Abstract

A central question linking ecology with evolutionary biology is how environmental heterogeneity can drive adaptive genetic divergence among populations. We examined adaptive divergence of four stream insects from six adjacent catchments in Japan by combining field measures of habitat and resource components with genome scans of non-neutral Amplified Fragment Length Polymorphism (AFLP) loci. Neutral genetic variation was used to measure gene flow and non-neutral genetic variation was used to test for adaptive divergence. We identified the environmental characteristics contributing to divergence by comparing genetic distances at non-neutral loci between sites with Euclidean distances for each of 15 environmental variables. Comparisons were made using partial Mantel tests to control for geographic distance. In all four species, we found strong evidence for non-neutral divergence along environmental gradients at between 6 and 21 loci per species. The relative contribution of these environmental variables to each species' ecological niche was quantified as the specialization index, S, based on ecological data. In each species, the variable most significantly correlated with genetic distance at non-neutral loci was the same variable along which each species was most narrowly distributed (i.e., highest S). These were gradients of elevation (two species), chlorophyll-a, and ammonia-nitrogen. This adaptive divergence occurred in the face of ongoing gene flow (F st = 0.01–0.04), indicating that selection was strong enough to overcome homogenization at the landscape scale. Our results suggest that adaptive divergence is pronounced, occurs along different environmental gradients for different species, and may consistently occur along the narrowest components of species' niche.

Highlights

  • Adaptive genetic divergence among populations within species is an evolutionary process on the way towards ecological speciation [1] and is thought to be an important driver of the formation and maintenance of biodiversity [2]

  • We identified environmental variables that are most likely to contribute to adaptive divergence for each species using Mantel tests, and compered the variables with those identified by the specialization index analyses

  • Values were lower at neutral loci than at non-neutral loci (Table 2) and the same was true for mean genetic variance within sampling sites (HW)

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Summary

Introduction

Adaptive genetic divergence among populations within species is an evolutionary process on the way towards ecological speciation [1] and is thought to be an important driver of the formation and maintenance of biodiversity [2]. Genome scans allow for the study of non-model organisms and a number of studies have reported evidence for genetic adaptation, where changes in allele frequencies at putatively adaptive loci are correlated with environmental changes across the species’ range (e.g., [14,15,16,17]). Such studies provide strong evidence for adaptive divergence among populations at one or more parts of the genome but are often limited to single species and a few environmental parameters. Natural populations are subject to many selective forces simultaneously, and several environmental factors may be responsible for the observed genetic divergence

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