{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,22]],"date-time":"2026-04-22T00:53:16Z","timestamp":1776819196107,"version":"3.51.2"},"reference-count":81,"publisher":"The Royal Society","issue":"2069","license":[{"start":{"date-parts":[[2026,4,22]],"date-time":"2026-04-22T00:00:00Z","timestamp":1776816000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,4,22]],"date-time":"2026-04-22T00:00:00Z","timestamp":1776816000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000154","name":"Division of Integrative Organismal Systems","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000154","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000052","name":"NIH Office of the Director","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000052","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,4,22]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Environmental perturbations often lead to the evolution of multiple traits. Determining whether shared genetic factors underlie multi-trait evolution is a central question in evolutionary biology. In the Mexican tetra, Astyanax mexicanus, cave-dwelling populations have repeatedly evolved multiple traits. The repeated evolution of these traits, paired with robust environmental differences between the surface and cave habitats, provide an opportunity to investigate the genetic basis of multi-trait evolution. Here, we investigate the extent to which shared genetic mechanisms underlie the repeated evolution of multiple traits in cavefish. Across cave populations, we find evidence for shared and distinct genetic mechanisms contributing to the evolution of individual traits. Further, multiple traits covary in cave\u2013surface F2 hybrids. Moreover, many of the same pairs of traits covary in independently evolved cave populations. Finally, multiple traits differ between pigmented and albino F2 fish. Quantification of these traits in surface fish with mutations in the albinism gene oculocutaneous albinism 2 (oca2) reveals that mutations in oca2 reduce bottom-dwelling behaviour in A. mexicanus. Together, these findings suggest that multi-trait evolution occurs repeatedly through shared genetic factors across A. mexicanus cave populations. These results are consistent with pleiotropy and\/or linkage playing a large role in multi-trait evolution in this species.<\/jats:p>","DOI":"10.1098\/rspb.2025.2719","type":"journal-article","created":{"date-parts":[[2026,4,22]],"date-time":"2026-04-22T00:11:34Z","timestamp":1776816694000},"source":"Crossref","is-referenced-by-count":0,"title":["Analysis of multi-trait evolution across independently evolved cavefish populations reveals shared and independent evolution of suites of traits"],"prefix":"10.1098","volume":"293","author":[{"given":"Stefan","family":"Choy","sequence":"first","affiliation":[{"name":"Lehigh University 1 , , ,","place":["Bethlehem, PA, USA, 18015"],"department":["Department of Biological Sciences"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maya","family":"Enriquez","sequence":"additional","affiliation":[{"name":"University of Minnesota Twin Cities 2 , , ,","place":["Minneapolis, MN, USA, 55108"],"department":["Department of Ecology, Evolution, and Behavior"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rianna","family":"Ambosie","sequence":"additional","affiliation":[{"name":"Lehigh University 1 , , ,","place":["Bethlehem, PA, USA, 18015"],"department":["Department of Biological Sciences"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Aubrey E.","family":"Manning","sequence":"additional","affiliation":[{"name":"Lehigh University 1 , , ,","place":["Bethlehem, PA, USA, 18015"],"department":["Department of Biological Sciences"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Briley","family":"Mullin","sequence":"additional","affiliation":[{"name":"Lehigh University 1 , , ,","place":["Bethlehem, PA, USA, 18015"],"department":["Department of Biological Sciences"]},{"name":"University of California Davis 3 , , ,","place":["Davis, CA, USA, 95616"],"department":["Department of Entomology and Nematology"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Roberto","family":"Rodriguez-Morales","sequence":"additional","affiliation":[{"name":"Lehigh University 1 , , ,","place":["Bethlehem, PA, USA, 18015"],"department":["Department of Biological Sciences"]},{"name":"University of Puerto Rico 4 , ,","place":["San Juan, Puerto Rico, 00936"],"department":["Department of Anatomy and Neurobiology"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jennah","family":"Abdelaziz","sequence":"additional","affiliation":[{"name":"Lehigh University 1 , , ,","place":["Bethlehem, PA, USA, 18015"],"department":["Department of Biological Sciences"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sarah","family":"Jacobson","sequence":"additional","affiliation":[{"name":"University of Minnesota Twin Cities 2 , , ,","place":["Minneapolis, MN, USA, 55108"],"department":["Department of Ecology, Evolution, and Behavior"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Evan","family":"Lloyd","sequence":"additional","affiliation":[{"name":"Florida State University 5 , , ,","place":["Tallahassee, FL, USA, 32304"],"department":["Department of Biological Science"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Naresh","family":"Padmanaban","sequence":"additional","affiliation":[{"name":"Florida Atlantic University 6 , , ,","place":["Boca Raton, FL, USA, 