1932

Abstract

Parenting is considered a key evolutionary innovation that contributed to the diversification and expansion of vertebrates. However, we know little about how such diversity evolved. Amphibians are an ideal group in which to identify the ecological factors that have facilitated or constrained the evolution of different forms of parental care. Among, but also within, the three amphibian orders—Anura, Caudata, and Gymnophiona—there is a high level of variation in habitat use, fertilization mode, mating systems, and parental sex roles. Recent work using broad phylogenetic, experimental, and physiological approaches has helped to uncover the factors that have selected for the evolution of care and transitions between different forms of parenting. Here, we highlight the exceptional diversity of amphibian parental care, emphasize the unique opportunities this group offers for addressing key questions about the evolution of parenting, and give insights into promising novel directions of research.

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2023-11-02
2024-06-18
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Literature Cited

  1. Alford RA. 1999. Ecology: resource use, competition and predation. Tadpoles. The Biology of Anuran Larvae RW McDiarmid, R Altig 240–78. Chicago: Univ. Chicago Press
    [Google Scholar]
  2. Altig R, McDiarmid RW. 2007. Morphological diversity and evolution of egg and clutch structure in amphibians. Herpetol. Monogr. 21:1–32
    [Google Scholar]
  3. Balshine S 2012. Patterns of parental care in vertebrates. The Evolution of Parental Care NJ Royle, PT Smiseth, M Kölliker 62–80. Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  4. Barnett JB, Michalis C, Anderson HM, McEwen BL, Yeager J et al. 2020. Imperfect transparency and camouflage in glass frogs. PNAS 117:12885–90
    [Google Scholar]
  5. Beck KB, Loretto M-C, Ringler M, Hödl W, Pašukonis A. 2017. Relying on known or exploring for new? Movement patterns and reproductive resource use in a tadpole-transporting frog. PeerJ 5:e3745
    [Google Scholar]
  6. Bickford DP. 2004. Differential parental care behaviors of arboreal and terrestrial microhylid frogs from Papua New Guinea. Behav. Ecol. Sociobiol 55:402–9
    [Google Scholar]
  7. Bourne GR. 1998. Amphisexual parental behavior of a terrestrial breeding frog Eleutherodactylus johnstonei in Guyana. Behav. Ecol. 9:1–7
    [Google Scholar]
  8. Brooks OL, James JJ, Saporito RA. 2023. Maternal chemical defenses predict offspring defenses in a dendrobatid poison frog. Oecologia 201:385–96
    [Google Scholar]
  9. Brown JL, Morales VR, Summers K. 2010. A key ecological trait drove the evolution of biparental care and monogamy in an amphibian. Am. Nat. 175:436–46
    [Google Scholar]
  10. Brown JL, Twomey E, Morales VR, Summers K. 2008. Phytotelm size in relation to parental care and mating strategies in two species of Peruvian poison frogs. Behaviour 145:1139–65
    [Google Scholar]
  11. Brust DG. 1993. Maternal brood care by Dendrobates pumilio: a frog that feeds its young. J. Herpetol. 27:96–98
    [Google Scholar]
  12. Buxton VL, Sperry JH. 2016. Reproductive decisions in anurans: a review of how predation and competition affects the deposition of eggs and tadpoles. BioScience 67:26–38
    [Google Scholar]
  13. Cabeza-Alfaro O, Valenzuela-Sánchez A, Alvarado-Rybak M, Serrano JM, Azat C. 2021. First case of male alloparental care in amphibians: tadpole stealing in Darwin's frogs. Endang. Species Res. 45:331–35
    [Google Scholar]
