Abstract

Conceptual models of adaptive divergence and ecological speciation in sympatry predict differential resource use, phenotype–environment correlations, and reduced gene flow among diverging phenotypes. While these predictions have been assessed in past studies, connections among them have rarely been assessed collectively. We examined relationships among phenotypic, ecological, and genetic variation in Arctic charr (Salvelinus alpinus) from six Icelandic localities that have undergone varying degrees of divergence into sympatric benthic and pelagic morphs. We characterized morphological variation with geometric morphometrics, tested for differential resource use between morphs using stable isotopes, and inferred the amount of gene flow from single nucleotide polymorphisms. Analysis of stable isotopic signatures indicated that sympatric morphs showed similar difference in resource use across populations, likely arising from the common utilization of niche space within each population. Carbon isotopic signature was also a significant predictor of individual variation in body shape and size, suggesting that variation in benthic and pelagic resource use is associated with phenotypic variation. The estimated percentage of hybrids between sympatric morphs varied across populations (from 0% to 15.6%) but the majority of fish had genotypes (ancestry coefficients) characteristic of pure morphs. Despite evidence of reduced gene flow between sympatric morphs, we did not detect the expected negative relationship between divergence in resource use and gene flow. Three lakes showed the expected pattern, but morphs in the fourth showed no detectable hybridization and had relatively low differences in resource use between them. This coupled with the finding that resource use and genetic differentiation had differential effects on body shape variation across populations suggests that reproductive isolation maintains phenotypic divergence between benthic and pelagic morphs when the effects of resource use are relatively low. Our ability to assess relationships between phenotype, ecology, and genetics deepens our understanding of the processes underlying adaptive divergence in sympatry.

Highlights

  • Understanding the processes by which adaptive divergence and barriers to gene flow evolve between subpopulations remains a challenging problem in evolutionary biology

  • We examined relationships among variation in body shape and size, resource use, and gene flow in benthic and pelagic morphs of Icelandic Arctic charr that vary in phenotypic divergence

  • The weaker relationship between the body shape matrices can be explained by the finding that differences in resource use between the benthic and pelagic morphs in Galtaból and Vatnshlíðarvatn were much smaller than those in Ϸingvallavatn and Svínavatn; the effects of genetic divergence were relatively high in all populations based on the patterns of genetic structuring and low numbers of hybrids overall. These findings suggest that genetic divergence, and low levels of gene flow, between benthic and pelagic morphs in Galtaból and Vatnshlíðarvatn have a greater impact in driving divergence in body shape than resource use

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Summary

Introduction

Understanding the processes by which adaptive divergence and barriers to gene flow evolve between subpopulations remains a challenging problem in evolutionary biology. The rapid build-­up of reproductive isolating mechanisms is expected to result in strong genetic population structuring due to reduced gene flow between diverging subpopulations. This sequence of events may eventually lead to speciation (Muschick et al, 2020; Nosil et al, 2009; Rundle & Nosil, 2005; Schumer et al, 2017), the frequency of this outcome is still debated (Bird et al, 2012; Coyne & Orr, 2004; Mallet et al, 2009). Determining how the different elements interact, and perhaps reinforce each other, to promote adaptive divergence and speciation will provide a better understanding how phenotypic variation is partitioned in the presence of gene flow

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