Ecological load and balancing selection in circumboreal barnacles

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 million years 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.

A historically balanced locus under recent directional selection in responding to changed nitrogen conditions during modern maize breeding

“…According to the previous study (76; 77), the locus under balancing selection has an elevated nucleotide diversity ( π ), Tajima’s D, and site frequency spectrum. Utilizing Sorghum bicolor alleles as the ancestral state, we calculated the site frequency spectrum for each block at the selection region.…”

From tides to nucleotides: Genomic signatures of adaptation to environmental heterogeneity in barnacles

“…Data from Maine was obtained from Schmidt and Rand ( 1999 ). For RI, additional temperature data was obtained from (Nunez, Rong, et al, 2020 ). The RI data which we collected includes the period from 11 July to 9 August 2018.…”

“…These differential ecological pressures have drastic consequences on both life‐history (Bertness et al, 1991 ) and morphological traits in barnacles (Figure 1c ; Figure S1 ). Moreover, the stark contrast between strong selection at the adult stage and the free‐swimming planktonic larvae results in the problem of ecological genetic load (Nunez, Rong, et al, 2020 ). That is, since larvae often settle in new habitats every generation, any beneficial allele inherited from its parent may be neutral or deleterious, and, consequentially, fitness maximization within a microhabitat becomes a problem.…”

“…Previous work in Semibalanus has argued that the life history of this species is a good fit for the Levene ( 1953 ) model of spatially heterogeneous selection. For example, in their recent paper, Nunez, Rong, et al, ( 2020 ) revealed the existence of hundreds of loci across the genome which harbour trans‐species polymorphisms and show molecular signatures canonically associated with long‐term balancing selection. As such, the study provides evidence supporting the hypothesis that spatially heterogeneous selection plays a key role in the maintenance of adaptation.…”

“…Is zonation localized to particular areas in the genome? Is the genetic basis of ecological zonation fueled by young, short‐lived, alleles, or by old, balanced polymorphisms (e.g., those discovered in Nunez, Rong, et al, 2020 )? While S. balanoides experiences ecological stressors at multiple spatial scales, we have chosen to focus our study at the spatial scale of the rocky intertidal since it has been exhaustively characterized in the species.…”