Population genomics of rapidly invading lionfish in the Caribbean reveals signals of range expansion in the absence of spatial population structure.

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bors, E. K., Herrera, S., Morris, J. A., Jr., & Shank, T. M. Population genomics of rapidly invading lionfish in the Caribbean reveals signals of range expansion in the absence of spatial population structure. Ecology and Evolution, 9(6), (2019):3306-3320, doi:10.1002/ece3.4952.Range expansions driven by global change and species invasions may have significant genomic, evolutionary, and ecological implications. During range expansions, strong genetic drift characterized by repeated founder events can result in decreased genetic diversity with increased distance from the center of the historic range, or the point of invasion. The invasion of the Indo‐Pacific lionfish, Pterois volitans, into waters off the US East Coast, Gulf of Mexico, and Caribbean Sea provides a natural system to study rapid range expansion in an invasive marine fish with high dispersal capabilities. We report results from 12,759 single nucleotide polymorphism loci sequenced by restriction enzyme‐associated DNA sequencing for nine P. volitans sampling areas in the invaded range, including Florida and other sites throughout the Caribbean, as well as mitochondrial control region D‐loop data. Analyses revealed low to no spatially explicit metapopulation genetic structure, which is partly consistent with previous finding of little structure within ocean basins, but partly divergent from initial reports of between‐basin structure. Genetic diversity, however, was not homogeneous across all sampled sites. Patterns of genetic diversity correlate with invasion pathway. Observed heterozygosity, averaged across all loci within a population, decreases with distance from Florida while expected heterozygosity is mostly constant in sampled populations, indicating population genetic disequilibrium correlated with distance from the point of invasion. Using an FST outlier analysis and a Bayesian environmental correlation analysis, we identified 256 and 616 loci, respectively, that could be experiencing selection or genetic drift. Of these, 24 loci were shared between the two methods.We thank the many participants of the Gulf and Caribbean Fisheries Institute for providing lionfish samples from around the Caribbean region, as well as Dr. Bernard Castillo at the University of the Virgin Islands and Kristian Rogers at the Biscayne Bay National Park. We would like to acknowledge Alex Bogdanoff at NOAA, Beaufort NC, for assistance with sample acquisition; Camrin Braun at WHOI, for assistance with the calculation of oceanic distances between sites; Dr. Tom Schultz at Duke Marine Lab and Dr. Margaret Hunter at USGS for discussions concerning ongoing population genetic projects; and Jack Cook at the WHOI Graphics department for his assistance in generating maps of the study area. We would like to extend a special thank you to Dr. John Wakeley of Harvard University for assistance in the interpretation of data. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant No. 1122374. Sequencing funding was provided in part by the PADI Foundation Grant No. 14904. Additional research support was provided by the Woods Hole Oceanographic Institution (WHOI) Ocean Ventures Fund, the Coastal Ocean Institute at WHOI, the National Science Foundation (OCE‐1131620 to TMS), and the James Education Fund for Ocean Exploration within the Ocean Exploration Institute at WHOI. Publication of this paper was supported, in part, by the Henry Mastin Graduate Student Fund administered by the Oregon State University Department of Fisheries and Wildlife. Finally, we sincerely thank the reviewers and editors who helped to strengthen this manuscript

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