the studied acinetobacters. Finally, nutrient source and the origin (sample type and country) of isolates also predicted the ability of the acinetobacters to assimilate nitrogen-rich compounds. Overall, these results demonstrate inter-clade variation in the potential of the acinetobacters as nitrogen scavengers and suggest that nutritional dependences might influence interactions between bacteria and yeasts in floral nectar.

  View details for DOI 10.1007/s00248-020-01671-x

  View details for PubMedID 33404822

• Yeast-nectar interactions: metacommunities and effects on pollinators. Current opinion in insect science Jacquemyn, H., Pozo, M. I., Alvarez-Perez, S., Lievens, B., Fukami, T. 2020

  Abstract

  About 90% of all flowering plant species are pollinated by animals. Animals are attracted to flowers because they often provide food in the form of nectar and pollen. While floral nectar is assumed to be initially sterile, it commonly becomes colonized by yeasts after animals have visited the flowers. Although yeast communities in floral nectar appear simple, community assembly depends on a complex interaction between multiple factors. Yeast colonization has a significant effect on the scent of floral nectar, foraging behavior of insects and nectar consumption. Consumption of nectar colonized by yeasts has been shown to improve bee fitness, but effects largely depended on yeast species. Altogether, these results indicate that dispersal, colonization history and nectar chemistry strongly interact and have pronounced effects on yeast metacommunities and as result bee foraging behavior and fitness. Future research directions to better understand the dynamics of plant-microbe-pollinator interactions are discussed.

  View details for DOI 10.1016/j.cois.2020.09.014

  View details for PubMedID 33065340

• Intensive farming drives long-term shifts in avian community composition. Nature Hendershot, J. N., Smith, J. R., Anderson, C. B., Letten, A. D., Frishkoff, L. O., Zook, J. R., Fukami, T., Daily, G. C. 2020; 579 (7799): 393–96

  Abstract

  Agricultural practices constitute both the greatest cause of biodiversity loss and the greatest opportunity for conservation1,2, given the shrinking scope of protected areas in many regions. Recent studies have documented the high levels of biodiversity-across many taxa and biomes-that agricultural landscapes can support over the short term1,3,4. However, little is known about the long-term effects of alternative agricultural practices on ecological communities4,5 Here we document changes in bird communities in intensive-agriculture, diversified-agriculture and natural-forest habitats in 4 regions of Costa Rica over a period of 18 years. Long-term directional shifts in bird communities were evident in intensive- and diversified-agricultural habitats, but were strongest in intensive-agricultural habitats, where the number of endemic and International Union for Conservation of Nature (IUCN) Red List species fell over time. All major guilds, including those involved in pest control, pollination and seed dispersal, were affected. Bird communities in intensive-agricultural habitats proved more susceptible to changes in climate, with hotter and drier periods associated with greater changes in community composition in these settings. These findings demonstrate that diversified agriculture can help to alleviate the long-term loss of biodiversity outside natural protected areas1.

  View details for DOI 10.1038/s41586-020-2090-6

  View details for PubMedID 32188954

• Greater local diversity under older species pools may arise from enhanced competitive equivalence. Ecology letters Leopold, D. R., Fukami, T. n. 2020

  Abstract

  Ecological communities typically contain more species when located within geologically older regions. This pattern is traditionally attributed to the long-term accumulation of species in the regional species pool, with local species interactions playing a minor role. We provide evidence suggesting a more important role of local species interactions than generally assumed. We assembled 320 communities of root-associated fungi under 80 species pools, varying species pool richness and the mean age of the sites from which the fungi were collected across a 4-myr soil chronosequence. We found that local diversity increased more with increasing species pool richness when species were from older sites. We also found that older species pools had lower functional and phylogenetic diversity, indicating greater competitive equivalence among species. Our results suggest that older regions have higher local richness not simply because older pools are more speciose but also because species have evolved traits that allow them to locally co-occur.

  View details for DOI 10.1111/ele.13647

  View details for PubMedID 33216438

• Land-use change has host-specific influences on avian gut microbiomes. The ISME journal San Juan, P. A., Hendershot, J. N., Daily, G. C., Fukami, T. 2019

  Abstract

  Human modification of the environment, particularly through land-use change, often reduces animal species diversity. However, the effect of land-use change on the gut microbiome of wildlife in human-dominated landscapes is not well understood despite its potential consequences for host health. We sought to quantify the effect of land-use change on wild bird gut microbiomes in a countryside landscape in Costa Rica, comprising a range of habitat types, ranging from primary and secondary forests to diversified and monoculture farms. We collected 280 fresh fecal samples from individuals belonging to six common species of saltator, thrushes, and warblers at 24 sites across this land-use gradient. Through 16S rRNA community profiling, we found that bacterial species composition responded to host species identity more strongly than to habitat type. In addition, we found evidence that habitat type affected microbial composition only for two of the six bird species. Our findings indicate that some host species and their microbiota may be more vulnerable to human disturbances than others.

  View details for DOI 10.1038/s41396-019-0535-4

  View details for PubMedID 31624349

• Sexual Dimorphism and Species Diversity: from Clades to Sites. Trends in ecology & evolution Tsuji, K., Fukami, T. 2019

  Abstract

  A variety of relationships have been observed between sexual dimorphism and species diversity, from positive to negative and nonsignificant. Although many hypotheses have been proposed to explain these relationships, it has proven difficult to understand why patterns are so variable. Most studies on this topic have used clades as phylogenetically independent replicates for pattern analysis, but a few recent studies took an alternative approach, using sites as spatially independent replicates. We discuss how the new, site-based studies complement the traditional, clade-based studies and argue that the combined use of the two approaches will be more powerful than either alone in understanding environmental factors that produce variation in sexual dimorphism-species diversity relationships.

  View details for DOI 10.1016/j.tree.2019.09.001

  View details for PubMedID 31623865

• Yeast-Bacterium Interactions: The Next Frontier in Nectar Research TRENDS IN PLANT SCIENCE Alvarez-Perez, S., Lievens, B., Fukami, T. 2019; 24 (5): 393–401

  View details for DOI 10.1016/j.tplants.2019.01.012

  View details for Web of Science ID 000465084400005

• High-resolution mapping reveals that microniches in the gastric glands control Helicobacter pylori colonization of the stomach PLOS BIOLOGY Fung, C., Tan, S., Nakajima, M., Skoog, E. C., Camarillo-Guerrero, L., Klein, J. A., Lawley, T. D., Solnick, J. V., Fukami, T., Amieva, M. R. 2019; 17 (5)

  View details for DOI 10.1371/journal.pbio.3000231

  View details for Web of Science ID 000470189800004

• Applying modern coexistence theory to priority effects PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Grainger, T., Letten, A. D., Gilbert, B., Fukami, T. 2019; 116 (13): 6205–10

  View details for DOI 10.1073/pnas.1803122116

  View details for Web of Science ID 000462382800060

• Applying modern coexistence theory to priority effects. Proceedings of the National Academy of Sciences of the United States of America Grainger, T. N., Letten, A. D., Gilbert, B., Fukami, T. 2019

  Abstract

  Modern coexistence theory is increasingly used to explain how differences between competing species lead to coexistence versus competitive exclusion. Although research testing this theory has focused on deterministic cases of competitive exclusion, in which the same species always wins, mounting evidence suggests that competitive exclusion is often historically contingent, such that whichever species happens to arrive first excludes the other. Coexistence theory predicts that historically contingent exclusion, known as priority effects, will occur when large destabilizing differences (positive frequency-dependent growth rates of competitors), combined with small fitness differences (differences in competitors' intrinsic growth rates and sensitivity to competition), create conditions under which neither species can invade an established population of its competitor. Here we extend the empirical application of modern coexistence theory to determine the conditions that promote priority effects. We conducted pairwise invasion tests with four strains of nectar-colonizing yeasts to determine how the destabilizing and fitness differences that drive priority effects are altered by two abiotic factors characterizing the nectar environment: sugar concentration and pH. We found that higher sugar concentrations increased the likelihood of priority effects by reducing fitness differences between competing species. In contrast, higher pH did not change the likelihood of priority effects, but instead made competition more neutral by bringing both fitness differences and destabilizing differences closer to zero. This study demonstrates how the empirical partitioning of priority effects into fitness and destabilizing components can elucidate the pathways through which environmental conditions shape competitive interactions.

  View details for PubMedID 30850518

• Yeast-Bacterium Interactions: The Next Frontier in Nectar Research. Trends in plant science Alvarez-Perez, S., Lievens, B., Fukami, T. 2019

  Abstract

  Beyond its role as a reward for pollinators, floral nectar also provides a habitat for specialized and opportunistic yeasts and bacteria. These microbes modify nectar chemistry, often altering mutualistic relationships between plants and pollinators in ways that we are only beginning to understand. Many studies on this multi-partite system have focused on either yeasts or bacteria without consideration of yeast-bacterium interactions, but recent evidence suggests that such interactions drive the assembly of nectar microbial communities and its consequences for pollination. Unexplored potential mechanisms of yeast-bacterium interactions include the formation of physical complexes, nutritional interactions, antibiosis, signaling-based interactions, and horizontal gene transfer. We argue that studying these mechanisms can elucidate how nectar microbial communities are established and affect plant fitness via pollinators.

  View details for PubMedID 30792076

• High-resolution mapping reveals that microniches in the gastric glands control Helicobacter pylori colonization of the stomach. PLoS biology Fung, C. n., Tan, S. n., Nakajima, M. n., Skoog, E. C., Camarillo-Guerrero, L. F., Klein, J. A., Lawley, T. D., Solnick, J. V., Fukami, T. n., Amieva, M. R. 2019; 17 (5): e3000231

  Abstract

  Lifelong infection of the gastric mucosa by Helicobacter pylori can lead to peptic ulcers and gastric cancer. However, how the bacteria maintain chronic colonization in the face of constant mucus and epithelial cell turnover in the stomach is unclear. Here, we present a new model of how H. pylori establish and persist in stomach, which involves the colonization of a specialized microenvironment, or microniche, deep in the gastric glands. Using quantitative three-dimensional (3D) confocal microscopy and passive CLARITY technique (PACT), which renders tissues optically transparent, we analyzed intact stomachs from mice infected with a mixture of isogenic, fluorescent H. pylori strains with unprecedented spatial resolution. We discovered that a small number of bacterial founders initially establish colonies deep in the gastric glands and then expand to colonize adjacent glands, forming clonal population islands that persist over time. Gland-associated populations do not intermix with free-swimming bacteria in the surface mucus, and they compete for space and prevent newcomers from establishing in the stomach. Furthermore, bacterial mutants deficient in gland colonization are outcompeted by wild-type (WT) bacteria. Finally, we found that host factors such as the age at infection and T-cell responses control bacterial density within the glands. Collectively, our results demonstrate that microniches in the gastric glands house a persistent H. pylori reservoir, which we propose replenishes the more transient bacterial populations in the superficial mucosa.

