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Ecological divergence in sympatry causes gene misexpression in hybrids
Author(s) -
McGirr Joseph A.,
Martin Christopher H.
Publication year - 2020
Publication title -
molecular ecology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 2.619
H-Index - 225
eISSN - 1365-294X
pISSN - 0962-1083
DOI - 10.1111/mec.15512
Subject(s) - biology , sympatry , allopatric speciation , sympatric speciation , reproductive isolation , ecological speciation , adaptive radiation , evolutionary biology , coregonus , gene , hybrid , ecology , genetics , gene flow , population , genetic variation , phylogenetics , demography , botany , sociology , fishery , fish <actinopterygii>
Ecological speciation occurs when reproductive isolation evolves as a byproduct of adaptive divergence between populations. Selection favouring gene regulatory divergence between species could result in transgressive levels of gene expression in F1 hybrids that may lower hybrid fitness. We combined 58 resequenced genomes with 124 transcriptomes to identify patterns of hybrid gene misexpression that may be driven by adaptive regulatory divergence within a young radiation of Cyprinodon pupfishes, which consists of a dietary generalist and two trophic specialists—a molluscivore and a scale‐eater. We found more differential gene expression between closely related sympatric specialists than between allopatric generalist populations separated by 1,000 km. Intriguingly, 9.6% of genes that were differentially expressed between sympatric species were also misexpressed in F1 hybrids. A subset of these genes were in highly differentiated genomic regions and enriched for functions important for trophic specialization, including head, muscle and brain development. These regions also included genes that showed evidence of hard selective sweeps and were significantly associated with oral jaw length—the most rapidly diversifying skeletal trait in this radiation. Our results indicate that divergent ecological selection in sympatry can contribute to hybrid gene misexpression which may act as a reproductive barrier between nascent species.