Comparative genomics reveals divergent thermal selection in warm‐ and cold‐tolerant marine mussels

Abstract

Investigating the history of natural selection among closely related species can elucidate how genomes diverge in response to disparate environmental pressures. Molecular evolutionary approaches can be integrated with knowledge of gene functions to examine how evolutionary divergence may affect ecologically relevant traits such as temperature tolerance and species distribution limits. Here, we integrate transcriptome‐wide analyses of molecular evolution with knowledge from physiological studies to develop hypotheses regarding the functional classes of genes under positive selection in one of the world's most widespread invasive species, the warm‐tolerant marine mussel Mytilus galloprovincialis. Based on existing physiological information, we test the hypothesis that genomic functions previously linked to divergent temperature adaptation at the whole‐organism level show accelerated molecular divergence between warm‐adapted M. galloprovincialis and cold‐adapted congeners. Combined results from codon model tests and analyses of polymorphism and divergence reveal that divergent selection has affected genomic functions previously associated with species‐specific expression responses to heat stress, namely oxidative stress defence and cytoskeletal stabilization. Examining specific loci implicated in thermal tolerance among Mytilus species (based on interspecific biochemical or expression patterns), we find close functional similarities between known thermotolerance candidate genes under positive selection and positively selected loci under predicted genomic functions (those associated with divergent expression responses). Taken together, our findings suggest a contribution of temperature‐dependent selection in the molecular divergence between warm‐ and cold‐adapted Mytilus species that is largely consistent with results from physiological studies. More broadly, this study provides an example of how independent experimental evidence from ecophysiological investigations can inform evolutionary hypotheses about molecular adaptation in closely related nonmodel species.

Trans-Atlantic Distribution and Introgression as Inferred from Single Nucleotide Polymorphism: Mussels Mytilus and Environmental Factors

“…While M. edulis has been shown to start their spawning in late spring, M. trossulus generally starts later in the summer [116,117], paving a possibility for M. trossulus to dominate areas with longer-lasting sea ice. Popovic and Riginos [118] summarized data on distribution and temperature of four Mytilus taxa in Northern Hemisphere and demonstrated that M. galloprovincialis inhabits waters characterized by much higher mean surface temperature in comparison with M. edulis and M. trossulus. M. galloprovincialis has physiological and metabolic adaptations to higher sea water temperature in comparison with M. edulis and M. trossulus [119][120][121][122].…”

“…Mantle transcriptome comparison among Mytilus taxa has been performed by Malachowicz and Wenne [123]. While Fraïsse et al [44] demonstrated some SNP loci under selection (outliers), Popovic and Riginos [118] used transcriptome analysis for temperature selection studies in Mytilus specimens from natural environments. Their study performed on 24 individuals of Mytilus congeners collected from natural environments differing in temperature suggested a positive temperature-dependent selection as a factor influencing molecular divergence between warm and cold tolerant Mytilus taxa.…”

Pre‐introduction introgression contributes to parallel differentiation and contrasting hybridization outcomes between invasive and native marine mussels

“…Three contigs provided especially strong evidence for genetic parallelism following introduction, with high differentiation at the same nucleotide positions (max F ST > 0.4) when considering joint outcomes across both population pairs in permutation tests ( p < .001; Figure 2a). Suggestively, Contig33253 returned a top blastn hit to the M. galloprovincialis hsp90‐2 gene encoding heat‐shock protein 90 (HSP90); HSPs and other oxidative stress‐related proteins have been shown to evolve under positive selection in M. galloprovincialis (Popovic & Riginos, 2020) and may also be targets of repeated selection within introduced environments or during long‐distance transport experienced by migrant larvae in the ballast water of container ships.…”

Gene expression plasticity, genetic variation and fatty acid remodelling in divergent populations of a tropical bivalve species

“…Environmental pressure might also favor the frequency of adaptive alleles at the scale of the population which would confer heritable changes modifications to specific environmental conditions. For instance, natural selection has contributed to the higher thermal tolerance and increased invasive potential of the blue M. galloprovencialis compared to other Mytilus species (Popovic & Riginos, 2020; Saarman, Kober, Simison, & Pogson, 2017). In C. gigas , natural selection and/or local adaption on thermal performances shaped the fine-scale structure of populations living in a highly-connected and temperature-contrasted area (Li et al, 2018).…”