Genetic differences that accumulate between species can result from the action of either random genetic drift or natural selection. However, the relative importance of drift vs. selection in causing the differences observed between species remains poorly understood. This study will use closely related species of Strongylocentrotid sea urchins to address several fundamental questions in the field of evolutionary genetics. First, what proportion of the genetic changes observed between species has been caused by natural selection? Second, have the selected changes occurred recently within existing species or do they reflect adaptation occurring further back in time? Third, what are the specific DNA regions that show evidence of past natural selection and can these changes be explained by known biological processes (such as reproduction or disease resistance)? The PIs will use complete genome sequences from eight species of sea urchin to investigate these questions. Their results will provide new insights into the importance of selection as a force for genome evolution.
This project will initiate collaborations between biologists and biological statisticians. Undergraduates will participate in the project and learn techniques of experimental design and data analysis. The project places a high priority on the dissemination of computational and analytic tools to the broader scientific community.
All adaptive evolution ultimately occurs by the substitutions of mutations in DNA sequences driven by the process of natural selection. However, mutations may also accumulate between species by purely random processes (a mechanism called random genetic drift) and hence understanding the relative roles of drift versus selection has been a focus of molecular evolutionary studies for many decades. Recent advances in next-generation DNA sequencing technologies have provided exciting new opportunities to study adaptive molecular evolution using complete genome data (i.e., the complete assembly of genes in a species). The focus of our project was to investigate the genome-wide signals of natural selection in a novel group of marine invertebrates (nine sea urchin species belonging to the family Strongylocentrotidae). One important factor that affects the efficacy of natural selection is population size. Theory predicts that in species with extremely large populations (such as sea urchins), natural selection can effectively control the adaptive substitution of mutations with very small effects. Our project successfully documented the action of extremely weak selection on the preferred usage of synonymous codons (that arise from the degeneracy of the genetic code). We obtained evidence for selection favoring the efficient and/or accurate translation of messenger RNA intermediaries into proteins as well as the three-dimensional stability of these RNA intermediaries. Our study also suggested that the patterns of preferred codon usage cannot be explained by mutational bias, a mechanism widely documented in other groups such as mammals. Theory also predicts that species with large population sizes can experience more efficient adaptive molecular evolution of their protein-coding genes (a process called positive Darwinian selection). We found that approximately 28% of sea urchin protein-coding genes experienced positive selection, which is similar to that previously reported for fruit flies (33%) but dramatically higher than that observed for mammals (3%). Positively selected genes were enriched for those functioning in the innate immune system, cell adhesion, biomineralization, and fertilization (both sperm and egg proteins). Although the sea urchins studied had diversified into habitats varying in temperature, depth, and available food resources, we were unable to document any differences in the rates of adaptive molecular evolution to these different environments. Overall, our results suggest that natural selection has played a pervasive role in shaping the genome-wide patterns of molecular evolution in sea urchins.
