Mark Christopher Bitter

All Publications

• Evolutionary adaptation under climate change:Aedessp. demonstrates potential to adapt to warming. bioRxiv : the preprint server for biology Couper, L. I., Dodge, T. O., Hemker, J. A., Kim, B. Y., Exposito-Alonso, M., Brem, R. B., Mordecai, E. A., Bitter, M. C. 2024

  Abstract

  Climate warming is expected to shift the distributions of mosquitoes and mosquito-borne diseases, facilitating expansions at cool range edges and contractions at warm edges. However, whether mosquito populations could maintain their warm range edges through evolutionary adaptation remains unknown. Here, we investigate the potential for thermal adaptation in Aedes sierrensis , a congener of the major disease vector species that experiences large thermal gradients in its native range, by assaying tolerance to prolonged and acute heat exposure, and their genetic basis in a diverse, field-derived population. We found pervasive evidence of heritable genetic variation in acute heat tolerance, which phenotypically trades off with tolerance to prolonged heat exposure. A simple evolutionary model based on our data shows that, under most scenarios, the estimated maximum rate of evolutionary adaptation in mosquito heat tolerance exceeds that of projected climate warming. Our findings indicate that natural mosquito populations likely have the potential to track projected warming via genetic adaptation. Prior climate-based projections may thus underestimate the range of mosquito and mosquito-borne disease distributions under future climate conditions.Significance Statement: Global change may have profound impacts on the distribution of mosquito-borne diseases, which collectively cause nearly one million deaths each year. Accurately predicting these impacts is critical for disease control preparedness, and will depend, in part, on whether mosquitoes can adapt to warming-a key open question. Using experimental and genomic data from a relative of major vector species that already experiences a wide thermal gradient, we find that natural mosquito populations have high levels of genetically-based variation in heat tolerance that could enable adaptation on pace with warming. Incorporating the potential for adaptive responses may therefore be necessary for accurate predictions of mosquito-borne disease distributions under warming, which is critical for preparing mosquito control interventions.

  View details for DOI 10.1101/2024.08.23.609454

  View details for PubMedID 39229052

• Continuously fluctuating selection reveals fine granularity of adaptation. Nature Bitter, M. C., Berardi, S., Oken, H., Huynh, A., Lappo, E., Schmidt, P., Petrov, D. A. 2024

  Abstract

  Temporally fluctuating environmental conditions are a ubiquitous feature of natural habitats. Yet, how finely natural populations adaptively track fluctuating selection pressures via shifts in standing genetic variation is unknown1,2. Here we generated genome-wide allele frequency data every 1-2 generations from a genetically diverse population of Drosophila melanogaster in extensively replicated field mesocosms from late June to mid-December (a period of approximately 12 total generations). Adaptation throughout the fundamental ecological phases of population expansion, peak density and collapse was underpinned by extremely rapid, parallel changes in genomic variation across replicates. Yet, the dominant direction of selection fluctuated repeatedly, even within each of these ecological phases. Comparing patterns of change in allele frequency to an independent dataset procured from the same experimental system demonstrated that the targets of selection are predictable across years. In concert, our results reveal a fitness relevance of standing variation that is likely to be masked by inference approaches based on static population sampling or insufficiently resolved time-series data. We propose that such fine-scaled, temporally fluctuating selection may be an important force contributing to the maintenance of functional genetic variation in natural populations and an important stochastic force impacting genome-wide patterns of diversity at linked neutral sites, akin to genetic draft.

  View details for DOI 10.1038/s41586-024-07834-x

  View details for PubMedID 39143223

  View details for PubMedCentralID 8385344

• 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

• Molecular basis of ocean acidification sensitivity and adaptation in Mytilus galloprovincialis. iScience Kapsenberg, L., Bitter, M. C., Miglioli, A., Aparicio-Estalella, C., Pelejero, C., Gattuso, J., Dumollard, R. 2022; 25 (8): 104677

  Abstract

  Predicting the potential for species adaption to climate change is challenged by the need to identify the physiological mechanisms that underpin species vulnerability. Here, we investigated the sensitivity to ocean acidification in marine mussels during early development, and specifically the trochophore stage. Using RNA and DNA sequencing and in situ RNA hybridization, we identified developmental processes associated with abnormal development and rapid adaptation to low pH. Trochophores exposed to low pH seawater exhibited 43 differentially expressed genes. Gene annotation and in situ hybridization of differentially expressed genes point to pH sensitivity of (1) shell field development and (2) cellular stress response. Five genes within these two processes exhibited shifts in allele frequencies indicative of a potential for rapid adaptation. This case study contributes direct evidence that protecting species' existing genetic diversity is a critical management action to facilitate species resilience to climate change.