  14. Carvajal-Castro JD, Vargas-Salinas F, Casas-Cardona S, Rojas B, Santos JC. 2021. Aposematism facilitates the diversification of parental care strategies in poison frogs. Sci. Rep. 11:19047
    [Google Scholar]
  15. Caspers BA, Steinfartz S, Krause ET. 2015. Larval deposition behaviour and maternal investment of females reflect differential habitat adaptation in a genetically diverging salamander population. Behav. Ecol. Sociobiol. 69:407–13
    [Google Scholar]
  16. Crump ML. 1996. Parental care among the Amphibia. Parental Care: Evolution, Mechanisms, and Adaptive Significance JS Rosenblatt, CT Snowdon 109–44. Adv. Study Behav. 25 New York: Elsevier
    [Google Scholar]
  17. Crump ML. 2015. Anuran reproductive modes: evolving perspectives. J. Herpetol. 49:1–16
    [Google Scholar]
  18. Cuestas Carrillo JF, Santana DJ, Prado CP 2022. Body condition of females during tadpole attendance and its potential costs in a Neotropical foam-nesting frog (Leptodactylus podicipinus). Ethol. Ecol. Evol. 35:2208–21
    [Google Scholar]
  19. del Pino EM. 2018. The extraordinary biology and development of marsupial frogs (Hemiphractidae) in comparison with fish, mammals, birds, amphibians and other animals. Mech. Dev. 154:2–11
    [Google Scholar]
  20. Delia J, Bravo-Valencia L, Warkentin KM. 2017. Patterns of parental care in Neotropical glassfrogs: fieldwork alters hypotheses of sex-role evolution. J. Evol. Biol. 30:898–914
    [Google Scholar]
  21. Delia J, Bravo-Valencia L, Warkentin KM. 2020. The evolution of extended parental care in glassfrogs: Do egg-clutch phenotypes mediate coevolution between the sexes?. Ecol. Monogr. 90:e01411
    [Google Scholar]
  22. Delia JRJ, Ramírez-Bautista A, Summers K. 2013. Parents adjust care in response to weather conditions and egg dehydration in a Neotropical glassfrog. Behav. Ecol. Sociobiol. 67:557–69
    [Google Scholar]
  23. Diesel R, Baurle G, Vogel P. 1995. Cave breeding and froglet transport: a novel pattern of anuran brood care in the Jamaican frog, Eleutherodactylus cundalli. Copeia 1995.354–60
    [Google Scholar]
  24. Ding J, Liao N, Zheng Y, Yang L, Zhou H et al. 2020. The composition and function of pigeon milk microbiota transmitted from parent pigeons to squabs. Front. Microbiol. 11:1789
    [Google Scholar]
  25. Dugas MB, Moore MP, Martin RA, Richards-Zawacki CL, Sprehn CG. 2016. The pay-offs of maternal care increase as offspring develop, favouring extended provisioning in an egg-feeding frog. J. Evol. Biol. 29:1977–85
    [Google Scholar]
  26. Endler JA. 2015. Writing scientific papers, with special reference to evolutionary ecology. Evol. Ecol. 29:465–78
    [Google Scholar]
  27. Erich M, Ringler M, Hödl W, Ringler E. 2015. Brood-partitioning behaviour in unpredictable environments: hedging the bets?. Behav. Ecol. Sociobiol. 69:1011–17
    [Google Scholar]
  28. Fischer EK, Hauber ME, Bell AM. 2021. Back to the basics? Transcriptomics offers integrative insights into the role of space, time and the environment for gene expression and behaviour. Biol. Lett. 17:20210293
    [Google Scholar]
  29. Fischer EK, Nowicki JP, O'Connell LA 2019a. Evolution of affiliation: patterns of convergence from genomes to behaviour. Phil. Trans. R. Soc. B 374:20180242
    [Google Scholar]
  30. Fischer EK, O'Connell LA 2020. Hormonal and neural correlates of care in active versus observing poison frog parents. Horm. Behav. 120:104696
    [Google Scholar]
  31. Fischer EK, Roland AB, Moskowitz NA, Tapia EE, Summers K et al. 2019b. The neural basis of tadpole transport in poison frogs. Proc. R. Soc. B 286:20191084
    [Google Scholar]
