The Role of Standing Variation in Geographic Convergent Adaptation

Abstract

The extent to which populations experiencing shared selective pressures adapt through a shared genetic response is relevant to many questions in evolutionary biology. In a number of well studied traits and species, it appears that convergent evolution within species is common. In this paper, we explore how standing, genetic variation contributes to convergent genetic responses in a geographically spread population, extending our previous work on the topic. Geographically limited dispersal slows the spread of each selected allele, hence allowing other alleles – newly arisen mutants or present as standing variation – to spread before any one comes to dominate the population. When such alleles meet, their progress is substantially slowed – if the alleles are selectively equivalent, they mix slowly, dividing the species range into a random tessellation, which can be well understood by analogy to a Poisson process model of crystallization. In this framework, we derive the geographic scale over which a typical allele is expected to dominate, the time it takes the species to adapt as a whole, and the proportion of adaptive alleles that arise from standing variation. Finally, we explore how negative pleiotropic effects of alleles before an environment change can bias the subset of alleles that contribute to the species’ adaptive response. We apply the results to the many geographically localized G6PD deficiency alleles thought to confer resistance to malaria, where the large mutational target size makes it a likely candidate for adaptation from standing variation, despite the selective cost of G6PD deficiency alleles in the absence of malaria. We find the numbers and geographic spread of these alleles matches our predictions reasonably well, consistent with the view that they arose from a combination of standing variation and new mutations since the advent of malaria. Our results suggest that much of adaptation may be geographically local even when selection pressures are homogeneous. Therefore, we argue that caution must be exercised when arguing that strongly geographically restricted alleles are necessarily the outcome of local adaptation. We close by discussing the implications of these results for ideas of species coherence and the nature of divergence between species.

Spatial and temporal heterogeneity in climate change limits species' dispersal capabilities and adaptive potential

“…Finally, our results are also broadly consistent with recent studies demonstrating that complex genetic architectures can constrain rapid evolutionary responses and prevent the fixation of beneficial alleles (Chevin and Hospital 2008) and that standing genetic variation can result in parallel adaptations to shared selection pressures across fragmented landscapes (Ralph and Coop 2015). Thus, ultimately, a trait's genetic architecture, potential plasticity, variation within a population, and distribution across a population's range must all be considered in addition to the degree of habitat fragmentation in a population's dispersal matrix when assessing the potential for evolutionary rescue (Kopp and Matuszewski 2014).…”

Parallel genetic evolution and speciation from standing variation

“…5). Together, these results indicate that adaptive walks from standing variation in our simulations involved more-slightly smaller-steps and are more "meandering" than adaptive walks from new mutation alone, which use fewer-slightly larger-and more direct steps (but see Ralph and Coop 2015). These differences in the properties of alleles fixed in simulations initiated with versus without standing variation contribute to the patterns of phenotypic segregation variance that ultimately determine the fitness of hybrids.…”

“…Some of our conclusions will change under alternative assumptions. Some assumptions-for example a lack of recurrent de novo mutation or gene flow-reduce the extent of genetic parallelism (Nosil and Flaxman 2011;Anderson and Harmon 2014;Ralph and Coop 2015;Barghi et al 2019). We also assumed universal pleiotropy and future work examining the effect of modularity on our results-especially on changes in parallelism with the angle of divergence-would be valuable.…”

The probability of parallel genetic evolution from standing genetic variation

“…For instance, in the stickleback, Gasterosteus aculeatus, repeated adaptation to freshwater is thought to involve genes already segregating at low frequencies within the marine populations (Colosimo et al, 2005). In cases like these, the presence of adaptive alleles in the ancestral population can have a significant effect on the probability of parallel evolution, influencing both the long-term probability of parallel adaptation and the rate at which adaptation occurs (Ralph & Coop, 2015). Our focus here is to enhance our understanding of parallel evolution by developing a genetically explicit multilocus framework for predicting the probability of parallel evolution from standing genetic variation.…”