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Cited by 79Amphibian and Reptile BiologySubterranean biodiversity and taxonomyEvolution and Paleontology Studies

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EVOLUTION OF PAEDOMORPHOSIS IN PLETHODONTID SALAMANDERS: ECOLOGICAL CORRELATES AND RE-EVOLUTION OF METAMORPHOSIS

Bonett, Ronald M., Steffen, Michael A., Lambert, Shea M., Wiens, John J., Chippindale, Paul T.·2014·Evolution
DOI 10.1111/evo.12274
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Abstract

Life-history modes can profoundly impact the biology of a species, and a classic example is the dichotomy between metamorphic (biphasic) and paedomorphic (permanently aquatic) life-history strategies in salamanders. However, despite centuries of research on this system, several basic questions about the evolution of paedomorphosis in salamanders have not been addressed. Here, we use a nearly comprehensive, time-calibrated phylogeny of spelerpine plethodontids to reconstruct the evolution of paedomorphosis and to test if paedomorphosis is (1) reversible; (2) associated with living in caves; (3) associated with relatively dry climatic conditions on the surface; and (4) correlated with limited range size and geographic dispersal. We find that paedomorphosis arose multiple times in spelerpines. We also find evidence for re-evolution of metamorphosis after several million years of paedomorphosis in a lineage of Eurycea from the Edwards Plateau region of Texas. We also show for the first time using phylogenetic comparative methods that paedomorphosis is highly correlated with cave-dwelling, arid surface environments, and small geographic range sizes, providing insights into both the causes and consequences of this major life history transition.

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Research works printed but not linked: 93

  1. AmphibiaWeb, 2013, Information on amphibian biology and conservation
  2. Bendik, 2013, Body length shrinkage in an endangered amphibian is associated with drought, J. Zool., 290, 35, 10.1111/jzo.12009 · DOI
  3. Bendik, 2013, Biogeography, phylogeny, and morphological evolution in central Texas cave and spring salamanders (Eurycea), BMC Evol. Biol, 13, 201, 10.1186/1471-2148-13-201 · DOI
  4. Birand, 2012, Patterns of species ranges, speciation, and extinction, Am. Nat., 179, 1, 10.1086/663202 · DOI
  5. Boardman, 2011, First Mio-Pliocene salamander fauna from the southern Appalachians, Palaeontologia Electronica, 14, 16
  6. Bonett, 2004, Speciation, phylogeography and evolution of live history and morphology in the salamanders of the Eurycea multiplicata complex, Mol. Ecol., 13, 1189, 10.1111/j.1365-294X.2004.02130.x · DOI
  7. Bonett, 2006, Streambed microstructure predicts evolution of development and life history mode in the plethodontid salamander Eurycea tynerensis, BMC Biol., 4, 6, 10.1186/1741-7007-4-6 · DOI
  8. Bonett, 2010, Molecular mechanisms of corticosteroid synergy with thyroid hormone during tadpole metamorphosis, Gen. Comp. Endocr., 168, 209, 10.1016/j.ygcen.2010.03.014 · DOI
  9. Bonett, 2013, Biogeography and body size shuffling of aquatic salamander communities on a shifting refuge, Proc. R. Soc. Lond. Ser. B-Biol. Sci., 280, 20130200, 10.1098/rspb.2013.0200 · DOI
  10. Brandley, 2008, Rates and patterns in the evolution of snake-like body form in squamate reptiles: evidence for repeated re-evolution of lost digits and long-term persistence of intermediate body forms, Evolution, 62, 2042, 10.1111/j.1558-5646.2008.00430.x · DOI
  11. Brown, 2010, When trees grow too long: investigating the causes of highly inaccurate Bayesian branch length estimates, Syst. Biol., 59, 145, 10.1093/sysbio/syp081 · DOI
  12. Bruce, 1976, Population structure, life history, and evolution of paedogenesis in the salamander Eurycea neotenes, Copeia, 1976, 242, 10.2307/1443942 · DOI
