Mitochondrial genotype influences the response to cold stress in the European green crab, Carcinus maenas

Abstract

Hybrid zones provide natural experiments in recombination within and between genomes that may have strong effects on organismal fitness. On the East Coast of North America, two distinct lineages of the European green crab (Carcinus maenas) have been introduced in the last two centuries. These two lineages with putatively different adaptive properties have hybridized along the coast of the eastern Gulf of Maine, producing new nuclear and mitochondrial combinations that show clinal variation correlated with water temperature. To test the hypothesis that mitochondrial or nuclear genes have effects on thermal tolerance, we first measured the response to cold stress in crabs collected throughout the hybrid zone, then sequenced the mitochondrial CO1 gene and two nuclear single nucleotide polymorphisms (SNPs) representative of nuclear genetic lineage. Mitochondrial haplotype had a strong association with the ability of crabs to right themselves at 4.5°C that was sex specific: haplotypes originally from northern Europe gave male crabs an advantage while there was no haplotype effect on righting in female crabs. By contrast, the two nuclear SNPs that were significant outliers in a comparison between northern and southern C. maenas populations had no effect on righting response at low temperature. These results add C. maenas to the shortlist of ectotherms in which mitochondrial variation has been shown to affect thermal tolerance, and suggest that natural selection is shaping the structure of the hybrid zone across the Gulf of Maine. Our limited genomic sampling does not eliminate the strong possibility that mito-nuclear co-adaptation may play a role in the differences in thermal phenotypes documented here. Linkage between mitochondrial genotype and thermal tolerance suggests a role for local adaptation in promoting the spread of invasive populations of C. maenas around the world.

Diversity, divergence and density: How habitat and hybrid zone dynamics maintain a genomic cline in an intertidal barnacle

“…How the diversity recovered in B. glandula maps to functional and taxonomic distinctions (Vellend, 2018) seems approachable with respect to the different performance of diversity of the two types at distinct latitudes (Wares & Skoczen, 2019). Similarly strong mitochondrial signatures of overall physiological and adaptive performance occur in green crabs (Coyle et al, 2019), ribbed mussels (Fields et al, 2012), and numerous other marine organisms (Sanford & Kelly, 2011). Here, we strengthen support for what the mitochondrial diversity of B.…”

“…Our study has three broader implications. The first relates to the warming ocean along the California coast, where others have noted poleward shifts in the ranges of rocky-intertidal species and lineages in the last few decades (e.g, Barry et al 1995;Dawson et al, 2010;Sanford et al, 2019 (Coyle et al, 2019;Pringle et al, 2011Pringle et al, , 2017Wares & Pringle, 2008).…”

Mitochondria and the thermal limits of ectotherms

“…In a hybrid zone between Atlantic killifish (F. heteroclitus) subspecies that differ in both thermal tolerance and mitochondrial genotype, there is no association between mitochondrial genotype and CT max (Healy et al, 2018). In contrast, in the invasive European green crab (Carcinus maenas), there is a significant sex-specific association between low-temperature tolerance and mitochondrial genotype in a North American hybrid zone (Coyle et al, 2019), suggesting a clear role for mitochondrial processes in determining lower critical limits in this species, although the underlying mechanism remains unknown.…”

Of telomeres and temperature: Measuring thermal effects on telomeres in ectothermic animals

“…Exposure to higher-than-normal temperatures can increase the ratio of mitochondrial ROS/ATP production (Roussel & Voituron, 2020) and induce oxidative damage associated with certain mitochondrial phenotypes (Pichaud et al, 2020). For example, mitochondrial function can differ across geographical thermal clines and with mitochondrial genotypes (Coyle et al, 2019;Faria et al, 2020;Fitzpatrick et al, 2019) and change through acclimation effects across seasons (Liang et al, 2017). Indeed, cold acclimation in F I G U R E 4 Thermal performance curves (TPCs) for several performances in within an individual organism, or the mean of a population or of a species in a particular thermal environment: antioxidant activity, mitochondrial function, telomerase activity, general cellular metabolism and growth.…”