{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T03:43:59Z","timestamp":1791517439899,"version":"4.3.4"},"reference-count":89,"publisher":"The Royal Society","issue":"2055","license":[{"start":{"date-parts":[[2025,9,1]],"date-time":"2025-09-01T00:00:00Z","timestamp":1756684800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/royalsociety.org\/-\/media\/journals\/author\/Licence-to-Publish-20062019-final.pdf"},{"start":{"date-parts":[[2025,9,1]],"date-time":"2025-09-01T00:00:00Z","timestamp":1756684800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/royalsociety.org\/journals\/ethics-policies\/data-sharing-mining\/"}],"funder":[{"DOI":"10.13039\/100000155","name":"Division of Environmental Biology","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000155","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["royalsocietypublishing.org"],"crossmark-restriction":true},"short-container-title":["Proc. R. Soc. B."],"published-print":{"date-parts":[[2025,9]]},"abstract":"<jats:p>Transitioning between disparate environments presents new physical challenges, and metamorphosis can provide solutions. The life cycles of most amphibians involve an aquatic-to-terrestrial transition and concomitant metamorphosis, but shifts in developmental timing (heterochrony) have also produced a wide variety of aquatic-only and terrestrial-only forms. Thyroid hormone (TH) signalling can govern the timing of tissue transformation and may be a key mechanism behind the relationship between development and diversification of some metamorphic traits. Here, we show that life cycle mode and cave adaptation (troglomorphy) through heterochrony primarily explain variation in salamander eyes and retina. Across levels of organization (organ\/tissue), heterochrony led to serial reductions in the visual system of larval-form paedomorphs that lost metamorphosis. This pattern is compounded in larval-form paedomorphic lineages that subsequently transitioned to subterranean environments and evolved troglomorphic traits. Following Haller\u2019s Rule, visual system investment declines across ontogeny but at a faster rate in paedomorphs and even faster (for eye size) in troglomorphs. Thyroid hormone typically increases eye size during metamorphosis; however, we show that responsiveness is reduced in paedomorphs and lost or reversed in troglomorphs. Salamander visual system variation is an example of how alterations to hormone-mediated transformation can shift developmental trajectories and compound phenotypic modifications as species move into more divergent environments.<\/jats:p>","DOI":"10.1098\/rspb.2025.0910","type":"journal-article","created":{"date-parts":[[2025,9,23]],"date-time":"2025-09-23T23:06:39Z","timestamp":1758668799000},"update-policy":"https:\/\/doi.org\/10.1098\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["Compounding heterochrony shapes the salamander visual system across adaptive zones"],"prefix":"10.1098","volume":"292","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2708-3446","authenticated-orcid":true,"given":"Ronald M.","family":"Bonett","sequence":"first","affiliation":[{"name":"Department of Biological Science, University of Tulsa","place":["Tulsa, USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emily L.","family":"Bierbaum","sequence":"additional","affiliation":[{"name":"Department of Biological Science, University of Tulsa","place":["Tulsa, USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander J.","family":"Hess","sequence":"additional","affiliation":[{"name":"Department of Biological Science, University of Tulsa","place":["Tulsa, USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samantha D.","family":"Trame","sequence":"additional","affiliation":[{"name":"Department of Biological Science, University of