[en] Observations on the ontogeny and diversity of salamanders provided some of the earliest evidence that shifts in developmental trajectories have made a substantial contribution to the evolution of animal forms. Since the dawn of evo-devo there have been major advances in understanding developmental mechanisms, phylogenetic relationships, evolutionary models, and an appreciation for the impact of ecology on patterns of development (eco-evo-devo). Molecular phylogenetic analyses have converged on strong support for the majority of branches in the Salamander Tree of Life, which includes 764 described species. Ancestral reconstructions reveal repeated transitions between life cycle modes and ecologies. The salamander fossil record is scant, but key Mesozoic species support the antiquity of life cycle transitions in some families. Colonization of diverse habitats has promoted phenotypic diversification and sometimes convergence when similar environments have been independently invaded. However, unrelated lineages may follow different developmental pathways to arrive at convergent phenotypes. This article summarizes ecological and endocrine based causes of life cycle transitions in salamanders, as well as consequences to body size, genome size, and skeletal structure. Salamanders offer a rich source of comparisons for understanding how the evolution of developmental patterns has led to phenotypic diversification following shifts to new adaptive zones.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Denoël, Mathieu ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire d'Écologie et de Conservation des Amphibiens
Language :
English
Title :
Repeated ecological and life cycle transitions make salamanders an ideal model for evolution and development
Publication date :
June 2022
Journal title :
Developmental Dynamics
ISSN :
1058-8388
eISSN :
1097-0177
Publisher :
John Wiley & Sons, Hoboken, United States - New York
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] NSF - National Science Foundation [US-VA] [US-VA]
Commentary :
This paper is published by Wiley (see DOI). It is part of the special issue: Salamander Models for Elucidating Mechanisms of Developmental Biology, Evolution & Regeneration/Repair: Part Two
Wake DB. Comparative osteology and evolution of the lungless salamanders, family Plethodontidae. Mem S California Acad Sci. 1966;4:1-111.
Wake DB. Homoplasy: the result of natural selection, or evidence of design limitations? Am Nat. 1991;138:543-567.
Weins JJ, Bonett RM, Chippindale PT. Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships. Syst Biol. 2005;54:91-110.
Bonett RM, Blair AL. Evidence for complex life cycle constraints on salamander body form diversification. PNAS. 2017;114:9936-9941.
Parra-Olea G, Wake DB. Extreme morphological and ecological homoplasy in tropical salamanders. PNAS. 2001;98:7888-7891.
Wiens JJ, Chippindale PT, Hillis DM. When are phylogenetic analyses misled by convergence? A case study in Texas cave salamanders. Syst Biol. 2003;52:501-514.
Whiteman HH. Evolution of facultative paedomorphosis in salamanders. Q Rev Biol. 1994;69:205-221.
Ryan TJ, Semlitsch RD. Intraspecific heterochrony and life history evolution: decoupling somatic and sexual development in a facultatively paedomorphic salamander. PNAS. 1998;95:5643-5648.
Denoël M, Joly P, Whiteman HH. Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biol Rev. 2005;80:663-671.
Morvan-Dubois G, Demeneix BA, Sachs LM. Xenopus laevis as a model for studying thyroid hormone signalling: from development to metamorphosis. Mol Cell Endocrinol. 2008;293:71-79.
Beck CW, Belmonte JCI, Christen B. Beyond early development: Xenopus as an emerging model for the study of regenerative mechanisms. Dev Dyn. 2009;238:1226-1248.
Shi YB. Animal metamorphosis. New York, USA: Academic Press; 2013.
Voss SR, Epperlein HH, Tanaka EM. Ambystoma mexicanum, the axolotl: a versatile amphibian model for regeneration, development, and evolution studies. Cold Spring Harb Protoc. 2009;8:pdb-emo128.
Ziermann JM, Diogo R. Cranial muscle development in the model organism Ambystoma mexicanum: implications for tetrapod and vertebrate comparative and evolutionary morphology and notes on ontogeny and phylogeny. Anat Rec. 2013;296:1031-1048.
Vlaskalin T, Wong CJ, Tsilfidis C. Growth and apoptosis during larval forelimb development and adult forelimb regeneration in the newt (Notophthalmus viridescens). Dev Genes Evol. 2004;214:423-431.
Kurosaka H, Takano-Yamamoto T, Yamashiro T, Agata T. Comparison of molecular and cellular events during lower jaw regeneration of newt (Cynops pyrrhogaster) and west African clawed frog (Xenopus tropicalis). Dev Dyn. 2008;237:354-365.
Hayashi T, Yokotani N, Tane S, et al. Molecular genetic system for regenerative studies using newts. Develop Growth Differ. 2013;55:229-236.
