Experimental evolution of adaptive divergence under varying degrees of gene flow

Abstract

Adaptive divergence is the key evolutionary process generating biodiversity by means of natural selection. Yet, the conditions under which it can arise in the presence of gene flow remain contentious. To address this question, we subjected 132 sexually reproducing fission yeast populations sourced from two independent genetic backgrounds to disruptive ecological selection and manipulated the level of migration between environments. Contrary to theoretical expectations, adaptive divergence was most pronounced when migration was either absent ('allopatry') or maximal ('sympatry'), but was much reduced at intermediate rates ('parapatry', 'local mating'). This effect was apparent across central life history components (survival, asexual growth, and mating), but differed in magnitude between ancestral genetic backgrounds. The evolution of some fitness components was constrained by pervasive negative correlations (trade-off between asexual growth and mating), while others changed direction under the influence of migration (e.g. survival and mating). In allopatry, adaptive divergence was mainly conferred by standing genetic variation and resulted in ecological specialization. In sympatry, divergence was mainly mediated by novel mutations enriched in a subset of genes and was characterized by the repeated emergence of two strategies: an ecological generalist and an asexual growth specialist. Multiple loci showed consistent evidence for antagonistic pleiotropy across migration treatments and provide a conceptual link between adaptation and divergence. This evolve-and-resequence experiment demonstrates that rapid ecological differentiation can arise even under high rates of gene flow. It further highlights that adaptive trajectories are governed by complex interactions of gene flow, ancestral variation and genetic correlations. MainAdaptive divergence describes the emergence of new forms from a shared common ancestor by adaptation to different environmental conditions. As such, it is key to the formation of new species by means of natural selection 1,2 . In geographic isolation, divergent selection readily promotes ecological specialisation which over time can result in reproductive barriers between populations 3-6 . In the presence of gene flow, however, the conditions enabling adaptive divergence are difficult to predict [7][8][9] . Homogenizing gene flow may impede adaptive divergence and promote generalist phenotypes exploiting a broader ecological spectrum 10,11 .Alternatively, gene flow may promote divergence by supplying adaptive genetic variation or by modifying genetic correlations which can alter evolutionary constraints and open new evolutionary trajectories 12,13 . In general, the relationship between gene flow and adaptive divergence is expected to decline monotonically (i.e. less divergence with higher gene flow) * * * * * * * * * * * * * * α Genetic Background β Genetic Background b.

Experimental evolution of local adaptation under unidimensional and multidimensional selection

“…2 Local adaptation is an important component of within-species diversity, and an increase in local adaptation is also a vital step toward ecological speciation, providing an extrinsic form of reproductive isolation. 3,4 The strength of local adaptation and the speed at which it increases depends on environmental factors, such as the strength of selection and gene flow, 5,6 and genomic conditions, such as the amount and distribution of standing genetic variation 7,8 and the genomic architecture. 9,10 One variable that has received far less attention, however, is the number of simultaneous divergent selection pressures experienced by a population, i.e., the dimensionality of divergent selection.…”

A polygenic architecture with habitat‐dependent effects underlies ecological differentiation in Silene

“…However, strong evidence for conditional neutrality is fundamentally difficult to provide, because this would require evidence for the absence of an effect in one of the habitats (Anderson et al ., 2014; Mee & Yeaman, 2019). Interestingly, antagonistic pleiotropy appears to be detected more readily in controlled experimental evolution studies with microorganisms than in natural settings with higher plants or insects (Gompert & Messina, 2016; Bono et al ., 2017; Wadgymar et al ., 2017; Tusso et al ., 2021). This is probably a consequence of the control of selective agents in experiments as opposed to natural sites where both selective agents and traits under selection may vary (Wadgymar et al ., 2017).…”

AF-vapeR: A multivariate genome scan for detecting parallel evolution using allele frequency change vectors

“…Beyond studies of repeatability, this approach may be well-suited to evolve-and-resequence experiments (e.g. (Barghi et al, 2019; Rudman et al, 2021; Tusso et al, 2021)), where replication is common and allele frequency change may be moderate and recorded after only a few generations. Because patterns of parallelism break down over time, seen here with ALX1 haplotypes in finches, our approach is best-suited to intra-specific comparisons, or those among relatively young clades.…”