An official website of the United States government
Abstract As climate change advances, environmental gradients may decouple, generating novel multivariate environments that stress wild populations. A commonly invoked mechanism of evolutionary rescue is adaptive gene flow tracking climate shifts, but gene flow from populations inhabiting similar conditions on one environmental axis could cause maladaptive introgression when populations are adapted to different environmental variables that do not shift together. Genomic architecture can play an important role in determining the effectiveness and relative magnitudes of adaptive gene flow and in situ adaptation. This may have direct consequences for how species respond to climate change but is often overlooked. Here, we simulated microevolutionary responses to environmental change under scenarios defined by variation in the polygenicity, linkage, and genetic redundancy of two independent traits, one of which is adapted to a gradient that shifts under climate change. We used these simulations to examine how genomic architecture influences evolutionary outcomes under climate change. We found that climate‐tracking (up‐gradient) gene flow, though present in all scenarios, was strongly constrained under scenarios of lower linkage and higher polygenicity and redundancy, suggesting in situ adaptation as the predominant mechanism of evolutionary rescue under these conditions. We also found that high polygenicity caused increased maladaptation and demographic decline, a concerning result given that many climate‐adapted traits may be polygenic. Finally, in scenarios with high redundancy, we observed increased adaptive capacity. This finding adds to the growing recognition of the importance of redundancy in mediating in situ adaptive capacity and suggests opportunities for better understanding the climatic vulnerability of real populations.
more »
« less
Does gene flow aggravate or alleviate maladaptation to environmental stress in small populations?
Abstract Environmental change can expose populations to unfamiliar stressors, and maladaptive responses to those stressors may result in population declines or extirpation. Although gene flow is classically viewed as a cause of maladaptation, small and isolated populations experiencing high levels of drift and little gene flow may be constrained in their evolutionary response to environmental change. We provide a case study using the model Trinidadian guppy system that illustrates the importance of considering gene flow and genetic drift when predicting (mal)adaptive response to acute stress. We compared population genomic patterns and acute stress responses of inbred guppy populations from headwater streams either with or without a recent history of gene flow from a more diverse mainstem population. Compared to “no‐gene flow” analogues, we found that populations with recent gene flow showed higher genomic variation and increased stress tolerance—but only when exposed to a stress familiar to the mainstem population (heat shock). All headwater populations showed similar responses to a familiar stress in headwater environments (starvation) regardless of gene flow history, whereas exposure to an entirely unfamiliar stress (copper sulfate) showed population‐level variation unrelated to environment or recent evolutionary history. Our results suggest that (mal)adaptive responses to acutely stressful environments are determined in part by recent evolutionary history and in part by previous exposure. In some cases, gene flow may provide the variation needed to persist, and eventually adapt, in the face of novel stress.
more »
« less
- Award ID(s):
- 1722621
- PAR ID:
- 10441431
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Evolutionary Applications
- Volume:
- 12
- Issue:
- 7
- ISSN:
- 1752-4571
- Format(s):
- Medium: X Size: p. 1402-1416
- Size(s):
- p. 1402-1416
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Effective population size affects the efficacy of selection, rate of evolution by drift and neutral diversity levels. When species are subdivided into multiple populations connected by gene flow, evolutionary processes can depend on global or local effective population sizes. Theory predicts that high levels of diversity might be maintained by gene flow, even very low levels of gene flow, consistent with species long‐term effective population size, but tests of this idea are mostly lacking. Here, we show thatLycaeidesbutterfly populations maintain low contemporary (variance) effective population sizes (e.g. ~200 individuals) and thus evolve rapidly by genetic drift. However, populations harboured high levels of genetic diversity consistent with an effective population size several orders of magnitude larger. We hypothesized that the differences in the magnitude and variability of contemporary versus long‐term effective population sizes were caused by gene flow of sufficient magnitude to maintain diversity but only subtly affect evolution on generational timescales. Consistent with this hypothesis, we detected low but nontrivial gene flow among populations. Furthermore, using short‐term population‐genomic time‐series data, we documented patterns consistent with predictions from this hypothesis, including a weak but detectable excess of evolutionary change in the direction of the mean (migrant gene pool) allele frequencies across populations and consistency in the direction of allele frequency change over time. The documented decoupling of diversity levels and short‐term change by drift inLycaeideshas implications for our understanding of contemporary evolution and the maintenance of genetic variation in the wild.more » « less
