pp 1-44 | Cite as

Advancing Understanding of Amphibian Evolution, Ecology, Behavior, and Conservation with Massively Parallel Sequencing

  • W. Chris FunkEmail author
  • Kelly R. Zamudio
  • Andrew J. Crawford
Part of the Population Genomics book series


Genomics has great potential to advance understanding of amphibian evolution, ecology, and behavior, as well as to improve conservation of this highly imperiled class of vertebrates. However, application of new massively parallel sequencing technology to amphibians lags behind its application to other vertebrates, due in part to their large, repetitive genomes, making genome assembly challenging. The goal of our chapter is to outline ways in which population genomics – coupled with field biology, experiments, and modeling – can deepen our understanding of basic and applied questions in amphibian evolutionary ecology and conservation. We start by discussing potential applications of genomics to several long-standing questions in amphibian evolution, ecology, and behavior, including phylogenetic relationships, phylogeography, sex chromosome evolution, population structure and demography, local adaptation, and mating systems and sexual selection. We then highlight opportunities for improving amphibian conservation with genomics, focusing on hybridization, disease evolution and ecology, and captive breeding programs. Next, we provide strategies for moving amphibian genomics forward in the face of challenges such as few available reference genomes and large repetitive genomes, including a bold proposal for whole genome sequencing of a minimum of one species per amphibian family. We conclude by providing suggestions for maximizing the potential of genomics to advance understanding of amphibian evolutionary ecology and conservation and recommendations for getting started in genomics.


Amphibian Local adaptation Massively parallel sequencing Population genomics 



We thank Daryl Trumbo, Emily Moriarty Lemmon, Mathew Fujita, and Guillermo Velo-Antón for providing helpful comments on the manuscript and Guillermo Velo-Antón and Ian J. Wang for photos. We acknowledge funding from the National Science Foundation Rules of Life grant (DEB 1838282) to WCF.


  1. Abbott JK, Norden AK, Hansson B. Sex chromosome evolution: historical insights and future perspectives. Proc R Soc B Biol Sci. 2017;284:20162806.Google Scholar
  2. Adams EM, Jones AG, Arnold SJ. Multiple paternity in a natural population of a salamander with long-term sperm storage. Mol Ecol. 2005;14:1803–10.Google Scholar
  3. Alexander AM, Su YC, Oliveros CH, Olson KV, Travers SL, Brown RM. Genomic data reveals potential for hybridization, introgression, and incomplete lineage sorting to confound phylogenetic relationships in an adaptive radiation of narrow-mouth frogs. Evolution. 2017;71:475–88.Google Scholar
  4. Allendorf FW. Genetics and the conservation of natural populations: allozymes to genomes. Mol Ecol. 2017;26:420–30.Google Scholar
  5. Allendorf FW, Phelps SR. Use of allelic frequencies to describe population structure. Can J Fish Aquat Sci. 1981;38:1507–14.Google Scholar
  6. Allendorf FW, Hohenlohe PA, Luikart G. Genomics and the future of conservation genetics. Nat Rev Genet. 2010;11:697–709.Google Scholar
  7. Allendorf FW, Luikart G, Aitken SN. Conservation and the genetics of populations. 2nd ed. Oxford: Wiley-Blackwell; 2013.Google Scholar
  8. AmphibiaWeb. University of California, Berkeley, 2018. Accessed 30 Sept 2018.
  9. Anderson E, Stebbins GL. Hybridization as an evolutionary stimulus. Evolution. 1954;8:378–88.Google Scholar
  10. Andrés JA, Bogdanowicz SM. Isolating microsatellite loci: looking back, looking ahead. Methods Mol Biol. 2011;772:211–32.Google Scholar
  11. Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA. Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet. 2016;17:81–92.Google Scholar
  12. Arnold ML. Natural hybridization and evolution. Oxford: Oxford University Press; 1997.Google Scholar
  13. Ashman TL, Bachtrog D, Blackmon H, Goldherg EE, Hahn MW, Kirkpatrick M, et al. Tree of sex: a database of sexual systems. Sci Data. 2014;1:140015.Google Scholar
  14. Austin JD, Gorman TA, Bishop D, Moler P. Genetic evidence of contemporary hybridization in one of North America’s rarest anurans, the Florida bog frog. Anim Conserv. 2011;14:553–61.Google Scholar
  15. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, et al. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst. 1987;18:489–522.Google Scholar
  16. Avise JC, Jones AG, Walker D, DeWoody JA. Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annu Rev Genet. 2002;36:19–45.Google Scholar
  17. Bachtrog D. A dynamic view of sex chromosome evolution. Curr Opin Genet Dev. 2006;16:578–85.Google Scholar
  18. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One. 2008;3:e3376.Google Scholar
  19. Balkenhol N, Cushman SA, Storfer AT, Waits LP. Landscape genetics: concepts, methods, applications. Oxford: Wiley-Blackwell; 2016.Google Scholar
  20. Barrow LN, Ralicki HF, Emme SA, Lemmon EM. Species tree estimation of north American chorus frogs (Hylidae: Pseudacris) with parallel tagged amplicon sequencing. Mol Phylogenet Evol. 2014;75:78–90.Google Scholar
  21. Barrow LN, Soto-Centeno JA, Warwick AR, Lemmon AR, Lemmon EM. Evaluating hypotheses of expansion from refugia through comparative phylogeography of south-eastern Coastal Plain amphibians. J Biogeogr. 2017;44:2692–705.Google Scholar
  22. Barrow LN, Lemmon AR, Lemmon EM. Targeted sampling and target capture: assessing phylogeographic concordance with genome-wide data. Syst Biol. 2018;