  13. Burnham, 2002, Model selection and multi-model inference: a practical information theoretic approach
  14. Camp, 2009, A new genus and species of lungless salamander (family Plethodontidae) from the Appalachian highlands of the southeastern United States, J. Zool., 279, 86, 10.1111/j.1469-7998.2009.00593.x · DOI
  15. Chippindale, 2000, Phylogenetic relationships and systematic revision of central Texas hemidactyliine plethodontid salamanders, Herpetol. Monogr., 14, 1, 10.2307/1467045 · DOI
  16. Chippindale, 2004, Phylogenetic evidence for a major reversal of life-history evolution in plethodontid salamanders, Evolution, 58, 2809, 10.1111/j.0014-3820.2004.tb01632.x · DOI
  17. Cooper, 2008, Macroecology and extinction risk correlates of frogs, Global Ecol. Biogeogr., 17, 211, 10.1111/j.1466-8238.2007.00355.x · DOI
  18. Davis, 2013, Exploring power and parameter estimation of the BiSSE method for analyzing species diversification, BMC Evol. Biol., 13, 38, 10.1186/1471-2148-13-38 · DOI
  19. Denöel, 2005, Evolutionary ecology of facultative paedomorphosis in newts and salamanders, Biol. Rev., 80, 663, 10.1017/S1464793105006858 · DOI · Paper page
  20. Denver, 2009, Stress hormones mediate environment-genotype interactions during amphibian development, Gen. Comp. Endocr., 164, 20, 10.1016/j.ygcen.2009.04.016 · DOI
  21. Dent, 1968, Metamorphosis: a problem in developmental biology, 271
  22. Dollo, 1893, Les lois de l'évolution, Bulletin de la Société Belge de Géologie, de Paléontologie et d'Hydrobiologie, 7, 164
  23. Drummond, 2007, BEAST: Bayesian evolutionary analysis by sampling trees, BMC Evol. Biol., 7, 214, 10.1186/1471-2148-7-214 · DOI
  24. Duellman, 1986, Biology of amphibians
  25. Dundee, 1957, Partial metamorphosis induced in Typhlomolge rathbuni, Copeia, 1957, 52, 10.2307/1440522 · DOI
  26. Eastman, 2011, Correlations of life-history and distributional-range variation with salamander diversification rates: evidence for species selection, Syst. Biol., 60, 503, 10.1093/sysbio/syr020 · DOI
  27. Emel, 2011, Considering alternative life history modes and genetic divergence in conservation: a case study of the Oklahoma salamander, Conser. Genet., 12, 1243, 10.1007/s10592-011-0226-9 · DOI
  28. Garland, 1993, Phylogenetic analysis of covariance by computer simulation, Syst. Biol., 42, 265, 10.1093/sysbio/42.3.265 · DOI · Paper page
  29. Goldberg, 2008, On phylogenetic tests of irreversible evolution, Evolution, 62, 2727, 10.1111/j.1558-5646.2008.00505.x · DOI
  30. Goricki, 2006, Structure and evolution of the mitochondrial control region and flanking sequences in the European cave salamander Proteus anguinus, Gene, 378, 31, 10.1016/j.gene.2006.04.016 · DOI
  31. Gould, 1977, Ontogeny and phylogeny
  32. Heled, 2010, Bayesian inference of species trees from multilocus data, Mol. Biol. Evol., 27, 570, 10.1093/molbev/msp274 · DOI · Paper page
  33. Hillis, 2001, A new species of subterranean blind salamander (Plethodontidae: Hemidactyliini: Eurycea: Typhlomolge) from Austin, Texas, and a systematic revision of central Texas paedomorphic salamanders, Herpetologica, 57, 247
  34. Holman, 2006, Fossil salamanders of North America, 10.2979/4082.0 · DOI
  35. Huelsenbeck, 2001, MRBAYES: Bayesian inference of phylogenetic trees, Bioinformatics, 17, 754, 10.1093/bioinformatics/17.8.754 · DOI · Paper page
  36. Ives, 2010, Phylogenetic logistic regression for binary dependent variables, Syst. Biol., 59, 9, 10.1093/sysbio/syp074 · DOI
  37. Jablonski, 2008, Extinction and the spatial dynamics of biodiversity, Proc. Natl. Acad. Sci. U.S.A., 105, 11528, 10.1073/pnas.0801919105 · DOI · Paper page
  38. Kezer, 1952, Thyroxine-induced metamorphosis of the neotenic salamanders Eurycea tynerensis and Eurycea neotenes, Copeia, 1952, 234, 10.2307/1439269 · DOI
