Transcriptome‐wide patterns of divergence during allopatric evolution

Abstract

Recent studies have revealed repeated patterns of genomic divergence associated with species formation. Such patterns suggest that natural selection tends to target a set of available genes, but is also indicative that closely related taxa share evolutionary constraints that limit genetic variability. Studying patterns of genomic divergence among populations within the same species may shed light on the underlying evolutionary processes. Here, we examine transcriptome-wide divergence and polymorphism in the marine copepod Tigriopus californicus, a species where allopatric evolution has led to replicate sets of populations with varying degrees of divergence and hybrid incompatibility. Our analyses suggest that relatively small effective population sizes have resulted in an exponential decline of shared polymorphisms during population divergence and also facilitated the fixation of slightly deleterious mutations within allopatric populations. Five interpopulation comparisons at three different stages of divergence show that nonsynonymous mutations tend to accumulate in a specific set of proteins. These include proteins with central roles in cellular metabolism, such as those encoded in mtDNA, but also include an additional set of proteins that repeatedly show signatures of positive selection during allopatric divergence. Although our results are consistent with a contribution of nonadaptive processes, such as genetic drift and gene expression levels, generating repeatable patterns of genomic divergence in closely related taxa, they also indicate that adaptive evolution targeting a specific set of genes contributes to this pattern. Our results yield insights into the predictability of evolution at the gene level.

Integrative Approaches for Studying Mitochondrial and Nuclear Genome Co-evolution in Oxidative Phosphorylation

“…Confounding factors include demographic processes (e.g., population size change and structure), background selection, and heterogeneous mutation and recombination rates. Given that mitochondrial and nuclear genomes can have largely independent evolutionary histories (e.g., different introgression patterns and mutation load), knowledge of the demographic history of the study system is especially useful to interpret patterns of mitonuclear co-evolution (Bar-Yaacov et al, 2015; Morales et al, 2016a,b; Pereira et al, 2016; Sloan et al, 2016). Given that mitonuclear co-evolution is likely to respond to environmental variation (Burton et al, 2013), approaches to detecting selection that rely on gene-environment associations could be particularly useful to identify candidate loci under selection (Rellstab et al, 2015; Forester et al, 2016).…”

“…A natural follow-up is to look for evidence of natural selection in nuclear-encoded mitochondrial genes and signals of mitonuclear co-evolutionary adaptation (Mishmar et al, 2006; Gagnaire et al, 2012; Bar-Yaacov et al, 2015; Pereira et al, 2016). For example, such approaches have identified supernumerary and assembly factors of OXPHOS complex I implicated in local adaptation (Garvin et al, 2016; Morales et al, 2016a).…”

“…Pereira et al (2016) recently approximated the contribution of genetic drift and natural selection in T. californicus divergence by comparing whole-transcriptome sequences of allopatric populations at different stages of divergence (Pereira et al, 2016). They found that the pattern of shared polymorphism could be partially explained by genetic drift, as lower effective population sizes led to less shared polymorphism between populations, and higher mutation load.…”

Population Genomics of Marine Zooplankton

“…The rapid rate of evolutionary divergence of mitochondrial genes is thought to contribute to the potential for local adaptation, but may also cause low hybrid fitness by disrupting gene complexes (Burton et al 2013). The mitochondrial genome has been sequenced (Barreto et al 2011;Pereira et al 2016). A genomic SNP linkage map (Foley et al 2011) and a partial draft genome (https://i5k.nal.usda.gov/Tigriopus_californicus) serve as useful resources for characterizing population genetic diversity and structure.…”

History repeats itself: genomic divergence in copepods

“…This is precisely what Pereira et al . () set out to do using marine copepods Tigriopus californicus , and present their results in this issue of Molecular Ecology. They show that evolution can be repeatable and even partly predictable, at least at the molecular level.…”