  23. Barton N, Bengtsson BO. The barrier to genetic exchange between hybridizing populations. Heredity. 1986;57:357–76.Google Scholar
  24. Bataille A, Fong JJ, Cha M, Wogan GOU, Baek HJ, Lee H, et al. Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians. Mol Ecol. 2013;22:4196–209.Google Scholar
  25. Bataille A, Cashins SD, Grogan L, Skerratt LF, Hunter D, McFadden M, et al. Susceptibility of amphibians to chytridiomycosis is associated with MHC class II conformation. Proc R Soc B Biol Sci. 2015;282:20143127.Google Scholar
  26. Beaumont MA, Balding DJ. Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol. 2004;13:969–80.Google Scholar
  27. Beaumont MA, Nichols RA. Evaluating loci for use in the genetic analysis of population structure. Proc R Soc B Biol Sci. 1996;263:1619–26.Google Scholar
  28. Beebee TJC. Conservation genetics of amphibians. Heredity. 2005;95:423–7.Google Scholar
  29. Bell RC, MacKenzie JB, Hickerson MJ, Chavarria KL, Cunningham M, Williams S, et al. Comparative multi-locus phylogeography confirms multiple vicariance events in co-distributed rainforest frogs. Proc R Soc B Biol Sci. 2012;279:991–9.Google Scholar
  30. Bell RC, Drewes RC, Zamudio KR. Reed frog diversification in the Gulf of Guinea: overseas dispersal, the progression rule, and in situ speciation. Evolution. 2015;69:904–15.Google Scholar
  31. Bell RC, Parra JL, Badjedjea G, Barej MF, Blackburn DC, Burger M, et al. Idiosyncratic responses to climate-driven forest fragmentation and marine incursions in reed frogs from Central Africa and the Gulf of Guinea Islands. Mol Ecol. 2017;26:5223–44.Google Scholar
  32. Bernardi G, Wiley EO, Mansour H, Miller MR, Orti G, Haussler D, et al. The fishes of genome 10K. Mar Genomics. 2012;7:3–6.Google Scholar
  33. Berven KA. The genetic basis of altitudinal variation in the wood frog Rana sylvatica. I. An experimental analysis of life history traits. Evolution. 1982;36:962–83.Google Scholar
  34. Bhattacharya D, Marfo CA, Li D, Lane M, Khokha MK. CRISPR/Cas9: an inexpensive, efficient loss of function tool to screen human disease genes in Xenopus. Dev Biol. 2015;408:196–204.Google Scholar
  35. Black WC IV, Baer CF, Antolin MF, DuTeau NM. Population genomics: genome-wide sampling of insect populations. Annu Rev Entomol. 2001;46:441–69.Google Scholar
  36. Bogart JP. Evolution of anuran karyotypes. In: Vial JL, editor. Evolutionary biology of the anurans. Missouri: University of Missouri Press; 1973. p. 337–49.Google Scholar
  37. Burton TM, Likens GE. Energy flow and nutrient cycling in salamander populations in the Hubbard Brook Experimental Forest, New Hampshire. Ecology. 1975;56:1068–80.Google Scholar
  38. Camacho-Sanchez M, Burraco P, Gomez-Mestre I, Leonard JA. Preservation of RNA and DNA from mammal samples under field conditions. Mol Ecol Resour. 2013;13:663–73.Google Scholar
  39. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A. 2011;108:4516–22.Google Scholar
  40. Catchen JM, Hohenlohe PA, Bernatchez L, Funk WC, Andrews KR, Allendorf FW. Unbroken: RADseq remains a powerful tool for understanding the genetics of adaptation in natural populations. Mol Ecol Resour. 2017;17:362–5.Google Scholar
  41. Chakrabarty P, Faircloth BC, Alda F, Ludt WB, McMahan CD, Near TJ, et al. Phylogenomic systematics of Ostariophysan fishes: ultraconserved elements support the surprising non-monophyly of Characiformes. Syst Biol. 2017;66:881–95.Google Scholar
  42. Che RB, Sun YN, Wang RX, Xu TJ. Transcriptomic analysis of endangered Chinese salamander: identification of immune, sex and reproduction-related genes and genetic markers. PLoS One. 2014;9:e87940.Google Scholar
  43. Chen YH, Cheng WC, Yu HT, Kam YC. Genetic relationship between offspring and guardian adults of a rhacophorid frog and its care effort in response to paternal share. Behav Ecol Sociobiol. 2011;65:2329–39.Google Scholar
  44. Claussen J, Keck DD, Hiesey WM. Experimental studies on the nature of species. III. Environmental responses of climatic races of Achillea. Washington: Carnegie Institution of Washington Publication; 1948. p. 581.Google Scholar
  45. Coop G, Witonsky D, Di Rienzo A, Pritchard JK. Using environmental correlations to identify loci underlying local adaptation. Genetics. 2010;185:1411–23.Google Scholar
  46. Crawford AJ. Huge populations and old species of Costa Rican and Panamanian dirt frogs inferred from mitochondrial and nuclear gene sequences. Mol Ecol. 2003;12:2525–40.Google Scholar
  47. Crawford AJ, Lips KR, Bermingham E. Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proc Natl Acad Sci U S A. 2010;107:13777–82.Google Scholar
  48. Crispo E. Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow. J Evol Biol. 2008;21:1460–9.Google Scholar
  49. D’Aloia CC, Bogdanowicz SM, Harrison RG, Buston PM. Cryptic genetic diversity and spatial patterns of admixture within Belizean marine reserves. Conserv Genet. 2017;18:211–23.Google Scholar
  50. Denton RD, Kudra RS, Malcom JW, Du Preez L, Malone JH. The African Bullfrog (Pyxicephalus adspersus) genome unites the two ancestral ingredients for making vertebrate sex chromosomes. bioRxiv. 2018;
  51. Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR. NEESTIMATOR v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour. 2014;14:209–14.Google Scholar
  52. Dowling TE, Secor CL. The role of hybridization and introgression in the diversification of animals. Annu Rev Ecol Syst. 1997;28:593–619.Google Scholar
  53. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969–73.Google Scholar