  39. Kohlsdorf, 2010, Data and data-interpretation in the study of limb evolution: a reply to Galis et al., on the re-evolution of digits in the lizard genus Bachia, Evolution, 64, 2477
  40. Kozak, 2010, Accelerated rates of climatic-niche evolution underlie rapid species diversification, Ecol. Lett., 13, 1378, 10.1111/j.1461-0248.2010.01530.x · DOI
  41. Kozak, 2006, Gene lineages and eastern North American palaeodrainage basins: phylogeography and speciation in salamanders of the Eurycea bislineata species complex, Mol. Ecol., 15, 191, 10.1111/j.1365-294X.2005.02757.x · DOI
  42. Kozak, 2009, Can parallel diversification occur in sympatry? Repeated patterns of body-size evolution in co-existing clades of North American salamanders, Evolution, 63, 1769, 10.1111/j.1558-5646.2009.00680.x · DOI
  43. Krenz, 1995, Mating and ovoposition in paedomorphic Ambystoma talpoideum proceeds the arrival of terrestrial males, Herpetologica, 51, 387
  44. Lamb, 2012, Digits lost or gained? Evidence for pedal evolution in the dwarf salamander complex (Eurycea, Plethodontidae), PLoS One, 7, e37544, 10.1371/journal.pone.0037544 · DOI
  45. Lynch, 2010, Did egg-laying boas break Dollo's law? Phylogenetic evidence for reversal to oviparity in sand boas (Eryx: Boidae), Evolution, 64, 207, 10.1111/j.1558-5646.2009.00790.x · DOI
  46. Maddison, 2007, Estimating a binary character's effect on speciation and extinction, Syst. Biol., 56, 701, 10.1080/10635150701607033 · DOI
  47. Marshall, 1994, Dollo's law and the death and resurrection of genes, Proc. Natl. Acad. Sci. U.S.A., 91, 12283, 10.1073/pnas.91.25.12283 · DOI
  48. Milner, 1983, Evolution, time and space: the emergence of the biosphere, 431
  49. Moran, 1994, Adaptation and constraint in the complex life cycles of animals, Annu. Rev. Ecol. Syst., 25, 573, 10.1146/annurev.es.25.110194.003041 · DOI · Paper page
  50. Mueller, 2006, Evolutionary rates, divergence dates, and the performance of mitochondrial genes in Bayesian phylogenetic analysis, Syst. Biol., 55, 289, 10.1080/10635150500541672 · DOI
  51. Mueller, 2004, Morphological homoplasy, life history evolution, and historical biogeography of plethodontid salamanders inferred from complete mitochondrial genomes, Proc. Natl. Acad. Sci. U.S.A., 101, 13820, 10.1073/pnas.0405785101 · DOI
  52. Niemiller, 2008, Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies, Mol. Ecol., 17, 2258, 10.1111/j.1365-294X.2008.03750.x · DOI
  53. Nylander, 2004, Program distributed by the author
  54. Pagel, 1994, Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters, Proc. R. Soc. Lond. Ser. B-Biol. Sci., 255, 37, 10.1098/rspb.1994.0006 · DOI · Paper page
  55. Pagel, 2006, Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo, Am. Nat., 167, 808, 10.1086/503444 · DOI · Paper page
  56. Pagel, 2004, Bayesian estimation of ancestral character states on phylogenies, Syst. Biol., 53, 673, 10.1080/10635150490522232 · DOI
  57. Petranka, 1998, Salamanders of the U. S. and Canada
  58. Potter, 1960, Thyroxin induced metamorphosis in a neotenic salamander, Eurycea nana Bishop, Zool. Ser. A. & M. College of Texas, 1, 1
  59. Pyron, 2011, A large-scale phylogeny of Amphibia including over 2,800 species, and a revised classification of extant frogs, salamanders, and caecilians, Mol. Phylogenet. Evol., 61, 543, 10.1016/j.ympev.2011.06.012 · DOI
  60. Ree, 2008, Maximum-likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis, Syst. Biol., 57, 4, 10.1080/10635150701883881 · DOI
  61. Ree, 2005, A likelihood framework for inferring the evolution of geographic range on phylogenetic trees, Evolution, 59, 2299, 10.1111/j.0014-3820.2005.tb00940.x · DOI
  62. Revell , L. J. 2012 Phytools: phylogenetic tools for comparative biology (and other things) http://faculty.umb.edu/liam.revell/phytools/ · DOI