Kumar A, Gates PB, Czarkwiani A, Brockes JP. An orphan gene is necessary for preaxial digit formation during salamander limb development. Nat Commun. 2015;6:8684.
Suzuki M, Hayashi T, Inoue T, et al. Cas9 ribonucleoprotein complex allows direct and rapid analysis of coding and noncoding regions of target genes in Pleurodeles waltl development and regeneration. Dev Biol. 2018;443:127-136.
Joven A, Elewa A, Simon A. Model systems for regeneration: salamanders. Development. 2019;146:dev167700.
Roelants K, Gower DJ, Wilkinson M, et al. Global patterns of diversification in the history of modern amphibians. PNAS. 2007;104:887-892.
Hime PM, Lemmon AR, Lemmon ECM, et al. Phylogenomics reveals ancient gene tree discordance in the amphibian tree of life. Syst Biol. 2021;70:49-66.
Estes R. The fossil record of amphiumid salamanders. Breviora. 1969;322:1-11.
DeMar DG Jr. A new fossil salamander (Caudata, Proteidae) from the upper cretaceous (Maastrichtian) Hell Creek formation, Montana, USA. J Vertebr Paleontol. 2013;33:588-598.
Gardner JD. Revision of Habrosaurus Gilmore (Caudata; Sirenidae) and relationships among sirenid salamanders. Paléo. 2003;46:1089-1122.
Wilbur HM. Complex life cycles. Annu Rev Ecol Syst. 1980;11:67-93.
Laudet V. The origins and evolution of vertebrate metamorphosis. Curr Biol. 2011;21:R726-R737.
Holman JA. Fossil Salamanders of North America. Bloomington, IN: Indiana University Press; 2006.
Bonett RM, Trujano-Alvarez AL, Williams MJ, Timpe EK. Biogeography and body size shuffling of aquatic salamander communities on a shifting refuge. Proc R Soc B. 2013;280:20130200.
Bonett RM, Steffen MA, Lambert SM, Wiens JJ, Chippindale PT. Evolution of paedomorphosis in plethodontid salamanders: ecological correlates and re-evolution of metamorphosis. Evolution. 2014;68:466-482.
Mathiron AGE, Lena J-P, Baouch S, Denoël M. The ‘male escape hypothesis’: sex-biased metamorphosis in response to climatic drivers in a facultatively paedomorphic amphibian. Proc R Soc B. 2017;284:20170176.
Wake DB, Hanken J. Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis? Int J Dev Biol. 1996;40:859-869.
Wake DB. Adaptive radiation of salamanders in middle American cloud forests. Ann Mo Bot Gard. 1987;74:242-264.
Bonett RM, Steffen MA, Robison GA. Heterochrony repolarized: a phylogenetic analysis of developmental timing in plethodontid salamanders. EvoDevo. 2014;5:27.
Greven H. Larviparity and pueriparity. In: Sever DM, ed. Reproductive Biology and Phylogeny of Urodela. Vol 1. Plymouth, UK: Science Publishers, Inc.; 2003.
Buckley D, Alcobendas M, García-París M, Wake MH. Heterochrony, cannibalism, and the evolution of viviparity in Salamandra salamandra. Evol Dev. 2007;9:105-115.
Buckley D. Evolution of viviparity in salamanders (Amphibia, Caudata). eLS 2012.
Velo-Antón G, Santos X, Sanmartín-Villar I, Cordero-Rivera A, Buckley D. Intraspecific variation in clutch size and maternal investment in pueriparous and larviparous Salamandra salamandra females. Evol Ecol. 2015;29:185-204.
Semlitsch RD. Paedomorphosis in Ambystoma talpoideum: effects of density, food, and pond drying. Ecology. 1987;68:994-1002.
Denoël M, Ficetola GF. Heterochrony in a complex world: disentangling environmental processes of facultative paedomorphosis in an amphibian. J Anim Ecol. 2014;83:606-615.
Denoël M, Ficetola GF, Sillero N, et al. Traditionally managed landscapes do not prevent amphibian decline and the extinction of paedomorphosis. Ecol Monogr. 2019;89:e01347.
Bonett RM, Chippindale PT. Streambed microstructure predicts evolution of development and life history mode in the plethodontid salamander, Eurycea tynerensis. BMC Biol. 2006;4:1-12.
Emel SL, Bonett RM. Considering alternative life history modes and genetic divergence in conservation: a case study of the Oklahoma salamander. Conserv Genet. 2011;12:1243-1259.
Healy WR. Population consequences of alternative life histories in Notophthalmus v. viridescens. Copeia. 1974;1974:221-229.
Denoël M. Seasonal variation of morph ratio in facultatively paedomorphic populations of the palmate newt Triturus helveticus. Acta Oecol. 2006;29:165-170.