  54. Duellman WE, Trueb L. Biology of amphibians. New York: McGraw-Hill Book; 1986.Google Scholar
  55. Eckert CG, Samis KE, Lougheed SC. Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol. 2008;17:1170–88.Google Scholar
  56. Edmands S. Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol. 2007;16:463–75.Google Scholar
  57. Edwards RJ, Tuipulotu DE, Amos TG, O’Meally D, Richardson MF, Russell TL, et al. Draft genome assembly of the invasive cane toad, Rhinella marina. GigaScience. 2018;7:giy095.Google Scholar
  58. Elewa A, Wang H, Talavera-López C, Joven A, Brito G, Kumar A, Hameed LS, Penrad-Mobayed M, Yao Z, Zamani N, Abbas Y, Abdullayev I, Sandberg R, Grabherr M, Andersson B, Simon A. Reading and editing the Pleurodeles waltl genome reveals novel features of tetrapod regeneration. Nat Commun. 2017;8:2286.Google Scholar
  59. Elinson RP. Inheritance and expression of a sex-linked enzyme in the frog, Rana clamitans. Biochem Genet. 1983;21:435–42.Google Scholar
  60. Elliott TA, Gregory TR. What’s in a genome? The C-value enigma and the evolution of eukaryotic genome content. Philos Trans R Soc B Biol Sci. 2015;370:20140331.Google Scholar
  61. Ellison AR, Savage AE, DiRenzo GV, Langhammer P, Lips KR, Zamudio KR. Fighting a losing battle: vigorous immune response countered by pathogen suppression of host defenses in the chytridiomycosis-susceptible frog Atelopus zeteki. G3: Genes Genom Genet. 2014;4:1275–89.Google Scholar
  62. Ellison AR, Tunstall T, DiRenzo GV, Hughey MC, Rebollar EA, Belden LK, et al. More than skin deep: functional genomic basis for resistance to amphibian chytridiomycosis. Genome Biol Evol. 2015;7:286–98.Google Scholar
  63. Ellison AR, DiRenzo GV, McDonald CA, Lips KR, Zamudio KR. First in vivo Batrachochytrium dendrobatidis transcriptomes reveal mechanisms of host exploitation, host-specific gene expression, and expressed genotype shifts. G3: Genes Genom Genet. 2017;7:269–78.Google Scholar
  64. Endler JA. Natural selection in the wild. Monogr Popul Biol. 1986;21:1–336.Google Scholar
  65. Ezaz T, Sarre SD, O’Meally D, Graves JAM, Georges A. Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenet Genome Res. 2009;127:249–60.Google Scholar
  66. Faircloth BC, McCormack JE, Crawford NG, Harvey MG, Brumfield RT, Glenn TC. Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales. Syst Biol. 2012;61:717–26.Google Scholar
  67. Faith DP. Conservation evaluation and phylogenetic diversity. Biol Conserv. 1992;61:1–10.Google Scholar
  68. Farrer RA, Weinert LA, Bielby J, Garner TWJ, Balloux F, Clare F, et al. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc Natl Acad Sci U S A. 2011;108:18732–6.Google Scholar
  69. Farrer RA, Henk DA, Garner TWJ, Balloux F, Woodhams DC, Fisher MC. Chromosomal copy number variation, selection and uneven rates of recombination reveal cryptic genome diversity linked to pathogenicity. PLoS Genet. 2013;9:e1003703.Google Scholar
  70. Farrer RA, Martel A, Verbrugghe E, Abouelleil A, Ducatelle R, Longcore JE, et al. Genomic innovations linked to infection strategies across emerging pathogenic chytrid fungi. Nat Commun. 2017;8:14742.Google Scholar
  71. Fei JF, Schuez M, Tazaki A, Taniguchi Y, Roensch K, Tanaka EM. CRISPR-mediated genomic deletion of Sox2 in the axolotl shows a requirement in spinal cord neural stem cell amplification during tail regeneration. Stem Cell Rep. 2014;3:444–59.Google Scholar
  72. Feng YJ, Blackburn DC, Liang D, Hillis DM, Wake DB, Cannatella DC, et al. Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous-Paleogene boundary. Proc Natl Acad Sci U S A. 2017;114:E5864–E70.Google Scholar
  73. Fernandez ME, Goszczynski DE, Liron JP, Villegas-Castagnasso EE, Carino MH, Ripoli MV, et al. Comparison of the effectiveness of microsatellites and SNP panels for genetic identification, traceability and assessment of parentage in an inbred Angus herd. Genet Mol Biol. 2013;36:185–U94.Google Scholar
  74. Ficetola GF, Bonin A. Conserving adaptive genetic diversity in dynamic landscapes. Mol Ecol. 2011;20:1569–71.Google Scholar
  75. Ficetola GF, Stock M. Do hybrid-origin polyploid amphibians occupy transgressive or intermediate ecological niches compared to their diploid ancestors? J Biogeogr. 2016;43:703–15.Google Scholar
  76. Fisher RA. The genetical theory of natural selection. Oxford: Clarendon Press; 1930.Google Scholar
  77. Fisher MC, Garner TWJ, Walker SF. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu Rev Microbiol. 2009;63:291–310.Google Scholar
  78. Fites JS, Ramsey JP, Holden WM, Collier SP, Sutherland DM, Reinert LK, et al. The invasive chytrid fungus of amphibians paralyzes lymphocyte responses. Science. 2013;342:366–9.Google Scholar
  79. Fitzpatrick BM, Shaffer HB. Hybrid vigor between native and introduced salamanders raises new challenges for conservation. Proc Natl Acad Sci U S A. 2007;104:15793–8.Google Scholar
  80. Fitzpatrick BM, Johnson JR, Kump DK, Shaffer HB, Smith JJ, Voss SR. Rapid fixation of non-native alleles revealed by genome-wide SNP analysis of hybrid tiger salamanders. BMC Evol Biol. 2009;9:176.Google Scholar
  81. Fitzpatrick BM, Johnson JR, Kump DK, Smith JJ, Voss SR, Shaffer HB. Rapid spread of invasive genes into a threatened native species. Proc Natl Acad Sci U S A. 2010;107:3606–10.Google Scholar
  82. Foll M, Gaggiotti O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics. 2008;180:977–93.Google Scholar
  83. Fong JJ, Brown JM, Fujita MK, Boussau B. A phylogenomic approach to vertebrate phylogeny supports a turtle-archosaur affinity and a possible paraphyletic Lissamphibia. PLoS One. 2012;7:e48990.Google Scholar