  32. Fischer EK, Roland AB, Moskowitz NA, Vidoudez C, Ranaivorazo N et al. 2019c. Mechanisms of convergent egg provisioning in poison frogs. Curr. Biol. 29:4145–51.e3
    [Google Scholar]
  33. Forester DC. 1984. Brooding behavior by the mountain dusky salamander: Can the female's presence reduce clutch desiccation?. Herpetologica 40:105–9
    [Google Scholar]
  34. Fouilloux CA, Serrano Rojas SJ, Carvajal-Castro JD, Valkonen JK, Gaucher P et al. 2021. Pool choice in a vertical landscape: tadpole-rearing site flexibility in phytotelm-breeding frogs. Ecol. Evol. 11:9021–38
    [Google Scholar]
  35. Frost DR. 2023. Amphibian Species of the World: An Online Reference. Version 6.1. American Museum of Natural History https://amphibiansoftheworld.amnh.org/index.php
    [Google Scholar]
  36. Furness AI, Capellini I. 2019. The evolution of parental care diversity in amphibians. Nat. Commun. 10:4709
    [Google Scholar]
  37. Furness AI, Venditti C, Capellini I. 2022. Terrestrial reproduction and parental care drive rapid evolution in the trade-off between offspring size and number across amphibians. PLOS Biol 20:e3001495
    [Google Scholar]
  38. Goicoechea O, Garrido O, Jorquera B. 1986. Evidence for a trophic paternal-larval relationship in the frog Rhinoderma darwinii. J. Herpetol. 20:168–78
    [Google Scholar]
  39. Gomez-Mestre I, Pyron RA, Wiens JJ. 2012. Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs. Evolution 66:3687–700
    [Google Scholar]
  40. Gould J. 2021. Safety bubbles: a review of the proposed functions of froth nesting among anuran amphibians. Ecologies 2:112–37
    [Google Scholar]
  41. Goyes Vallejos J, Grafe TU, Wells KD 2019. Factors influencing tadpole deposition site choice in a frog with male parental care: an experimental field study. Ethology 125:29–39
    [Google Scholar]
  42. Green AJ. 1999. Implications of pathogenic fungi for life-history evolution in amphibians. Funct. Ecol. 13:573–75
    [Google Scholar]
  43. Guex G-D, Greven H. 1994. Structural and physiological aspects of viviparity in Salamandra atra. Mertensiella 4:161–208
    [Google Scholar]
  44. Haddad CFB, Prado CPA. 2005. Reproductive modes in frogs and their unexpected diversity in the Atlantic forest of Brazil. BioScience 55:207–17
    [Google Scholar]
  45. Hakala SM, Fujioka H, Gapp K, De Gasperin O, Genzoni E et al. 2022. Socially transferred materials: why and how to study them. Trends Ecol. Evol. 38:446–58
    [Google Scholar]
  46. Hettyey A, Pearman PB. 2003. Social environment and reproductive interference affect reproductive success in the frog Rana latastei. Behav. Ecol. 14:294–300
    [Google Scholar]
  47. Hödl W. 1990. Reproductive diversity in Amazonian lowland frogs. Fortschr. Zool. 38:41–60
    [Google Scholar]
  48. Houston AI, Székely T, McNamara JM. 2005. Conflict between parents over care. Trends Ecol. Evol. 20:33–38
    [Google Scholar]
  49. Ingram GJ, Anstis M, Corben CJ. 1975. Observations on the Australian leptodactylid frog, Assa darlingtoni. Herpetologica 31:425–29
    [Google Scholar]
  50. IUCN 2022. The IUCN Red List of Threatened Species. Version 2022–2. Int. Union Conserv. Nat. http://www.iucnredlist.org
    [Google Scholar]
  51. Jared C, Mailho-Fontana PL, SGS Jared, Kupfer A, Delabie JHC et al. 2019. Life history and reproduction of the neotropical caecilian Siphonops annulatus (Amphibia, Gymnophiona, Siphonopidae), with special emphasis on parental care. Acta Zool 100:292–302
    [Google Scholar]
