Ecological diversification of sea catfishes is accompanied by genome-wide signatures of positive selection

Melissa Rincon-Sandoval, Rishi De-Kayne, Stephen D. Shank, Stacy Pirro, Alfred Ko’ou, Linelle Abueg, Alan Tracey, Jackie Mountcastle, Brian O’Toole, Jennifer Balacco, Giulio Formenti, Erich D. Jarvis, Dahiana Arcila, Sergei L. Kosakovsky Pond, Aaron Davis, Devin D. Bloom and Ricardo Betancur-R ()
Additional contact information
Melissa Rincon-Sandoval: The University of Oklahoma
Rishi De-Kayne: University of California Santa Cruz
Stephen D. Shank: Temple University
Stacy Pirro: Iridian Genomes
Alfred Ko’ou: University 134
Linelle Abueg: The Rockefeller University
Alan Tracey: The Rockefeller University
Jackie Mountcastle: The Rockefeller University
Brian O’Toole: The Rockefeller University
Jennifer Balacco: The Rockefeller University
Giulio Formenti: The Rockefeller University
Erich D. Jarvis: The Rockefeller University
Dahiana Arcila: University of California San Diego
Sergei L. Kosakovsky Pond: Temple University
Aaron Davis: James Cook University
Devin D. Bloom: Western Michigan University
Ricardo Betancur-R: University of California San Diego

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract Habitat transitions have shaped the evolutionary trajectory of many clades. Sea catfishes (Ariidae) have repeatedly undergone ecological transitions, including colonizing freshwaters from marine environments, leading to an adaptive radiation in Australia and New Guinea alongside non-radiating freshwater lineages elsewhere. Here, we generate and analyze one long-read reference genome and 66 short-read whole genome assemblies, in conjunction with genomic data for 54 additional species. We investigate how three major ecological transitions have shaped genomic variation among ariids over their ~ 50 million-year evolutionary history. Our results show that relatively younger freshwater lineages exhibit a higher incidence of positive selection than their more ancient marine counterparts. They also display a larger disparity in body shapes, a trend that correlates with a heightened occurrence of positive selection on genes associated with body size and elongation. Although positive selection in the Australia and New Guinea radiation does not stand out compared to non-radiating lineages overall, selection across the prolactin gene family during the marine-to-freshwater transition suggests that strong osmoregulatory adaptations may have facilitated their colonization and radiation. Our findings underscore the significant role of selection in shaping the genome and organismal traits in response to habitat shifts across macroevolutionary scales.

Date: 2024
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DOI: 10.1038/s41467-024-54184-3

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