  View details for PubMedID 31048876

• Community-wide consequences of sexual dimorphism: evidence from nectar microbes in dioecious plants ECOLOGY Tsuji, K., Fukami, T. 2018; 99 (11): 2476–84

  Abstract

  Intraspecific trait variation is receiving renewed interest as a factor affecting the structure of multi-species communities within and across trophic levels. One pervasive form of intraspecific trait variation is sexual dimorphism in animals and plants, which might exert large effects particularly on the communities of host-associated organisms, but the extent of these effects is not well understood. We investigated whether host-associated microbial communities developed differently in the floral nectar of female and male individuals of the dioecious shrubs, Eurya emarginata and E. japonica. We found that nectar-colonizing microbes such as bacteria and fungi were more than twice as prevalent and, overall, more than 10 times as abundant in male flowers as in female flowers. Microbial species composition also differed between flower sexes. To examine potential mechanisms behind these differences, we manipulated the frequency of flower visitation by animals and the order of arrival of microbial species to nectar. Animal visitation frequency affected microbial communities more greatly in male flowers, while arrival order affected them more in female flowers. These sex-specific effects appeared attributable to differences in how animals and microbes altered the chemical characteristics of nectar that limited microbial growth. Taken together, our results provide evidence that sexual dimorphism can have large effects on the structure of host-associated communities.

  View details for PubMedID 30216955

• Vertical foraging shifts in Hawaiian forest birds in response to invasive rat removal PLOS ONE Rankin, E., Knowlton, J. L., Gruner, D. S., Flaspohler, D. J., Giardina, C. P., Leopold, D. R., Buckardt, A., Pitt, W. C., Fukami, T. 2018; 13 (9): e0202869

  Abstract

  Worldwide, native species increasingly contend with the interacting stressors of habitat fragmentation and invasive species, yet their combined effects have rarely been examined. Direct negative effects of invasive omnivores are well documented, but the indirect effects of resource competition or those caused by predator avoidance are unknown. Here we isolated and examined the independent and interactive effects of invasive omnivorous Black rats (Rattus rattus) and forest fragment size on the interactions between avian predators and their arthropod prey. Our study examines whether invasive omnivores and ecosystem fragment size impact: 1) the vertical distribution of arthropod species composition and abundance, and 2) the vertical profile of foraging behaviors of five native and two non-native bird species found in our study system. We predicted that the reduced edge effects and greater structural complexity and canopy height of larger fragments would limit the total and proportional habitat space frequented by rats and thus limit their impact on both arthropod biomass and birds' foraging behavior. We experimentally removed invasive omnivorous Black rats across a 100-fold (0.1 to 12 ha) size gradient of forest fragments on Hawai'i Island, and paired foraging observations of forest passerines with arthropod sampling in the 16 rat-removed and 18 control fragments. Rat removal was associated with shifts in the vertical distribution of arthropod biomass, irrespective of fragment size. Bird foraging behavior mirrored this shift, and the impact of rat removal was greater for birds that primarily eat fruit and insects compared with those that consume nectar. Evidence from this model study system indicates that invasive rats indirectly alter the feeding behavior of native birds, and consequently impact multiple trophic levels. This study suggests that native species can modify their foraging behavior in response to invasive species removal and presumably arrival through behavioral plasticity.

  View details for PubMedID 30248110

• Species coexistence through simultaneous fluctuation-dependent mechanisms PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Letten, A. D., Dhami, M. K., Ke, P., Fukami, T. 2018; 115 (26): 6745–50

  View details for DOI 10.1073/pnas.1801846115

  View details for Web of Science ID 000436245000076

• Contrasting effects of yeasts and bacteria on floral nectar traits ANNALS OF BOTANY Vannette, R. L., Fukami, T. 2018; 121 (7): 1343–49

  View details for DOI 10.1093/aob/mcy032

  View details for Web of Science ID 000434870300014

• Nectar yeasts: a natural microcosm for ecology. Yeast (Chichester, England) Chappell, C. R., Fukami, T. 2018; 35 (6): 417–23

  Abstract

  The species of yeasts that colonize floral nectar can modify the mutualistic relationships between plants and pollinators by changing the chemical properties of nectar. Recent evidence supporting this possibility has led to increased interest among ecologists in studying these fungi as well as the bacteria that interact with them in nectar. Although not fully explored, nectar yeasts also constitute a promising natural microcosm that can be used to facilitate development of general ecological theory. We discuss the methodological and conceptual advantages of using nectar yeasts from this perspective, including simplicity of communities, tractability of dispersal, replicability of community assembly, and the ease with which the mechanisms of species interactions can be studied in complementary experiments conducted in the field and the laboratory. To illustrate the power of nectar yeasts as a study system, we discuss several topics in community ecology, including environmental filtering, priority effects, and metacommunity dynamics. An exciting new direction is to integrate metagenomics and comparative genomics into nectar yeast research to address these fundamental ecological topics.

  View details for PubMedID 29476620

• Nectar yeasts: a natural microcosm for ecology YEAST Chappell, C. R., Fukami, T. 2018; 35 (6): 417–23

  View details for DOI 10.1002/yea.3311

  View details for Web of Science ID 000434281100002

• Eco-Evolutionary Buffering: Rapid Evolution Facilitates Regional Species Coexistence despite Local Priority Effects AMERICAN NATURALIST Wittmann, M. J., Fukami, T. 2018; 191 (6): E171–E184

  Abstract

  Inhibitory priority effects, in which early-arriving species exclude competing species from local communities, are thought to enhance regional species diversity via community divergence. Theory suggests, however, that these same priority effects make it difficult for species to coexist in the region unless individuals are continuously supplied from an external species pool, often an unrealistic assumption. Here we develop an eco-evolutionary hypothesis to solve this conundrum. We build a metacommunity model in which local priority effects occur between two species via interspecific interference. Within each species there are two genotypes: one is more resistant to interspecific interference than the other but pays a fitness cost for its resistance. Because of this trade-off, species evolve to become less resistant as they become regionally more common. Rare species can then invade some local patches and consequently recover in regional frequency. This "eco-evolutionary buffering" enables the regional coexistence of species despite local priority effects, even in the absence of immigration from an external species pool. Our model predicts that eco-evolutionary buffering is particularly effective when local communities are small and connected by infrequent dispersal.

  View details for DOI 10.1086/697187

  View details for Web of Science ID 000432225200001

  View details for PubMedID 29750553

• Genomic diversity of a nectar yeast clusters into metabolically, but not geographically, distinct lineages MOLECULAR ECOLOGY Dhami, M. K., Hartwig, T., Letten, A. D., Banf, M., Fukami, T. 2018; 27 (8): 2067–76

  Abstract

  Both dispersal limitation and environmental sorting can affect genetic variation in populations, but their contribution remains unclear, particularly in microbes. We sought to determine the contribution of geographic distance (as a proxy for dispersal limitation) and phenotypic traits (as a proxy for environmental sorting), including morphology, metabolic ability and interspecific competitiveness, to the genotypic diversity in a nectar yeast species, Metschnikowia reukaufii. To measure genotypic diversity, we sequenced the genomes of 102 strains of M. reukaufii isolated from the floral nectar of hummingbird-pollinated shrub, Mimulus aurantiacus, along a 200-km coastline in California. Intraspecific genetic variation showed no detectable relationship with geographic distance, but could be grouped into three distinct lineages that correlated with metabolic ability and interspecific competitiveness. Despite ample evidence for strong competitive interactions within and among nectar yeasts, a full spectrum of the genotypic and phenotypic diversity observed across the 200-km coastline was represented even at a scale as small as 200 m. Further, more competitive strains were not necessarily more abundant. These results suggest that dispersal limitation and environmental sorting might not fully explain intraspecific diversity in this microbe and highlight the need to also consider other ecological factors such as trade-offs, source-sink dynamics and niche modification.

  View details for PubMedID 29446179

• The ecology of insect-yeast relationships and its relevance to human industry PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES Madden, A. A., Epps, M., Fukami, T., Irwin, R. E., Sheppard, J., Sorger, D., Dunn, R. R. 2018; 285 (1875)

  Abstract

  Many species of yeast are integral to human society. They produce many of our foods, beverages and industrial chemicals, challenge us as pathogens, and provide models for the study of our own biology. However, few species are regularly studied and much of their ecology remains unclear, hindering the development of knowledge that is needed to improve the relationships between humans and yeasts. There is increasing evidence that insects are an essential component of ascomycetous yeast ecology. We propose a 'dispersal-encounter hypothesis' whereby yeasts are dispersed by insects between ephemeral, spatially disparate sugar resources, and insects, in turn, obtain the benefits of an honest signal from yeasts for the sugar resources. We review the relationship between yeasts and insects through three main examples: social wasps, social bees and beetles, with some additional examples from fruit flies. Ultimately, we suggest that over the next decades, consideration of these ecological and evolutionary relationships between insects and yeasts will allow prediction of where new yeast diversity is most likely to be discovered, particularly yeasts with traits of interest to human industry.

  View details for PubMedID 29563264

• Contrasting effects of yeasts and bacteria on floral nectar traits. Annals of botany Vannette, R. L., Fukami, T. 2018

  Abstract

  Background and Aims: Flowers can be highly variable in nectar volume and chemical composition, even within the same plant, but the causes of this variation are not fully understood. One potential cause is nectar-colonizing bacteria and yeasts, but experimental tests isolating their effects on wildflowers are largely lacking. This study examines the effects of dominant species of yeasts and bacteria on the hummingbird-pollinated shrub, Mimulus aurantiacus, in California.Methods: Wildflowers were inoculated with field-relevant titres of either the yeast Metschnikowia reukaufii or the bacterium Neokomagataea sp. (formerly Gluconobacter sp.), both isolated from M. aurantiacus nectar. Newly opened flowers were bagged, inoculated, harvested after 3 d and analysed for microbial abundance, nectar volume, and sugar and amino acid concentration and composition.Key Results: Yeast inoculation reduced amino acid concentration and altered amino acid composition, but had no significant effect on nectar volume or sugar composition. In contrast, bacterial inoculation increased amino acid concentration, enhanced the proportion of nectar sugars comprised by monosaccharides, and reduced nectar volume.Conclusions: The results presented suggest that microbial inhabitants of floral nectar can make nectar characteristics variable among flowers through divergent effects of yeasts and bacteria on nectar chemistry and availability, probably modifying plant-pollinator interactions.

  View details for PubMedID 29562323

• Priority effects can persist across floral generations in nectar microbial metacommunities OIKOS Toju, H., Vannette, R. L., Gauthier, M. L., Dhami, M. K., Fukami, T. 2018; 127 (3): 345–52

  View details for DOI 10.1111/oik.04243

  View details for Web of Science ID 000426652500002

• Priority effects are weakened by a short, but not long, history of sympatric evolution. Proceedings. Biological sciences Zee, P. C., Fukami, T. 2018; 285 (1871)

  Abstract

  Priority effects, or the effects of species arrival history on local species abundances, have been documented in a range of taxa. However, factors determining the extent to which priority effects affect community assembly remain unclear. Using laboratory populations of the bacterium Pseudomonas fluorescens, we examined whether shared evolutionary history affected the strength of priority effects. We hypothesized that sympatric evolution of populations belonging to the same guild would lead to niche differentiation, resulting in phenotypic complementarity that weakens priority effects. Consistent with this hypothesis, we found that priority effects tended to be weaker in sympatrically evolved pairs of immigrating populations than in allopatrically evolved pairs. Furthermore, priority effects were weaker under higher phenotypic complementarity. However, these patterns were observed only in populations with a relatively short history of sympatric evolution, and disappeared when populations had evolved together for a long time. Together, our results suggest that the evolutionary history of organismal traits may dictate the strength of priority effects and, consequently, the extent of historical contingency in the assembly of ecological communities.