Cayuela H, Valenzuela-Sánchez A, Teulier L, et al. Determinants and consequences of dispersal in vertebrates with complex life cycles: a review of pond-breeding amphibians. Q Rev Biol. 2020;95:1-36.
Grayson KL, Bailey LL, Wilbur HM. Life history benefits of residency in a partially migrating pond-breeding amphibian. Ecology. 2011;92:1236-1246.
Liang F, Changyuan Y. Amphibians of China. Vol 1. Beijing, China: Science Press; 2016.
Etheridge K. The energetics of estivating sirenid salamanders (Siren lacertina and Pseudobranchus striatus). Herpetologica. 1990;46:407-414.
Smith ME, Secor SM. Physiological responses to fasting and estivation for the three-toed Amphiuma (Amphiuma tridactylum). Physiol Biochem Zool. 2017;90:240-256.
Jarvis LE. Terrestrial ecology of juvenile great crested newts (Triturus cristatus) in a woodland area. Herpetol J. 2016;26:287-296.
Denoël M, Joly P. Adaptive significance of facultative paedomorphosis in Triturus alpestris (Amphibia, Caudata): resource partitioning in an alpine lake. Freshw Biol. 2001;46:1387-1396.
Blankers T, Adams DC, Wiens JJ. Ecological radiation with limited morphological diversification in salamanders. J Evol Biol. 2012;25:634-646.
Baken EK, Adams DC. Macroevolution of arboreality in salamanders. Ecol Evol. 2019;9:7005-7016.
Gould SJ. Ontogeny and Phylogeny. Cambridge, MA: Harvard University Press; 1977.
Alberch P, Gould SJ, Oster GF, Wake DB. Size and shape in ontogeny and phylogeny. Paleobiology. 1979;5:296-317.
McKinney ML, KJ MN. Heterochrony. The Evolution of Ontogeny. New York: Plenum Press; 1991.
Bonett RM. In: Nuño de la Rosa L, de la Müller G, eds. Heterochrony. Evolutionary Developmental Biology. Springer International Publishing; 2018:1-14.
Denoël M, Joly P. Neoteny and progenesis as two heterochronic processes involved in paedomorphosis in Triturus alpestris (Amphibia: Caudata). Proc R Soc B. 2000;267:1481-1485.
Bonett RM. An integrative endocrine model for the evolution of developmental timing and life history of plethodontids and other salamanders. Copeia. 2016;104:209-221.
Norris DO, Carr JA. Vertebrate Endocrinology. New York, USA: Academic Press; 2020.
Buchholz DR, Paul BD, Fu L, Shi Y-B. Molecular and developmental analyses of thyroid hormone receptor function in Xenopus laevis, the African clawed frog. Gen Comp Endocrinol. 2006;145:1-19.
Denver RJ. Stress hormones mediate environment-genotype interactions during amphibian development. Gen Comp Endocrinol. 2009;164:20-31.
Johnson CK, Voss SR. Salamander paedomorphosis: linking thyroid hormone to life history and life cycle evolution. Curr Top Dev Biol. 2013;103:229-258.
Vu M, Trudeau VL. Neuroendocrine control of spawning in amphibians and its practical applications. Gen Comp Endocrinol. 2016;234:28-39.
Gudernatsch JF. Feeding experiments on tadpoles: I. the influence of specific organs given as food on growth and differentiation. A contribution to the knowledge of organs with internal secretion. Rouxs Arch Dev Biol. 1912;35:457-483.
Allen BM. The response of Bufo larvae to different concentrations of thyroxin. Anat Rec. 1932;54:45-64.
Allen BM. Extirpation of the hypophysis and thyroid glands of Rana pipiens. Science. 1916;44:755-757.
Allen BM. The results of thyroid removal in the larvae of Rana pipiens. J Exp Zool. 1918;24:499-519.
Hoskins ER, Hoskins MM. Growth and development of amphibia as affected by thyroidectomy. J Exp Zool. 1919;29:1-69.
Hanaoka Y. Uptake of 131I by the thyroid gland during metamorphosis in Xenopus. J Fac Sci, Hokkaido Univ, Ser 6. 1966;16:106-112.
Dent JN. The embryonic development of Plethodon cinereus as correlated with the differentiation and functioning of the thyroid gland. J Morphol. 1942;71:577-601.
Hanken J, Jennings DH, Olsson L. Mechanistic basis of life-history evolution in anuran amphibians: direct development. Am Zool. 1997;37:160-171.
Elinson RP. Metamorphosis in a frog that does not have a tadpole. Curr Top Dev Biol. 2013;103:259-276.