-
Heyer, Evelyne (Ed.)Abstract Structural variants have a considerable impact on human genomic diversity. However, their evolutionary history remains mostly unexplored. Here, we developed a new method to identify potentially adaptive structural variants based on a similarity-based analysis that incorporates genotype frequency data from 26 populations simultaneously. Using this method, we analyzed 57,629 structural variants and identified 576 structural variants that show unusual population differentiation. Of these putatively adaptive structural variants, we further showed that 24 variants are multiallelic and overlap with coding sequences, and 20 variants are significantly associated with GWAS traits. Closer inspection of the haplotypic variation associated with these putatively adaptive and functional structural variants reveals deviations from neutral expectations due to: 1) population differentiation of rapidly evolving multiallelic variants, 2) incomplete sweeps, and 3) recent population-specific negative selection. Overall, our study provides new methodological insights, documents hundreds of putatively adaptive variants, and introduces evolutionary models that may better explain the complex evolution of structural variants.more » « less
-
Social interactions with conspecifics are key to the fitness of most animals and, through the transmission opportunities they provide, are also key to the fitness of their parasites. As a result, research to date has largely focused on the role of host social behavior in imposing selection on parasites, particularly their virulence and transmission phenotypes. However, host social behavior also influences the distribution of parasites among hosts, with implications for their evolution through non-random mating, gene flow, and genetic drift, and thus ability to respond to that selection. Here, we review the paucity of empirical studies on parasites, and draw from empirical studies of free-living organisms and population genetic theory to propose several mechanisms by which host social behavior potentially drives parasite evolution through these less-well studied mechanisms. We focus on the guppy host and Gyrodactylus (Monogenea) ectoparasitic flatworm system and follow a spatially hierarchical outline to highlight that social behavior varies between individuals, and between host populations across the landscape, generating a mosaic of ecological and evolutionary outcomes for their infecting parasites. We argue that the guppy-Gyrodactylus system presents a unique opportunity to address this fundamental knowledge gap in our understanding of the connection between host social behavior and parasite evolution. Individual differences in host social behavior generates fine-scale changes in the spatial distribution of parasite genotypes, shape the size, and diversity of their infecting parasite populations and may generate non-random mating on, and non-random transmission between hosts. While at population and metapopulation level, variation in host social behavior interacts with landscape structure to affect parasite gene flow, effective population size, and genetic drift to alter the coevolutionary potential of local adaptation.more » « less
-
Abstract Gene flow into populations can increase additive genetic variation and introduce novel beneficial alleles, thus facilitating adaptation. However, gene flow may also impede adaptation by disrupting beneficial genotypes, introducing deleterious alleles, or creating novel dominant negative interactions. While theory and fieldwork have provided insight into the effects of gene flow, direct experimental tests are rare. Here, we evaluated the effects of gene flow on adaptation in the nematode Caenorhabditis elegans during exposure to the bacterial parasite, Serratia marcescens. We evolved hosts against nonevolving parasites for 10 passages while controlling host gene flow and source population. We used source nematode populations with three different genetic backgrounds (one similar to the sink population and two different) and two evolutionary histories (previously adapted to S. marcescens or naive). We found that populations with gene flow exhibited greater increases in parasite resistance than those without gene flow. Additionally, gene flow from adapted populations resulted in greater increases in resistance than gene flow from naive populations, particularly with gene flow from novel genetic backgrounds. Overall, this work demonstrates that gene flow can facilitate adaptation and suggests that the genetic architecture and evolutionary history of source populations can alter the sink population’s response to selection.more » « less