  84. Francois O, Martins H, Caye K, Schoville SD. Controlling false discoveries in genome scans for selection. Mol Ecol. 2016;25:454–69.Google Scholar
  85. Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, et al. Predicting the probability of outbreeding depression. Conserv Biol. 2011;25:465–75.Google Scholar
  86. Frichot E, Schoville SD, Bouchard G, Francois O. Testing for associations between loci and environmental gradients using latent factor mixed models. Mol Biol Evol. 2013;30:1687–99.Google Scholar
  87. Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, et al. The amphibian tree of life. Bull Am Mus Nat Hist. 2006;297:1–370.Google Scholar
  88. Fuentes-Pardo AP, Ruzzante DE. Whole-genome sequencing approaches for conservation biology: advantages, limitations and practical recommendations. Mol Ecol. 2017;26:5369–406.Google Scholar
  89. Funk WC, Greene AE, Corn PS, Allendorf FW. High dispersal in a frog species suggests that it is vulnerable to habitat fragmentation. Biol Lett. 2005;1:13–6.Google Scholar
  90. Funk WC, Caldwell JP, Peden CE, Padial JM, Riva IDL, Cannatella DC. Tests of biogeographic hypotheses for diversification in the Amazonian forest frog, Physalaemus petersi. Mol Phylogenet Evol. 2007;44:825–37.Google Scholar
  91. Funk WC, Pearl CA, Draheim HM, Adams MJ, Mullins TD, Susan MH. Range-wide phylogeographic analysis of the spotted frog complex (Rana luteiventris and Rana pretiosa) in northwestern North America. Mol Phylogenet Evol. 2008;49:198–210.Google Scholar
  92. Funk WC, Mckay JK, Hohenlohe PA, Allendorf FW. Harnessing genomics for delineating conservation units. Trends Ecol Evol. 2012;27:489–96.Google Scholar
  93. Funk WC, Murphy MA, Hoke KL, Muths E, Amburgey SM, Lemmon EM, et al. Elevational speciation in action? Restricted gene flow associated with adaptive divergence across an altitudinal gradient. J Evol Biol. 2016;29:241–52.Google Scholar
  94. Gamble T, Zarkower D. Identification of sex-specific molecular markers using restriction site-associated DNA sequencing. Mol Ecol Resour. 2014;14:902–13.Google Scholar
  95. Gamble T, Coryell J, Ezaz T, Lynch J, Scantlebury DP, Zarkower D. Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Mol Biol Evol. 2015;32:1296–309.Google Scholar
  96. García-R JC, Crawford AJ, Mendoza AM, Ospina O, Cardenas H, Castro F. Comparative phylogeography of direct-developing frogs (Anura: Craugastoridae: Pristimantis) in the southern Andes of Colombia. PLoS One. 2012;7:e46077.Google Scholar
  97. Garrick RC, Bonatelli IAS, Hyseni C, Morales A, Pelletier TA, Perez MF, et al. The evolution of phylogeographic data sets. Mol Ecol. 2015;24:1164–71.Google Scholar
  98. Gazoni T, Haddad CFB, Narimatsu H, Cabral-de-Mello DC, Lyra ML, Parise-Maltempi PP. More sex chromosomes than autosomes in the Amazonian frog Leptodactylus pentadactylus. Chromosoma. 2018;127:269–78.Google Scholar
  99. Gerchen JF, Reichert SJ, Rohr JT, Dieterich C, Kloas W, Stock M. A single transcriptome of a green toad (Bufo viridis) yields candidate genes for sex determination and -differentiation and non-anonymous population genetic markers. PLoS One. 2016;11:e0156419.Google Scholar
  100. Ghalambor CK, Hoke KL, Ruell EW, Fischer EK, Reznick DN, Hughes KA. Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature. 2015;525:372–5.Google Scholar
  101. Glaubitz JC, Rhodes OE, Dewoody JA. Prospects for inferring pairwise relationships with single nucleotide polymorphisms. Mol Ecol. 2003;12:1039–47.Google Scholar
  102. Glenn TC. Field guide to next-generation DNA sequencers. Mol Ecol Resour. 2011;11:759–69.Google Scholar
  103. Gomez-Mestre I, Pyron RA, Wiens JJ. Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs. Evolution. 2012;66:3687–700.Google Scholar
  104. Gompert Z, Fordyce JA, Forister ML, Shapiro AM, Nice CC. Homoploid hybrid speciation in an extreme habitat. Science. 2006;314:1923–5.Google Scholar
  105. Grant PR, Grant BR. Hybridization of bird species. Science. 1992;256:193–7.Google Scholar
  106. Grant BR, Grant PR. Fission and fusion of Darwin’s finches populations. Philos Trans R Soc B Biol Sci. 2008;363:2821–9.Google Scholar
  107. Gregory TR. Animal genome size database. 2011. Scholar
  108. Griffith SC, Owens IPF, Thuman KA. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol. 2002;11:2195–212.Google Scholar
  109. Guerrero RF, Kirkpatrick M, Perrin N. Cryptic recombination in the ever-young sex chromosomes of hylid frogs. J Evol Biol. 2012;25:1947–54.Google Scholar
  110. Guo BC, Lu D, Liao WB, Merila J. Genomewide scan for adaptive differentiation along altitudinal gradient in the Andrew’s toad Bufo andrewsi. Mol Ecol. 2016;25:3884–900.Google Scholar
  111. Haldane JBS. A mathematical theory of natural and artificial selection. VI. Isolation. Proc Camb Philos Soc. 1930;26:220–30.Google Scholar
  112. Hammond SA, Warren RL, Vandervalk BP, Kucuk E, Khan H, Gibb EA, et al. The North American bullfrog draft genome provides insight into hormonal regulation of long noncoding RNA. Nat Commun. 2017;8:1433.Google Scholar
  113. Hardie DC, Gregory TR, Hebert PDN. From pixels to picograms: a beginners’ guide to genome quantification by Feulgen image analysis densitometry. J Histochem Cytochem. 2002;50:735–49.Google Scholar
  114. Harding G, Griffiths RA, Pavajeau L. Developments in amphibian captive breeding and reintroduction programs. Conserv Biol. 2016;30:340–9.Google Scholar
  115. Harrison RG. Hybrids and hybrid zones: historical perspective. In: Hybrid zones and the evolutionary process. Oxford: Oxford University Press; 1993. p. 3–12.Google Scholar