Tulsa","place":["Tulsa, USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0003-5319-9834","authenticated-orcid":true,"given":"Campbell W.","family":"Eckhardt","sequence":"additional","affiliation":[{"name":"Department of Biological Science, University of Tulsa","place":["Tulsa, USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Madison A.","family":"Herrboldt","sequence":"additional","affiliation":[{"name":"Department of Biological Science, University of Tulsa","place":["Tulsa, USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carissa N.","family":"McGouran","sequence":"additional","affiliation":[{"name":"Department of Biological Science, University of Tulsa","place":["Tulsa, USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew D.","family":"Kolozsvary","sequence":"additional","affiliation":[{"name":"Department of Biological Science, University of Tulsa","place":["Tulsa, USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sydney","family":"Sowell","sequence":"additional","affiliation":[{"name":"Department of Biological Science, University of Tulsa","place":["Tulsa, USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ann Marie","family":"Flusche","sequence":"additional","affiliation":[{"name":"Department of Biological Science, University of Tulsa","place":["Tulsa, USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rhiannon","family":"McGlone","sequence":"additional","affiliation":[{"name":"Department of Biological Science, University of Tulsa","place":["Tulsa, USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"175","published-online":{"date-parts":[[2025,9,24]]},"reference":[{"key":"e_1_3_8_2_2","volume-title":"Ontogeny and phylogeny","author":"Gould SJ","year":"1977","unstructured":"Gould SJ. 1977 Ontogeny and phylogeny. Cambridge, MA: Harvard University Press."},{"key":"e_1_3_8_3_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0094837300006588"},{"key":"e_1_3_8_4_2","doi-asserted-by":"publisher","DOI":"10.1666\/0094-8373(2005)031[0354:EMOOHA]2.0.CO;2"},{"key":"e_1_3_8_5_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1525-142X.2006.00141.x"},{"key":"e_1_3_8_6_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-319-32979-6_71"},{"key":"e_1_3_8_7_2","volume-title":"Biology of amphibians","author":"Duellman WE","year":"1986","unstructured":"Duellman WE, Trueb L. 1986 Biology of amphibians. New York, NY: McGraw-Hill. (doi:10.2307\/1445022)"},{"key":"e_1_3_8_8_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-022-34474-4"},{"key":"e_1_3_8_9_2","volume-title":"Animal metamorphosis","author":"Shi YB","year":"2013","unstructured":"Shi YB. 2013 Animal metamorphosis. San Diego, CA: Academic Press."},{"key":"e_1_3_8_10_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ygcen.2009.04.016"},{"key":"e_1_3_8_11_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-7998.1996.tb05451.x"},{"key":"e_1_3_8_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/B978-0-12-385979-2.00008-3"},{"key":"e_1_3_8_13_2","doi-asserted-by":"publisher","DOI":"10.1643\/OT-15-269"},{"key":"e_1_3_8_14_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-017-00996-5"},{"key":"e_1_3_8_15_2","doi-asserted-by":"publisher","DOI":"10.1002\/dvdy.373"},{"key":"e_1_3_8_16_2","first-page":"859","article-title":"Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis?","volume":"40","author":"Wake DB","year":"1996","unstructured":"Wake DB, Hanken J. 1996 Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis? Int. J. Dev. Biol. 40, 859\u2013869.","journal-title":"Int. J. Dev. Biol."