Csenge Petak, Lapo Frati, Reid S. Brennan, and Melissa H. Pespeni
The genetic basis of local adaptation to environmental variability is poorly understood, and few studies have investigated genetic regulatory regions for their role in local adaptation to environmental variability. However, mutations in these regions may be important for adaptation to variability, particularly for broadly distributed species across spatially and temporally varying environments. Variation in regulatory regions can change the expression of nearby genes, facilitating local adaptation. These regulatory regions may also underlie molecular mechanisms of phenotypic plasticity, critical for resilience to sudden environmental change.
Csenge Petak et al. of the University of Vermont, Burlington, addressed this knowledge gap by testing for signatures of local adaptation to temporal pH variability in the purple sea urchin. The purple sea urchin range encompasses a heterogeneous seascape, where northern Pacific coastal populations experience more variability in pH and higher frequency of low pH events due to upwelling. Importantly, low pH conditions are negatively associated with biomineralization ability and body size of urchin larvae, which can impede development.
In their study, Petak et al. sequenced whole genomes of 140 purple sea urchin individuals collected from seven range-wide sites, ranging from Fogarty Creek, OR, to San Diego, CA. Despite finding no population structure across 1,700 km of seascape, they found that putatively adaptive genetic variants were strongly correlated with pH variability, associated with biomineralization and ion homeostasis, and largely found in genetic regulatory regions. This is an interesting paradox where extensive gene flow exists, but there are also population-level differences at specific loci correlated with adaptation to local environmental variability. The paradox could be explained by high genetic diversity in combination with low linkage disequilibrium, or high-fecundity, large populations that are responsive to strong selection.
While many of the genetic variants associated with local adaptation to pH variability were found in regulatory regions, some were found in genes. However, putatively adaptive variants were uncommon in proteins connected in a protein-protein interaction network and in genes expressed during early development. Given this, Petak et al. conclude that loci with low pleiotropic effects are particularly important for local adaptation to environmental variability.
In conclusion, the authors found that genetic variation in regulatory regions and in genes of low pleiotropic effect was driving local adaptation to temporal pH variability. Notably, genetic variation involved in local adaptation to pH variability was not found in key developmental genes. This set of results implies that the diversity of genetic variation found in purple sea urchins contributes to plastic responses which promote survival in low pH conditions. In a broader context, the genetic variation observed in regulatory regions will likely play a crucial role in potential future adaptation to ocean acidification from global climate change.
This article was presented as part of the 2022 Vice Presidential Symposium at the annual meetings of the American Society of Naturalists in Cleveland, Ohio.