Regard E. Cytophysiology of the amphibian thyroid gland, through larval development and metamorphosis. Int Rev Cytol Suppl. 1978;52:81-118.
Suzuki S, Suzuki M. Changes in thyroidal and plasma lodine compounds during and after metamorphosis of the bullfrog, Rana catesbeiana. Gen Comp Endocrinol. 1981;45:74-81.
Alberch P, Gale EA, Larsen PR. Plasma T4 and T3 levels in naturally metamorphosing Eurycea bislineata (Amphibia; Plethodontidae). Gen Comp Endocrinol. 1986;61:153-162.
Norman MF, Carr JA, Norris DO. Adenohypophysial-thyroid activity of the tiger salamander, Ambystoma tigrinum, as a function of metamorphosis and captivity. J Exp Zool. 1987;242:55-66.
Voss SR, Kump DK, Walker JA, Shaffer HB, Voss GJ. Thyroid hormone responsive QTL and the evolution of paedomorphic salamanders. Heredity. 2012;109:293-298.
Noble GK. The 'retrograde metamorphosis' of the Sirenidae; experiments on the functional activity of the thyroid of the perennibranchs. Anat Rec. 1924;29:100.
Noble GK, Farris EJ. A metamorphic change produced in Cryptobranchus by thyroid solutions. Anat Rec. 1929;42:59.
Kezer J. Thyroxine-induced metamorphosis of the neotenic salamanders Eurycea tynerensis and Eurycea neotenes. Copeia. 1952;4:234-237.
Kobayashi H, Gorbman A. Thyroid function in Amphiuma. Gen Comp Endocrinol. 1962;2:279-282.
Švob M, Musafija A, Frank F, et al. Response of tail fin of Proteus anguinus to thyroxine. J Exp Zool. 1973;184:341-343.
Safi R, Vlaeminck-Guillem V, Duffraisse M, et al. Pedomorphosis revisited: thyroid hormone receptors are functional in Necturus maculosus. Evol Dev. 2006;8:284-292.
Aran RP, Steffen MA, Martin SD, Lopez OI, Bonett RM. Reduced effects of thyroid hormone on gene expression and metamorphosis in a paedomorphic plethodontid salamander. J Exp Zool B Mol Dev Evol. 2014;322B:294-303.
Vlaeminck-Guillem V, Safi R, Guillem P, Leteurtre E, Duterque-Coquillaud M, Laudet V. Thyroid hormone receptor expression in the obligatory paedomorphic salamander Necturus maculosus. Int J Dev Biol. 2004;50:553-560.
Crespi EJ, Williams TD, Jessop TS, Delehanty B. Life history and the ecology of stress: how do glucocorticoid hormones influence life-history variation in animals? Funct Ecol. 2013;27:93-106.
Gomez-Mestre I, Kulkarni S, Buchholz DR. Mechanisms and consequences of developmental acceleration in tadpoles responding to pond drying. PLoS One. 2013;8:e84266.
Glennemeier KA, Denver RJ. Role for corticoids in mediating the response of Rana pipiens tadpoles to intraspecific competition. J Exp Zool. 2002;292:32-40.
Middlemis Maher J, Werner EE, Denver RJ. Stress hormones mediate predator-induced phenotypic plasticity in amphibian tadpoles. Proc R Soc B. 2013;280:20123075.
Bonett RM, Hoopfer ED, Denver RJ. Molecular mechanisms of corticosteroid synergy with thyroid hormone during tadpole metamorphosis. Gen Comp Endocrinol. 2010;168:209-219.
Kulkarni SS, Buchholz DR. Beyond synergy: corticosterone and thyroid hormone have numerous interaction effects on gene regulation in Xenopus tropicalis tadpoles. Endocrinology. 2012;153:5309-5324.
Bagamasbad PD, Bonett RM, Sachs L, et al. Deciphering the regulatory logic of an ancient, ultraconserved nuclear receptor enhancer module. Mol Endocrinol. 2015;29:856-872.
Bonett RM, Hu F, Bagamasbad P, Denver RJ. Stressor and glucocorticoid-dependent induction of the immediate early gene Krüppel-like factor 9 (KLF9): implications for neural development and plasticity. Endocrinology. 2009;150:1757-1765.
Sachs LM, Buchholz DR. Insufficiency of thyroid hormone in frog metamorphosis and the role of glucocorticoids. Front Endocrinol. 2019;10:287.
Shewade LH, Schoephoerster JA, Patmann MD, Kulkarni SS, Buchholz DR. Corticosterone is essential for survival through frog metamorphosis. Endocrinology. 2020;161:bqaa193.