33431"]},{"name":"Florida Atlantic University Harriet L Wilkes Honors College 7 , , ,","place":["Jupiter, FL, USA, 33458"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Allison","family":"Kimmel","sequence":"additional","affiliation":[{"name":"Lehigh University 1 , , ,","place":["Bethlehem, PA, USA, 18015"],"department":["Department of Biological Sciences"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Solomia","family":"Lapko","sequence":"additional","affiliation":[{"name":"Lehigh University 1 , , ,","place":["Bethlehem, PA, USA, 18015"],"department":["Department of Biological Sciences"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-3063-1148","authenticated-orcid":false,"given":"Isabel","family":"Carino-Bazan","sequence":"additional","affiliation":[{"name":"Lehigh University 1 , , ,","place":["Bethlehem, PA, USA, 18015"],"department":["Department of Biological Sciences"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Helena","family":"Biland\u017eija","sequence":"additional","affiliation":[{"name":"Ruder Boskovic Institute Division of Molecular Biology 8 , ,","place":["Zagreb, Croatia, 10000"],"department":["Division of Molecular Biology"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alex C.","family":"Keene","sequence":"additional","affiliation":[{"name":"TAMU 9 , , ,","place":["College Station, TX, USA, 77843"],"department":["Department of Biology"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Erik R.","family":"Duboue","sequence":"additional","affiliation":[{"name":"Florida Atlantic University Harriet L Wilkes Honors College 7 , , ,","place":["Jupiter, FL, USA, 33458"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3163-3436","authenticated-orcid":false,"given":"Suzanne E.","family":"McGaugh","sequence":"additional","affiliation":[{"name":"University of Minnesota Twin Cities 2 , , ,","place":["Minneapolis, MN, USA, 55108"],"department":["Department of Ecology, Evolution, and Behavior"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3286-2954","authenticated-orcid":false,"given":"Johanna E.","family":"Kowalko","sequence":"additional","affiliation":[{"name":"Lehigh University 1 , , ,","place":["Bethlehem, PA, USA, 18015"],"department":["Department of Biological Sciences"]}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"175","published-online":{"date-parts":[[2026,4,22]]},"reference":[{"key":"2026042120112735400_R1","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1038\/sj.hdy.6800861","article-title":"Genetics, development and evolution of adaptive pigmentation in vertebrates","volume":"97","author":"Hoekstra","year":"2006","journal-title":"Heredity"},{"key":"2026042120112735400_R2","doi-asserted-by":"crossref","first-page":"565","DOI":"10.2307\/1936109","article-title":"An analysis of background color-matching in amphibians and reptiles","volume":"45","author":"Norris","year":"1964","journal-title":"Ecology"},{"key":"2026042120112735400_R3","volume-title":"Studies of mammalian ecology in Southwestern North America, with special attention to the colors of desert mammals","author":"Dice","year":"1937"},{"key":"2026042120112735400_R4","unstructured":"Luke\n              CA\n            \n          . 1989Color as a Phenotypically Plastic Character in the Side-Blotched Lizard. PhD Thesis, University of California, Uta Stansburiana."},{"key":"2026042120112735400_R5","doi-asserted-by":"crossref","first-page":"13040","DOI":"10.1073\/pnas.1202111109","article-title":"Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na, K-ATPase","volume":"109","author":"Dobler","year":"2012","journal-title":"Proc. Natl Acad. Sci. 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USA"},{"key":"2026042120112735400_R9","doi-asserted-by":"crossref","DOI":"10.5962\/bhl.title.27468","volume-title":"The genetical theory of natural selection","author":"Fisher","year":"1930"},{"key":"2026042120112735400_R10","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1111\/j.0014-3820.2000.tb00002.x","article-title":"Adaptation and the cost of complexity","volume":"54","author":"Orr","year":"2000","journal-title":"Evolution"},{"key":"2026042120112735400_R11","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1098\/rspb.2003.2635","article-title":"Two steps forward, one step back: the pleiotropic effects of favoured alleles","volume":"271","author":"Otto","year":"2004","journal-title":"Proc. R. Soc. 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Ecol."},{"key":"2026042120112735400_R15","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.0020109","article-title":"The genetic architecture of parallel armor plate reduction in threespine sticklebacks","volume":"2","author":"Colosimo","year":"2004","journal-title":"PLoS Biol."},{"key":"2026042120112735400_R16","doi-asserted-by":"crossref","first-page":"1047","DOI":"10.1534\/g3.112.003079","article-title":"Genetic architecture of variation in the lateral line sensory system of threespine sticklebacks","volume":"2","author":"Wark","year":"2012","journal-title":"G3"},{"key":"2026042120112735400_R17","doi-asserted-by":"crossref","first-page":"1884","DOI":"10.1016\/j.cub.2013.07.058","article-title":"Genetic and neural modularity underlie the evolution of schooling behavior in threespine sticklebacks","volume":"23","author":"Greenwood","year":"2013","journal-title":"Curr. 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Ecol."