The response of a metapopulation to a changing environment

A species distributed across heterogeneous environments may adapt to local conditions. Szep et al. (2021, Evolution) modelled this process in the infinite island model, finding the stationary distribution of allele frequencies and deme sizes. We extend this to ask how a metapopulation responds to changes in carrying capacity, selection strength, or migration rate, restricting attention to fixed deme size ("soft selection"). We develop a "fixed-state" approximation (accurate when migration is rare) which assumes that the loci are near fixation. Under this approximation, polymorphism is only possible for a narrow range of habitat proportions when selection is weak compared to drift, but for a much wider range otherwise. When local conditions (Ns or Nm) change in a single deme, it takes a time of ~1/m to reach the new equilibrium. However, even withmany loci, there can be substantial fluctuations in net adaptation, due to the bimodal allele frequency distributions at each locus. Thus, in a finite metapopulation, variation may gradually be lost by chance, even if it would persist with infinitely many demes. When conditions change across the whole metapopulation, there can be rapid response, accurately predicted by the fixed-state approximation when Nm <<1.

The evolution and fate of diversity under hard and soft selection

How genetic variation arises and persists over evolutionary time despite the depleting effects of natural selection remains a long-standing question. Here, we investigate the impacts of two extreme forms of population regulation—at the level of the total, mixed population (hard selection) and at the level of local, spatially distinct patches (soft selection)—on the emergence and fate of diversity under strong divergent selection. We find that while the form of population regulation has little effect on rates of diversification, it can modulate the long-term fate of genetic variation, diversity being more readily maintained under soft selection compared to hard selection. The mechanism responsible for coexistence is negative frequency-dependent selection which, while present initially under both forms of population regulation, persists over the long-term only under soft selection. Importantly, coexistence is robust to continued evolution of niche specialist types under soft selection but not hard selection. These results suggest that soft selection could be a general mechanism for the maintenance of ecological diversity over evolutionary time scales.

The Evolution and Fate of Diversity Under Hard and Soft Selection

How genetic variation arises and persists over evolutionary time despite the depleting effects of natural selection remains a long-standing question. Here, we investigate the impacts of two extreme forms of population regulation – at the level of the total, mixed population (hard selection) and at the level of local, spatially distinct patches (soft selection) – on the emergence and fate of diversity under strong divergent selection. We find that while the form of population regulation has little effect on rates of diversification it can modulate the long-term fate of genetic variation, diversity being more readily maintained under soft selection compared to hard selection. The mechanism responsible for coexistence is negative frequency dependent selection which, while present initially under both forms of population regulation, persists over the long-term only under soft selection. Importantly, coexistence is robust to continued evolution of niche specialist types under soft selection but not hard selection. These results suggest that soft selection could be a general mechanism for the maintenance of ecological diversity over evolutionary time scales.

Genomic signatures of evolutionary rescue in bats surviving white-nose syndrome

Rapid evolution of advantageous traits following abrupt environmental change can help populations grow and avoid extinction through evolutionary rescue. Here, we provide the first genetic evidence for rapid evolution in bat populations affected by white-nose syndrome (WNS). By comparing genetic samples from before and after little brown bat populations were decimated by WNS, we identified signatures of soft selection on standing genetic variation. This selection occurred at multiple loci in genes linked to hibernation behavior rather than immune function, suggesting that differences in hibernation strategy have allowed these bats to survive infection with WNS. Through these findings, we suggest that evolutionary rescue can be a conservationrelevant process even in slowly reproducing taxa threatened with extinction.

The effect of offspring number on the adaptation speed of a polygenic trait

There is increasing evidence that rapid phenotypic adaptation of quantitative traits is not uncommon in nature. However, the circumstances under which rapid adaptation of polygenic traits occurs are not yet understood. Building on previous concepts of soft selection, i.e. frequency and density dependent selection, I developed and tested the hypothesis that adaptation speed of a polygenic trait depends on the number of offspring per breeding pair in a randomly mating diploid population. Using individual based modelling on a range of offspring per parent (2-200) in populations of various size (100-10000 individuals), I could show that the by far largest proportion of variance (42%) was explained by the offspring number, regardless of genetic trait architecture (10-50 loci, different locus contribution distributions). In addition, it was possible to identify the majority of the responsible loci and account for even more of the observed phenotypic change with a moderate population size. The simulation results suggest that offspring numbers may a crucial factor for the adaptation speed of quantitative loci. Moreover, as large offspring numbers translates to a large phenotypic variance in the offspring of each parental pair, this genetic bet hedging strategy increases the chance to contribute to the next generation in unpredictable environments.