},{"key":"e_1_3_8_17_2","doi-asserted-by":"publisher","DOI":"10.1111\/evo.12274"},{"key":"e_1_3_8_18_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-642-72713-9"},{"key":"e_1_3_8_19_2","doi-asserted-by":"publisher","DOI":"10.1002\/neu.480210707"},{"key":"e_1_3_8_20_2","doi-asserted-by":"publisher","DOI":"10.1086\/285370"},{"key":"e_1_3_8_21_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.es.25.110194.003041"},{"key":"e_1_3_8_22_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1703877114"},{"key":"e_1_3_8_23_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-017-0268-6"},{"key":"e_1_3_8_24_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-020-1225-3"},{"key":"e_1_3_8_25_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msae049"},{"key":"e_1_3_8_26_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1420-9101.1992.5040549.x"},{"key":"e_1_3_8_27_2","first-page":"224","volume-title":"Cave biodiversity: speciation and diversity of subterranean fauna","author":"Niemiller ML","year":"2022","unstructured":"Niemiller ML, Carter ET, Fenolio DB, Gluesenkamp AG, Phillips JG. 2022 Subterranean colonization and diversification of cave-dwelling salamanders. In Cave biodiversity: speciation and diversity of subterranean fauna (ed. JJ Wynne), pp. 224\u2013270. Baltimore, MD: John Hopkins University Press."},{"key":"e_1_3_8_28_2","doi-asserted-by":"publisher","DOI":"10.2307\/1535679"},{"key":"e_1_3_8_29_2","doi-asserted-by":"publisher","DOI":"10.1002\/jez.1401560207"},{"key":"e_1_3_8_30_2","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1051240307"},{"key":"e_1_3_8_31_2","first-page":"1","article-title":"North American troglobitic salamanders: some aspects of modification in cave habitats with special reference to Gyrinophilus palleucus","volume":"33","author":"Brandon RA","year":"1971","unstructured":"Brandon RA. 1971 North American troglobitic salamanders: some aspects of modification in cave habitats with special reference to Gyrinophilus palleucus. Bull. Nat. Speleol. Soc. 33, 1\u201321.","journal-title":"Bull. Nat. Speleol. Soc."},{"key":"e_1_3_8_32_2","doi-asserted-by":"publisher","DOI":"10.2307\/1540499"},{"key":"e_1_3_8_33_2","doi-asserted-by":"publisher","DOI":"10.2307\/2405381"},{"key":"e_1_3_8_34_2","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1051890204"},{"key":"e_1_3_8_35_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2435.2000.00404.x"},{"key":"e_1_3_8_36_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-7998.2006.00227.x"},{"key":"e_1_3_8_37_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2020.1393"},{"key":"e_1_3_8_38_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10682-021-10102-3"},{"key":"e_1_3_8_39_2","volume-title":"The vertebrate eye and its adaptive radiation","author":"Walls GL","year":"1942","unstructured":"Walls GL. 1942 The vertebrate eye and its adaptive radiation. Bloomfield Hills, MI: Cranbrook Press. (doi:10.5962\/bhl.title.7369)"},{"key":"e_1_3_8_40_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1525-142X.2008.00256.x"},{"key":"e_1_3_8_41_2","doi-asserted-by":"publisher","DOI":"10.1086\/285307"},{"key":"e_1_3_8_42_2","doi-asserted-by":"publisher","DOI":"10.1159\/000114147"},{"key":"e_1_3_8_43_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.91.11.4796"},{"key":"e_1_3_8_44_2","doi-asserted-by":"publisher","DOI":"10.1023\/A:1016032400147"},{"key":"e_1_3_8_45_2","doi-asserted-by":"publisher","DOI":"10.1007\/s11692-020-09497-8"},{"key":"e_1_3_8_46_2","doi-asserted-by":"publisher","DOI":"10.1093\/iob\/obad015"},{"key":"e_1_3_8_47_2","first-page":"138","article-title":"Die struktur des auges bei urodelen verschiedener k\u00f6rpergr\u00f6\u00dfe","volume":"62","author":"M\u04e7ller A","year":"1951","unstructured":"M\u04e7ller A. 1951 Die struktur des auges bei urodelen verschiedener k\u00f6rpergr\u00f6\u00dfe. Zool. J. Physiol. 62, 138\u2013182.","journal-title":"Zool. J. Physiol."},{"key":"e_1_3_8_48_2","first-page":"322","article-title":"A comparative study of eye size in three Chinese salamanders (Urodela: Hynobiidae)","volume":"4","author":"Lv Y","year":"2014","unstructured":"Lv Y, Xiong J, Chen W, Sun Y, Zhang X, Zhang L. 2014 A comparative study of eye size in three Chinese salamanders (Urodela: Hynobiidae). Russ. J. Herpetol. 