Sterner ZR, Shewade LH, Mertz KM, Sturgeon SM, Buchholz DR. Glucocorticoid receptor is required for survival through metamorphosis in the frog Xenopus tropicalis. Gen Comp Endocrinol. 2020;291:113419.
Denoël M. How do paedomorphic newts cope with lake drying? Ecography. 2003;26:405-410.
Beachy CK, Ryan TJ, Bonett RM. How metamorphosis is different in Plethodontids: larval life history perspectives on life-cycle evolution. Herpetologica. 2017;73:252-258.
Kühn ER, Groef BD, Grommen SVH, der Greyton SV, Darras VM. Low submetamorphic doses of dexamethasone and thyroxine induce complete metamorphosis in the axolotl (Ambystoma mexicanum) when injected together. Gen Comp Endocrinol. 2004;137:141-147.
Kühn ER, Groef BD, der Greyton SV, Darras VM. Corticotropin-releasing hormone-mediated metamorphosis in the neotenic axolotl Ambystoma mexicanum: synergistic involvement of thyroxine and corticoids on brain type II deiodinase. Gen Comp Endocrinol. 2005;143:75-81.
Salthe SN, Mechan JS. Reproductive and courtship patterns. In: Lofts B, ed. Physiology of the Amphibia. Vol 2. New York and London: Academic Press; 1974.
Griffiths RA. Newts and Salamanders of Europe. London: T. & A. D. Poyser Natural History; 1996.
Canavero A, Arim M. Clues supporting photoperiod as the main determinant of seasonal variation in amphibian activity. J Nat Hist. 2009;43:2975-2984.
Dervo BK, Bærum KM, Skurdal J, Museth J. Effects of temperature and precipitation on breeding migrations of amphibian species in southeastern Norway. Scientifica. 2016;2016:2016.
Werner JK. Temperature-photoperiod effects on spermatogenesis in the salamander Plethodon cinereus. Copeia. 1969;1969:592-602.
Paniagua R, Fraile B, Sáez FJ. Effects of photoperiod and temperature on testicular function in amphibians. Histol Histopathol. 1990;5:365-378.
Delgado MJ, Alonso-Gómez AL, Alonso-Bedate M. Role of environmental temperature and photoperiod in regulation of seasonal testicular activity in the frog, Rana perezi. Can J Phys. 1992;70:1348-1352.
Horseman ND, Smith CA, Culley DD Jr. Effects of age and photoperiod on ovary size and condition in bullfrogs (Rana catesbeiana Shaw) (Amphibia, Anura, Ranidae). J Herpetol. 1978;12:287-290.
Saidapur SK, Hoque B. Effect of photoperiod and temperature on ovarian cycle of the frog Rana tigrina (Daud.). J Biosci. 1995;20:445-452.
Fitzpatrick LC. Life history patterns of storage and utilization of lipids for energy in amphibians. Am Zool. 1976;16:725-732.
Bender MC, Hu C, Pelletier C, Denver RJ. To eat or not to eat: ontogeny of hypothalamic feeding controls and a role for leptin in modulating life-history transition in amphibian tadpoles. Proc R Soc B. 2018;285:1-10.
Boswell T, Dunn IC, Wilson PW, Joseph N, Burt DW, Sharp PJ. Identification of a non-mammalian leptin-like gene: characterization and expression in the tiger salamander (Ambystoma tigrinum). Gen Comp Endocrinol. 2006;146:157-166.
Flood DEK, Fernandino JI, Langlois VS. Thyroid hormones in male reproductive development: evidence for direct crosstalk between the androgen and thyroid hormone axes. Gen Comp Endocrinol. 2013;192:2-14.
Duarte-Guterman P, Navarro-Martín L, Trudeau VL. Mechanisms of crosstalk between endocrine systems: regulation of sex steroid hormone synthesis and action by thyroid hormones. Gen Comp Endocrinol. 2014;203:69-85.
Wakahara M. Spermatogenesis is extraordinarily accelerated in metamorphosis-arrested larvae of a salamander, Hynobius retardatus. Experientia. 1994;50:94-98.
Kanki K, Wakahara M. Precocious testicular growth in metamorphosis-arrested larvae of a salamander Hynobius retardatus: role of thyroid-stimulating hormone. J Exp Zool. 1999;283:548-558.
Rot-Nikcevic I, Wassersug RJ. Arrested development in Xenopus laevis tadpoles: how size constrains metamorphosis. J Exp Biol. 2004;207:2133-2145.
Gray KM, Janssens PA. Gonadal hormones inhibit the induction of metamorphosis by thyroid hormones in Xenopus laevis tadpoles in vivo, but not in vitro. Gen Comp Endocrinol. 1990;77:202-211.
