Linking genotype to phenotype in a changing ocean: inferring the genomic architecture of a blue mussel stress response with genome‐wide association

Abstract

A key component to understanding the evolutionary response to a changing climate is linking underlying genetic variation to phenotypic variation in stress response. Here, we use a genome-wide association approach (GWAS) to understand the genetic architecture of calcification rates under simulated climate stress. We take advantage of the genomic gradient across the blue mussel hybrid zone (Mytilus edulis and Mytilus trossulus) in the Gulf of Maine (GOM) to link genetic variation with variance in calcification rates in response to simulated climate change. Falling calcium carbonate saturation states are predicted to negatively impact many marine organisms that build calcium carbonate shells - like blue mussels. We sampled wild mussels and measured net calcification phenotypes after exposing mussels to a 'climate change' common garden, where we raised temperature by 3°C, decreased pH by 0.2 units and limited food supply by filtering out planktonic particles >5 μm, compared to ambient GOM conditions in the summer. This climate change exposure greatly increased phenotypic variation in net calcification rates compared to ambient conditions. We then used regression models to link the phenotypic variation with over 170 000 single nucleotide polymorphism loci (SNPs) generated by genotype by sequencing to identify genomic locations associated with calcification phenotype, and estimate heritability and architecture of the trait. We identified at least one of potentially 2-10 genomic regions responsible for 30% of the phenotypic variation in calcification rates that are potential targets of natural selection by climate change. Our simulations suggest a power of 13.7% with our study's average effective sample size of 118 individuals and rare alleles, but a power of >90% when effective sample size is 900.

Standing genetic variation fuels rapid adaptation to ocean acidification

“…As pH tolerance has been shown to exhibit heritability in Mytilus spp. 34,35 , it is possible that multigenerational selection may indeed allow the population to ultimately recover the offset in shell-size observed in this experiment.…”

“…Accordingly, we observed elevation of phenotypic variation in the low-pH treatment on days 3 and 7, coinciding with the inferred period of heightened selection (between days 0 and 6). Kingston et al 35 similarly showed that stressful conditions (low pH, high temperature, and low food conditions) released phenotypic variation in calcification rates in two species of Mytilus mussels, and went on to link this variation to a number of loci of moderate effect 35 . While an important avenue of future research is determining which CGV mechanisms (genotype-by-genotype or genotype-by-environment interactions) may be producing such patterns, the economic and ecological importance of marine mussels, as well as their global exposure to declining seawater pH, highlight the need to conserve standing variation in order to allow the adaptive capacity of natural populations to play out as climate change progresses.…”

Response to selection for increasing resistance to the spring mortality outbreaks in Mytilus edulis occurring in France since 2014

“…The realized heritability to increase survival of M. edulis during a spring mortality outbreak was very high (> 0.55) ( Table 3). Most of the heritabilities estimated in mussel species have been reported for growth parameters (Bai et al, 2017;Brichette et al, 2001;Nguyen et al, 2014;Toro et al, 2004), shell nacre color (Bai et al, 2017), mantle color, toxin accumulation A C C E P T E D M A N U S C R I P T (Pino-Querido et al, 2015), and more recently calcification (Kingston et al, 2018).…”

Species identification based on a semi-diagnostic marker: Evaluation of a simple conchological test for distinguishing blue mussels Mytilus edulis L. and M. trossulus Gould

“…As for the samples from the other contact zones, all American samples and two out of five Norwegian samples were from saline habitats, while all the others were from brackish habitats. Salinity conditions in the sampling localities were either taken from the literature [27][28][29][30][31][32] or, in case of the few American and the Barents Sea open coast localities, predicted based on the presence or absence of large rivers nearby.…”