Genome-wide signatures of synergistic epistasis during parallel adaptation in a Baltic Sea copepod

Abstract

The role of epistasis in driving adaptation has remained an unresolved problem dating back to the Evolutionary Synthesis. In particular, whether epistatic interactions among genes could promote parallel evolution remains unexplored. To address this problem, we employ an Evolve and Resequence (E&R) experiment, using the copepod Eurytemora affinis, to elucidate the evolutionary genomic response to rapid salinity decline. Rapid declines in coastal salinity at high latitudes are a predicted consequence of global climate change. Based on time-resolved pooled whole-genome sequencing, we uncover a remarkably parallel, polygenic response across ten replicate selection lines, with 79.4% of selected alleles shared between lines by the tenth generation of natural selection. Using extensive computer simulations of our experiment conditions, we find that this polygenic parallelism is consistent with positive synergistic epistasis among alleles, far more so than other mechanisms tested. Our study provides experimental and theoretical support for a novel mechanism promoting repeatable polygenic adaptation, a phenomenon that may be common for selection on complex physiological traits.

Mechanisms of Na+ uptake from freshwater habitats in animals

“…Experimental evolution studies also revealed NHA paralogs as genetic targets of selection during rapid salinity decline in the laboratory (Stern et al, 2022). Of the NHA paralogs, the E. affinis paralogs NHA7 and NHA5 showed evolutionary shifts in gene expression between ancestral saline and recently derived freshwater populations, supporting the importance of NHA function during rapid salinity transitions (Posavi et al, 2020;Lee, 2021).…”

“…Frontiers in Physiology frontiersin.org implicating NHA paralogs in freshwater adaptation (Posavi et al, 2020;Stern and Lee, 2020;Stern et al, 2022). Single-cell RNA sequencing could greatly improve our knowledge on the diverse ionocyte subtypes in fish and would potentially help identify new Na + uptake pathways in specific cell types (Leguen et al, 2015;Xue et al, 2015).…”

“…Several evolutionary genomic studies implicate NHA paralogs as important contributors to freshwater adaptation ( Posavi et al, 2020 ; Stern and Lee, 2020 ; Lee, 2021 ; Stern et al, 2022 ). Population genomic studies of the copepod Eurytemora affinis species complex have found that gene paralogs of NHA exhibit signatures of natural selection between ancestral saline and recently freshwater invading populations ( Stern and Lee, 2020 ; Lee, 2021 ; Stern et al, 2022 ).…”

“…Several evolutionary genomic studies implicate NHA paralogs as important contributors to freshwater adaptation ( Posavi et al, 2020 ; Stern and Lee, 2020 ; Lee, 2021 ; Stern et al, 2022 ). Population genomic studies of the copepod Eurytemora affinis species complex have found that gene paralogs of NHA exhibit signatures of natural selection between ancestral saline and recently freshwater invading populations ( Stern and Lee, 2020 ; Lee, 2021 ; Stern et al, 2022 ). Often the same SNPs (single nucleotide polymorphisms) were under selection across repeated saline to freshwater invasion events, suggesting that the same functional sites are evolving within the ion transporter protein.…”

Resolving marine–freshwater transitions by diatoms through a fog of discordant gene trees

“…Diatoms exhibit high levels of inter- and intraspecific variation in gene expression in response to reduced salinity (Nakov et al 2020; Pinseel et al 2022), providing numerous targets for natural selection to optimize gene expression for a particular salinity environment (López-Maury et al 2008; Bedford and Hartl 2009; Gomez-Mestre and Jovani 2013). Finally, differences in codon usage (Prabha et al 2017), nucleotide substitution rates (Mitterboeck et al 2016), transposable element activity (Yuan et al 2018), epigenetic responses (Artemov et al 2017), and epistatic interactions (Stern et al 2022) have been implicated in adaptation to freshwaters in other groups. The genomic resources and phylogenetic framework presented here represent an important advance towards identifying the genes and evolutionary processes underpinning freshwater adaptation by diatoms.…”