Hogan NS, Duarte P, Wade MG, Lean DR, Trudeau VL. Estrogenic exposure affects metamorphosis and alters sex ratios in the northern leopard frog (Rana pipiens): identifying critically vulnerable periods of development. Gen Comp Endocrinol. 2008;156:515-523.
Denoël M, Drapeau L, Oromi N, Winandy L. The role of predation risk in metamorphosis versus behavioural avoidance: a sex-specific study in a facultative paedomorphic amphibian. Oecologia. 2019;189:637-645.
Schluter D, Price TD, Rowe L. Conflicting selection pressures and life history trade-offs. Proc R Soc B. 1991;246:11-17.
Moran NA. Adaptation and constraint in the complex life cycles of animals. Annu Rev Ecol Syst. 1994;25:573-600.
Sherratt E, Vidal-García M, Anstis M, Keogh JS. Adult frogs and tadpoles have different macroevolutionary patterns across the Australian continent. Nat Ecol Evol. 2017;1:1385-1391.
Bonett RM, Hess AJ, Ledbetter NM. Facultative transitions have trouble committing, but stable life cycles predict salamander genome size evolution. Evol Biol. 2020;47:111-122.
Bruce RC. Size-mediated tradeoffs in life-history traits in dusky salamanders. Copeia. 2013;2013:262-267.
Phung TX, Nascimento JCS, Novarro AJ, Wiens JJ. Correlated and decoupled evolution of adult and larval body size in frogs. Proc R Soc B. 2020;287:20201474.
Hairston NG Sr. Species packing in Desmognathus salamanders: experimental demonstration of predation and competition. Am Nat. 1986;127:266-291.
Kozak KH, Larson A, Bonett RM, Harmon LJ. Phylogenetic analysis of ecomorphological divergence, community structure, and diversification rates in dusky salamanders (Plethodontidae: Desmognathus). Evolution. 2005;59:2000-2016.
Kozak KH, Mendyk RW, Wiens JJ. Can parallel diversification occur in sympatry? Repeated patterns of body-size evolution in coexisting clades of north American salamanders. Evolution. 2009;63:1769-1784.
Miaud C, Guyetant R, Faber H. Age, size, and growth of the alpine newt, Triturus alpestris (Urodela: Salamandridae), at high altitude and a review of life-history trait variation throughout its range. Herpetologica. 2000;56:135-144.
Grossenbacher K. Untersuchungen zur Entwicklungsgeschwindigkeit der Larven von Triturus a. alpestris (Laurenti 1768), Bufo B. bufo (Linnaeus 1758) und Rana t. temporaria (Linnaeus 1758) aus Populationen verschiedener Hoehenstufen in den Schweizer Alpen [PhD Thesis]. Bern: Universität Bern; 1979.
Fasola M. Resource partitioning by three species of newts during their aquatic phase. Ecography. 1993;16:73-81.
Whiteman HH, Wissinger S, Denoël M, Mecklin C, Gerlanc N, Gutrich J. Larval growth in polyphenic salamanders: making the best of a bad lot. Oecologia. 2012;168:109-118.
Denoël M. On the identification of paedomorphic and overwintering larval newts based on cloacal shape: review and guidelines. Curr Zool. 2017;63:165-173.
Ivanović A, Cvijanović M, Denoël M, Slijepčević M, Kalezić ML. Facultative paedomorphosis and the pattern of inter- and intraspecific variation in cranial skeleton: lessons from European newts (Ichthyosaura alpestris and Lissotriton vulgaris). Zoomorphology. 2014;133:99-109.
Denoël M, Ivanović A, Džukić G, Kalezić ML. Sexual size dimorphism in the evolutionary context of facultative paedomorphosis: insights from European newts. BMC Evol Biol. 2009;9:278.
Lejeune B, Bissey L, Didaskalou EA, Sturaro N, Lepoint G, Denoël M. Progenesis as an intrinsic factor of ecological opportunity in a polyphenic amphibian. Funct Ecol. 2021;35:546-560.
Denoël M, Drapeau L, Winandy L. Reproductive fitness consequences of progenesis: sex-specific payoffs in safe and risky environments. J Evol Biol. 2019;32:629-637.
Wiens JJ, Hoverman JT. Digit reduction, body size, and paedomorphosis in salamanders. Evol Dev. 2008;10:449-463.
Gregory TR. Nucleotypic effects without nuclei: genome size and erythrocyte size in mammals. Genome. 2000;43:895-901.
Licht LE, Lowcock LA. Genome size and metabolic rate in salamanders. Comp Biochem Physiol B. 1991;100B:83-92.
Vinogradov AE. Nucleotypic effect in homeotherms: body-mass-corrected basal metabolic rate of mammals is related to genomic size. Evolution. 1995;49:1249-1259.
