Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification

Abstract

Adaptive diversification is driven by selection in ecologically different environments. In absence of geographical barriers to dispersal, this adaptive divergence (AD) may be constrained by gene flow (GF). And yet the reverse may also be true, with AD constraining GF (i.e. Ôecological speciationÕ). Both of these causal effects have frequently been inferred from the presence of negative correlations between AD and GF in natureyet the bi-directional causality warrants caution in such inferences. We discuss how the ability of correlative studies to infer causation might be improved through the simultaneous measurement of multiple ecological and evolutionary variables. On the one hand, inferences about the causal role of GF can be made by examining correlations between AD and the potential for dispersal. On the other hand, inferences about the causal role of AD can be made by examining correlations between GF and environmental differences. Experimental manipulations of dispersal and environmental differences are a particularly promising approach for inferring causation. At present, the best studies find strong evidence that GF constrains AD and some studies also find the reverse. Improvements in empirical approaches promise to eventually allow general inferences about the relative strength of different causal interactions during adaptive diversification.

Cryptic invasion drives phenotypic changes in central European threespine stickleback

“…1). This is consistent with theoretical predictions (Räsänen and Hendry 2008) and suggests that increased gene flow and admixture resulted in phenotypic shifts, which may even override local selection on lateral plate phenotypes (Raeymaekers et al 2014;Ferchaud and Hansen 2016). Gene flow and subsequent admixture, rather Fig.…”

Non-random gene flow: an underappreciated force in evolution and ecology

“…Given this impact, it is imperative to also consider whether the main betweenpopulation evolutionary process (i.e., gene flow) is random or non-random with respect to genotype, and the consequences of this distinction. Random gene flow has been the standard assumption of evolutionary genetic models [3,8], and this might be appropriate for most loci within a genome. However, few evolutionary models consider whether gene flow is random or non-random with respect to functional genotypes, and mostly these directly model the evolution of the dispersal traits themselves (e.g., [41]).…”

“…The remaining evolutionary processes are typically viewed as sources of genetic variation for selection to act upon [3][4][5], or as forces that constrain the adaptive effects of natural selection [6][7][8][9]. For example, gene flow is widely assumed to counteract the effect of natural selection [8] by introducing maladaptive foreign alleles into a locally adapted population [10].…”

“…For example, gene flow is widely assumed to counteract the effect of natural selection [8] by introducing maladaptive foreign alleles into a locally adapted population [10]. Most evolutionary models assume that dispersal is random with respect to genotype [3,8,11]. That is, in each generation, some fraction of individuals m ij disperse from population i to population j, and these dispersers carry the same allele frequency as the donor population i (or for small populations, a random sample of donor alleles).…”

Decoupling of differentiation between traits and their underlying genes in response to divergent selection

“…Interest in the speed of adaptive differentiation in heterogeneous landscapes has increased recently (Kawecki, 2008;Lopez et al, 2008;Bjorklund et al, 2009). Evolutionary responses are often inferred from the divergence or differentiation of adaptive traits observed in a set of populations undergoing divergent selection (Hendry et al, 2001;Crispo, 2008;Rasanen and Hendry, 2008) or from the molecular divergence of genes of adaptive relevance (Kapralov and Filatov, 2006;Nosil et al, 2009). Furthermore there is an increasing concern about the rate of response of natural populations to ongoing climate change (Aitken et al, 2008).…”