  52. Jungfer K-H, Böhme W 1991. The backpack strategy of parental care in frogs, with notes on froglet-carrying in Stefania evansi (Boulenger, 1904) (Anura: Hylidae: Hemiphractinae). Rev. Française d'Aquariol. 18:91–96
    [Google Scholar]
  53. Kaminsky SK, Linsenmair KE, Grafe TU. 1999. Reproductive timing, nest construction and tadpole guidance in the African pig-nosed frog, Hemisus marmoratus. J. Herpetol. 33:119–23
    [Google Scholar]
  54. Kupfer A, Maxwell E, Reinhard S, Kuehnel S 2016. The evolution of parental investment in caecilian amphibians: a comparative approach. Biol. J. Linn. Soc. 119:4–14
    [Google Scholar]
  55. Kusano T, Sakai A, Hatanaka S. 2006. Ecological functions of the foam nests of the Japanese treefrog, Rhacophorus arboreus (Amphibia, Rhacophoridae). Herpetol. J. 16:163–69
    [Google Scholar]
  56. Lange L, Bégué L, Brischoux F, Lourdais O. 2021. The costs of being a good dad: Egg-carrying and clutch size impair locomotor performance in male midwife toads (Alytes obstetricans). Biol. J. Linn. Soc. 132:270–82
    [Google Scholar]
  57. Lange L, Brischoux F, Lourdais O. 2022. Benefits of paternal thermoregulation: Male midwife toads select warmer temperature to shorten embryonic development. Behav. Ecol. Sociobiol. 76:48
    [Google Scholar]
  58. Lauer A, Simon MA, Banning JL, André E, Duncan K, Harris RN. 2007. Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia 2007.630–40
    [Google Scholar]
  59. LeGros D. 2011. Communal oviposition in the Northern two-lined Salamander (Eurycea bislineata) in Algonquin Provincial Park, Ontario. Can. Field Nat 4:363–65
    [Google Scholar]
  60. Liang M-F, Huang C-H, Kam Y-C. 2002. Effects of intermittent feeding on the growth of oophagous (Chirixalus eiffingeri) and herbivorous (Chirixalus idiootocus) tadpoles from Taiwan. J. Zool. 256:207–13
    [Google Scholar]
  61. Liu Y, Day LB, Summers K, Burmeister SS. 2019. A cognitive map in a poison frog. J. Exp. Biol. 222:jeb197467
    [Google Scholar]
  62. Lourenço-de-Moraes R, Ferreira RB, Mira-Mendes CV, Zocca CZ, Medeiros T et al. 2016. Escalated antipredator mechanisms of two neotropical marsupial treefrogs. Herpetol. J. 26:237–44
    [Google Scholar]
  63. Luz Nunes-de-Almeida CH, Batista Haddad CF, Toledo LF 2021. A revised classification of the amphibian reproductive modes. Salamandra 57:413–27
    [Google Scholar]
  64. Magnusson WE, Hero J-M. 1991. Predation and the evolution of complex oviposition behaviour in Amazon rainforest frogs. Oecologia 86:310–18
    [Google Scholar]
  65. Martin KL, Carter AL. 2013. Brave new propagules: terrestrial embryos in anamniotic eggs. Integr. Comp. Biol. 53:233–47
    [Google Scholar]
  66. Neff BD. 2003. Decisions about parental care in response to perceived paternity. Nature 422:716–19
    [Google Scholar]
  67. Okada S, Fukuda Y, Takahashi MK. 2015. Paternal care behaviors of Japanese giant salamander Andrias japonicus in natural populations. J. Ethol. 33:1–7
    [Google Scholar]
  68. Oneto F, Ottonello D, Pastorino MV, Salvidio S. 2010. Posthatching parental care in salamanders revealed by infrared video surveillance. J. Herpetol. 44:649–53
    [Google Scholar]
  69. Oriazola G, Braña F. 2003. Oviposition behaviour and vulnerability of eggs to predation in four newt species (genus Triturus). Herpetol. J. 13:121–24
    [Google Scholar]
  70. Pašukonis A, Beck KB, Fischer M-T, Weinlein S, Stückler S, Ringler E. 2017. Induced parental care in a poison frog: a tadpole cross-fostering experiment. J. Exp. Biol. 220:3949–54
    [Google Scholar]
  71. Pašukonis A, Serrano-Rojas SJ, Fischer M-T, Loretto M-C, Shaykevich DA et al. 2022. Contrasting parental roles shape sex differences in poison frog space use but not navigational performance. eLife 11:e80483
