The environmentally tuned transcriptomes ofMytilusmussels

Abstract

Transcriptomics is a powerful tool for elucidating the molecular mechanisms that underlie the ability of organisms to survive and thrive in dynamic and changing environments. Here, we review the major contributions in this field, and we focus on studies of mussels in the genus Mytilus, which are well-established models for the study of ecological physiology in fluctuating environments. Our review is organized into four main sections. First, we illustrate how the abiotic forces of the intertidal environment drive the rhythmic coupling of gene expression to diel and tidal cycles in Mytilus californianus. Second, we discuss the challenges and pitfalls of conducting transcriptomic studies in field-acclimatized animals. Third, we examine the link between transcriptomic responses to environmental stress and biogeographic distributions in blue mussels, Mytilus trossulus and Mytilus galloprovincialis. Fourth, we present a comparison of transcriptomic datasets and identify 175 genes that share common responses to heat stress across Mytilus species. Taken together, these studies demonstrate that transcriptomics can provide an informative snapshot of the physiological state of an organism within an environmental context. In a comparative framework, transcriptomics can reveal how natural selection has shaped patterns of transcriptional regulation that may ultimately influence biogeography.

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

“…Specifically, branch‐site models identified two homologues under positive selection using inference based on the LRT statistic (Table ). The first homologue had a blastx annotation to a small heat shock protein of the α‐crystallin protein family and Heat Shock Protein 25 (HSP25; based on Mytilus californianus expressed sequence tag [EST] annotations; GenBank accession ES737726), which is up‐regulated in heat‐stressed Mytilus congeners (Connor & Gracey, ; Lockwood et al, ). The branch‐site model also identified a single codon with a high Bayesian posterior probability of positive selection at site 185 (albeit not significant; BEB p = .905) encoding a functional amino acid substitution in M. galloprovincialis (Figure ).…”

“…We obtained specific loci previously identified as thermotolerance candidate genes based on their biochemical or expression patterns among Mytilus congeners in physiological investigations (Table ). Gene sets included thermotolerance candidates for (a) divergent functional adaptation ( n = 2; i.e., cMDH , IDH, Fields et al, ; Lockwood & Somero, ); (b) species‐specific differential expression under heat‐stress ( n = 96; Lockwood et al, ); and (c) shared transcriptional responses in three Mytilus congeners under acute heat stress ( n = 175; Connor & Gracey, ; Lockwood et al, ). A total of 273 thermotolerance candidate genes were assigned to reference transcripts using reciprocal best hits in proteinortho version 5.13 (Lechner et al, ), but only a small proportion of candidate loci (36/273) were matched to complete orthologues in all four taxa.…”

“…Mytilus galloprovincialis is the only Mytilus species that is known to have established invasive populations outside of its native range in the Mediterranean Sea, including introductions in California, South Africa and Australia (Branch & Steffani, ; McDonald & Koehn, ; Popovic, Matias, Bierne, & Riginos, ). Over the last two decades, the genus Mytilus has become an important comparative system for studying links between species distribution limits, marine invasive success and thermal physiology, and there is a growing body of experimental evidence for understanding key molecular functions involved in environmental adaptation in this group (Lockwood, Connor, & Gracey, ). The genus Mytilus therefore holds many advantages of a nearly model organism, with a breadth of ecophysiological studies and functional insights into the genetic basis of thermal adaptation, despite life history features that do not allow for accessible inbred lines or multiple generations required to link physiological differences to their genetic basis.…”

“…Ecophysiological studies investigating the role of environmental adaptation in setting species distributions have largely focused on M. galloprovincialis in the northeastern Pacific, where introduced populations have displaced native Mytilus trossulus in central and southern California (Figure a; Braby & Somero, ; Geller, ; Rawson, Agrawal, & Hilbish, ). Physiological studies have implicated interspecific differences in temperature tolerance as a primary factor explaining species distribution limits and the ability of introduced M. galloprovincialis to outcompete native congeners in warm habitats where their distributions overlap (Fields, Zuzow, & Tomanek, ; Lockwood et al, ; Lockwood & Somero, ; Figure b). Indeed, comparative physiological and biochemical investigations have demonstrated marked differences between Mytilus species, consistent with higher warm‐temperature tolerance in introduced M. galloprovincialis relative to cold‐adapted congeners (e.g., temperature‐dependent gene expression, Hofmann & Somero, ; Lockwood et al, ; proteomic response, Tomanek & Zuzow, ; Fields et al, ; Tomanek, ; metabolic enzyme activity, Fields, Rudomin, & Somero, ; Lockwood & Somero, ; and cardiac function, Braby & Somero, ; reviewed in Lockwood & Somero, ; Lockwood et al, ).…”

“…Physiological investigations have also provided insight into the genetic basis of thermal tolerance differences among Mytilus species (Lockwood et al, ). Fixed amino acid substitutions in two metabolic enzymes have been sufficient to explain functional divergence in protein heat sensitivity conferring temperature tolerance between warm‐ and cold‐adapted Mytilus species (i.e., cytosolic malate dehydrogenase, cMDH, Fields et al, ; isocitrate dehydrogenase, IDH, Lockwood & Somero, ).…”