The interaction of resource use and gene flow on the phenotypic divergence of benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)

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.

Variation in the genomic basis of parallel phenotypic and ecological divergence in benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)

“…Þingvallavatn and Svínavatn showed the expected pattern with significant numbers of RDA outlier loci and regions located in high F ST regions. Moreover, the population with a relatively low amount of phenotypic and ecological divergence (Vatnshlíðarvatn) (Brachmann et al, 2021) showed no detectable RDA outliers. However, the low degree of phenotypic and ecological divergence between morphs in Vatnshlíðarvatn probably limits the statistical power of outlier detection methods, resulting in no detectable outliers.…”

“…To detect genome wide signatures of selection associated with body shape and size variation, we characterized morphological variation using landmark‐based geometric morphometrics. The set of homologous landmarks used within these analyses have been previously defined and used in Brachmann et al (2021). Briefly, the analysis was based on 25 landmarks placed on individual images using TpsDig (Rohlf, 1990).…”

“…We captured benthic and pelagic morphs of Arctic charr from four geographically separated lakes in Iceland (designated as populations hereafter) during 2013-2015 (Table 1). The current analysis is based on the same set of fish used previously to assess the relationships among phenotypic, ecological, and genetic variation (Brachmann et al, 2021). The sample sizes per morph per population used here ranged from 25 to 64 individuals.…”

“…The lakes Galtaból, Svínavatn, and Vatnshlíðarvatn contain a single pair of sympatric benthic and pelagic morphs while Ϸingvallavatn contains three sympatric morphs, two benthic morphs and a single pelagic morph. Although earlier studies indicated that Svínavatn contains three morphs (two pelagic and one benthic morphs; Gíslason et al, 1999), recent work (Brachmann et al, 2021) indicates that the two pelagic groups of fish are neither genetically nor ecologically differentiated so we consider them as a single morph for the current analysis. Fish were caught during morph specific spawning periods using gill nets ranging in mesh sizes from 5-50 mm.…”

“…Relationships between trophic and phenotypic variation suggests that resource use within benthic and pelagic habitats is the agent of selection driving divergence in body shape and size (targets of selection) (Brachmann et al, 2021; Doenz et al, 2019; Franklin et al, 2018). The findings that benthic and pelagic morphs are genetically differentiated (Gíslason et al, 1999; Guðbrandsson et al, 2019; Kapralova et al, 2011) and that greater divergence in resource use can be associated with less genetic admixture (Brachmann et al, 2021) suggest that diet divergence may be associated with reduced gene flow between morphs. Studies of the genomic basis of phenotypic divergence in Arctic charr indicate that the degree of genomic parallelism (identity of outlier loci) appear to be relatively low across populations despite high phenotypic parallelism (Jacobs et al, 2020; Salisbury et al, 2020).…”