    [Google Scholar]
  72. Pašukonis A, Trenkwalder K, Ringler M, Ringler E, Mangione R et al. 2016. The significance of spatial memory for water finding in a tadpole-transporting frog. Anim. Behav. 116:89–98
    [Google Scholar]
  73. Poo S, Bickford DP. 2013. The adaptive significance of egg attendance in a South-East Asian tree frog. Ethology 119:671–79
    [Google Scholar]
  74. Poo S, Evans TA, Tan MK, Bickford DP. 2016. Dynamic switching in predator attack and maternal defence of prey. Biol. J. Linn. Soc. 118:901–10
    [Google Scholar]
  75. Ringler E, Beck KB, Weinlein S, Huber L, Ringler M. 2017. Adopt, ignore, or kill? Male poison frogs adjust parental decisions according to their territorial status. Sci. Rep. 7:43544
    [Google Scholar]
  76. Ringler E, Pašukonis A, Fitch WT, Huber L, Hödl W, Ringler M. 2015. Flexible compensation of uniparental care: female poison frogs take over when males disappear. Behav. Ecol. 26:1219–25
    [Google Scholar]
  77. Ringler E, Pašukonis A, Ringler M, Huber L. 2016. Sex-specific offspring discrimination reflects respective risks and costs of misdirected care in a poison frog. Anim. Behav. 114:173–79
    [Google Scholar]
  78. Ringler E, Szipl G, Harrigan RJ, Bartl-Binder P, Mangione R, Ringler M. 2018. Hierarchical decision-making balances current and future reproductive success. Mol. Ecol. 27:2289–301
    [Google Scholar]
  79. Rodrigues AP, Giaretta AA, da Silva, Daniele R, Facure KG. 2011. Reproductive features of three maternal-caring species of Leptodactylus (Anura: Leptodactylidae) with a report on alloparental care in frogs. J. Nat. Hist. 45:2037–47
    [Google Scholar]
  80. Rojas B. 2014. Strange parental decisions: fathers of the dyeing poison frog deposit their tadpoles in pools occupied by large cannibals. Behav. Ecol. Sociobiol. 68:551–59
    [Google Scholar]
  81. Royle NJ, Smiseth PT, Kölliker M. 2012. The Evolution of Parental Care Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  82. Santos JC, Cannatella DC. 2011. Phenotypic integration emerges from aposematism and scale in poison frogs. PNAS 108:6175–80
    [Google Scholar]
  83. Schlippe Justicia L, Fouilloux CA, Rojas B 2022. Poison frog social behaviour under global change: potential impacts and future challenges. Acta Ethol https://doi.org/10.1007/s10211-022-00400-6
    [Google Scholar]
  84. Schulte LM. 2013. Feeding or avoiding? Facultative egg feeding in a Peruvian poison frog (Ranitomeya variabilis). Ethol. Ecol. Evol 26:58–68
    [Google Scholar]
  85. Schulte LM, Ringler E, Rojas B, Stynoski JL. 2020. Developments in amphibian parental care research: history, present advances and future perspectives. Herpetol. Monogr. 34:71–97
    [Google Scholar]
  86. Schulte LM, Saporito RA, Davison I, Summers K. 2016. The palatability of Neotropical poison frogs in predator-prey systems: Do alkaloids make the difference?. Biotropica 49:23–26
    [Google Scholar]
  87. Schulte LM, Summers K. 2017. Searching for hormonal facilitators. Are vasotocin and mesotocin involved in parental care behaviors in poison frogs?. Physiol. Behav. 174:74–82
    [Google Scholar]
  88. Schulte LM, Summers K. 2021. Who cares for the eggs? Analysis of egg attendance behaviour in Ranitomeya imitator, a poison frog with biparental care. Behaviour 159:603–14
    [Google Scholar]
  89. Schulte LM, Yeager J, Schulte R, Veith M, Werner P et al. 2011. The smell of success: choice of larval rearing sites by means of chemical cues in a Peruvian poison frog. Anim. Behav. 81:1147–54