4, 322\u2013325. (doi:10.30906\/1026-2296-2014-21-4-322-325)","journal-title":"Russ. J. Herpetol."},{"key":"e_1_3_8_49_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1525-142X.2006.00099.x"},{"key":"e_1_3_8_50_2","doi-asserted-by":"publisher","DOI":"10.3389\/fendo.2019.00194"},{"key":"e_1_3_8_51_2","doi-asserted-by":"publisher","DOI":"10.1002\/dvdy.479"},{"key":"e_1_3_8_52_2","doi-asserted-by":"publisher","DOI":"10.1002\/neu.480210704"},{"key":"e_1_3_8_53_2","doi-asserted-by":"publisher","DOI":"10.1089\/105072503770867183"},{"key":"e_1_3_8_54_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2011.04.005"},{"key":"e_1_3_8_55_2","first-page":"44","volume-title":"Organization and development of the embryo","author":"Harrison R","year":"1969","unstructured":"Harrison R. 1969 Harrison stages and description of normal development of the spotted salamander, Ambystoma punctatum (Linn). In Organization and development of the embryo (ed. S Wilens), pp. 44\u201366. New Haven, CT: Yale University Press."},{"key":"e_1_3_8_56_2","unstructured":"AmphibiaWeb. 2024 AmphibiaWeb. See http:\/\/amphibiaweb.org\/."},{"key":"e_1_3_8_57_2","volume-title":"Histological and histochemical methods: theory and practice","author":"Kiernan JA","year":"1990","unstructured":"Kiernan JA. 1990 Histological and histochemical methods: theory and practice. New York, NY: Pergamon Press."},{"key":"e_1_3_8_58_2","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902890302"},{"key":"e_1_3_8_59_2","unstructured":"Gregory TR. 2024 Animal genome size database. See http:\/\/www.genomesize.com."},{"key":"e_1_3_8_60_2","doi-asserted-by":"publisher","DOI":"10.1086\/711019"},{"key":"e_1_3_8_61_2","doi-asserted-by":"publisher","DOI":"10.1086\/503444"},{"key":"e_1_3_8_62_2","doi-asserted-by":"publisher","DOI":"10.1002\/ecy.4252"},{"key":"e_1_3_8_63_2","doi-asserted-by":"publisher","DOI":"10.1186\/s12862-014-0226-8"},{"key":"e_1_3_8_64_2","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/syad012"},{"key":"e_1_3_8_65_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1558-5646.2012.01619.x"},{"key":"e_1_3_8_66_2","volume-title":"Model selection and multi-model inference: a practical information theoretic approach","author":"Burnham KP","year":"2002","unstructured":"Burnham KP, Anderson D. 2002 Model selection and multi-model inference: a practical information theoretic approach, 2nd edn. New York, NY: Springer-Verlag.","edition":"2"},{"key":"e_1_3_8_67_2","unstructured":"Orme D Freckleton RP Thomas GH Petzoldt T Fritz SA Isaac N. 2013 caper: Comparative analyses of phylogenetics and evolution in R. (doi:10.32614\/CRAN.package.caper)"},{"key":"e_1_3_8_68_2","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/syu005"},{"key":"e_1_3_8_69_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1994.0006"},{"key":"e_1_3_8_70_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.0014-3820.2004.tb01632.x"},{"key":"e_1_3_8_71_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1558-5646.2011.01426.x"},{"key":"e_1_3_8_72_2","doi-asserted-by":"publisher","DOI":"10.1111\/mec.16868"},{"key":"e_1_3_8_73_2","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1051490406"},{"key":"e_1_3_8_74_2","doi-asserted-by":"publisher","DOI":"10.5038\/1827-806X.6.3.7"},{"key":"e_1_3_8_75_2","first-page":"1","article-title":"Comparative osteology and evolution of the lungless salamanders, family Plethodontidae","volume":"4","author":"Wake DB","year":"1966","unstructured":"Wake DB. 1966 Comparative osteology and evolution of the lungless salamanders, family Plethodontidae. Mem. S Calif. Acad. Sci. 4, 1\u2013111. (doi:10.5962\/bhl.title.146947)","journal-title":"Mem. S Calif. Acad. Sci."