Vinogradov AE. Nucleotypic effect in homeotherms: body-mass independent resting metabolic rate of passerine birds is related to genome size. Evolution. 1997;51:220-225.
Gregory TR. A bird's-eye view of the C-value enigma: genome size, cell size, and metabolic rate in the class Aves. Evolution. 2002;56:121-130.
Gregory TR. The Evolution of the Genome. New York, USA: Elsevier; 2005.
Starostova Z, Kubička L, Konarzewski M, Kozłowski J, Kratochvíl L. Cell size but not genome size affects scaling of metabolic rate in eyelid geckos. Am Nat. 2009;174:E100-E105.
Jockusch EL. An evolutionary correlate of genome size change in plethodontid salamanders. Proc R Soc B. 1997;264:597-604.
Gregory TR. Genome size and developmental complexity. Genetica. 2002;115:131-146.
Sessions SK, Larson A. Developmental correlates of genome size in plethodontid salamanders and their implications for genome evolution. Evolution. 1987;41:1239-1251.
Wake DB, Marks SB. Development and evolution of plethodontid salamanders: a review of prior studies and a prospectus for future research. Herpetologica. 1993;49:194-203.
Brown DD, Dawid IB. Specific gene amplification in oocytes. Science. 1968;160:272-280.
Ledbetter NM, Bonett RM. Terrestriality constrains salamander limb diversification: implications for the evolution of pentadactyly. J Evol Biol. 2019;32:1-11.
Martin C, Gordon R. Differentiation trees, a junk DNA molecular clock, and the evolution of neoteny in salamanders. J Evol Biol. 1995;8:339-354.
Sessions SK. Evolutionary cytogenetics in salamanders. Chromosom Res. 2008;16:183-201.
Goin OB, Goin CJ, Bachmann K. DNA and amphibian life history. Copeia. 1968;1968:532-540.
Lertzman-Lepofsky G, Mooers AØ, Greenberg DA. Ecological constraints associated with genome size across salamander lineages. Proc R Soc B. 2019;286:20191780.
Roth G, Nishikawa KC, Wake DB. Genome size, secondary simplification, and the evolution of the brain in salamanders. Brain Behav Evol. 1997;50:50-59.
Wake DB, Wake MH, Specht CD. Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science. 2011;331:1032-1035.
Lynch M, Conery JS. The origins of genome complexity. Science. 2003;302:1401-1405.
Itgen MW, Prša P, Janža R, et al. Genome size diversification in central American bolitoglossine salamanders (Caudata: Plethodontidae). Copeia. 2019;107:560-566.
Mohlhenrich ER, Mueller RL. Genetic drift and mutational hazard in the evolution of salamander genomic gigantism. Evolution. 2016;70:2865-2878.
Liedtke HC, Gower DJ, Wilkinson M, Gómez-Mestre I. Macroevolutionary shift in the size of amphibian genomes and the role of life history and climate. Nat Ecol Evol. 2018;2:1792-1799.
Decena-Segarra LP, Bizjak-Mali L, Kladnik A, Sessions SK, Rovito SM. Miniaturization, genome size, and biological size in a diverse clade of salamanders. Am Nat. 2020;196:634-648.
Cavalier-Smith T. Coevolution of vertebrate genome, cell, and nuclear sizes. In: Ghiara G, ed. Symposium on the Evolution of Terrestrial Vertebrates. Mucchi: Modena; 1991:51-86.
Beaulieu JM, Leitch IJ, Patel S, Pendharkar A, Knight CA. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytol. 2008;179:975-986.
Mueller RL. Genome biology and the evolution of cell-size diversity. Cold Spring Harb Perspect Biol. 2015;7:a019125.
Roth G, Rottluff B, Grunwald W, Hanken J, Linke R. Miniaturization in plethodontid salamanders (Caudata: Plethodontidae) and its consequences for the brain and visual system. Biol J Linn Soc. 1990;40:165-190.
Hanken J, Wake DB. Miniaturization of body size: organismal consequences and evolutionary significance. Annu Rev Ecol Evol Syst. 1993;24:501-519.
Levy DL, Heald R. Biological scaling problems and solutions in amphibians. Cold Spring Harb Perspect Biol. 2016;8:a019166.
Grigoryan EN, Radugina EA. Behavior of stem-like cells, precursors for tissue regeneration in Urodela, under conditions of microgravity. Stem Cells Dev. 2019;28:423-437.
Sessions SK, Wake DB. Forever young: linking regeneration and genome size in salamanders. Dev Dyn. 2020; in press.
Ferner JW. A review of marking techniques for amphibians and reptiles. Society for the Study of Amphibians and Reptiles; 1979.