  View details for PubMedID 29386363

• Priority effects are weakened by a short, but not long, history of sympatric evolution PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES Zee, P. C., Fukami, T. 2018; 285 (1871)

  View details for DOI 10.1098/rspb.2017.1722

  View details for Web of Science ID 000423774700001

• Species coexistence through simultaneous fluctuation-dependent mechanisms. Proceedings of the National Academy of Sciences of the United States of America Letten, A. D., Dhami, M. K., Ke, P. J., Fukami, T. n. 2018

  Abstract

  Understanding the origins and maintenance of biodiversity remains one of biology's grand challenges. From theory and observational evidence, we know that variability in environmental conditions through time is likely critical to the coexistence of competing species. Nevertheless, experimental tests of fluctuation-driven coexistence are rare and have typically focused on just one of two potential mechanisms, the temporal storage effect, to the neglect of the theoretically equally plausible mechanism known as relative nonlinearity of competition. We combined experiments and simulations in a system of nectar yeasts to quantify the relative contribution of the two mechanisms to coexistence. Resource competition models parameterized from single-species assays predicted the outcomes of mixed-culture competition experiments with 83% accuracy. Model simulations revealed that both mechanisms have measurable effects on coexistence and that relative nonlinearity can be equal or greater in magnitude to the temporal storage effect. In addition, we show that their effect on coexistence can be both antagonistic and complementary. These results falsify the common assumption that relative nonlinearity is of negligible importance, and in doing so reveal the importance of testing coexistence mechanisms in combination.

  View details for PubMedID 29895689

• Role of priority effects in the early-life assembly of the gut microbiota. Nature reviews. Gastroenterology & hepatology Sprockett, D. n., Fukami, T. n., Relman, D. A. 2018; 15 (4): 197–205

  Abstract

  Understanding how microbial communities develop is essential for predicting and directing their future states. Ecological theory suggests that community development is often influenced by priority effects, in which the order and timing of species arrival determine how species affect one another. Priority effects can have long-lasting consequences, particularly if species arrival history varies during the early stage of community development, but their importance to the human gut microbiota and host health remains largely unknown. Here, we explore how priority effects might influence microbial communities in the gastrointestinal tract during early childhood and how the strength of priority effects can be estimated from the composition of the microbial species pool. We also discuss factors that alter microbial transmission, such as delivery mode, diet and parenting behaviours such as breastfeeding, which can influence the likelihood of priority effects. An improved knowledge of priority effects has the potential to inform microorganism-based therapies, such as prebiotics and probiotics, which are aimed at guiding the microbiota towards a healthy state.

  View details for PubMedID 29362469

• Geographical Variation in Community Divergence: Insights from Tropical Forest Monodominance by Ectomycorrhizal Trees AMERICAN NATURALIST Fukami, T., Nakajima, M., Fortunel, C., Fine, P. A., Baraloto, C., Russo, S. E., Peay, K. G. 2017; 190: S105–S122

  Abstract

  Convergence occurs in both species traits and community structure, but how convergence at the two scales influences each other remains unclear. To address this question, we focus on tropical forest monodominance, in which a single, often ectomycorrhizal (EM) tree species occasionally dominates forest stands within a landscape otherwise characterized by diverse communities of arbuscular mycorrhizal (AM) trees. Such monodominance is a striking potential example of community divergence resulting in alternative stable states. However, it is observed only in some tropical regions. A diverse suite of AM and EM trees locally codominate forest stands elsewhere. We develop a hypothesis to explain this geographical difference using a simulation model of plant community assembly. Simulation results suggest that in a region with a few EM species (e.g., South America), EM trees experience strong selection for convergent traits that match the abiotic conditions of the environment. Consequently, EM species successfully compete against other species to form monodominant stands via positive plant-soil feedbacks. By contrast, in a region with many EM species (e.g., Southeast Asia), species maintain divergent traits because of complex plant-soil feedbacks, with no species having traits that enable monodominance. An analysis of plant trait data from Borneo and Peruvian Amazon was inconclusive. Overall, this work highlights the utility of geographical comparison in understanding the relationship between trait convergence and community convergence.

  View details for DOI 10.1086/692439

  View details for Web of Science ID 000406102900008

  View details for PubMedID 28731828

• Priority effects are interactively regulated by top-down and bottom-up forces: evidence from wood decomposer communities ECOLOGY LETTERS Leopold, D. R., Wilkie, J., Dickie, I. A., Allen, R. B., Buchanan, P. K., Fukami, T. 2017; 20 (8): 1054–63

  Abstract

  Both top-down (grazing) and bottom-up (resource availability) forces can determine the strength of priority effects, or the effects of species arrival history on the structure and function of ecological communities, but their combined influences remain unresolved. To test for such influences, we assembled experimental communities of wood-decomposing fungi using a factorial manipulation of fungivore (Folsomia candida) presence, nitrogen availability, and fungal assembly history. We found interactive effects of all three factors on fungal species composition and wood decomposition 1 year after the fungi were introduced. The strength of priority effects on community structure was affected primarily by nitrogen availability, whereas the strength of priority effects on decomposition rate was interactively regulated by nitrogen and fungivores. These results demonstrate that top-down and bottom-up forces jointly determine how strongly assembly history affects community structure and function.

  View details for PubMedID 28677298

• Dispersal enhances beta diversity in nectar microbes ECOLOGY LETTERS Vannette, R. L., Fukami, T. 2017; 20 (7): 901–10

  Abstract

  Dispersal is considered a key driver of beta diversity, the variation in species composition among local communities, but empirical tests remain limited. We manipulated dispersal of nectar-inhabiting bacteria and yeasts via flower-visiting animals to examine how dispersal influenced microbial beta diversity among flowers. Contrary to the prevailing view that dispersal lowers beta diversity, we found beta diversity was highest when dispersal was least limited. Our analysis suggested that this unexpected pattern might have resulted from stronger priority effects under increased dispersal. Dispersal is highly stochastic, generating variability in species arrival history and consequently the potential for community divergence via priority effects, in these and likely many other microbial, plant, and animal communities. Yet most previous experiments eliminated this possibility. We suggest that the positive effects of dispersal on beta diversity, like the one we report here, may have been greatly underappreciated.

  View details for PubMedID 28597955

• Movements of four native Hawaiian birds across a naturally fragmented landscape JOURNAL OF AVIAN BIOLOGY Knowlton, J. L., Flaspohler, D. J., Paxton, E. H., Fukami, T., Giardina, C. P., Gruner, D. S., Rankin, E. 2017; 48 (7): 921–31

  View details for DOI 10.1111/jav.00924

  View details for Web of Science ID 000407250900003

• Linking modern coexistence theory and contemporary niche theory ECOLOGICAL MONOGRAPHS Letten, A. D., Ke, P., Fukami, T. 2017; 87 (2): 161-177

  View details for DOI 10.1002/ecm.1242

  View details for Web of Science ID 000400406300001

• Evolutionary priority effects persist in anthropogenically created habitats, but not through nonnative plant invasion. New phytologist Brandt, A. J., Lee, W. G., Tanentzap, A. J., Hayman, E., Fukami, T., Anderson, B. J. 2017

  Abstract

  Evolutionary priority effects, where early-arriving lineages occupy niche space via diversification and preclude dominance of later arrivals, have been observed in alpine and forest communities. However, the potential for evolutionary priority effects to persist in an era of rapid global change remains unclear. Here, we use a natural experiment of historical disturbance in New Zealand to test whether anthropogenic changes in available habitat and nonnative invasion eliminate the role of evolutionary priority effects in community assembly. We also test whether evolutionary priority effects diminish with decreasing resource availability. Older plant clades, as estimated by clade crown age, were relatively more abundant in both primary and secondary grassland. Relative abundance in primary grassland decreased with clade stem age, but only weakly. However, for both clade age estimates, relative abundance decreased with age when nonnative biomass was high and soil moisture was low. Our data show that patterns in community structure consistent with evolutionary priority effects can occur in both primary and secondary grasslands, the latter created by anthropogenic disturbance. However, nonnative invasion may overwhelm the effect of immigration timing on community dominance, possibly as a result of high immigration rates and preadaptation to anthropogenically modified environments.

  View details for DOI 10.1111/nph.14544

  View details for PubMedID 28407248

• Non-target effects of fungicides on nectar-inhabiting fungi of almond flowers ENVIRONMENTAL MICROBIOLOGY REPORTS Schaeffer, R. N., Vannette, R. L., Brittain, C., Williams, N. M., Fukami, T. 2017; 9 (2): 79-84

  Abstract

  Nectar mediates interactions between plants and pollinators in natural and agricultural systems. Specialized microorganisms are common nectar inhabitants, and potentially important mediators of plant-pollinator interactions. However, their diversity and role in mediating pollination services in agricultural systems are poorly characterized. Moreover, agrochemicals are commonly applied to minimize crop damage, but may present ecological consequences for non-target organisms. Assessment of ecological risk has tended to focus on beneficial macroorganisms such as pollinators, with less attention paid to microorganisms. Here, using culture-independent methods, we assess the impact of two widely-used fungicides on nectar microbial community structure in the mass-flowering crop almond (Prunus dulcis). We predicted that fungicide application would reduce fungal richness and diversity, whereas competing bacterial richness would increase, benefitting from negative effects on fungi. We found that fungicides reduced fungal richness and diversity in exposed flowers, but did not significantly affect bacterial richness, diversity, or community composition. The relative abundance of Metschnikowia OTUs, nectar specialists that can impact pollination, was reduced by both fungicides. Given growing recognition of the importance of nectar microorganisms as mediators of plant-pollinator mutualisms, future research should consider the impact of management practices on plant-associated microorganisms and consequences for pollination services in agricultural landscapes.

  View details for DOI 10.1111/1758-2229.12501

  View details for Web of Science ID 000397493300003

• Precipitation alters the strength of evolutionary priority effects in forest community assembly of pteridophytes and angiosperms JOURNAL OF ECOLOGY Brandt, A. J., Tanentzap, A. J., Leopold, D. R., Heenan, P. B., Fukami, T., Lee, W. G. 2016; 104 (6): 1673-1681

  View details for DOI 10.1111/1365-2745.12640

  View details for Web of Science ID 000385915200016

• Genetic basis of priority effects: insights from nectar yeast. Proceedings. Biological sciences Dhami, M. K., Hartwig, T., Fukami, T. 2016; 283 (1840): -?

  Abstract

  Priority effects, in which the order of species arrival dictates community assembly, can have a major influence on species diversity, but the genetic basis of priority effects remains unknown. Here, we suggest that nitrogen scavenging genes previously considered responsible for starvation avoidance may drive priority effects by causing rapid resource depletion. Using single-molecule sequencing, we de novo assembled the genome of the nectar-colonizing yeast, Metschnikowia reukaufii, across eight scaffolds and complete mitochondrion, with gap-free coverage over gene spaces. We found a high rate of tandem gene duplication in this genome, enriched for nitrogen metabolism and transport. Both high-capacity amino acid importers, GAP1 and PUT4, present as tandem gene arrays, were highly expressed in synthetic nectar and regulated by the availability and quality of amino acids. In experiments with competitive nectar yeast, Candida rancensis, amino acid addition alleviated suppression of C. rancensis by early arrival of M. reukaufii, corroborating that amino acid scavenging may contribute to priority effects. Because niche pre-emption via rapid resource depletion may underlie priority effects in a broad range of microbial, plant and animal communities, nutrient scavenging genes like the ones we considered here may be broadly relevant to understanding priority effects.

