Widespread evidence for incipient ecological speciation: a meta‐analysis of isolation‐by‐ecology

Abstract

Ecologically mediated selection has increasingly become recognised as an important driver of speciation. The correlation between neutral genetic differentiation and environmental or phenotypic divergence among populations, to which we collectively refer to as isolation-by-ecology (IBE), is an indicator of ecological speciation. In a meta-analysis framework, we determined the strength and commonality of IBE in nature. On the basis of 106 studies, we calculated a mean effect size of IBE with and without controlling for spatial autocorrelation among populations. Effect sizes were 0.34 (95% CI 0.24-0.42) and 0.26 (95% CI 0.13-0.37), respectively, indicating that an average of 5% of the neutral genetic differentiation among populations was explained purely by ecological contrast. Importantly, spatial autocorrelation reduced IBE correlations for environmental variables, but not for phenotypes. Through simulation, we showed how the influence of isolation-by-distance and spatial autocorrelation of ecological variables can result in false positives or underestimated correlations if not accounted for in the IBE model. Collectively, this meta-analysis showed that ecologically induced genetic divergence is pervasive across time-scales and taxa, and largely independent of the choice of molecular marker. We discuss the importance of these results in the context of adaptation and ecological speciation and suggest future research avenues.

The challenge of separating signatures of local adaptation from those of isolation by distance and colonization history: The case of two white pines

“…Disentangling IBE from neutral patterns of genetic variation is challenging (Shafer & Wolf, 2013; Wang & Bradburd, 2014). For example, decreasing gene flow with increasing geographic distance due to restricted dispersal (i.e., isolation by distance, IBD; Wright, 1943) can produce patterns similar to IBE when geography is correlated with environmental variation (Meirmans, 2012; Orsini, Vanoverbeke, Swillen, Mergeay, & De Meester, 2013).…”

Competition-driven speciation in cichlid fish

“…Relative success of individual phenotypes on different habitat types will depend on resources available 3 and ecological interactions 4,5 (such as competition, predation or parasitism) that impose natural selection upon them. Examples where ecological speciation has been invoked are widespread 6,7 and there is abundant phylogenetic and population genetic evidence that the speciation process is frequently associated with divergent patterns of resource use. However, it is often unclear how selection has promoted the divergence of ecomorphs and driven associated assortative mating.…”

Union of phylogeography and landscape genetics

“…96) defined as reproductive isolation driven by ecological selection, in the presence or absence of gene flow (65,94,97,98). Importantly, landscape genetics has added many methods that allow one to examine isolation by distance using different metrics (e.g., resistance, geographic barriers, environmental factors, community interactions, and local adaptation) (53,93,95,99,100) although the link between these measures and broader ideas about how adaptation and natural selection in different environments drive speciation is less appreciated in the field (but see ref. 93).…”