  116. Hauser L, Baird M, Hilborn R, Seeb LW, Seeb JE. An empirical comparison of SNPs and microsatellites for parentage and kinship assignment in a wild sockeye salmon (Oncorhynchus nerka) population. Mol Ecol Resour. 2011;11:150–61.Google Scholar
  117. Haussler D, O’Brien SJ, Ryder OA, Barker FK, Clamp M, Crawford AJ, et al. Genome 10K: a proposal to obtain whole-genome sequence for 10,000 vertebrate species. J Hered. 2009;100:659–74.Google Scholar
  118. Hayes TB. Sex determination and primary sex differentiation in amphibians: genetic and developmental mechanisms. J Exp Zool. 1998;281:373–99.Google Scholar
  119. Heinicke MP, Lemmon AR, Lemmon EM, McGrath K, Hedges SB. Phylogenomic support for evolutionary relationships of New World direct-developing frogs (Anura: Terraranae). Mol Phylogenet Evol. 2018;118:145–55.Google Scholar
  120. Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V, et al. The genome of the western clawed frog Xenopus tropicalis. Science. 2010;328:633–6.Google Scholar
  121. Hillis DM, Green DM. Evolutionary changes of heterogametic sex in the phylogenetic history of amphibians. J Evol Biol. 1990;3:49–64.Google Scholar
  122. Hoban S, Kelley JL, Lotterhos KE, Antolin MF, Bradburd G, Lowry DB, et al. Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. Am Nat. 2016;188:379–97.Google Scholar
  123. Hoffmann M, Hilton-Taylor C, Angulo A, Bohm M, Brooks TM, Butchart SHM, et al. The impact of conservation on the status of the world’s vertebrates. Science. 2010;330:1503–9.Google Scholar
  124. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 2010;6:e1000862.Google Scholar
  125. Huang L, Li J, Anboukaria H, Luo ZH, Zhao M, Wu H. Comparative transcriptome analyses of seven anurans reveal functions and adaptations of amphibian skin. Sci Rep. 2016;6:24069.Google Scholar
  126. Hughes C. Integrating molecular techniques with field methods in studies of social behavior: a revolution results. Ecology. 1998;79:383–99.Google Scholar
  127. Irisarri I, Baurain D, Brinkmann H, Delsuc F, Sire JY, Kupfer A, et al. Phylotranscriptomic consolidation of the jawed vertebrate timetree. Nat Ecol Evol. 2017;1:1370–8.Google Scholar
  128. Isaac NJB, Redding DW, Meredith HM, Safi K. Phylogenetically-informed priorities for amphibian conservation. PLoS One. 2012;7:e43912.Google Scholar
  129. James TY, Litvintseva AP, Vilgalys R, Morgan JAT, Taylor JW, Fisher MC, et al. Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLoS Pathog. 2009;5:e1000458.Google Scholar
  130. James TY, Toledo LF, Rodder D, Leite DD, Belasen AM, Betancourt-Roman CM, et al. Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecol Evol. 2015;5:4079–97.Google Scholar
  131. Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014;346(6215):1320–31.Google Scholar
  132. Jockusch EL. An evolutionary correlate of genome size change in plethodontid salamanders. Proc R Soc B Biol Sci. 1997;264(1381):597–604.Google Scholar
  133. Johnson WE, Koepfli K. The role of genomics in conservation and reproductive sciences. Adv Exp Med Biol. 2014;753:71–96.Google Scholar
  134. Jones MR, Good JM. Targeted capture in evolutionary and ecological genomics. Mol Ecol. 2016;25:185–202.Google Scholar
  135. Joost S, Bonin A, Bruford MW, Despres L, Conord C, Erhardt G, et al. A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Mol Ecol. 2007;16(18):3955–69.Google Scholar
  136. Kaiser SA, Taylor SA, Chen N, Sillett TS, Bondra ER, Webster MS. A comparative assessment of SNP and microsatellite markers for assigning parentage in a socially monogamous bird. Mol Ecol Resour. 2017;17:183–93.Google Scholar
  137. Kardos M, Taylor HR, Ellegren H, Luikart G, Allendorf FW. Genomics advances the study of inbreeding depression in the wild. Evol Appl. 2016;9:1205–18.Google Scholar
  138. Kimura M, Crow JF. The measurement of the effective population number. Evolution. 1963;17:279–88.Google Scholar
  139. Kingman JFC. The coalescent. Stoch Process Appl. 1982;13:235–48.Google Scholar
  140. Koepfli KP, Paten B, O’Brien SJ, Scientists GKC. The Genome 10K Project: a way forward. Annu Rev Anim Biosci. 2015;3:57–111.Google Scholar
  141. Kupfer A, Wilkinson M, Gower DJ, Muller H, Jehle R. Care and parentage in a skin-feeding caecilian amphibian. J Exp Zool A Ecol Genet Physiol. 2008;309a:460–7.Google Scholar
  142. Lambert MR, Skelly DK, Ezaz T. Sex-linked markers in the North American green frog (Rana clamitans) developed using DArTseq provide early insight into sex chromosome evolution. BMC Genomics. 2016;17:844.Google Scholar
  143. Laurila A, Seppa P. Multiple paternity in the common frog (Rana temporaria): genetic evidence from tadpole kin groups. Biol J Linn Soc. 1998;63:221–32.Google Scholar
  144. Lemmon EM, Juenger TE. Geographic variation in hybridization across a reinforcement contact zone of chorus frogs (Pseudacris). Ecol Evol. 2017;7:9485–502.Google Scholar
  145. Lemmon AR, Emme SA, Lemmon EM. Anchored hybrid enrichment for massively high-throughput phylogenomics. Syst Biol. 2012;61:727–44.Google Scholar
  146. Liedtke HC, Gower DJ, Wilkinson M, Gomez-Mestre I. Macroevolutionary shift in the size of amphibian genomes and the role of life history and climate. Nat Ecol Evol. 2018;2:1792–9. Scholar
  147. Longcore JE, Pessier AP, Nichols DK. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia. 1999;91:219–27.Google Scholar
  148. Longo AV, Burrowes PA, Zamudio KR. Genomic studies of disease-outcome in host-pathogen dynamics. Integr Comp Biol. 2014;54:427–38.Google Scholar