  View details for DOI 10.1016/j.isci.2022.104677

  View details for PubMedID 35847553

• Fluctuating selection and global change: a synthesis and review on disentangling the roles of climate amplitude, predictability and novelty. Proceedings. Biological sciences Bitter, M. C., Wong, J. M., Dam, H. G., Donelan, S. C., Kenkel, C. D., Komoroske, L. M., Nickols, K. J., Rivest, E. B., Salinas, S., Burgess, S. C., Lotterhos, K. E. 2021; 288 (1957): 20210727

  Abstract

  A formidable challenge for global change biologists is to predict how natural populations will respond to the emergence of conditions not observed at present, termed novel climates. Popular approaches to predict population vulnerability are based on the expected degree of novelty relative to the amplitude of historical climate fluctuations experienced by a population. Here, we argue that predictions focused on amplitude may be inaccurate because they ignore the predictability of environmental fluctuations in driving patterns of evolution and responses to climate change. To address this disconnect, we review major findings of evolutionary theory demonstrating the conditions under which phenotypic plasticity is likely to evolve in natural populations, and how plasticity decreases population vulnerability to novel environments. We outline key criteria that experimental studies should aim for to effectively test theoretical predictions, while controlling for the degree of climate novelty. We show that such targeted tests of evolutionary theory are rare, with marine systems being overall underrepresented in this venture despite exhibiting unique opportunities to test theory. We conclude that with more robust experimental designs that manipulate both the amplitude and predictability of fluctuations, while controlling for the degree of novelty, we may better predict population vulnerability to climate change.

  View details for DOI 10.1098/rspb.2021.0727

  View details for PubMedID 34428970

  View details for PubMedCentralID PMC8385344

• Magnitude and Predictability of pH Fluctuations Shape Plastic Responses to Ocean Acidification. The American naturalist Bitter, M. C., Kapsenberg, L., Silliman, K., Gattuso, J. P., Pfister, C. A. 2021; 197 (4): 486-501

  Abstract

  AbstractPhenotypic plasticity is expected to facilitate the persistence of natural populations as global change progresses. The attributes of fluctuating environments that favor the evolution of plasticity have received extensive theoretical investigation, yet empirical validation of these findings is still in its infancy. Here, we combine high-resolution environmental data with a laboratory-based experiment to explore the influence of habitat pH fluctuation dynamics on the plasticity of gene expression in two populations of the Mediterranean mussel, Mytilus galloprovincialis. We linked differences in the magnitude and predictability of pH fluctuations in two habitats to population-specific gene expression profiles in ambient and stressful pH treatments. Our results demonstrate population-based differentiation in gene expression plasticity, whereby mussels native to a habitat exhibiting a large magnitude of pH fluctuations with low predictability display reduced phenotypic plasticity between experimentally imposed pH treatments. This work validates recent theoretical findings on evolution in fluctuating environments, suggesting that the predictability of fluctuating selection pressures may play a predominant role in shaping the phenotypic variation observed across natural populations.

  View details for DOI 10.1086/712930

  View details for PubMedID 33755541

• Standing genetic variation fuels rapid adaptation to ocean acidification. Nature communications Bitter, M. C., Kapsenberg, L., Gattuso, J. P., Pfister, C. A. 2019; 10 (1): 5821

  Abstract

  Global climate change has intensified the need to assess the capacity for natural populations to adapt to abrupt shifts in the environment. Reductions in seawater pH constitute a conspicuous global change stressor that is affecting marine ecosystems globally. Here, we quantify the phenotypic and genetic modifications associated with rapid adaptation to reduced seawater pH in the Mediterranean mussel, Mytilus galloprovincialis. We reared a genetically diverse larval population in two pH treatments (pHT 8.1 and 7.4) and tracked changes in the shell-size distribution and genetic variation through settlement. Additionally, we identified differences in the signatures of selection on shell growth in each pH environment. Both phenotypic and genetic data show that standing variation can facilitate adaptation to declines in seawater pH. This work provides insight into the processes underpinning rapid evolution, and demonstrates the importance of maintaining variation within natural populations to bolster species' adaptive capacity as global change progresses.

  View details for DOI 10.1038/s41467-019-13767-1

  View details for PubMedID 31862880

  View details for PubMedCentralID PMC6925106

• Ocean pH fluctuations affect mussel larvae at key developmental transitions. Proceedings. Biological sciences Kapsenberg, L., Miglioli, A., Bitter, M. C., Tambutté, E., Dumollard, R., Gattuso, J. P. 2018; 285 (1893): 20182381

  Abstract

  Coastal marine ecosystems experience dynamic fluctuations in seawater carbonate chemistry. The importance of this variation in the context of ocean acidification requires knowing what aspect of variability biological processes respond to. We conducted four experiments (ranging from 3 to 22 days) with different variability regimes (pHT 7.4-8.1) assessing the impact of diel fluctuations in carbonate chemistry on the early development of the mussel Mytilus galloprovincialis. Larval shell growth was consistently correlated to mean exposures, regardless of variability regimes, indicating that calcification responds instantaneously to seawater chemistry. Larval development was impacted by timing of exposure, revealing sensitivity of two developmental processes: development of the shell field, and transition from the first to the second larval shell. Fluorescent staining revealed developmental delay of the shell field at low pH, and abnormal development thereof was correlated with hinge defects in D-veligers. This study shows, for the first time, that ocean acidification affects larval soft-tissue development, independent from calcification. Multiple developmental processes additively underpin the teratogenic effect of ocean acidification on bivalve larvae. These results explain why trochophores are the most sensitive life-history stage in marine bivalves and suggest that short-term variability in carbonate chemistry can impact early larval development.

  View details for DOI 10.1098/rspb.2018.2381

  View details for PubMedID 30963891

  View details for PubMedCentralID PMC6304040