Abstract

Acorn barnacle adults experience environmental heterogeneity at various spatial scales of their circumboreal habitat, raising the question of how adaptation to high environmental variability is maintained in the face of strong juvenile dispersal and mortality. Here, we show that 4% of genes in the barnacle genome experience balancing selection across the entire range of the species. Many of these genes harbor mutations maintained across 2 My of evolution between the Pacific and Atlantic oceans. These genes are involved in ion regulation, pain reception, and heat tolerance, functions which are essential in highly variable ecosystems. The data also reveal complex population structure within and between basins, driven by the trans-Arctic interchange and the last glaciation. Divergence between Atlantic and Pacific populations is high, foreshadowing the onset of allopatric speciation, and suggesting that balancing selection is strong enough to maintain functional variation for millions of years in the face of complex demography.

Highlights

  • The relationship between genetic variation and adaptation to heterogeneous environments remains a central conundrum in evolutionary biology (Botero, et al 2015).Classical models of molecular evolution predict that populations should be locally adapted to maximize fitness (Williams 1966)

  • Principal component analysis (PCA), on the LD-thinned single nucleotide polymorphisms (SNPs), shows that variation is strongly subdivided by ocean basins (Fig. 1D)

  • The dichotomy of strong adult selection and high offspring dispersal means that any allele that is beneficial to parental fitness in one generation may be neutral or deleterious in the (Gillespie 1973)

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Summary

Introduction

The relationship between genetic variation and adaptation to heterogeneous environments remains a central conundrum in evolutionary biology (Botero, et al 2015).Classical models of molecular evolution predict that populations should be locally adapted to maximize fitness (Williams 1966). Many natural populations living in variable environments possess high dispersal capabilities, and harbor more variation than expected under classical models (Metz and Palumbi 1996; Mackay, et al 2012; Messer and Petrov 2013; Bergland, et al 2014). This disconnect between nature and theory has motivated the hypothesis that balancing selection, a process where selection favors multiple beneficial alleles at a given locus, is at play to maintain adaptations in these habitats (Levene 1953; Hedrick 2006)

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