Signs of Adaptation to Local pH Conditions across an Environmental Mosaic in the California Current Ecosystem

Abstract

Little is known about the potential for rapid evolution in natural populations in response to the high rate of contemporary climatic change. Organisms that have evolved in environments that experience high variability across space and time are of particular interest as they may harbor genetic variation that can facilitate evolutionary response to changing conditions. Here we review what is known about genetic capacity for adaptation in the purple sea urchin, Strongylocentrotus purpuratus, a species that has evolved in the upwelling ecosystem of the Northeast Pacific Ocean. We also present new results testing for adaptation to local pH conditions in six populations from Oregon to southern California. We integrate data on 19,493 genetic polymorphisms with data on local pH conditions. We find correlations between allele frequency and rank average time spent at pH <7.8 in 318 single-nucleotide polymorphisms in 275 genes. Two of the genes most correlated with local pH are a protein associated with the cytoskeleton and a proton pump, with functional roles in maintenance of cell volume and with internal regulation of pH, respectively. Across all loci tested, high correlations with local pH were concentrated in genes related to transport of ions, biomineralization, lipid metabolism, and cell-cell adhesion, functional pathways important for maintaining homeostasis at low pH. We identify a set of seven genes as top candidates for rapid evolutionary response to acidification of the ocean. In these genes, the putative low-pH-adapted allele, based on allele frequencies in natural populations, rapidly increases in frequency in purple sea urchin larvae raised at low pH. We also found that populations from localities with high pH show a greater change in allele frequency toward putative low-pH-adapted alleles under experimental acidification, compared with low-pH populations, suggesting that both natural and artificial selection favor the same alleles for response to low pH. These results illustrate that purple sea urchins may be adapted to local pH and suggest that this species may possess the genetic capacity for rapid evolution in response to acidification. This adaptive capacity likely comes from standing genetic variation maintained in nature by balancing selection across the spatial and temporal environmental mosaic that characterizes the California Current Ecosystem.

Exploring local adaptation and the ocean acidification seascape – studies in the California Current Large Marine Ecosystem

“…Recent efforts to characterize the nearshore carbonate chemistry of the California Current system (Fassbender et al, 2011;Feely et al, 2008;Hauri et al, 2009) suggest that biota of this region experience natural variation in pH due to latitudinally and temporally variable upwelling. Results from the OMEGAS sensor network indicate that acidification of coastal waters extends into the nearshore environments of the CCLME with low pH, undersaturated water reaching the rocky intertidal zone Pespeni et al, 2013c;Chan et al, 2014). Importantly, these data indicate that biota in the plankton and benthic marine organisms on shore face an exposure regime to low pH and undersaturated waters that is tremendously dynamic in time and space Chan et al, 2014).…”

“…1). Descriptions of intertidal sensors and sites and mooring configurations can be found elsewhere (Washburn et al, 2011;Evans et al, 2013;Pespeni et al, 2013c;Adams et al, 2013), but briefly, pH records shown in Fig. 2 are from custom-designed Durafet ® -based sensors deployed in open coast, intertidal rocky habitats to record at 10 min intervals.…”

Biochemical adaptation to ocean acidification

“…Local adaptation and differential selection of specific genotypes under acidified conditions has been shown to govern allele frequency of top candidate genes for OA responses (Pespeni et al, 2013). Purple urchin larvae (Strongylocentrotus purpuratus) locally adapted to less-acidic sites show this increase in allele frequency when exposed to pH stress, indicating that the adaptive capacity may be a result of standing genetic variation across the spatial-temporal habitats (Pespeni et al, 2013). Intraspecific comparisons with differing thermal habitats show how thermal plasticity can shape responses to pH stress.…”

“…Lohbeck et al, 2013;Reusch and Boyd, 2013). Comparative studies in organisms ( populations, species) living across ecological gradients in pH use a 'space for time' argument in inferring adaptive responses (Calosi et al, 2013, Pespeni et al, 2013. In this article, we review the physiological, biochemical and molecular differences observed in those responses to seek a deeper understanding of whether there is a generalizable 'biochemical adaptation' to ocean acidification.…”

Evolution of Marine Organisms under Climate Change at Different Levels of Biological Organisation

“…One possible approach for investigating the selection response using naturally assembled communities is through the use of natural analogues for future climate change, such as CO2 vents [26], or coastal upwelling sites [114,181]. These areas provide long-term chronic exposure to novel environmental conditions, and allow experimental work to capture an organism's response in fitness-related traits [26,182], such as reproductive success.…”