  View details for PubMedID 27708148

• Genetic basis of priority effects: insights from nectar yeast PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES Dhami, M. K., Hartwig, T., Fukami, T. 2016; 283 (1840)

  View details for DOI 10.1098/rspb.2016.1455

  View details for Web of Science ID 000386490000009

• Nonlinear, interacting responses to climate limit grassland production under global change PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Zhu, K., Chiariello, N. R., Tobeck, T., Fukami, T., Field, C. B. 2016; 113 (38): 10589-10594

  Abstract

  Global changes in climate, atmospheric composition, and pollutants are altering ecosystems and the goods and services they provide. Among approaches for predicting ecosystem responses, long-term observations and manipulative experiments can be powerful approaches for resolving single-factor and interactive effects of global changes on key metrics such as net primary production (NPP). Here we combine both approaches, developing multidimensional response surfaces for NPP based on the longest-running, best-replicated, most-multifactor global-change experiment at the ecosystem scale-a 17-y study of California grassland exposed to full-factorial warming, added precipitation, elevated CO2, and nitrogen deposition. Single-factor and interactive effects were not time-dependent, enabling us to analyze each year as a separate realization of the experiment and extract NPP as a continuous function of global-change factors. We found a ridge-shaped response surface in which NPP is humped (unimodal) in response to temperature and precipitation when CO2 and nitrogen are ambient, with peak NPP rising under elevated CO2 or nitrogen but also shifting to lower temperatures. Our results suggest that future climate change will push this ecosystem away from conditions that maximize NPP, but with large year-to-year variability.

  View details for DOI 10.1073/pnas.1606734113

  View details for PubMedID 27601643

• Forest area and connectivity influence root-associated fungal communities in a fragmented landscape ECOLOGY Vannette, R. L., Leopold, D. R., Fukami, T. 2016; 97 (9): 2374-2383

  Abstract

  Habitat fragmentation is well known to affect plant and animal diversity as a result of reduced habitat area and connectivity, but its effects on microorganisms are poorly understood. Using high-throughput sequencing of two regions of the rRNA gene, we studied the effects of forest area and connectivity on the diversity and composition of fungi associated with the roots of the dominant tree, Metrosideros polymorpha, in a lava-fragmented landscape on the Island of Hawaii. We found that local fungal diversity increased with forest area, whereas fungal species composition was correlated with fragment connectivity. Fragment size and connectivity were significant predictors even when we included environmental covariates, which were also associated with fungal diversity and composition. Fungal species composition was more similar among highly connected fragments than among poorly connected ones. We also identified individual taxa that varied in abundance with connectivity. Taken together, our results show that habitat fragmentation can alter microbial diversity and composition via differential response among fungal phyla and individual taxa to habitat connectivity.

  View details for DOI 10.1002/ecy.1472

  View details for Web of Science ID 000382527100021

• Forest area and connectivity influence root-associated fungal communities in a fragmented landscape. Ecology Vannette, R. L., Leopold, D. R., Fukami, T. 2016; 97 (9): 2374-2383

  Abstract

  Habitat fragmentation is well known to affect plant and animal diversity as a result of reduced habitat area and connectivity, but its effects on microorganisms are poorly understood. Using high-throughput sequencing of two regions of the rRNA gene, we studied the effects of forest area and connectivity on the diversity and composition of fungi associated with the roots of the dominant tree, Metrosideros polymorpha, in a lava-fragmented landscape on the Island of Hawaii. We found that local fungal diversity increased with forest area, whereas fungal species composition was correlated with fragment connectivity. Fragment size and connectivity were significant predictors even when we included environmental covariates, which were also associated with fungal diversity and composition. Fungal species composition was more similar among highly connected fragments than among poorly connected ones. We also identified individual taxa that varied in abundance with connectivity. Taken together, our results show that habitat fragmentation can alter microbial diversity and composition via differential response among fungal phyla and individual taxa to habitat connectivity.

  View details for DOI 10.1002/ecy.1472

  View details for PubMedID 27859069

• Convergence and divergence in a long-term old-field succession: the importance of spatial scale and species abundance ECOLOGY LETTERS Li, S., Cadotte, M. W., Meiners, S. J., Pu, Z., Fukami, T., Jiang, L. 2016; 19 (9): 1101-1109

  Abstract

  Whether plant communities in a given region converge towards a particular stable state during succession has long been debated, but rarely tested at a sufficiently long time scale. By analysing a 50-year continuous study of post-agricultural secondary succession in New Jersey, USA, we show that the extent of community convergence varies with the spatial scale and species abundance classes. At the larger field scale, abundance-based dissimilarities among communities decreased over time, indicating convergence of dominant species, whereas incidence-based dissimilarities showed little temporal tend, indicating no sign of convergence. In contrast, plots within each field diverged in both species composition and abundance. Abundance-based successional rates decreased over time, whereas rare species and herbaceous plants showed little change in temporal turnover rates. Initial abandonment conditions only influenced community structure early in succession. Overall, our findings provide strong evidence for scale and abundance dependence of stochastic and deterministic processes over old-field succession.

  View details for DOI 10.1111/ele.12647

  View details for PubMedID 27373449

• Hierarchical neighbor effects on mycorrhizal community structure and function. Ecology and evolution Moeller, H. V., Dickie, I. A., Peltzer, D. A., Fukami, T. 2016; 6 (15): 5416-5430

  Abstract

  Theory predicts that neighboring communities can shape one another's composition and function, for example, through the exchange of member species. However, empirical tests of the directionality and strength of these effects are rare. We determined the effects of neighboring communities on one another through experimental manipulation of a plant-fungal model system. We first established distinct ectomycorrhizal fungal communities on Douglas-fir seedlings that were initially grown in three soil environments. We then transplanted seedlings and mycorrhizal communities in a fully factorial experiment designed to quantify the direction and strength of neighbor effects by focusing on changes in fungal community species composition and implications for seedling growth (a proxy for community function). We found that neighbor effects on the composition and function of adjacent communities follow a dominance hierarchy. Specifically, mycorrhizal communities established from soils collected in Douglas-fir plantations were both the least sensitive to neighbor effects, and exerted the strongest influence on their neighbors by driving convergence in neighbor community composition and increasing neighbor seedling vigor. These results demonstrate that asymmetric neighbor effects mediated by ecological history can determine both community composition and function.

  View details for DOI 10.1002/ece3.2299

  View details for PubMedID 27551393

• A framework for priority effects JOURNAL OF VEGETATION SCIENCE Fukami, T., Mordecai, E. A., Ostling, A. 2016; 27 (4): 655–57

  View details for DOI 10.1111/jvs.12434

  View details for Web of Science ID 000379038500001

• Nectar microbes can reduce secondary metabolites in nectar and alter effects on nectar consumption by pollinators ECOLOGY Vannette, R. L., Fukami, T. 2016; 97 (6): 1410-1419

  Abstract

  Secondary metabolites that are present in floral nectar have been hypothesized to enhance specificity in plant-pollinator mutualism by reducing larceny by non-pollinators, including microorganisms that colonize nectar. However, few studies have tested this hypothesis. Using synthetic nectar, we conducted laboratory and field experiments to examine the effects of five chemical compounds found in nectar on the growth and metabolism of nectar-colonizing yeasts and bacteria, and the interactive effects of these compounds and nectar microbes on the consumption of nectar by pollinators. In most cases, focal compounds inhibited microbial growth, but the extent of these effects depended on compound identity, concentration, and microbial species. Moreover, most compounds did not substantially decrease sugar metabolism by microbes, and microbes reduced the concentration of some compounds in nectar. Using artificial flowers in the field, we also found that the common nectar yeast Metschnikowia reukaufii altered nectar consumption by small floral visitors, but only in nectar containing catalpol. This effect was likely mediated by a mechanism independent of catalpol metabolism. Despite strong compound-specific effects on microbial growth, our results suggest that the secondary metabolites tested here are unlikely to be an effective general defense mechanism for preserving nectar sugars for pollinators. Instead, our results indicate that microbial colonization of nectar could reduce the concentration of secondary compounds in nectar and, in some cases, reduce deterrence to pollinators.

  View details for DOI 10.1890/15-0858.1

  View details for Web of Science ID 000377219900005

  View details for PubMedID 27459772

• Plant and root endophyte assembly history: interactive effects on native and exotic plants ECOLOGY Sikes, B. A., Hawkes, C. V., Fukami, T. 2016; 97 (2): 484-493

  Abstract

  Differences in the arrival timing of plants and soil biota may result in different plant communities through priority effects, potentially affecting the success of native vs. exotic plants, but experimental evidence is largely lacking. We conducted a greenhouse experiment to investigate whether the assembly history of plants and fungal root endophytes could interact to influence plant emergence and biomass. We introduced a grass species and eight fungal species from one of three land-use types (undisturbed, disturbed, or pasture sites in a Florida scrubland) in factorial combinations. We then introduced all plants and fungi from the other land-use types 2 weeks later. Plant emergence was monitored for 6 months, and final plant biomass and fungal species composition assessed. The emergence and growth of the exotic Melinis repens and the native Schizacharyium niveum were affected negatively when introduced early with their "home" fungi, but early introduction of a different plant species or fungi from a different site type eliminated these negative effects, providing evidence for interactive priority effects. Interactive effects of plant and fungal arrival history may be an overlooked determinant of plant community structure and may provide an effective management tool to inhibit biological invasion and aid ecosystem restoration.

  View details for DOI 10.1890/15-0635.1

  View details for Web of Science ID 000371439800020

• Florivory and pollinator visitation: a cautionary tale. AoB PLANTS Tsuji, K., Dhami, M. K., Cross, D. J., Rice, C. P., Romano, N. H., Fukami, T. 2016; 8

  Abstract

  Florivory, or damage to flowers by herbivores, can make flowers less attractive to pollinators, potentially resulting in reduced plant fitness. However, not many studies have combined observations with experiments to assess the causal link between florivory and pollination. We conducted field observations at eight sites in northern California, combined with field experiments that involved artificial floral damage, to study the effect of florivory on pollination in the hummingbird-pollinated sticky monkeyflower, Mimulus aurantiacus We used two indicators of pollinator visitation, stigma closure and the presence of microorganisms in floral nectar. The field observations revealed that stigma closure was less frequent in damaged flowers than in intact flowers. In the experiments, however, floral damage did not decrease stigma closure or microbial detection in nectar. Instead, neighbouring flowers were similar for both indicators. These results suggest that the observed negative association between florivory and pollination is not causal and that the location of flowers is more important to pollinator visitation than florivory in these populations of M. aurantiacus.

  View details for DOI 10.1093/aobpla/plw036

  View details for PubMedID 27178063

• Mycorrhizal co-invasion and novel interactions depend on neighborhood context ECOLOGY Moeller, H. V., Dickie, I. A., Peltzer, D. A., Fukami, T. 2015; 96 (9): 2336-2347

  Abstract

  Biological invasions are a rapidly increasing driver of global change, yet fundamental gaps remain in our understanding of the factors determining the success or extent of invasions. For example, although most woody plant species depend on belowground mutualists such as mycorrhizal fungi and nitrogen-fixing bacteria, the relative importance of these mutualisms in conferring invasion success is unresolved. Here, we describe how neighborhood context (identity of nearby tree species) affects the formation of belowground ectomycorrhizal partnerships between fungi and seedlings of a widespread invasive tree species, Pseudotsuga menziesii (Douglas-fir), in New Zealand. We found that the formation of mycorrhizal partnerships, the composition of the fungal species involved in these partnerships, and the origin of the fungi (co-invading or native to New Zealand) all depend on neighborhood context. Our data suggest that nearby ectomycorrhizal host trees act as both a reservoir of fungal inoculum and a carbon source for late-successional and native fungi. By facilitating mycorrhization of P. menziesii seedlings, adult trees may alleviate mycorrhizal limitation at the P. menziesii invasion front. These results highlight the importance of studying biological invasions across multiple ecological settings to understand establishment success and invasion speed.

