Population genomics and adaptive evolution in the purple sea urchin, Strongylocentrotus purpuratus [electronic resource]
Keywords: Biology.

The overarching goal of this thesis research has been to determine if, how and when natural selection might act to lead to local adaptation in a high gene flow species distributed along a strong environmental gradient. The purple sea urchin lives from the cold waters of Alaska to the warmer waters of Baja California, Mexico. In accordance with their high dispersal potential as larvae, previous studies have found no population structure along the species range in mitochondrial and allozyme markers. This combination of potentially strong environmental selection and high neutral gene flow presents a stringent test for selection that requires a genome-wide approach in order to detect signals of selection. Restriction Site Tiling Analysis: accurate discovery and quantitative genotyping of genome-wide polymorphisms using nucleotide arrays (Pespeni et al. 2010 Genome Biology). Genome scanning approaches applied in model organisms are too costly and inaccurate for highly heterozygous out-crossed wild populations, while approaches applied in non-model organisms (e.g. AFLP and microsatellite markers) are anonymous with respect to gene function. To address this challenge, I developed a generally applicable technique, Restriction Site Tiling Analysis (RSTA), which uses a single genome sequence and high-density microarrays to detect polymorphisms and yield genotype data. The approach is 99.6% accurate. Genome scanning techniques such as this promise to generate significant advances in the identification of functionally important traits in ecologically interesting species. Population genomics reveals genetic differentiation in a high gene flow species, the purple sea urchin (Pespeni et al. 2010 Genome Biology). I compared the genomes of 20 individuals from Boiler Bay, Oregon and San Diego, California using 20 RSTA arrays. This experiment identified 12,431 polymorphisms and yielded individual genotype data for each locus. Principle components analysis spatially separated northern from southern urchin individuals. The observed FST distribution was significantly broader than 10,000 simulated panmictic distributions, revealing some 2.5-5% of loci driving the signal of differentiation. Outlier analyses detected 4 loci that may be subject to strong divergent selection, two transcription factors and two transporter proteins. Taken together these results show a strong signal of population differentiation in a small but significant fraction of the purple sea urchin genome. Genome-wide polymorphisms show the targets and timing of natural selection in the purple sea urchin (Pespeni et al. submitted). To determine if signals of population differentiation were due to drift or selection, I tested for the non-random distribution of high FST and high heterozygosity polymorphisms across the genome with respect to gene function and the timing- and tissue-specificity of gene expression. I found 1) highly significant enrichment for high FST polymorphisms in the regulatory regions of proteolysis genes, 2) over-representation of high FST polymorphisms in the coding regions of genes expressed exclusively in larvae and during development, and 3) highly significant enrichment for high heterozygosity polymorphisms dominated by immunity related proteins. These results illustrate the potential importance of adaptive gene regulation and amino acid divergence and the potential roles of divergent and balancing selection in different parts of the genome along the species range. Selection without clines: Molecular signatures of adaptation in the highly dispersing purple sea urchin, Strongylocentrotus purpuratus (Pespeni and Palumbi, in prep). The balance between gene flow and natural selection may result in distinct signals of selection depending on the environmental heterogeneity across the landscape of the species range. In this study I directly sequence 6 putative selected and 2 putative conserved or neutral nuclear genes in 165 purple sea urchins from 6 populations along the purple sea urchin species range from Canada to Mexico. I find signals of selection in all six candidate genes and little to no signal of selection in control genes. Results show: 1) several signals of selection at the nucleotide and amino acid levels, 2) clinal patterns in the cubilin receptor gene and in a Serine to Glycine polymorphism in the gaba-b receptor, and 3) a signal of local adaptation in San Diego purple sea urchins. Overall, patterns of genetic variation match predictions based on spatially balancing selection across a heterogeneous landscape and illustrate the value of following up on candidate loci identified in a genome-wide scan for selection.