  63. Roelants, 2007, Global patterns of diversification in the history of modern amphibians, Proc. Natl. Acad. Sci. USA, 104, 887, 10.1073/pnas.0608378104 · DOI
  64. Ronquist, 2003, MRBAYES 3: Bayesian phylogenetic inference under mixed models, Bioinformatics, 19, 1572, 10.1093/bioinformatics/btg180 · DOI
  65. Rose, 1996, An endocrine-based model for developmental and morphogenetic diversification in metamorphic and paedomorphic urodeles, J. Zool., 239, 253, 10.1111/j.1469-7998.1996.tb05451.x · DOI
  66. Ryan, 2000, The biology of plethodontid salamanders, 303, 10.1007/978-1-4615-4255-1_15 · DOI
  67. Ryan, 1998, Intraspecific heterochrony and life history evolution: decoupling somatic and sexual development in a facultatively paedomorphic salamander, Proc. Natl. Acad. Sci. USA, 95, 5643, 10.1073/pnas.95.10.5643 · DOI
  68. Safi, 2006, Paedomorphosis revisited: thyroid hormone receptors are functional in Necturus maculosus, Evol. Dev., 8, 284, 10.1111/j.1525-142X.2006.00099.x · DOI
  69. Semlitsch, 1987, Paedomorphosis in Ambystoma talpoideum: effects of density, food, and pond drying, Ecology, 68, 994, 10.2307/1938370 · DOI
  70. Semlitsch, 1990, Paedomorphosis in Ambystoma talpoideum: maintenance of population variation and alternate life-history pathways, Evolution, 44, 1604, 10.2307/2409340 · DOI
  71. Shaffer, 1984, Evolution in a paedomorphic lineage. I. An electrophoretic analysis of Mexican ambystomatid salamanders, Evolution, 38, 1194, 10.2307/2408628 · DOI
  72. Shaffer, 1996, Phylogenetic and mechanistic analysis of a developmentally integrated character complex: alternate life history modes in ambystomatid salamanders, Amer. Zool., 36, 24, 10.1093/icb/36.1.24 · DOI
  73. Sket, 1994, A black, non-troglomorphic amphibian from the karst of Slovenia: Proteus anguinus parkelj n. ssp. (Urodela: Proteidae), Bijdr. Dierk., 64, 33, 10.1163/26660644-06401002 · DOI
  74. Sprules, 1974, The adaptive significance of paedogenesis in North American species of Ambystoma (Amphibia: Caudata): an hypothesis, Can. J. Zool., 52, 393, 10.1139/z74-047 · DOI
  75. Stanley, 1986, Population-size, extinction, and speciation: the fission effect in Neogene Bivalvia, Paleobiology, 12, 89, 10.1017/S0094837300003006 · DOI
  76. Stearns, 1992, The evolution of life histories
  77. Sweet, 1977, Natural metamorphosis in Eurycea neotenes, and the generic allocation of the Texas Eurycea (Amphibia: Plethodontidae), Herpetologica, 33, 364
  78. Syme, 2012, Dispersal between shallow and abyssal seas and evolutionary loss and regain of compound eyes in cylindroleberidid ostracods: conflicting conclusions from different comparative methods, Syst. Biol., 61, 314, 10.1093/sysbio/syr085 · DOI
  79. Timpe, 2009, Phylogeography of the Brownback Salamander reveals patterns of local endemism in Southern Appalachian springs, Mol. Phylogenet. Evol., 52, 368, 10.1016/j.ympev.2009.03.023 · DOI
  80. Valenzuela, 2011, Chromosome number and sex determination coevolve in turtles, Evolution, 65, 1808, 10.1111/j.1558-5646.2011.01258.x · DOI
  81. Van Auken, 1981, An ecological comparison of upland deciduous and evergreen forests of central Texas, Amer. J. Bot., 68, 1249, 10.2307/2443048 · DOI
  82. Vieites, 2007, Rapid diversification and dispersal during periods of global warming by plethodontid salamanders, Proc. Natl. Acad. Sci. U.S.A., 104, 19903, 10.1073/pnas.0705056104 · DOI
  83. Voss, 2012, Thyroid hormone responsive QTL and the evolution of paedomorphic salamanders, Heredity, 109, 293, 10.1038/hdy.2012.41 · DOI
  84. Wake, 1966, Comparative osteology and evolution of the lungless salamanders, Family Plethodontidae, Mem. So. Cal. Acad., 4, 1
  85. Weisrock, 2006, Multiple nuclear gene sequences identify phylogenetic species boundaries in the rapidly radiating clade of Mexican ambystomatid salamanders, Mol. Ecol., 15, 2489, 10.1111/j.1365-294X.2006.02961.x · DOI
