Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags.

Paul A Hohenlohe,Susan Bassham,Paul D Etter,Eric A Johnson,William A Cresko,Nicholas Stiffler,David J Begun

doi:10.1371/journal.pgen.1000862

Paul A Hohenlohe, Susan Bassham + Show 5 more

Open Access

https://doi.org/10.1371/journal.pgen.1000862

Copy DOI

Journal: PLoS genetics	Publication Date: Feb 26, 2010
Citations: 1387	License type: CC BY 4.0

Affiliation: University of Oregon

Abstract

Next-generation sequencing technology provides novel opportunities for gathering genome-scale sequence data in natural populations, laying the empirical foundation for the evolving field of population genomics. Here we conducted a genome scan of nucleotide diversity and differentiation in natural populations of threespine stickleback (Gasterosteus aculeatus). We used Illumina-sequenced RAD tags to identify and type over 45,000 single nucleotide polymorphisms (SNPs) in each of 100 individuals from two oceanic and three freshwater populations. Overall estimates of genetic diversity and differentiation among populations confirm the biogeographic hypothesis that large panmictic oceanic populations have repeatedly given rise to phenotypically divergent freshwater populations. Genomic regions exhibiting signatures of both balancing and divergent selection were remarkably consistent across multiple, independently derived populations, indicating that replicate parallel phenotypic evolution in stickleback may be occurring through extensive, parallel genetic evolution at a genome-wide scale. Some of these genomic regions co-localize with previously identified QTL for stickleback phenotypic variation identified using laboratory mapping crosses. In addition, we have identified several novel regions showing parallel differentiation across independent populations. Annotation of these regions revealed numerous genes that are candidates for stickleback phenotypic evolution and will form the basis of future genetic analyses in this and other organisms. This study represents the first high-density SNP–based genome scan of genetic diversity and differentiation for populations of threespine stickleback in the wild. These data illustrate the complementary nature of laboratory crosses and population genomic scans by confirming the adaptive significance of previously identified genomic regions, elucidating the particular evolutionary and demographic history of such regions in natural populations, and identifying new genomic regions and candidate genes of evolutionary significance.

Highlights

Population genetics provides a rich and mathematically rigorous framework for understanding evolutionary processes in natural populations
Each site is expected to produce at most two Restriction-site Associated DNA (RAD) tags, and our sequencing effort recovered a large proportion of the expected RAD tags (Table S1)
Because of the dense coverage of single nucleotide polymorphisms (SNPs) across the genome, and our ability to sample numerous individuals in multiple populations, our findings are a significant extension of previous work

Summary

Introduction

Population genetics provides a rich and mathematically rigorous framework for understanding evolutionary processes in natural populations. In addition to estimating genomewide averages for such statistics, we can identify specific genomic regions that exhibit significantly increased or decreased differentiation among populations, indicating regions that have likely been under strong diversifying or stabilizing natural selection [9,30,31,32,33,34,35,36,37,38,39,40,41] These signatures of selection can be used to identify candidate pathways, genes and alleles for targeted functional analyses [42,43,44,45,46,47]

Methods

Results

Discussion

Conclusion