    [Google Scholar]
  90. Seshadri KS, Thaker M. 2022. Correlated evolution of parental care with dichromatism, colors, and patterns in anurans. Evolution 76:737–48
    [Google Scholar]
  91. Seymour RS, Bradford DF. 1995. Respiration of amphibian eggs. Physiol. Zool. 68:1–25
    [Google Scholar]
  92. Silva FR, Almeida-Neto M, do Prado VHM, Haddad CFB, de Cerqueira Rossa-Feres D. 2012. Humidity levels drive reproductive modes and phylogenetic diversity of amphibians in the Brazilian Atlantic Forest. J. Biogeogr. 39:1720–32
    [Google Scholar]
  93. Speed MP, Brockhurst MA, Ruxton GD. 2010. The dual benefits of aposematism: predator avoidance and enhanced resource collection. Evolution 64:1622–33
    [Google Scholar]
  94. Spring S, Lehner M, Huber L, Ringler E. 2019. Oviposition and father presence reduce clutch cannibalism by female poison frogs. Front. Zool. 16:8
    [Google Scholar]
  95. Stahlschmidt ZR. 2011. Taxonomic chauvinism revisited: insight from parental care research. PLOS ONE 6:e24192
    [Google Scholar]
  96. Stynoski JL. 2009. Discrimination of offspring by indirect recognition in an egg-feeding dendrobatid frog, Oophaga pumilio. Anim. Behav. 78:1351–56
    [Google Scholar]
  97. Stynoski JL, O'Connell LA 2017. Developmental morphology of granular skin glands in pre-metamorphic egg-eating poison frogs. Zoomorphology 136:219–24
    [Google Scholar]
  98. Stynoski JL, Shelton G, Stynoski P. 2014a. Maternally derived chemical defences are an effective deterrent against some predators of poison frog tadpoles (Oophaga pumilio). Biol. Lett. 10:20140187
    [Google Scholar]
  99. Stynoski JL, Torres-Mendoza Y, Sasa-Marin M, Saporito RA. 2014b. Evidence of maternal provisioning of alkaloid-based chemical defenses in the strawberry poison frog Oophaga pumilio. Ecology 95:587–93
    [Google Scholar]
  100. Sumida S, Martin KL. 1997. Amniote Origins. Completing the Transition to Land San Diego, CA: Academic
    [Google Scholar]
  101. Summers K 2019. Metabolism and parental care in ectotherms: a comment on Beekman et al. Behav. Ecol. 30:593–94
    [Google Scholar]
  102. Summers K, McKeon CS. 2004. The evolutionary ecology of phytotelmata use in neotropical poison frogs. Misc. Publ. Mus. Zool. Univ. Mich. 193:55–73
    [Google Scholar]
  103. Summers K, McKeon CS, Heying HE, Hall J, Patrick W. 2006. Social and environmental influences on egg size evolution in frogs. J. Zool. 271:225–32
    [Google Scholar]
  104. Taboada C, Delia J, Chen M, Ma C, Peng X et al. 2022. Glassfrogs conceal blood in their liver to maintain transparency. Science 378:1315–20
    [Google Scholar]
  105. Toro-Gómez MP, Carvajal-Castro JD, Casas-Cardona S, Vargas-Salinas F. 2022. Experimental evidence in a poison frog model suggests that tadpole transport on the dorsum may affects warning signal effectiveness in poison frogs. Evol. Ecol. 37:267–89
    [Google Scholar]
  106. Touchon JC, Worley JL. 2015. Oviposition site choice under conflicting risks demonstrates that aquatic predators drive terrestrial egg-laying. Proc. R. Soc. B 282:20150376
    [Google Scholar]
  107. Townsend DS. 1986. The costs of male parental care and its evolution in a neotropical frog. Behav. Ecol. Sociobiol. 19:187–95
    [Google Scholar]
  108. Trivers RL. 1972. Parental investment and sexual selection. Sexual Selection and the Descent of Man. 1871–1971 B Campbell 136–79. Chicago: Aldine
    [Google Scholar]
  109. Trivers RL. 1974. Parent–offspring conflict. Integr. Comp. Biol. 14:249–64
    [Google Scholar]