},{"key":"e_1_3_8_76_2","volume-title":"Tempo and mode in evolution","author":"Simpson GG","year":"1944","unstructured":"Simpson GG. 1944 Tempo and mode in evolution. New York, NY: Columbia University Press."},{"key":"e_1_3_8_77_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2011.2005"},{"key":"e_1_3_8_78_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00312059"},{"key":"e_1_3_8_79_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41583-019-0242-1"},{"key":"e_1_3_8_80_2","doi-asserted-by":"publisher","DOI":"10.1002\/jez.1401790203"},{"key":"e_1_3_8_81_2","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1050710307"},{"key":"e_1_3_8_82_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.017574"},{"key":"e_1_3_8_83_2","doi-asserted-by":"publisher","DOI":"10.23943\/princeton\/9780691151847.001.0001"},{"key":"e_1_3_8_84_2","doi-asserted-by":"publisher","DOI":"10.1093\/acprof:oso\/9780199601776.001.0001"},{"key":"e_1_3_8_85_2","doi-asserted-by":"publisher","DOI":"10.3389\/fevo.2019.00321"},{"key":"e_1_3_8_86_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2009.12.006"},{"key":"e_1_3_8_87_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-023-06638-9"},{"key":"e_1_3_8_88_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-94-011-3961-8"},{"key":"e_1_3_8_89_2","unstructured":"Bonett R et al. 2025 Compounding heterochrony shapes the salamander visual system across adaptive zones. Dryad Digital Repository. (doi:10.5061\/dryad.8931zcs04)"},{"key":"e_1_3_8_90_2","unstructured":"Bonett RM Bierbaum EL Hess AJ Trame SD Eckhardt CW Herrboldt MA et al. 2025 Supplementary material from: Compounding heterochrony shapes the salamander visual system across adaptive zones. Figshare. (doi:10.6084\/m9.figshare.c.8007259)"}],"container-title":["Proceedings of the Royal Society B: Biological Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rspb.2025.0910","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/full-xml\/10.1098\/rspb.2025.0910","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rspb.2025.0910","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,9,23]],"date-time":"2025-09-23T23:06:52Z","timestamp":1758668812000},"score":1,"resource":{"primary":{"URL":"https:\/\/royalsocietypublishing.org\/doi\/10.1098\/rspb.2025.0910"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,9]]},"references-count":89,"journal-issue":{"issue":"2055","published-print":{"date-parts":[[2025,9]]}},"alternative-id":["10.1098\/rspb.2025.0910"],"URL":"https:\/\/doi.org\/10.1098\/rspb.2025.0910","relation":{"has-review":[{"id-type":"doi","id":"10.1098\/RSPB.2025.0910\/v1\/review2","asserted-by":"object"},{"id-type":"doi","id":"10.1098\/RSPB.2025.0910\/v4\/decision1","asserted-by":"object"},{"id-type":"doi","id":"10.1098\/RSPB.2025.0910\/v4\/response1","asserted-by":"object"},{"id-type":"doi","id":"10.1098\/RSPB.2025.0910\/v1\/review1","asserted-by":"object"},{"id-type":"doi","id":"10.1098\/RSPB.2025.0910\/v2\/review1","asserted-by":"object"},{"id-type":"doi","id":"10.1098\/RSPB.2025.0910\/v2\/review2","asserted-by":"object"},{"id-type":"doi","id":"10.1098\/RSPB.2025.0910\/v1\/decision1","asserted-by":"object"},{"id-type":"doi","id":"10.1098\/RSPB.2025.0910\/v1\/review3","asserted-by":"object"},{"id-type":"doi","id":"10.1098\/RSPB.2025.0910\/v3\/decision1","asserted-by":"object"},{"id-type":"doi","id":"10.1098\/RSPB.2025.0910\/v3\/response1","asserted-by":"object"},{"id-type":"doi","id":"10.1098\/RSPB.2025.0910\/v2\/decision1","asserted-by":"object"}]},"ISSN":["1471-2954"],"issn-type":[{"value":"1471-2954","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,9]]},"assertion":[{"value":"2025-04-12","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-08-07","order":1,"name":"revised","label":"Revised","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-08-20","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-09-24","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"20250910"}}