Ecological diversification of sea catfishes is accompanied by genome-wide signatures of positive selection
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-radiati...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2024-11-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-54184-3 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849221094341345280 |
|---|---|
| author | 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 Ricardo Betancur-R |
| author_facet | 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 Ricardo Betancur-R |
| author_sort | Melissa Rincon-Sandoval |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-94d7d6badae4477888b08089ebcb2c77 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-94d7d6badae4477888b08089ebcb2c772024-11-24T12:32:59ZengNature PortfolioNature Communications2041-17232024-11-0115111510.1038/s41467-024-54184-3Ecological diversification of sea catfishes is accompanied by genome-wide signatures of positive selectionMelissa Rincon-Sandoval0Rishi De-Kayne1Stephen D. Shank2Stacy Pirro3Alfred Ko’ou4Linelle Abueg5Alan Tracey6Jackie Mountcastle7Brian O’Toole8Jennifer Balacco9Giulio Formenti10Erich D. Jarvis11Dahiana Arcila12Sergei L. Kosakovsky Pond13Aaron Davis14Devin D. Bloom15Ricardo Betancur-R16Department of Biology, The University of OklahomaDepartment of Ecology and Evolutionary Biology, University of California Santa CruzInstitute for Genomics and Evolutionary Medicine, Temple UniversityIridian GenomesSchool of Natural & Physical Sciences, The University of Papua New Guinea, University 134Vertebrate Genome Lab, The Rockefeller UniversityVertebrate Genome Lab, The Rockefeller UniversityVertebrate Genome Lab, The Rockefeller UniversityVertebrate Genome Lab, The Rockefeller UniversityVertebrate Genome Lab, The Rockefeller UniversityVertebrate Genome Lab, The Rockefeller UniversityVertebrate Genome Lab, The Rockefeller UniversityScripps Institution of Oceanography, University of California San DiegoInstitute for Genomics and Evolutionary Medicine, Temple UniversityCentre for Tropical Water and Aquatic Ecosystem Research, School of Marine and Tropical Biology, James Cook UniversityDepartment of Biological Sciences, Western Michigan UniversityScripps Institution of Oceanography, University of California San DiegoAbstract 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.https://doi.org/10.1038/s41467-024-54184-3 |
| spellingShingle | 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 Ricardo Betancur-R Ecological diversification of sea catfishes is accompanied by genome-wide signatures of positive selection Nature Communications |
| title | Ecological diversification of sea catfishes is accompanied by genome-wide signatures of positive selection |
| title_full | Ecological diversification of sea catfishes is accompanied by genome-wide signatures of positive selection |
| title_fullStr | Ecological diversification of sea catfishes is accompanied by genome-wide signatures of positive selection |
| title_full_unstemmed | Ecological diversification of sea catfishes is accompanied by genome-wide signatures of positive selection |
| title_short | Ecological diversification of sea catfishes is accompanied by genome-wide signatures of positive selection |
| title_sort | ecological diversification of sea catfishes is accompanied by genome wide signatures of positive selection |
| url | https://doi.org/10.1038/s41467-024-54184-3 |
| work_keys_str_mv | AT melissarinconsandoval ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT rishidekayne ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT stephendshank ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT stacypirro ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT alfredkoou ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT linelleabueg ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT alantracey ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT jackiemountcastle ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT brianotoole ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT jenniferbalacco ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT giulioformenti ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT erichdjarvis ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT dahianaarcila ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT sergeilkosakovskypond ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT aarondavis ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT devindbloom ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection AT ricardobetancurr ecologicaldiversificationofseacatfishesisaccompaniedbygenomewidesignaturesofpositiveselection |