},{"key":"2026042120112735400_R21","article-title":"Tracing the origin and evolution of supergene mimicry in butterflies","volume":"8","author":"Zhang","year":"2017","journal-title":"Nat. Commun."},{"key":"2026042120112735400_R22","doi-asserted-by":"crossref","first-page":"4397","DOI":"10.1111\/mec.14877","article-title":"The role of gene flow in rapid and repeated evolution of cave related traits in Mexican tetra, Astyanax mexicanus","volume":"27","author":"Herman","year":"2018","journal-title":"Mol. Ecol."},{"key":"2026042120112735400_R23","doi-asserted-by":"crossref","first-page":"95","DOI":"10.3897\/subtbiol.45.98434","article-title":"A new cave population of Astyanax mexicanus from Northern Sierra de El Abra, Tamaulipas, Mexico","volume":"45","author":"Miranda-Gamboa","year":"2023","journal-title":"Subterr. Biol."},{"key":"2026042120112735400_R24","doi-asserted-by":"crossref","first-page":"5626","DOI":"10.1111\/mec.17128","article-title":"Phylogeographic relationships and morphological evolution between cave and surface Astyanax mexicanus populations (De Filippi 1853) (Actinopterygii, Characidae)","volume":"32","author":"Gardu\u00f1o-S\u00e1nchez","year":"2023","journal-title":"Mol. Ecol."},{"key":"2026042120112735400_R25","doi-asserted-by":"crossref","DOI":"10.1186\/1471-2148-12-9","article-title":"Gene flow and population structure in the Mexican blind cavefish complex (Astyanax mexicanus)","volume":"12","author":"Bradic","year":"2012","journal-title":"BMC Evol. Biol."},{"key":"2026042120112735400_R26","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1007\/BF02161111","article-title":"A mendelian gene for albinism in natural cave fish","volume":"13","author":"\u015eado\u011flu","year":"1957","journal-title":"Experientia"},{"key":"2026042120112735400_R27","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1093\/oxfordjournals.jhered.a107917","article-title":"A second gene that affects eye and body color in Mexican blind cave fish","volume":"60","author":"Sadoglu","year":"1969","journal-title":"J. Hered."},{"key":"2026042120112735400_R28","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1007\/978-1-4613-1043-3_8","volume-title":"Evolutionary biology, vol. 23","author":"Wilkens","year":"1988"},{"key":"2026042120112735400_R29","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1093\/jhered\/93.1.19","article-title":"Mapping a cave fish genome: polygenic systems and regressive evolution","volume":"93","author":"Borowsky","year":"2002","journal-title":"J. Hered."},{"key":"2026042120112735400_R30","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1093\/icb\/43.4.531","article-title":"To see or not to see: evolution of eye degeneration in Mexican blind cavefish","volume":"43","author":"Jeffery","year":"2003","journal-title":"Integr. Comp. 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Hered."},{"key":"2026042120112735400_R40","doi-asserted-by":"crossref","first-page":"16933","DOI":"10.1073\/pnas.1317192110","article-title":"Convergence in feeding posture occurs through different genetic loci in independently evolved cave populations of Astyanax mexicanus","volume":"110","author":"Kowalko","year":"2013","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2026042120112735400_R41","doi-asserted-by":"crossref","first-page":"1874","DOI":"10.1016\/j.cub.2013.07.056","article-title":"Loss of schooling behavior in cavefish through sight-dependent and sight-independent mechanisms","volume":"23","author":"Kowalko","year":"2013","journal-title":"Curr. Biol."},{"key":"2026042120112735400_R42","doi-asserted-by":"crossref","first-page":"3694","DOI":"10.1016\/j.cub.2021.06.077","article-title":"Pleiotropic function of the oca2 gene underlies the evolution of sleep loss and albinism in cavefish","volume":"31","author":"O\u2019Gorman","year":"2021","journal-title":"Curr. Biol."},{"key":"2026042120112735400_R43","doi-asserted-by":"crossref","DOI":"10.1186\/1741-7007-10-108","article-title":"Evolution of an adaptive behavior and its sensory receptors promotes eye regression in blind cavefish","volume":"10","author":"Yoshizawa","year":"2012","journal-title":"BMC Biol."},{"key":"2026042120112735400_R44","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0080823","article-title":"A potential benefit of albinism in Astyanax cavefish: downregulation of the oca2 gene increases tyrosine and catecholamine levels as an alternative to melanin synthesis","volume":"8","author":"Biland\u017eija","year":"2013","journal-title":"PLoS One"},{"key":"2026042120112735400_R45","doi-asserted-by":"crossref","DOI":"10.1098\/rspb.2018.0243","article-title":"Behavioural changes controlled by catecholaminergic systems explain recurrent loss of pigmentation in cavefish","volume":"285","author":"Biland\u017eija","year":"2018","journal-title":"Proc. R. Soc. 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Evol."},{"key":"2026042120112735400_R48","doi-asserted-by":"crossref","first-page":"844","DOI":"10.1038\/nature02864","article-title":"Hedgehog signalling controls eye degeneration in blind cavefish","volume":"431","author":"Yamamoto","year":"2004","journal-title":"Nature"},{"key":"2026042120112735400_R49","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.ydbio.2009.03.003","article-title":"Pleiotropic functions of embryonic sonic hedgehog expression link jaw and taste bud amplification with eye loss during cavefish evolution","volume":"330","author":"Yamamoto","year":"2009","journal-title":"Dev. 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