Evolutionary change during experimental ocean acidification

Abstract

Rising atmospheric carbon dioxide (CO2) conditions are driving unprecedented changes in seawater chemistry, resulting in reduced pH and carbonate ion concentrations in the Earth's oceans. This ocean acidification has negative but variable impacts on individual performance in many marine species. However, little is known about the adaptive capacity of species to respond to an acidified ocean, and, as a result, predictions regarding future ecosystem responses remain incomplete. Here we demonstrate that ocean acidification generates striking patterns of genome-wide selection in purple sea urchins (Strongylocentrotus purpuratus) cultured under different CO2 levels. We examined genetic change at 19,493 loci in larvae from seven adult populations cultured under realistic future CO2 levels. Although larval development and morphology showed little response to elevated CO2, we found substantial allelic change in 40 functional classes of proteins involving hundreds of loci. Pronounced genetic changes, including excess amino acid replacements, were detected in all populations and occurred in genes for biomineralization, lipid metabolism, and ion homeostasis--gene classes that build skeletons and interact in pH regulation. Such genetic change represents a neglected and important impact of ocean acidification that may influence populations that show few outward signs of response to acidification. Our results demonstrate the capacity for rapid evolution in the face of ocean acidification and show that standing genetic variation could be a reservoir of resilience to climate change in this coastal upwelling ecosystem. However, effective response to strong natural selection demands large population sizes and may be limited in species impacted by other environmental stressors.

Fig. 1.

Growth and morphometrics of sea urchin larvae cultured at control pCO₂ (400 µatm; black bars) vs. elevated pCO₂ (900 µatm; gray bars). Results are from larvae collected on days 11, 13, 15, and 17 (postfertilization) of trial 1. Responses to CO₂ seldom differed among the four populations (ANOVA, CO₂ × population; P > 0.05), so results shown are for responses pooled across populations (n = 12–14 culture jars per CO₂ level). Drawings (based on ref. 49) illustrate the morphological features quantified. (A) Postoral rod length. (B) Postoral rod and body rod length. (C) Anterolateral rod length. (D) Body length at midline. (E) Stomach area. Error bars are +1 SE. *P < 0.05; **P < 0.005 (significant differences between CO₂ levels; ANOVA).

Fig. 2.

Change in allele frequency in 5 of 30 outlier polymorphisms with high treatment effect in response to elevated CO₂ (A–E; P < 0.0001) and one randomly selected polymorphism (F; P > 0.05). (A and B) Alanine aminotransferase 2 enzyme (A) and splicing factor 3b (B) show the greatest treatment effects and perform functions related to metabolism and RNA processing, respectively. (C) Echs1 protein (enoyl CoA hydratase) is a mitochondrial enzyme involved in lipid metabolism. (D and E) FGD6 regulates the cytoskeleton and cell shape (D), and the glutamate receptor is involved in ion transport (E). Red lines mark observed change in allele frequency between control (400 µatm–days 1 and 7 averaged) and treatment (900 µatm–day 7) cultures. An empirical null distribution (gray) was generated by the random permutation of samples and recalculation of treatment effect. These five genes span the diverse protein functions and range of change in allele frequency represented across the 30 outliers. See Table S3 for the complete list of 30 outlier genes with protein function annotations.

Fig. 3.

Summary schematic of predicted evolutionary forces and enrichment results (A) and observed protein function enrichment results for greater changes in allele frequency (B) between the four day and treatment combinations (populations averaged for each day and treatment). Arrows represent comparisons of allele frequencies between day and treatment combinations. Of the genes in enriched categories, 71% were in common after 1 d at 900 µatm and after 7 d at 900 µatm (Fig. 5).

Fig. 4.

Consistent changes in allele frequencies associated with elevated CO₂ in multiple SNPs within single genes. Genes are in functionally enriched categories related to lipid metabolism (highlighted in red), ion homeostasis (blue), or both (purple); these six genes represent many in these categories that have multiple SNPs per gene showing greater than average change in allele frequency and are enriched for response to high CO₂ after 1 and 7 d. For 13 of 18 SNPs shown, changes in allele frequency are in the same direction after 1 d in elevated CO₂ conditions (day 1–900 µatm) as after 7 d in elevated CO₂ conditions (day 7–900 µatm) relative to allele frequencies in the wild (day 1–400 µatm). See Fig. 5 for data from SNPs in genes enriched for change after both 1 and 7 d in high CO₂ culture. Numbers indicate base position of the polymorphism in the coding region of the gene. Bars are mean frequencies (±SE) in seven populations. Asterisks mark amino acid changing polymorphisms.

Fig. 5.

Selection in action. There is a greater magnitude of change in allele frequency after 7 d than 1 d in elevated CO₂ conditions (red and black, respectively) in the same suite of genes. Change in allele frequency for the same set of 4,782 SNPs comparing day 1–400 µatm with day 1–900 µatm (black) and day 1–900 µatm with day 7–900 µatm (red) are represented in each distribution. These SNPs are in the 601 genes in common (71% overlap) in functional categories enriched for change in allele frequency in response to high CO₂ conditions after 1 and 7 d (Tables S4 and S5). Distributions are significantly different (K-S test; P < 0.0001).