  149. Lopes CM, Sasso T, Valentini A, Dejean T, Martins M, Zamudio KR, et al. eDNA metabarcoding: a promising method for anuran surveys in highly diverse tropical forests. Mol Ecol Resour. 2017;17:904–14.Google Scholar
  150. Lowe WH, Likens GE, McPeek MA, Buso DC. Linking direct and indirect data on dispersal: isolation by slope in a headwater stream salamander. Ecology. 2006;87(2):334–9.Google Scholar
  151. Lowry DB, Hoban S, Kelley JL, Lotterhos KE, Reed LK, Antolin MF, et al. Breaking RAD: an evaluation of the utility of restriction site-associated DNA sequencing for genome scans of adaptation. Mol Ecol Resour. 2017;17:142–52.Google Scholar
  152. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P. The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet. 2003;4:981–94.Google Scholar
  153. Mallet J. Hybridization as an invasion of the genome. Trends Ecol Evol. 2005;20:229–37.Google Scholar
  154. Manel S, Schwartz MK, Luikart G, Taberlet P. Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol. 2003;18:189–97.Google Scholar
  155. Manel S, Perrier C, Pratlong M, Abi-Rached L, Paganini J, Pontarotti P, et al. Genomic resources and their influence on the detection of the signal of positive selection in genome scans. Mol Ecol. 2016;25:170–84.Google Scholar
  156. Martel A, Spitzen-van der Sluijs A, Blooi M, Bert W, Ducatelle R, Fisher MC, et al. Batrachochytrium salamandrivorans sp. nov causes lethal chytridiomycosis in amphibians. Proc Natl Acad Sci U S A. 2013;110:15325–9.Google Scholar
  157. Martel A, Blooi M, Adriaensen C, Van Rooij P, Beukema W, Fisher MC, et al. Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science. 2014;346:630–1.Google Scholar
  158. Mavárez J, Salazar CA, Bermingham E, Salcedo C, Jiggins CD, Linares M. Speciation by hybridization in Heliconius butterflies. Nature. 2006;441:868–71.Google Scholar
  159. McCartney-Melstad E, Shaffer HB. Amphibian molecular ecology and how it has informed conservation. Mol Ecol. 2015;24:5084–109.Google Scholar
  160. McCartney-Melstad E, Mount GG, Shaffer HB. Exon capture optimization in amphibians with large genomes. Mol Ecol Resour. 2016;16:1084–94.Google Scholar
  161. McCormack JE, Faircloth BC. Next-generation phylogenetics takes root. Mol Ecol. 2013;22:19–21.Google Scholar
  162. McCormack JE, Hird SM, Zellmer AJ, Carstens BC, Brumfield RT. Applications of next-generation sequencing to phylogeography and phylogenetics. Mol Phylogenet Evol. 2013;66:526–38.Google Scholar
  163. McKay JK, Latta RG. Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol. 2002;17:285–91.Google Scholar
  164. McKenzie VJ, Bowers RM, Fierer N, Knight R, Lauber CL. Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. ISME J. 2012;6:588–96.Google Scholar
  165. Miura I, Ohtani H, Nakamura M, Ichikawa Y, Saitoh K. The origin and differentiation of the heteromorphic sex chromosomes Z, W, X, and Y in the frog Rana rugosa, inferred from the sequences of a sex-linked gene, ADP/ATP translocase. Mol Biol Evol. 1998;15:1612–9.Google Scholar
  166. Morgan JAT, Vredenburg VT, Rachowicz LJ, Knapp RA, Stice MJ, Tunstall T, et al. Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proc Natl Acad Sci U S A. 2007;104:13845–50.Google Scholar
  167. Muralidhar P, de Sa FP, Haddad CFB, Zamudio KR. Kin-bias, breeding site selection and female fitness in a cannibalistic Neotropical frog. Mol Ecol. 2014;23:453–63.Google Scholar
  168. Myers EM, Zamudio KR. Multiple paternity in an aggregate breeding amphibian: the effects of reproductive skew on estimates of male reproductive success. Mol Ecol. 2004;13:1951–63.Google Scholar
  169. Nakamura M. Sex determination in amphibians. Semin Cell Dev Biol. 2009;20(3):271–82.Google Scholar
  170. Nali RC, Zamudio KR, Prado CPA. Microsatellite markers for Bokermannohyla species (Anura, Hylidae) from the Brazilian Cerrado and Atlantic Forest domains. Amphibia-Reptilia. 2014;35:355–60.Google Scholar
  171. Newman CE, Austin CC. Sequence capture and next-generation sequencing of ultraconserved elements in a large-genome salamander. Mol Ecol. 2016;25:6162–74.Google Scholar
  172. Nowoshilow S, Schloissnig S, Fei JF, Dahl A, Pang AWC, Pippel M, et al. The axolotl genome and the evolution of key tissue formation regulators. Nature. 2018;554:50–5.Google Scholar
  173. Nunziata SO, Lance SL, Scott DE, Lemmon EM, Weisrock DW. Genomic data detect corresponding signatures of population size change on an ecological time scale in two salamander species. Mol Ecol. 2017;26:1060–74.Google Scholar
  174. Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, et al. Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS One. 2013;8:e56802.Google Scholar
  175. Palo JU, O’Hara RB, Laugen AT, Laurila A, Primmers CR, Merilä J. Latitudinal divergence of common frog (Rana temporaria) life history traits by natural selection: evidence from a comparison of molecular and quantitative genetic data. Mol Ecol. 2003;12:1963–78.Google Scholar
  176. Paz A, Ibanez R, Lips KR, Crawford AJ. Testing the role of ecology and life history in structuring genetic variation across a landscape: a trait-based phylogeographic approach. Mol Ecol. 2015;24:3723–37.Google Scholar
  177. Peloso PLV, Frost DR, Richards SJ, Rodrigues MT, Donnellan S, Matsui M, et al. The impact of anchored phylogenomics and taxon sampling on phylogenetic inference in narrow-mouthed frogs (Anura, Microhylidae). Cladistics. 2016;32:113–40.Google Scholar
  178. Pennell MW, Mank JE, Peichel CL. Transitions in sex determination and sex chromosomes across vertebrate species. Mol Ecol. 2018;27:3950–63. Scholar