  86. Whiteman, 1994, Evolution of facultative paedomorphosis in salamanders, Q. Rev. Biol., 69, 205, 10.1086/418540 · DOI
  87. Wiens, 2007, Global patterns of species richness and diversification in amphibians, Am. Nat., 170, S86, 10.1086/519396 · DOI
  88. Wiens, 2011, Re-evolution of lost mandibular teeth in frogs after more than 200 million years, and re-evaluating Dollo's law, Evolution, 65, 1283, 10.1111/j.1558-5646.2011.01221.x · DOI
  89. Wiens, 2003, When are phylogenetic analyses misled by convergence? A case study in Texas cave salamanders, Syst. Biol., 52, 501, 10.1080/10635150390218222 · DOI
  90. Wiens, 2005, Ontogeny discombobulates phylogeny: paedomorphosis and salamander relationships, Syst. Biol., 54, 91, 10.1080/10635150590906037 · DOI
  91. Wiens, 2006, Rapid diversification, incomplete isolation, and the “speciation clock” in North American salamanders (genus Plethodon): testing the hybrid swarm hypothesis of rapid radiation, Evolution, 60, 2585
  92. Wilbur, 1973, Ecological aspects of amphibian metamorphosis, Science, 182, 1305, 10.1126/science.182.4119.1305 · DOI
  93. Zhang, 2009, Higher-level salamander relationships and divergence dates inferred from complete mitochondrial genomes, Mol. Phylogenet. Evol., 53, 492, 10.1016/j.ympev.2009.07.010 · DOI

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    “Such conditions characterise lower elevations, but harsher terrestrial environments may also result in similar selection (shifting the balance of resources away from terrestrial habitats), which may also explain the possible association with high mountain - ous habitat (Bonett et al., 2014).”
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Metadata

Authors
Bonett, R. M., Steffen, M. A., Lambert, S. M., Wiens, J. J., & Chippindale, P. T.
Affiliations
  • University of Tulsa (US)
  • University of Arizona (US)
  • The University of Texas at Arlington (US)
ORCID
Venue
Evolution
Publisher
Oxford University Press (OUP)
Published
2013-10-16
Volume
68
Issue
2
Pages
466-482
ISSN
0014-3820 (ISSN-L)
DOI
10.1111/evo.12274
OpenAlex
W1489582768
Cited by
79
References
0
Citations by year
2026: 4 · 2025: 6 · 2024: 6 · 2023: 4 · 2022: 5 · 2021: 7 · 2020: 4 · 2019: 6 · 2018: 6 · 2017: 6 · 2016: 9 · 2015: 10 · 2014: 6
FWCI
6.33
Type
journal article
Language
en
Open access
closed
Licence
doi.wiley.com/10.1002/tdm_license_1.1 (tdm, 685 d)
Locations
  • Evolution (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • University of Tulsa, an Austin Community Foundation
  • National Science Foundation (DEB 1050322, DEB 0331747, DEB 0129242)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Amphibian and Reptile Biology
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Subterranean biodiversity and taxonomy
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
Keywords
paedomorphosis, plethodontid salamanders, metamorphosis, re-evolution, life history evolution, cave dwellings, range size, geographic dispersal, Eurycea, Edwards Plateau, phylogenetic comparative analysis, time-calibrated phylogeny
MeSH terms
Animals, Climate, Metamorphosis, Biological, Phylogeny, Caudata, Evolution, Molecular, Genetic Speciation, Caves

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CoChat. (2026). Citation check: EVOLUTION OF PAEDOMORPHOSIS IN PLETHODONTID SALAMANDERS: ECOLOGICAL CORRELATES AND RE-EVOLUTION OF METAMORPHOSIS. https://app.cochat.ai/papers/10.1111/evo.12274
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Bonett, R. M., Steffen, M. A., Lambert, S. M., Wiens, J. J., & Chippindale, P. T. (2014). EVOLUTION OF PAEDOMORPHOSIS IN PLETHODONTID SALAMANDERS: ECOLOGICAL CORRELATES AND RE-EVOLUTION OF METAMORPHOSIS. Evolution. https://doi.org/10.1111/evo.12274