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

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Environmental variation experienced by a species across space and time can promote the maintenance of genetic diversity that may be adaptive in future global change conditions. Selection experiments have shown that purple sea urchin, Strongylocentrotus purpuratus, populations have adaptive genetic variation for surviving pH conditions at the “edge” (pH 7.5) of conditions experienced in nature. However, little is known about whether populations have genetic variation for surviving low-pH events beyond those currently experienced in nature or how variation in pH conditions affects organismal and genetic responses. Here, we quantified survival, growth, and allele frequency shifts in experimentally selected developing purple sea urchin larvae in static and variable conditions at three pH levels: pH 8.1 (control), pH 7.5 (edge-of-range), and pH 7.0 (extreme). Variable treatments recovered body size relative to static treatments, but resulted in higher mortality, suggesting a potential tradeoff between survival and growth under pH stress. However, within each pH level, allele frequency changes were overlapping between static and variable conditions, suggesting a shared genetic basis underlying survival to mean pH regardless of variability. In contrast, genetic responses to pH 7.5 (edge) versus pH 7.0 (extreme) conditions were distinct, indicating a unique genetic basis of survival. In addition, loci under selection were more likely to be in exonic regions than regulatory, indicating that selection targeted protein-coding variation. Loci under selection in variable pH 7.5 conditions, more similar to conditions periodically experienced in nature, performed functions related to lipid biosynthesis and metabolism, while loci under selection in static pH 7.0 conditions performed functions related to transmembrane and mitochondrial processes. While these results are promising in that purple sea urchin populations possess genetic variation for surviving extreme pH conditions not currently experienced in nature, they caution that increased acidification does not result in a linear response but elicits unique physiological stresses and survival mechanisms.

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

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