  179. Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One. 2012;7:e37135.Google Scholar
  180. Pie MR, Faircloth BC, Ribeiro LF, Bornschein MR, McCormack JE. Phylogenomics of montane frogs of the Brazilian Atlantic Forest is consistent with isolation in sky islands followed by climatic stability. Biol J Linn Soc. 2018;125:72–82.Google Scholar
  181. Polato NR, Gray MM, Gill BB, Becker CG, Casner KL, Flecker AS, et al. Genetic diversity and gene flow decline with elevation in montane mayflies. Heredity. 2017;119:107–16.Google Scholar
  182. Polato NR, Gill BA, Shah AA, Gray MM, Casner KL, Barthelet A, et al. Narrow thermal tolerance and low dispersal drive higher speciation in tropical mountains. Proc Natl Acad Sci U S A. 2018;
  183. Portik DM, Smith LL, Bi K. An evaluation of transcriptome-based exon capture for frog phylogenomics across multiple scales of divergence (Class: Amphibia, Order: Anura). Mol Ecol Resour. 2016;16:1069–83.Google Scholar
  184. Pritchard JK. Whole-genome sequencing data offer insights into human demography. Nat Genet. 2011;43:923–5.Google Scholar
  185. Pyron AR, Wiens JJ. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol Phylogenet Evol. 2011;61:543–83.Google Scholar
  186. Rhymer JM, Simberloff D. Extinction by hybridization and introgression. Annu Rev Ecol Syst. 1996;27:83–109.Google Scholar
  187. Richter-Boix A, Quintela M, Segelbacher G, Laurila A. Genetic analysis of differentiation among breeding ponds reveals a candidate gene for local adaptation in Rana arvalis. Mol Ecol. 2011;20:1582–600.Google Scholar
  188. Riley SPD, Shaffer HB, Voss SR, Fitzpatrick BM. Hybridization between a rare, native tiger salamander (Ambystoma californiense) and its introduced congener. Ecol Appl. 2003;13:1263–75.Google Scholar
  189. Ringler E, Ringler M, Jehle R, Hodl W. The female perspective of mating in A. femoralis, a territorial frog with paternal care – a spatial and genetic analysis. PLoS One. 2012;7:e40237.Google Scholar
  190. Rittmeyer EN, Allison A, Grundler MC, Thompson DK, Austin CC. Ecological guild evolution and the discovery of the world’s smallest vertebrate. PLoS One. 2012;7:e29797.Google Scholar
  191. Robertson LS, Cornman RS. Transcriptome resources for the frogs Lithobates clamitans and Pseudacris regilla, emphasizing antimicrobial peptides and conserved loci for phylogenetics. Mol Ecol Resour. 2014;14:178–83.Google Scholar
  192. Roelants K, Gower DJ, Wilkinson M, Loader SP, Biju SD, Guillaume K, et al. Global patterns of diversification in the history of modern amphibians. Proc Natl Acad Sci U S A. 2007;104:887–92.Google Scholar
  193. Rogers RL, Zhou L, Chu C, Márquez R, Corl A, Linderoth T, et al. Genomic takeover by transposable elements in the strawberry poison frog. Mol Biol Evol. 2018;
  194. Rokas A, Abbot P. Harnessing genomics for evolutionary insights. Trends Ecol Evol. 2009;24:192–200.Google Scholar
  195. Rosenblum EB, James TY, Zamudio KR, Poorten TJ, Ilut D, Rodriguez D, et al. Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proc Natl Acad Sci U S A. 2013;110:9385–90.Google Scholar
  196. Ruane S, Raxworthy CJ, Lemmon AR, Lemmon EM, Burbrink FT. Comparing species tree estimation with large anchored phylogenomic and small Sanger-sequenced molecular datasets: an empirical study on Malagasy pseudoxyrhophiine snakes. BMC Evol Biol. 2015;15:221.Google Scholar
  197. Ryan ME, Johnson JR, Fitzpatrick BM, Lowenstine LJ, Picco AM, Shaffer HB. Lethal effects of water quality on threatened California salamanders but not on co-occurring hybrid salamanders. Conserv Biol. 2013;27:95–102.Google Scholar
  198. Salthe SN, Duellman WE. Quantitative constraints associated with reproductive mode in anurans. In: Vial JL, editor. Evolutionary biology of anurans: contemporary research on major problems. Columbia: University of Missouri Press; 1973. p. 229–49.Google Scholar
  199. Savage AE, Zamudio KR. MHC genotypes associate with resistance to a frog-killing fungus. Proc Natl Acad Sci U S A. 2011;108:16705–10.Google Scholar
  200. Schloegel LM, Toledo LF, Longcore JE, Greenspan SE, Vieira CA, Lee M, et al. Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Mol Ecol. 2012;21:5162–77.Google Scholar
  201. Schmid M, Steinlein C, Bogart JP, Feichtinger W, Leon P, La Marca E, et al. The chromosomes of Terraranan frogs: insights into vertebrate cytogenetics. Cytogenet Genome Res. 2010;130:15–557.Google Scholar
  202. Schmid M, Evans B, Bogart JP. Polyploidy in Amphibia. Cytogenet Genome Res. 2015;145:315–30.Google Scholar
  203. Seigel RA, Dodd CK Jr. Translocation of amphibians: proven management method or experimental technique? Conserv Biol. 2002;16:552–4.Google Scholar
  204. Session AM, Uno Y, Kwon T, Hapman JAC, Toyoda A, Takahashi S, et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature. 2016;538:336–43.Google Scholar
  205. Shaffer HB, Gidis M, McCartney-Melstad E, Neal KM, Oyamaguchi HM, Tellez M, et al. Conservation genetics and genomics of amphibians and reptiles. Annu Rev Anim Biosci. 2015;3:113–38.Google Scholar
  206. Shen XX, Liang D, Feng YJ, Chen MY, Zhang PA. Versatile and highly efficient toolkit including 102 nuclear markers for vertebrate phylogenomics, tested by resolving the higher level relationships of the Caudata. Mol Biol Evol. 2013;30:2235–48.Google Scholar
  207. Slatkin M. Estimating levels of gene flow in natural populations. Genetics. 1981;99:323–35.Google Scholar
  208. Smith JJ, Timoshevskaya N, Timoshevskiy VA, Keinath MC, Hardy D, Voss SR. A chromosome-scale assembly of the enormous (32 Gb) axolotl genome. bioRxiv. 2018:373548.