  View details for Web of Science ID 000361152100003

• When do plant radiations influence community assembly? The importance of historical contingency in the race for niche space NEW PHYTOLOGIST Tanentzap, A. J., Brandt, A. J., Smissen, R. D., Heenan, P. B., Fukami, T., Lee, W. G. 2015; 207 (2): 468-479

  Abstract

  Plant radiations are widespread but their influence on community assembly has rarely been investigated. Theory and some evidence suggest that radiations can allow lineages to monopolize niche space when founding species arrive early into new bioclimatic regions and exploit ecological opportunities. These early radiations may subsequently reduce niche availability and dampen diversification of later arrivals. We tested this hypothesis of time-dependent lineage diversification and community dominance using the alpine flora of New Zealand. We estimated ages of 16 genera from published phylogenies and determined their relative occurrence across climatic and physical gradients in the alpine zone. We used these data to reconstruct occupancy of environmental space through time, integrating palaeoclimatic and palaeogeological changes. Our analysis suggested that earlier-colonizing lineages encountered a greater availability of environmental space, which promoted greater species diversity and occupancy of niche space. Genera that occupied broader niches were subsequently more dominant in local communities. An earlier time of arrival also contributed to greater diversity independently of its influence in accessing niche space. We suggest that plant radiations influence community assembly when they arise early in the occupancy of environmental space, allowing them to exclude later-arriving colonists from ecological communities by niche preemption.

  View details for DOI 10.1111/nph.13362

  View details for PubMedID 25771829

• Evolutionary priority effects in New Zealand alpine plants across environmental gradients JOURNAL OF BIOGEOGRAPHY Leopold, D. R., Tanentzap, A. J., Lee, W. G., Heenan, P. B., Fukami, T. 2015; 42 (4): 729-737

  View details for DOI 10.1111/jbi.12441

  View details for Web of Science ID 000350910100012

• Complex organism-environment feedbacks buffer species diversity against habitat fragmentation ECOGRAPHY Zee, P. C., Fukami, T. 2015; 38 (4): 370-379

  View details for DOI 10.1111/ecog.01027

  View details for Web of Science ID 000352626400005

• Historical Contingency in Community Assembly: Integrating Niches, Species Pools, and Priority Effects ANNUAL REVIEW OF ECOLOGY, EVOLUTION, AND SYSTEMATICS, VOL 46 Fukami, T. 2015; 46: 1-23

  View details for DOI 10.1146/annurev-ecolsys-110411-160340

  View details for Web of Science ID 000367292700001

• Temporal variation in fungal communities associated with tropical hummingbirds and nectarivorous bats FUNGAL ECOLOGY Belisle, M., Mendenhall, C. D., Brenes, F. O., Fukami, T. 2014; 12: 44-51

  View details for DOI 10.1016/j.funeco.2014.02.007

  View details for Web of Science ID 000346461200007

• Rapid evolution of adaptive niche construction in experimental microbial populations EVOLUTION Callahan, B. J., Fukami, T., Fisher, D. S. 2014; 68 (11): 3307-3316

  Abstract

  Many species engage in adaptive niche construction: modification of the local environment that increases the modifying organism's competitive fitness. Adaptive niche construction provides an alternative pathway to higher fitness, shaping the environment rather than conforming to it. Yet, experimental evidence for the evolutionary emergence of adaptive niche construction is lacking, leaving its role in evolution uncertain. Here we report a direct observation of the de novo evolution of adaptive niche construction in populations of the bacteria Pseudomonas fluorescens. In a laboratory experiment, we allowed several bacterial populations to adapt to a novel environment and assessed whether niche construction evolved over time. We found that adaptive niche construction emerged rapidly, within approximately 100 generations, and became ubiquitous after approximately 400 generations. The large fitness effect of this niche construction was dominated by the low fitness of evolved strains in the ancestrally modified environment: evolved niche constructors were highly dependent on their specific environmental modifications. Populations were subjected to frequent resetting of environmental conditions and severe reduction of spatial habitat structure, both of which are thought to make adaptive niche construction difficult to evolve. Our finding that adaptive niche construction nevertheless evolved repeatably suggests that it may play a more important role in evolution than generally thought.

  View details for DOI 10.1111/evo.12512

  View details for Web of Science ID 000344379800018

• Rapid evolution of adaptive niche construction in experimental microbial populations. Evolution; international journal of organic evolution Callahan, B. J., Fukami, T., Fisher, D. S. 2014; 68 (11): 3307-3316

  Abstract

  Many species engage in adaptive niche construction: modification of the local environment that increases the modifying organism's competitive fitness. Adaptive niche construction provides an alternative pathway to higher fitness, shaping the environment rather than conforming to it. Yet, experimental evidence for the evolutionary emergence of adaptive niche construction is lacking, leaving its role in evolution uncertain. Here we report a direct observation of the de novo evolution of adaptive niche construction in populations of the bacteria Pseudomonas fluorescens. In a laboratory experiment, we allowed several bacterial populations to adapt to a novel environment and assessed whether niche construction evolved over time. We found that adaptive niche construction emerged rapidly, within approximately 100 generations, and became ubiquitous after approximately 400 generations. The large fitness effect of this niche construction was dominated by the low fitness of evolved strains in the ancestrally modified environment: evolved niche constructors were highly dependent on their specific environmental modifications. Populations were subjected to frequent resetting of environmental conditions and severe reduction of spatial habitat structure, both of which are thought to make adaptive niche construction difficult to evolve. Our finding that adaptive niche construction nevertheless evolved repeatably suggests that it may play a more important role in evolution than generally thought.

  View details for DOI 10.1111/evo.12512

  View details for PubMedID 25138718

• Environmental variability counteracts priority effects to facilitate species coexistence: evidence from nectar microbes. Proceedings. Biological sciences / The Royal Society Tucker, C. M., Fukami, T. 2014; 281 (1778): 20132637-?

  Abstract

  The order of species arrival during community assembly can greatly affect species coexistence, but the strength of these effects, known as priority effects, appears highly variable across species and ecosystems. Furthermore, the causes of this variation remain unclear despite their fundamental importance in understanding species coexistence. Here, we show that one potential cause is environmental variability. In laboratory experiments using nectar-inhabiting microorganisms as a model system, we manipulated spatial and temporal variability of temperature, and examined consequences for priority effects. If species arrived sequentially, multiple species coexisted under variable temperature, but not under constant temperature. Temperature variability prevented extinction of late-arriving species that would have been excluded owing to priority effects if temperature had been constant. By contrast, if species arrived simultaneously, species coexisted under both variable and constant temperatures. We propose possible mechanisms underlying these results using a mathematical model that incorporates contrasting effects of microbial species on nectar pH and amino acids. Overall, our findings suggest that understanding consequences of priority effects for species coexistence requires explicit consideration of environmental variability.

  View details for DOI 10.1098/rspb.2013.2637

  View details for PubMedID 24430846

• Ectomycorrhizal fungal traits reflect environmental conditions along a coastal California edaphic gradient. FEMS microbiology ecology Moeller, H. V., Peay, K. G., Fukami, T. 2014; 87 (3): 797-806

  Abstract

  Multispecies mutualisms, such as the association between trees and ectomycorrhizal fungi, are often shaped by environmental context. Here, we explored the functional mechanisms underlying this environmental filtering. Using a single population of Pinus muricata (Bishop pine) growing along a strong edaphic gradient, we examined how environmental stress affected ectomycorrhizal fungi. The gradient spans c. 400000 years of soil age, and reduced nutrient availability and increased water stress dwarf trees on older sites. Fungal community composition shifted with nutrient and water availability and with the stature of the P. muricata host trees. Not only did pygmy trees host a taxonomically different fungal subset as compared to nonpygmy trees, but associated fungal communities also differed in life history strategies: trees in more stressful conditions hosted fungi with more carbon-intensive foraging strategies. Our results indicate a link between environmental controls of host nutritional status and turnover in the ectomycorrhizal fungal community. The transition to more energy-intensive strategies under nutrient stress may allow for close recycling of recalcitrant nutrient pools within the root zone and facilitate transport of nutrients and water over long distances. These results highlight the value of life history data to understanding the mechanistic underpinnings of species distributions.

  View details for DOI 10.1111/1574-6941.12265

  View details for PubMedID 24289145

• Non-Native Plants Disrupt Dual Promotion of Native Alpha and Beta Diversity (vol 48, pg 319, 2013) FOLIA GEOBOTANICA Fukami, T., Bellingham, P. J., Peltzer, D. A., Walker, L. R. 2014; 49 (1): 113–15

  View details for DOI 10.1007/s12224-014-9189-1

  View details for Web of Science ID 000334419400007

• Honey bees avoid nectar colonized by three bacterial species, but not by a yeast species, isolated from the bee gut. PloS one Good, A. P., Gauthier, M. L., Vannette, R. L., Fukami, T. 2014; 9 (1)

  View details for DOI 10.1371/journal.pone.0086494

  View details for PubMedID 24466119

• Historical contingency in species interactions: towards niche-based predictions ECOLOGY LETTERS Vannette, R. L., Fukami, T. 2014; 17 (1): 115-124

  Abstract

  The way species affect one another in ecological communities often depends on the order of species arrival. The magnitude of such historical contingency, known as priority effects, varies across species and environments, but this variation has proven difficult to predict, presenting a major challenge in understanding species interactions and consequences for community structure and function. Here, we argue that improved predictions can be achieved by decomposing species' niches into three components: overlap, impact and requirement. Based on classic theories of community assembly, three hypotheses that emphasise related, but distinct influences of the niche components are proposed: priority effects are stronger among species with higher resource use overlap; species that impact the environment to a greater extent exert stronger priority effects; and species whose growth rate is more sensitive to changes in the environment experience stronger priority effects. Using nectar-inhabiting microorganisms as a model system, we present evidence that these hypotheses complement the conventional hypothesis that focuses on the role of environmental harshness, and show that niches can be twice as predictive when separated into components. Taken together, our hypotheses provide a basis for developing a general framework within which the magnitude of historical contingency in species interactions can be predicted.

  View details for DOI 10.1111/ele.12204

  View details for PubMedID 24341984

• Honey bees avoid nectar colonized by three bacterial species, but not by a yeast species, isolated from the bee gut. PloS one Good, A. P., Gauthier, M. L., Vannette, R. L., Fukami, T. 2014; 9 (1)

  Abstract

  The gut microflora of the honey bee, Apis mellifera, is receiving increasing attention as a potential determinant of the bees' health and their efficacy as pollinators. Studies have focused primarily on the microbial taxa that appear numerically dominant in the bee gut, with the assumption that the dominant status suggests their potential importance to the bees' health. However, numerically minor taxa might also influence the bees' efficacy as pollinators, particularly if they are not only present in the gut, but also capable of growing in floral nectar and altering its chemical properties. Nonetheless, it is not well understood whether honey bees have any feeding preference for or against nectar colonized by specific microbial species. To test whether bees exhibit a preference, we conducted a series of field experiments at an apiary using synthetic nectar inoculated with specific species of bacteria or yeast that had been isolated from the bee gut, but are considered minor components of the gut microflora. These species had also been found in floral nectar. Our results indicated that honey bees avoided nectar colonized by the bacteria Asaia astilbes, Erwinia tasmaniensis, and Lactobacillus kunkeei, whereas the yeast Metschnikowia reukaufii did not affect the feeding preference of the insects. Our results also indicated that avoidance of bacteria-colonized nectar was caused not by the presence of the bacteria per se, but by the chemical changes to nectar made by the bacteria. These findings suggest that gut microbes may not only affect the bees' health as symbionts, but that some of the microbes may possibly affect the efficacy of A. mellifera as pollinators by altering nectar chemistry and influencing their foraging behavior.