Ott JA, Scott DE. Effects of toe-clipping and PIT-tagging on growth and survival in metamorphic Ambystoma opacum. J Herpetol. 1999;33:344-348.
Monaghan JR, Stier AC, Michonneau F, et al. Experimentally induced metamorphosis in axolotls reduces regenerative rate and fidelity. Regeneration. 2014;1:2-14.
Polezhayev LW. The loss and restoration of regenerative capacity in the limbs of tailless amphibia. Biol Rev. 1946;21:141-147.
Goss RJ. Principles of Regeneration. New York, NY: Academic Press; 1969.
Muneoka K, Holler-Dinsmore G, Bryant SV. Intrinsic control of regenerative loss in Xenopus laevis limbs. J Exp Zool. 1986;240:47-54.
Fröbisch NB, Shubin NH. Salamander limb development: integrating genes, morphology, and fossils. Dev Dyn. 2011;240:1087-1099.
Pierce SP, Clack JA, Hutchinson JR. Three-dimensional limb joint mobility in the early tetrapod Ichthyostega. Nature. 2012;486:523-526.
Pierce SP, Hutchinson JR, Clack JA. Historical perspectives on the evolution of tetrapodomorph movement. Integr Comp Biol. 2013;53:209-223.
Brockes JP, Gates P. Mechanisms underlying vertebrate limb regeneration: lessons from the salamander. Biochem Soc Trans. 2014;42:625-630.
Bonett RM, Phillips JG, Ledbetter NM, Martin SD, Lehman L. Rapid phenotypic evolution following shifts in life cycle complexity. Proc R Soc B. 2018;285:20172304.
Colleoni E, Denoël M, Padoa-Schioppa E, Scali S, Ficetola GF. Rensch's rule and sexual dimorphism in salamanders: patterns and potential processes. J Zool. 2014;293:143-151.
Reece JS, Mehta RS. Evolutionary history of elongation and maximum body length in moray eels (Anguilliformes: Muraenidae). Biol J Linn Soc. 2013;109:861-875.
Caldwell MW. "without a leg to stand on": on the evolution and development of axial elongation and limblessness in tetrapods. Can J Earth Sci. 2003;40:573-588.
Dwaraka VB, Voss SR. Towards comparative analyses of salamander limb regeneration. J Exp Zool. 2021;336:129-144.
Dequéant ML, Pourquié O. Segmental patterning of the vertebrate embryonic axis. Nat Rev Genet. 2008;9:370-382.
Duboc V, Logan MP. Regulation of limb bud initiation and limb-type morphology. Dev Dyn. 2011;240:1017-1027.
Buckley D, Molnár V, Németh G, Petneházy O, Vörös J. ‘Monster…-omics’: on segmentation, re-segmentation, and vertebrae formation in amphibians and other vertebrates. Front Zool. 2013;10:17.
Torok MA, Gardiner DM, Izpisúa-Belmonte JC, Bryant SV. Sonic hedgehog (shh) expression in developing and regenerating axolotl limbs. J Exp Zool. 1999;284:197-206.
Han MJ, An JY, Kim WS. Expression patterns of Fgf-8 during development and limb regeneration of the axolotl. Dev Dyn. 2001;220:40-48.
Christensen RN, Weinstein M, Tassava RA. Expression of fibroblast growth factors 4, 8, and 10 in limbs, flanks, and blastemas of Ambystoma. Dev Dyn. 2002;223:193-203.
Imokawa Y, Yoshizato K. Expression of Sonic hedgehog gene in regenerating newt limb blastemas recapitulates that in developing limb buds. PNAS. 1997;94:9159-9164.
Stocum DL, Dearlove GE. Epidermal-mesodermal interaction during morphogenesis of the limb regeneration blastema in larval salamanders. J Exp Zool. 1972;181:49-61.
Garza-Garcia AA, Driscoll PC, Brockes JP. Evidence for the local evolution of mechanisms underlying limb regeneration in salamanders. Integr Comp Biol. 2010;50:528-535.
Ward AB, Mehta RS. Axial elongation in fishes: using morphological approaches to elucidate developmental mechanisms in studying body shape. Integr Comp Biol. 2010;50:1106-1119.
Bajard L, Morelli LG, Ares S, Pécréaux J, Jülicher F, Oates AC. Wnt-regulated dynamics of positional information in zebrafish somitogenesis. Development. 2014;141:1381-1391.
Alberch P, Gale EA. A developmental analysis of an evolutionary trend: digital reduction in amphibians. Evolution. 1985;39:8-23.
Fabre AC, Bardua C, Bon M, et al. Metamorphosis shapes cranial diversity and rate of evolution in salamanders. Nat Ecol Evol. 2020;4:1129-1140.