TY - JOUR
T1 - Genomic resources for darters (Percidae: Etheostominae) provide insight into postzygotic barriers implicated in speciation
AU - Moran, Rachel L.
AU - Catchen, Julian M.
AU - Fuller, Rebecca C.
N1 - Funding Information:
The treatment of animals used in this study was in compliance with the University of Illinois Institutional Animal Care and Use Committee (IACUC) under protocol no. 17031. Collection of wild fish was approved by the Illinois Department of Natural Resources under Scientific Collecting Permit A16.4035. We thank Chris Cheng, Angel Rivera-Colón, and Niraj Rayamajhi for assistance with molecular work and RADseq library preparation. We are grateful to two anonymous reviewers and the McGaugh and Brandvain labs for their helpful comments on earlier versions of this article. We thank Floragenex, the University of Minnesota Genomics Center, and the University of Illinois at Urbana-Champaign Roy J. Carver Biotechnology Center for their consultation on this project and for performing the sequencing. This work was supported by the School of Integrative Biology (SIB) and the Program in Ecology, Evolution and Conservation Biology (PEEC) at the University of Illinois Urbana-Champaign (PEEC Summer Research Grant to R.L.M., SIB Harley J. van Cleave Award to R.L.M., SIB Hawkes Award to R.C.F. and J.M.C.), and by a Sigma Xi Grant-in-Aid of Research, a Society for Integrative and Comparative Biology Grant in Aid of Research, an American Society of Naturalists Student Research Award, a Society for the Study of Evolution Rosemary Grant Advanced Award, and a National Science Foundation Doctoral Dissertation Improvement Grant (IOS 1701676) to R.L.M. R.L.M. was supported a National Institute of Health Science Education Partnership Award (R25OD020203-01A1). J.M.C. was supported by a National Science Foundation Award (OPP 1645087). Illumina and PacBio reads have been submitted to NCBI SRA, the annotated whole genome assembly has been submitted to NCBI Genomes, and the transcriptome assembly has been submitted to NCBI TSA under BioProject accession number PRJNA556880.
PY - 2020/3/1
Y1 - 2020/3/1
N2 - Comparative genomic approaches are increasingly being used to study the evolution of reproductive barriers in nonmodel species. Although numerous studies have examined prezygotic isolation in darters (Percidae), investigations into postzygotic barriers have remained rare due to long generation times and a lack of genomic resources. Orangethroat and rainbow darters naturally hybridize and provide a remarkable example of male-driven speciation via character displacement. Backcross hybrids suffer from high mortality, which appears to promote behavioral isolation in sympatry. To investigate the genomic architecture of postzygotic isolation, we used Illumina and PacBio sequencing to generate a chromosome-level, annotated assembly of the orangethroat darter genome and high-density linkage maps for orangethroat and rainbow darters. We also analyzed genome-wide RADseq data from wild-caught adults of both species and laboratory-generated backcrosses to identify genomic regions associated with hybrid incompatibles. Several putative chromosomal translocations and inversions were observed between orangethroat and rainbow darters, suggesting structural rearrangements may underlie postzygotic isolation. We also found evidence of selection against recombinant haplotypes and transmission ratio distortion in backcross hybrid genomes, providing further insight into the genomic architecture of genetic incompatibilities. Notably, regions with high levels of genetic divergence between species were enriched for genes associated with developmental and meiotic processes, providing strong candidates for postzygotic isolating barriers. These findings mark significant contributions to our understanding of the genetic basis of reproductive isolation between species undergoing character displacement. Furthermore, the genomic resources presented here will be instrumental for studying speciation in darters, the most diverse vertebrate group in North America.
AB - Comparative genomic approaches are increasingly being used to study the evolution of reproductive barriers in nonmodel species. Although numerous studies have examined prezygotic isolation in darters (Percidae), investigations into postzygotic barriers have remained rare due to long generation times and a lack of genomic resources. Orangethroat and rainbow darters naturally hybridize and provide a remarkable example of male-driven speciation via character displacement. Backcross hybrids suffer from high mortality, which appears to promote behavioral isolation in sympatry. To investigate the genomic architecture of postzygotic isolation, we used Illumina and PacBio sequencing to generate a chromosome-level, annotated assembly of the orangethroat darter genome and high-density linkage maps for orangethroat and rainbow darters. We also analyzed genome-wide RADseq data from wild-caught adults of both species and laboratory-generated backcrosses to identify genomic regions associated with hybrid incompatibles. Several putative chromosomal translocations and inversions were observed between orangethroat and rainbow darters, suggesting structural rearrangements may underlie postzygotic isolation. We also found evidence of selection against recombinant haplotypes and transmission ratio distortion in backcross hybrid genomes, providing further insight into the genomic architecture of genetic incompatibilities. Notably, regions with high levels of genetic divergence between species were enriched for genes associated with developmental and meiotic processes, providing strong candidates for postzygotic isolating barriers. These findings mark significant contributions to our understanding of the genetic basis of reproductive isolation between species undergoing character displacement. Furthermore, the genomic resources presented here will be instrumental for studying speciation in darters, the most diverse vertebrate group in North America.
KW - speciation
KW - hybridization
KW - postzygotic isolation
KW - genetic incompatibilities
KW - chromosomal rearrangements
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U2 - 10.1093/molbev/msz260
DO - 10.1093/molbev/msz260
M3 - Article
C2 - 31688927
SN - 0737-4038
VL - 37
SP - 711
EP - 719
JO - Molecular biology and evolution
JF - Molecular biology and evolution
IS - 3
M1 - msz260
ER -