  View details for DOI 10.1371/journal.pone.0086494

  View details for PubMedID 24466119

• Sustaining ecosystem functions in a changing world: a call for an integrated approach JOURNAL OF APPLIED ECOLOGY Tomimatsu, H., Sasaki, T., Kurokawa, H., Bridle, J. R., Fontaine, C., Kitano, J., Stouffer, D. B., Vellend, M., Bezemer, T., Fukami, T., Hadly, E. A., van der Heijden, M. A., Kawata, M., Kefi, S., Kraft, N. B., McCann, K. S., Mumby, P. J., Nakashizuka, T., Petchey, O. L., Romanuk, T. N., Suding, K. N., Takimoto, G., Urabe, J., Yachi, S. 2013; 50 (5): 1124–30

  View details for DOI 10.1111/1365-2664.12116

  View details for Web of Science ID 000325079800005

• Non-Native Plants Disrupt Dual Promotion of Native Alpha and Beta Diversity FOLIA GEOBOTANICA Fukami, T., Bellingham, P. J., Peltzer, D. A., Walker, L. R. 2013; 48 (3): 319-333

  View details for DOI 10.1007/s12224-013-9175-z

  View details for Web of Science ID 000325816600003

• Patterns and Processes of Microbial Community Assembly MICROBIOLOGY AND MOLECULAR BIOLOGY REVIEWS Nemergut, D. R., Schmidt, S. K., Fukami, T., O'Neill, S. P., Bilinski, T. M., Stanish, L. F., Knelman, J. E., Darcy, J. L., Lynch, R. C., Wickey, P., Ferrenberg, S. 2013; 77 (3): 342-356

  Abstract

  Recent research has expanded our understanding of microbial community assembly. However, the field of community ecology is inaccessible to many microbial ecologists because of inconsistent and often confusing terminology as well as unnecessarily polarizing debates. Thus, we review recent literature on microbial community assembly, using the framework of Vellend (Q. Rev. Biol. 85:183-206, 2010) in an effort to synthesize and unify these contributions. We begin by discussing patterns in microbial biogeography and then describe four basic processes (diversification, dispersal, selection, and drift) that contribute to community assembly. We also discuss different combinations of these processes and where and when they may be most important for shaping microbial communities. The spatial and temporal scales of microbial community assembly are also discussed in relation to assembly processes. Throughout this review paper, we highlight differences between microbes and macroorganisms and generate hypotheses describing how these differences may be important for community assembly. We end by discussing the implications of microbial assembly processes for ecosystem function and biodiversity.

  View details for DOI 10.1128/MMBR.00051-12

  View details for Web of Science ID 000324164400002

  View details for PubMedID 24006468

• IBI* series winner. Integrating inquiry-based teaching with faculty research. Science Fukami, T. 2013; 339 (6127): 1536-1537

  View details for DOI 10.1126/science.1229850

  View details for PubMedID 23539590

• Plant-soil feedbacks: the past, the present and future challenges JOURNAL OF ECOLOGY van der Putten, W. H., Bardgett, R. D., Bever, J. D., Bezemer, T. M., Casper, B. B., Fukami, T., Kardol, P., Klironomos, J. N., Kulmatiski, A., Schweitzer, J. A., Suding, K. N., van de Voorde, T. F., Wardle, D. A. 2013; 101 (2): 265-276

  View details for DOI 10.1111/1365-2745.12054

  View details for Web of Science ID 000317923300001

• Consequences of plant-soil feedbacks in invasion JOURNAL OF ECOLOGY Suding, K. N., Harpole, W. S., Fukami, T., Kulmatiski, A., MacDougall, A. S., Stein, C., van der Putten, W. H. 2013; 101 (2): 298-308

  View details for DOI 10.1111/1365-2745.12057

  View details for Web of Science ID 000317923300004

• Complex plant-soil interactions enhance plant species diversity by delaying community convergence JOURNAL OF ECOLOGY Fukami, T., Nakajima, M. 2013; 101 (2): 316-324

  View details for DOI 10.1111/1365-2745.12048

  View details for Web of Science ID 000317923300006

• Animals in a bacterial world, a new imperative for the life sciences PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA McFall-Ngai, M., Hadfield, M. G., Bosch, T. C., Carey, H. V., Domazet-Loso, T., Douglas, A. E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S. F., Hentschel, U., King, N., Kjelleberg, S., Knoll, A. H., Kremer, N., Mazmanian, S. K., Metcalf, J. L., Nealson, K., Pierce, N. E., Rawls, J. F., Reid, A., Ruby, E. G., Rumpho, M., Sanders, J. G., Tautz, D., Wernegreen, J. J. 2013; 110 (9): 3229-3236

  Abstract

  In the last two decades, the widespread application of genetic and genomic approaches has revealed a bacterial world astonishing in its ubiquity and diversity. This review examines how a growing knowledge of the vast range of animal-bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of animal biology. Specifically, we highlight recent technological and intellectual advances that have changed our thinking about five questions: how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other's genomes; how does normal animal development depend on bacterial partners; how is homeostasis maintained between animals and their symbionts; and how can ecological approaches deepen our understanding of the multiple levels of animal-bacterial interaction. As answers to these fundamental questions emerge, all biologists will be challenged to broaden their appreciation of these interactions and to include investigations of the relationships between and among bacteria and their animal partners as we seek a better understanding of the natural world.

  View details for DOI 10.1073/pnas.1218525110

  View details for Web of Science ID 000315841900016

  View details for PubMedID 23391737

  View details for PubMedCentralID PMC3587249

• Nectar bacteria, but not yeast, weaken a plant-pollinator mutualism. Proceedings. Biological sciences / The Royal Society Vannette, R. L., Gauthier, M. L., Fukami, T. 2013; 280 (1752): 20122601-?

  Abstract

  Mutualistic interactions are often subject to exploitation by species that are not directly involved in the mutualism. Understanding which organisms act as such 'third-party' species and how they do so is a major challenge in the current study of mutualistic interactions. Here, we show that even species that appear ecologically similar can have contrasting effects as third-party species. We experimentally compared the effects of nectar-inhabiting bacteria and yeasts on the strength of a mutualism between a hummingbird-pollinated shrub, Mimulus aurantiacus, and its pollinators. We found that the common bacterium Gluconobacter sp., but not the common yeast Metschnikowia reukaufii, reduced pollination success, seed set and nectar consumption by pollinators, thereby weakening the plant-pollinator mutualism. We also found that the bacteria reduced nectar pH and total sugar concentration more greatly than the yeasts did and that the bacteria decreased glucose concentration and increased fructose concentration whereas the yeasts affected neither. These distinct changes to nectar chemistry may underlie the microbes' contrasting effects on the mutualism. Our results suggest that it is necessary to understand the determinants of microbial species composition in nectar and their differential modification of floral rewards to explain the mutual benefits that plants and pollinators gain from each other.

  View details for DOI 10.1098/rspb.2012.2601

  View details for PubMedID 23222453

• Nectar bacteria, but not yeast, weaken a plant - pollinator mutualism PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES Vannette, R. L., Gauthier, M. L., Fukami, T. 2013; 280 (1752)

  Abstract

  Mutualistic interactions are often subject to exploitation by species that are not directly involved in the mutualism. Understanding which organisms act as such 'third-party' species and how they do so is a major challenge in the current study of mutualistic interactions. Here, we show that even species that appear ecologically similar can have contrasting effects as third-party species. We experimentally compared the effects of nectar-inhabiting bacteria and yeasts on the strength of a mutualism between a hummingbird-pollinated shrub, Mimulus aurantiacus, and its pollinators. We found that the common bacterium Gluconobacter sp., but not the common yeast Metschnikowia reukaufii, reduced pollination success, seed set and nectar consumption by pollinators, thereby weakening the plant-pollinator mutualism. We also found that the bacteria reduced nectar pH and total sugar concentration more greatly than the yeasts did and that the bacteria decreased glucose concentration and increased fructose concentration whereas the yeasts affected neither. These distinct changes to nectar chemistry may underlie the microbes' contrasting effects on the mutualism. Our results suggest that it is necessary to understand the determinants of microbial species composition in nectar and their differential modification of floral rewards to explain the mutual benefits that plants and pollinators gain from each other.

  View details for DOI 10.1098/rspb.2012.2601

  View details for Web of Science ID 000312591600020

  View details for PubMedID 23222453

  View details for PubMedCentralID PMC3574316

• Rat invasion of islands alters fungal community structure, but not wood decomposition rates OIKOS Peay, K. G., Dickie, I. A., Wardle, D. A., Bellingham, P. J., Fukami, T. 2013; 122 (2): 258-264

  View details for DOI 10.1111/j.1600-0706.2012.20813.x

  View details for Web of Science ID 000313748900011

• Context matters: volunteer bias, small sample size, and the value of comparison groups in the assessment of research-based undergraduate introductory biology lab courses. Journal of microbiology & biology education : JMBE Brownell, S. E., Kloser, M. J., Fukami, T., Shavelson, R. J. 2013; 14 (2): 176-182

  Abstract

  The shift from cookbook to authentic research-based lab courses in undergraduate biology necessitates the need for evaluation and assessment of these novel courses. Although the biology education community has made progress in this area, it is important that we interpret the effectiveness of these courses with caution and remain mindful of inherent limitations to our study designs that may impact internal and external validity. The specific context of a research study can have a dramatic impact on the conclusions. We present a case study of our own three-year investigation of the impact of a research-based introductory lab course, highlighting how volunteer students, a lack of a comparison group, and small sample sizes can be limitations of a study design that can affect the interpretation of the effectiveness of a course.

  View details for DOI 10.1128/jmbe.v14i2.609

  View details for PubMedID 24358380

• Soil-mediated indirect impacts of an invasive predator on plant growth BIOLOGY LETTERS Wardle, D. A., Bellingham, P. J., Fukami, T., Bonner, K. I. 2012; 8 (4): 574-577

  Abstract

  While several studies have shown that invasive plant effects on soil biota influence subsequent plant performance, corresponding studies on how invasive animals affect plants through influencing soil biota are lacking. This is despite the fact that invasive animals often indirectly alter the below-ground subsystem. We studied 18 offshore islands in northern New Zealand, half of which have been invaded by rats that are predators of seabirds and severely reduce their densities, and half of which remain non-invaded; invasion of rats thwarts seabird transfer of resources from ocean to land. We used soil from each island in a glasshouse experiment involving soil sterilization treatments to determine whether rat invasion indirectly influences plant growth through the abiotic pathway (by impairing seabird-driven inputs to soil) or the biotic pathway (by altering the soil community). Rat invasion greatly impaired plant growth but entirely through the abiotic pathway. Plant growth was unaffected by the soil community or its response to invasion, meaning that the responses of plants and soil biota to invasion are decoupled. Our results provide experimental evidence for the powerful indirect effects that predator-instigated cascades can exert on plant and ecosystem productivity, with implications for the restoration of island ecosystems by predator removal.

