Rare genetic variation and balanced polymorphisms are important for survival in global change conditions

Abstract

17Standing genetic variation is important for population persistence in extreme 18 environmental conditions. While some species may have the capacity to adapt to predicted 19 average future global change conditions, the ability to survive extreme events is largely 20 unknown. We used single generation selection experiments on hundreds of thousands of 21Strongylocentrotus purpuratus sea urchin larvae generated from wild-caught adults to identify 22 adaptive genetic variation responsive to moderate (pH 8.0) and extreme (pH 7.5) low pH 23 conditions. Sequencing genomic DNA from pools of larvae, we identified consistent changes in 24 allele frequencies across replicate cultures of both conditions and observed increased linkage 25 disequilibrium around selected loci, revealing selection on recombined standing genetic 26 variation. We found that loci responding uniquely to either selection regime were at low starting 27 allele frequencies while variants that responded to both pH conditions (11.6% of selected 28 variants) started at high frequencies. Loci under selection performed functions related to 29 energetics, pH tolerance, cell growth, and actin/cytoskeleton dynamics. These results highlight 30 that persistence in future conditions will require two classes of genetic variation: common, pH-31 responsive variants maintained by balancing selection in a heterogeneous environment, and rare 32 variants, particularly for extreme conditions, that must be maintained by large population sizes. 33

Present and Future Adaptation of Marine Species Assemblages: DNA-Based Insights into Climate Change from Studies of Physiology, Genomics, and Evolution

“…The experimental acidification in the studies above utilized a low pH treatment within the bounds of what is frequently experienced by purple sea urchins in nature, pH 7.8 (900 ppm pCO 2 ; Hofmann et al, 2011;Evans et al, 2013Evans et al, , 2015. Rearing larvae in moderate (pH 8.0) and extreme (pH 7.5) low pH conditions, Brennan et al (2019) found purple urchin larvae to have adaptive standing genetic variation for survival in extreme low pH conditions that show correlated responses to moderate low pH conditions (Figure 4; Brennan et al, 2019). Interestingly, two classes of genetic variation emerge as useful for survival in low pH conditions: (1) variants that respond to both pH conditions and are maintained at high frequency in natural populations, and (2) relatively rare genetic variants that respond to either pH condition (Brennan et al, 2019).…”

“…Rearing larvae in moderate (pH 8.0) and extreme (pH 7.5) low pH conditions, Brennan et al (2019) found purple urchin larvae to have adaptive standing genetic variation for survival in extreme low pH conditions that show correlated responses to moderate low pH conditions (Figure 4; Brennan et al, 2019). Interestingly, two classes of genetic variation emerge as useful for survival in low pH conditions: (1) variants that respond to both pH conditions and are maintained at high frequency in natural populations, and (2) relatively rare genetic variants that respond to either pH condition (Brennan et al, 2019). These results emphasize (1) the importance of environmental variation that potentially leads to balancing selection in the maintenance of common adaptive variants (Levene, 1953), and (2) the importance of large population sizes for the maintenance of rare genetic variation that is adaptive in global change conditions.…”

“…Modified from Pespeni et al (2013c) (b) Correlated changes in allele frequency in moderate and extreme low-pH responsive alleles. FromBrennan et al (2019) The geographic distribution of different levels of genetic structure. Twenty-two of 50 species of marine invertebrates show some level of significant structure along the North American west coast.…”