  110. Tumulty J, Morales VR, Summers K. 2014. The biparental care hypothesis for the evolution of monogamy: experimental evidence in an amphibian. Behav. Ecol. 25:262–70
    [Google Scholar]
  111. Vacher J-P, Kok PJ, Rodrigues MT, Lima JD, Lorenzini A et al. 2017. Cryptic diversity in Amazonian frogs: integrative taxonomy of the genus Anomaloglossus (Amphibia: Anura: Aromobatidae) reveals a unique case of diversification within the Guiana Shield. Mol. Phylogenet. Evol. 112:158–73
    [Google Scholar]
  112. Vági B, Marsh D, Katona G, Végvári Z, Freckleton RP et al. 2022. The evolution of parental care in salamanders. Sci. Rep. 12:16655
    [Google Scholar]
  113. Vági B, Végvári Z, Liker A, Freckleton RP, Székely T. 2019. Parental care and the evolution of terrestriality in frogs. Proc. R. Soc. B 286:20182737
    [Google Scholar]
  114. Vági B, Végvári Z, Liker A, Freckleton RP, Székely T. 2020. Climate and mating systems as drivers of global diversity of parental care in frogs. Global Ecol. Biogeogr. 29:1373–86
    [Google Scholar]
  115. Valencia-Aguilar A, Guayasamin JM, Prado CPA. 2021. Alloparental care in glassfrogs: Males care for unrelated clutches only when associated with their own. Sci. Rep. 11:1386
    [Google Scholar]
  116. Velo-Antón G, García-París M, Galán P, Cordero Rivera A 2007. The evolution of viviparity in holocene islands: ecological adaptation versus phylogenetic descent along the transition from aquatic to terrestrial environments. J. Zool. Syst. Evol. Res. 45:345–52
    [Google Scholar]
  117. Vieites DR, Nieto-Román S, Barluenga M, Palanca A, Vences M, Meyer A. 2004. Post-mating clutch piracy in an amphibian. Nature 431:305–8
    [Google Scholar]
  118. Villanueva ED, Brooks OL, Bolton SK, Savastano N, Schulte LM, Saporito RA. 2022. Maternal provisioning of alkaloid defenses are present in obligate but not facultative egg feeding dendrobatids. J. Chem. Ecol. 48:900–9
    [Google Scholar]
  119. 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. 40:859–69
    [Google Scholar]
  120. Wake MH, Dickie R. 1998. Oviduct structure and function and reproductive modes in amphibians. J. Exp. Zool. 282:477–506
    [Google Scholar]
  121. Warkentin KM. 1995. Adaptive plasticity in hatching age. A response to predation risk trade-offs. PNAS 92:3507–10
    [Google Scholar]
  122. Warkentin KM, Gomez-Mestre I, McDaniel JG. 2005. Development, surface exposure, and embryo behavior affect oxygen levels in eggs of the red-eyed treefrog, Agalychnis callidryas. Physiol. Biochem. Zool 78:956–66
    [Google Scholar]
  123. Warne RW, Catenazzi A. 2016. Pouch brooding marsupial frogs transfer nutrients to developing embryos. Biol. Lett. 12:20160673
    [Google Scholar]
  124. Wells KD. 2007. The Ecology and Behavior of Amphibians Chicago: Univ. Chicago Press
    [Google Scholar]
  125. Weygoldt P. 1987. Evolution of parental care in dart poison frogs (Amphibia: Anura: Dendrobatidae). Z. Zool. Syst. Evolutionsforsch. 25:51–67
    [Google Scholar]
  126. Wilkinson M, Kupfer A, Marques-Porto R, Jeffkins H, Antoniazzi MM, Jared C. 2008. One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona). Biol. Lett. 4:358–61
    [Google Scholar]
  127. Winkler DW. 1987. A general model for parental care. Am. Nat. 130:526–43
    [Google Scholar]
  128. Yang Y, Servedio MR, Richards-Zawacki CL. 2019. Imprinting sets the stage for speciation. Nature 574:99–102
    [Google Scholar]
  129. Zamudio KR, Bell RC, Nali RC, Haddad CFB, Prado CPA. 2016. Polyandry, predation, and the evolution of frog reproductive modes. Am. Nat. 188:S41–61
    [Google Scholar]
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