Journal
MOLECULAR ECOLOGY
Volume 23, Issue 16, Pages 3944-3956Publisher
WILEY
DOI: 10.1111/mec.12720
Keywords
barrier to gene flow; evolutionary genomics; Gasterosteus aculeatus; genetic hitchhiking; genome scan; population divergence
Funding
- National Institute for Mathematical and Biological Synthesis (NSF) [EF-0830858]
- National Institutes of Health [GM56693]
- Natural Sciences and Engineering Research Council of Canada
- European Research Council
- Swiss National Science Foundation [CRSII3_136293, PZ00P3_126391/1]
- University of Basel
- Freiwillige Akademische Gesellschaft Basel
- Swiss National Science Foundation (SNF) [CRSII3_136293, PZ00P3_126391] Funding Source: Swiss National Science Foundation (SNF)
- Direct For Biological Sciences
- Div Of Biological Infrastructure [1300426] Funding Source: National Science Foundation
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Parallel adaptation is common and may often occur from shared genetic variation, but the genomic consequences of this process remain poorly understood. We first use individual-based simulations to demonstrate that comparisons between populations adapted in parallel to similar environments from shared variation reveal a characteristic genomic signature around a selected locus: a low-divergence valley centred at the locus and flanked by twin peaks of high divergence. This signature is initiated by the hitchhiking of haplotype tracts differing between derived populations in the broader neighbourhood of the selected locus (driving the high-divergence twin peaks) and shared haplotype tracts in the tight neighbourhood of the locus (driving the low-divergence valley). This initial hitchhiking signature is reinforced over time because the selected locus acts as a barrier to gene flow from the source to the derived populations, thus promoting divergence by drift in its close neighbourhood. We next empirically confirm the peak-valley-peak signature by combining targeted and RAD sequence data at three candidate adaptation genes in multiple marine (source) and freshwater (derived) populations of threespine stickleback. Finally, we use a genome-wide screen for the peak-valley-peak signature to discover additional genome regions involved in parallel marine-freshwater divergence. Our findings offer a new explanation for heterogeneous genomic divergence and thus challenge the standard view that peaks in population divergence harbour divergently selected loci and that low-divergence regions result from balancing selection or localized introgression. We anticipate that genome scans for peak-valley-peak divergence signatures will promote the discovery of adaptation genes in other organisms.
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