  View details for DOI 10.1098/rsbl.2012.0201

  View details for Web of Science ID 000306361700027

  View details for PubMedID 22496079

  View details for PubMedCentralID PMC3391483

• Area and the rapid radiation of Hawaiian Bidens (Asteraceae) JOURNAL OF BIOGEOGRAPHY Knope, M. L., Morden, C. W., Funk, V. A., Fukami, T. 2012; 39 (7): 1206-1216

  View details for DOI 10.1111/j.1365-2699.2012.02687.x

  View details for Web of Science ID 000305452500002

• Flowers as Islands: Spatial Distribution of Nectar-Inhabiting Microfungi among Plants of Mimulus aurantiacus, a Hummingbird-Pollinated Shrub MICROBIAL ECOLOGY Belisle, M., Peay, K. G., Fukami, T. 2012; 63 (4): 711-718

  Abstract

  Microfungi that inhabit floral nectar offer unique opportunities for the study of microbial distribution and the role that dispersal limitation may play in generating distribution patterns. Flowers are well-replicated habitat islands, among which the microbes disperse via pollinators. This metapopulation system allows for investigation of microbial distribution at multiple spatial scales. We examined the distribution of the yeast, Metschnikowia reukaufii, and other fungal species found in the floral nectar of the sticky monkey flower, Mimulus aurantiacus, a hummingbird-pollinated shrub, at a California site. We found that the frequency of nectar-inhabiting microfungi on a given host plant was not significantly correlated with light availability, nectar volume, or the percent cover of M. aurantiacus around the plant, but was significantly correlated with the location of the host plant and loosely correlated with the density of flowers on the plant. These results suggest that dispersal limitation caused by spatially nonrandom foraging by pollinators may be a primary factor driving the observed distribution pattern.

  View details for DOI 10.1007/s00248-011-9975-8

  View details for PubMedID 22080257

• Introduced Canopy Tree Species Effect on the Soil Microbial Community in a Montane Tropical Forest PACIFIC SCIENCE Lynch, H. B., Epps, K. Y., Fukami, T., Vitousek, P. M. 2012; 66 (2): 141-150

  View details for DOI 10.2984/66.2.4

  View details for Web of Science ID 000303625400004

• Phylogenetic relatedness predicts priority effects in nectar yeast communities PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES Peay, K. G., Belisle, M., Fukami, T. 2012; 279 (1729): 749-758

  Abstract

  Priority effects, in which the outcome of species interactions depends on the order of their arrival, are a key component of many models of community assembly. Yet, much remains unknown about how priority effects vary in strength among species in a community and what factors explain this variation. We experimented with a model natural community in laboratory microcosms that allowed us to quantify the strength of priority effects for most of the yeast species found in the floral nectar of a hummingbird-pollinated shrub at a biological preserve in northern California. We found that priority effects were widespread, with late-arriving species experiencing strong negative effects from early-arriving species. However, the magnitude of priority effects varied across species pairs. This variation was phylogenetically non-random, with priority effects stronger between closer relatives. Analysis of carbon and amino acid consumption profiles indicated that competition between closer relatives was more intense owing to higher ecological similarity, consistent with Darwin's naturalization hypothesis. These results suggest that phylogenetic relatedness between potential colonists may explain the strength of priority effects and, as a consequence, the degree to which community assembly is historically contingent.

  View details for DOI 10.1098/rspb.2011.1230

  View details for PubMedID 21775330

• Do assembly history effects attenuate from species to ecosystem properties? A field test with wood-inhabiting fungi ECOLOGY LETTERS Dickie, I. A., Fukami, T., Wilkie, J. P., Allen, R. B., Buchanan, P. K. 2012; 15 (2): 133-141

  Abstract

  Assembly history, or the order of species arrival, can have wide-ranging effects on species, communities and ecosystems. However, it remains unclear whether assembly history primarily affects individual species, with effects attenuating at the level of communities and ecosystems or, alternatively, has consistent effect sizes across increasing levels of ecological organisation. We address this question using a field-based manipulation of assembly history of wood-inhabiting fungi. The largest effect sizes were observed for the frequency of some individual species, and mean effect sizes were lower for community metrics of fungi immigrating from the regional species pool. There was little evidence, however, of attenuation in effect sizes at the ecosystem level (carbon, nitrogen, decomposition) in comparison to the species or community level. These results indicate that assembly history can have strong effects on ecosystem properties even under natural levels of environmental variability.

  View details for DOI 10.1111/j.1461-0248.2011.01722.x

  View details for Web of Science ID 000298848200007

  View details for PubMedID 22188588

• Evolutionary history, immigration history, and the extent of diversification in community assembly FRONTIERS IN MICROBIOLOGY Knope, M. L., Forde, S. E., Fukami, T. 2012; 3

  Abstract

  During community assembly, species may accumulate not only by immigration, but also by in situ diversification. Diversification has intrigued biologists because its extent varies even among closely related lineages under similar ecological conditions. Recent research has suggested that some of this puzzling variation may be caused by stochastic differences in the history of immigration (relative timing and order of immigration by founding populations), indicating that immigration and diversification may affect community assembly interactively. However, the conditions under which immigration history affects diversification remain unclear. Here we propose the hypothesis that whether or not immigration history influences the extent of diversification depends on the founding populations' prior evolutionary history, using evidence from a bacterial experiment. To create genotypes with different evolutionary histories, replicate populations of Pseudomonas fluorescens were allowed to adapt to a novel environment for a short or long period of time (approximately 10 or 100 bacterial generations) with or without exploiters (viral parasites). Each evolved genotype was then introduced to a new habitat either before or after a standard competitor genotype. Most genotypes diversified to a greater extent when introduced before, rather than after, the competitor. However, introduction order did not affect the extent of diversification when the evolved genotype had previously adapted to the environment for a long period of time without exploiters. Diversification of these populations was low regardless of introduction order. These results suggest that the importance of immigration history in diversification can be predicted by the immigrants' evolutionary past. The hypothesis proposed here may be generally applicable in both micro- and macro-organisms.

  View details for DOI 10.3389/fmicb.2011.00273

  View details for Web of Science ID 000208863600042

  View details for PubMedCentralID PMC3253546

• Integrating Teaching and Research in Undergraduate Biology Laboratory Education PLOS BIOLOGY Kloser, M. J., Brownell, S. E., Chiariello, N. R., Fukami, T. 2011; 9 (11)

  View details for DOI 10.1371/journal.pbio.1001174

  View details for PubMedID 22110400

• Community assembly: alternative stable states or alternative transient states? ECOLOGY LETTERS Fukami, T., Nakajima, M. 2011; 14 (10): 973-984

  Abstract

  The concept of alternative stable states has long been a dominant framework for studying the influence of historical contingency in community assembly. This concept focuses on stable states, yet many real communities are kept in a transient state by disturbance, and the utility of predictions for stable states in explaining transient states remains unclear. Using a simple model of plant community assembly, we show that the conditions under which historical contingency affects community assembly can differ greatly for stable versus transient states. Differences arise because the contribution of such factors as mortality rate, environmental heterogeneity and plant-soil feedback to historical contingency changes as community assembly proceeds. We also show that transient states can last for a long time relative to immigration rate and generation time. These results argue for a conceptual shift of focus from alternative stable states to alternative transient states for understanding historical contingency in community assembly.

  View details for DOI 10.1111/j.1461-0248.2011.01663.x

  View details for PubMedID 21790934

• Linking community and ecosystem dynamics through spatial ecology ECOLOGY LETTERS Massol, F., Gravel, D., Mouquet, N., Cadotte, M. W., Fukami, T., Leibold, M. A. 2011; 14 (3): 313-323

  Abstract

  Classical approaches to food webs focus on patterns and processes occurring at the community level rather than at the broader ecosystem scale, and often ignore spatial aspects of the dynamics. However, recent research suggests that spatial processes influence both food web and ecosystem dynamics, and has led to the idea of 'metaecosystems'. However, these processes have been tackled separately by 'food web metacommunity' ecology, which focuses on the movement of traits, and 'landscape ecosystem' ecology, which focuses on the movement of materials among ecosystems. Here, we argue that this conceptual gap must be bridged to fully understand ecosystem dynamics because many natural cases demonstrate the existence of interactions between the movements of traits and materials. This unification of concepts can be achieved under the metaecosystem framework, and we present two models that highlight how this framework yields novel insights. We then discuss patches, limiting factors and spatial explicitness as key issues to advance metaecosystem theory. We point out future avenues for research on metaecosystem theory and their potential for application to biological conservation.

  View details for DOI 10.1111/j.1461-0248.2011.01588.x

  View details for Web of Science ID 000287528600014

  View details for PubMedID 21272182

• Evolutionary history, immigration history, and the extent of diversification in community assembly. Frontiers in microbiology Knope, M. L., Forde, S. E., Fukami, T. 2011; 2: 273-?

  Abstract

  During community assembly, species may accumulate not only by immigration, but also by in situ diversification. Diversification has intrigued biologists because its extent varies even among closely related lineages under similar ecological conditions. Recent research has suggested that some of this puzzling variation may be caused by stochastic differences in the history of immigration (relative timing and order of immigration by founding populations), indicating that immigration and diversification may affect community assembly interactively. However, the conditions under which immigration history affects diversification remain unclear. Here we propose the hypothesis that whether or not immigration history influences the extent of diversification depends on the founding populations' prior evolutionary history, using evidence from a bacterial experiment. To create genotypes with different evolutionary histories, replicate populations of Pseudomonas fluorescens were allowed to adapt to a novel environment for a short or long period of time (approximately 10 or 100 bacterial generations) with or without exploiters (viral parasites). Each evolved genotype was then introduced to a new habitat either before or after a standard competitor genotype. Most genotypes diversified to a greater extent when introduced before, rather than after, the competitor. However, introduction order did not affect the extent of diversification when the evolved genotype had previously adapted to the environment for a long period of time without exploiters. Diversification of these populations was low regardless of introduction order. These results suggest that the importance of immigration history in diversification can be predicted by the immigrants' evolutionary past. The hypothesis proposed here may be generally applicable in both micro- and macro-organisms.

  View details for DOI 10.3389/fmicb.2011.00273

  View details for PubMedID 22291685

• From Populations to Ecosystems Theoretical Foundations for a New Ecological Synthesis (Book Review) SCIENCE Book Review Authored by: Fukami, T. 2010; 330 (6007): 1049–50

  View details for DOI 10.1126/science.1197441

  View details for Web of Science ID 000284374700024

• Assembly history dictates ecosystem functioning: evidence from wood decomposer communities ECOLOGY LETTERS Fukami, T., Dickie, I. A., Wilkie, J. P., Paulus, B. C., Park, D., Roberts, A., Buchanan, P. K., Allen, R. B. 2010; 13 (6): 675-684

  Abstract

  Community assembly history is increasingly recognized as a fundamental determinant of community structure. However, little is known as to how assembly history may affect ecosystem functioning via its effect on community structure. Using wood-decaying fungi as a model system, we provide experimental evidence that large differences in ecosystem functioning can be caused by small differences in species immigration history during community assembly. Direct manipulation of early immigration history resulted in three-fold differences in fungal species richness and composition and, as a consequence, differences of the same magnitude in the rate of decomposition and carbon release from wood. These effects - which were attributable to the history-dependent outcome of competitive and facilitative interactions - were significant across a range of nitrogen availabilities observed in natural forests. Our results highlight the importance of considering assembly history in explaining ecosystem functioning.

  View details for DOI 10.1111/j.1461-0248.2010.01465.x

  View details for PubMedID 20412280

• Assembly history dictates ecosystem functioning: evidence from wood decomposer communities Ecology Letters Fukami T, Dickie IA, Wilkie JP, Paulus BC, Park D, Roberts A, Buchanan PK, Allen RB 2010; 13: 675-684
• Direct and indirect effects of rats: does rat eradication restore ecosystem functioning of New Zealand seabird islands? BIOLOGICAL INVASIONS Mulder, C. P., Grant-Hoffman, M. N., Towns, D. R., Bellingham, P. J., Wardle, D. A., Durrett, M. S., Fukami, T., Bonner, K. I. 2009; 11 (7): 1671-1688

  View details for DOI 10.1007/s10530-008-9396-x

  View details for Web of Science ID 000267886200013

• Empirical and theoretical challenges in aboveground-belowground ecology OECOLOGIA van der Putten, W. H., Bardgett, R. D., de Ruiter, P. C., Hol, W. H., Meyer, K. M., Bezemer, T. M., Bradford, M. A., Christensen, S., Eppinga, M. B., Fukami, T., Hemerik, L., Molofsky, J., Schaedler, M., Scherber, C., Strauss, S. Y., Vos, M., Wardle, D. A. 2009; 161 (1): 1-14

  Abstract

  A growing body of evidence shows that aboveground and belowground communities and processes are intrinsically linked, and that feedbacks between these subsystems have important implications for community structure and ecosystem functioning. Almost all studies on this topic have been carried out from an empirical perspective and in specific ecological settings or contexts. Belowground interactions operate at different spatial and temporal scales. Due to the relatively low mobility and high survival of organisms in the soil, plants have longer lasting legacy effects belowground than aboveground. Our current challenge is to understand how aboveground-belowground biotic interactions operate across spatial and temporal scales, and how they depend on, as well as influence, the abiotic environment. Because empirical capacities are too limited to explore all possible combinations of interactions and environmental settings, we explore where and how they can be supported by theoretical approaches to develop testable predictions and to generalise empirical results. We review four key areas where a combined aboveground-belowground approach offers perspectives for enhancing ecological understanding, namely succession, agro-ecosystems, biological invasions and global change impacts on ecosystems. In plant succession, differences in scales between aboveground and belowground biota, as well as between species interactions and ecosystem processes, have important implications for the rate and direction of community change. Aboveground as well as belowground interactions either enhance or reduce rates of plant species replacement. Moreover, the outcomes of the interactions depend on abiotic conditions and plant life history characteristics, which may vary with successional position. We exemplify where translation of the current conceptual succession models into more predictive models can help targeting empirical studies and generalising their results. Then, we discuss how understanding succession may help to enhance managing arable crops, grasslands and invasive plants, as well as provide insights into the effects of global change on community re-organisation and ecosystem processes.

  View details for DOI 10.1007/s00442-009-1351-8

  View details for Web of Science ID 000267345500001

  View details for PubMedID 19412705

  View details for PubMedCentralID PMC2700873

• Long-Term Effects of Predator Arrival Timing on Prey Community Succession AMERICAN NATURALIST Olito, C., Fukami, T. 2009; 173 (3): 354-362

  Abstract

  The stochastic arrival of competing species and their subsequent interactions have been highlighted as principal forces underlying biotic historical effects in community assembly. However, despite the widely recognized effect of predation on prey communities, the effects that the stochastic arrival of predators may have on assembling communities are poorly understood. We used a microbial microcosm experiment to investigate whether the timing of predator arrival to a prey community undergoing naturalistic succession affected species abundances and community diversity. Predator arrival timing affected the long-term abundance of a prey species that was persistent throughout succession in the absence of predators. Our data indicate that this timing effect occurred indirectly via transient interactions between early-successional prey species and predators. Specifically, we suggest that transient early-successional prey species served as a springboard for early-arriving (but not late-arriving) predators, allowing the exploiting predators to increase their abundances and subsequently alter long-term community dynamics. These results show that the history of predator arrival can have lasting consequences for community structure in ecological succession.

  View details for DOI 10.1086/596538

  View details for Web of Science ID 000263126800011

  View details for PubMedID 19183067

• Immigration history controls diversification in experimental adaptive radiation NATURE Fukami, T., Beaumont, H. J., Zhang, X., Rainey, P. B. 2007; 446 (7134): 436-439

  Abstract

  Diversity in biological communities is a historical product of immigration, diversification and extinction, but the combined effect of these processes is poorly understood. Here we show that the order and timing of immigration controls the extent of diversification. When an ancestral bacterial genotype was introduced into a spatially structured habitat, it rapidly diversified into multiple niche-specialist types. However, diversification was suppressed when a niche-specialist type was introduced before, or shortly after, introduction of the ancestral genotype. In contrast, little suppression occurred when the same niche specialist was introduced relatively late. The negative impact of early arriving immigrants was attributable to the historically sensitive outcome of interactions involving neutral competition and indirect facilitation. Ultimately, the entire boom-and-bust dynamics of adaptive radiation were altered. These results demonstrate that immigration and diversification are tightly linked processes, with small differences in immigration history greatly affecting the evolutionary emergence of diversity.

  View details for DOI 10.1038/nature05629

  View details for Web of Science ID 000245079500039

  View details for PubMedID 17377582

• Alternative stable states, trait dispersion and ecological restoration OIKOS Fukami, T., Lee, W. G. 2006; 113 (2): 353-356

  View details for DOI 10.1111/j.2006.0030-1299.14563.x

  View details for Web of Science ID 000237655400017

• Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecology Letters Fukami T, Wardle DA, Bellingham PJ, Mulder CPH, Towns DR, Yeates GW, Bonner KI, Durrett MS, Grant-Hoffman MN, Williamson WM 2006; 9: 1299-1307
• Species divergence and trait convergence in experimental plant community assembly ECOLOGY LETTERS Fukami, T., Bezemer, T. M., Mortimer, S. R., van der Putten, W. H. 2005; 8 (12): 1283-1290

  View details for DOI 10.1111/j.1461-0248.2005.00829.x

  View details for Web of Science ID 000233313500005

• Integrating internal and external dispersal in metacommunity assembly: preliminary theoretical analyses ECOLOGICAL RESEARCH Fukami, T. 2005; 20 (6): 623-631

  View details for DOI 10.1007/s11284-005-0092-3

  View details for Web of Science ID 000233245400001

• Long-term ecological dynamics: reciprocal insights from natural and anthropogenic gradients PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES Fukami, T., Wardle, D. A. 2005; 272 (1577): 2105-2115

  Abstract

  Many ecological dynamics occur over time-scales that are well beyond the duration of conventional experiments or observations. One useful approach to overcome this problem is extrapolation of temporal dynamics from spatial variation. We review two complementary variants of this approach that have been of late increasingly employed: the use of natural gradients to infer anthropogenic effects and the use of anthropogenic gradients to infer natural dynamics. Recent studies have considered a variety of naturally occurring gradients associated with climate, CO2, disturbance and biodiversity gradients, as well as anthropogenic gradients such as those created by biological invasions, habitat fragmentation and land abandonment. These studies show that natural gradients are useful in predicting long-term consequences of human-induced environmental changes, whereas anthropogenic gradients are helpful in inferring the mechanisms behind natural dynamics because covarying factors are often more clearly understood in anthropogenic gradients than in natural gradients. We classify these studies into several categories, each with different strengths and weaknesses, and outline how the limitations can be overcome by combining the gradient-based approach with other approaches. Overall, studies reviewed here demonstrate that the development of basic ecological concepts and the application of these concepts to environmental problems can be more effective when conducted complementarily than when pursued separately.

  View details for DOI 10.1098/rspb.2005.3277

  View details for Web of Science ID 000232634600001

  View details for PubMedID 16191623

  View details for PubMedCentralID PMC1559953

• Dispersal, spatial scale, and species diversity in a hierarchically structured experimental landscape ECOLOGY LETTERS Cadotte, M. W., Fukami, T. 2005; 8 (5): 548-557

  Abstract

  Although there has been growing interest in the effect of dispersal on species diversity, much remains unknown about how dispersal occurring at multiple scales influences diversity. We used an experimental microbial landscape to determine whether dispersal occurring at two different scales - among local communities and among metacommunities - affects diversity differently. At the local scale, dispersal initially had a positive effect and subsequently a neutral effect on diversity, whereas at the metacommunity and landscape scales, dispersal showed a consistently negative effect. The timing in which dispersal affected beta diversity also differed sharply between local communities and metacommunities. These patterns were explained by scale- and time-dependent effects of dispersal in allowing spread of species and in removing spatial refuges from predators. Our results suggest that the relative contribution of opposing mechanisms by which dispersal affects diversity changes considerably over time and space in hierarchical landscapes in which dispersal occurs at multiple scales.

  View details for DOI 10.1111/j.1461-0248.2005.00750.x

  View details for Web of Science ID 000228397000011

  View details for PubMedID 21352459

• Species divergence and trait convergence in experimental plant community assembly. Ecology Letters Fukami, T., Bezemer, TM, Mortimer, SR, Van der Putten, WH 2005; 8: 1283-1290
• Constructing nature: Laboratory models as necessary tools for investigating complex ecological communities ADVANCES IN ECOLOGICAL RESEARCH, VOL. 37: POPULATION DYNAMICS AND LABORATORY ECOLOGY Cadotte, M. W., Drake, J. A., Fukami, T. 2005; 37: 333-353

  View details for Web of Science ID 000232368100011

• Assembly history interacts with ecosystem size to influence species diversity ECOLOGY Fukami, T. 2004; 85 (12): 3234-3242

  View details for DOI 10.1890/04-0340

  View details for Web of Science ID 000226297500006

• Community assembly along a species pool gradient: implications for multiple-scale patterns of species diversity POPULATION ECOLOGY Fukami, T. 2004; 46 (2): 137-147

  View details for DOI 10.1007/s10144-004-0182-z

  View details for Web of Science ID 000223956800005

• Productivity-biodiversity relationships depend on the history of community assembly NATURE Fukami, T., Morin, P. J. 2003; 424 (6947): 423-426

  Abstract

  Identification of the causes of productivity-species diversity relationships remains a central topic of ecological research. Different relations have been attributed to the influence of disturbance, consumers, niche specialization and spatial scale. One unexplored cause is the history of community assembly, the partly stochastic sequential arrival of species from a regional pool of potential community members. The sequence of species arrival can greatly affect community structure. If assembly sequence interacts with productivity to influence diversity, different sequences can contribute to variation in productivity-diversity relationships. Here we report a test of this hypothesis by assembling aquatic microbial communities at five productivity levels using four assembly sequences. About 30 generations after assembly, productivity-diversity relationships took various forms, including a positive, a hump-shaped, a U-shaped and a non-significant pattern, depending on assembly sequence. This variation resulted from idiosyncratic joint effects of assembly sequence, productivity and species identity on species abundances. We suggest that the history of community assembly should be added to the growing list of factors that influence productivity-biodiversity patterns.

  View details for DOI 10.1038/nature01785

  View details for Web of Science ID 000184318400042

  View details for PubMedID 12879069

• On similarity among local communities in biodiversity experiments OIKOS Fukami, T., Naeem, S., Wardle, D. A. 2001; 95 (2): 340-348

  View details for Web of Science ID 000172433800016

• Sequence effects of disturbance on community structure OIKOS Fukami, T. 2001; 92 (2): 215-224

  View details for DOI 10.1034/j.1600-0706.2001.920203.x

  View details for Web of Science ID 000167560700003