  209. Soltis DE, Morris AB, McLachlan JS, Manos PS, Soltis PS. Comparative phylogeography of unglaciated eastern North America. Mol Ecol. 2006;15:4261–93.Google Scholar
  210. Soria-Carrasco V, Gompert Z, Comeault AA, Farkas TE, Parchman TL, Johnston JS, et al. Stick insect genomes reveal natural selection’s role in parallel speciation. Science. 2014;344:738–42.Google Scholar
  211. Stegen G, Pasmans F, Schmidt BR, Rouffaer LO, Van Praet S, Schaub M, et al. Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans. Nature. 2017;544:353–6.Google Scholar
  212. Steiner CC, Putnam AS, Hoeck PEA, Ryder OA. Conservation genomics of threatened animal species. Annu Rev Anim Biosci. 2013;1:261–81.Google Scholar
  213. Stinchcombe JR, Hoekstra HE. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity. 2008;100:158–70.Google Scholar
  214. Storfer A, Mech SG, Reudink MW, Ziemba RE, Warren J, Collins JP. Evidence for introgression in the endangered Sonora tiger salamander, Ambystoma tigrinum stebbinsi (Lowe). Copeia. 2004;2004:783–396.Google Scholar
  215. Storfer A, Eastman JM, Spear SF. Modern molecular methods for amphibian conservation. Bioscience. 2009;59:559–71.Google Scholar
  216. Streicher JW, Miller EC, Guerrero PC, Correa C, Ortiz JC, Crawford AJ, et al. Evaluating methods for phylogenomic analyses, and a new phylogeny for a major frog clade (Hyloidea) based on 2214 loci. Mol Phylogenet Evol. 2018;119:128–43.Google Scholar
  217. Summers K, Amos W. Behavioral, ecological, and molecular genetic analyses of reproductive strategies in the Amazonian dart-poison frog, Dendrobates ventrimaculatus. Behav Ecol. 1997;8:260–7.Google Scholar
  218. Sun C, Shepard DB, Chong RA, Arriaza JL, Hall K, Castoe TA, et al. LTR Retrotransposons contribute to genomic gigantism in plethodontid salamanders. Genome Biol Evol. 2012;4:168–83.Google Scholar
  219. Sun YB, Xiong ZJ, Xiang XY, Liu SP, Zhou WW, Tu XL, et al. Whole-genome sequence of the Tibetan frog Nanorana parkeri and the comparative evolution of tetrapod genomes. Proc Natl Acad Sci U S A. 2015;112:E1257–E62.Google Scholar
  220. Taberlet P, Coissac E, Hajibabaei M, Rieseberg LH. Environmental DNA. Mol Ecol. 2012;21:1789–93.Google Scholar
  221. Thrasher DJ, Butcher BG, Campagna L, Webster MS, Lovette IJ. Double-digest RAD sequencing outperforms microsatellite loci at assigning paternity and estimating relatedness: a proof of concept in a highly promiscuous bird. Mol Ecol Resour. 2018;18:953–65.Google Scholar
  222. Toews DPL, Taylor SA, Vallender R, Brelsford A, Butcher BG, Messer PW, et al. Plumage genes and little else distinguish the genomes of hybridizing warblers. Curr Biol. 2016;26:2313–8.Google Scholar
  223. Tokarska M, Marshall T, Kowalczyk R, Wojcik JM, Pertoldi C, Kristensen TN, et al. Effectiveness of microsatellite and SNP markers for parentage and identity analysis in species with low genetic diversity: the case of European bison. Heredity. 2009;103:326–32.Google Scholar
  224. Trenham PC, Marsh DM. Amphibian translocation programs: reply to Seigel and Dodd. Conserv Biol. 2002;16:555–6.Google Scholar
  225. Trumbo DR, Epstein B, Hohenlohe PA, Alford RA, Schwarzkopf L, Storfer A. Mixed population genomics support for the central marginal hypothesis across the invasive range of the cane toad (Rhinella marina) in Australia. Mol Ecol. 2016;25:4161–76.Google Scholar
  226. Urban MC, Richardson JL, Freidenfelds NA, Drake DL, Fischer JF, Saunders PP. Microgeographic adaptation of wood frog tadpoles to an apex predator. Copeia. 2017;105:451–61.Google Scholar
  227. Valentini A, Taberlet P, Miaud C, Civade R, Herder J, Thomsen PF, et al. Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding. Mol Ecol. 2016;25:929–42.Google Scholar
  228. Vieites DR, Nieto-Román S, Barluenga M, Palanca A, Vences M, Meyer A. Post-mating clutch piracy in an amphibian. Nature. 2004;431:305–8.Google Scholar
  229. Vinogradov AE. Genome size and GC-percent in vertebrates as determined by flow cytometry: the triangular relationship. Cytometry. 1998;31:100–9.Google Scholar
  230. Vorburger C, Reyer HU. A genetic mechanism of species replacement in European waterfrogs? Conserv Genet. 2003;4:141–55.Google Scholar
  231. Wang Z, Gerstein M, Snyder M. RNA-seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009;10:57–63.Google Scholar
  232. Wang G-D, Zhang B-L, Zhou W-W, Li Y-X, Jin J-Q, Shao Y, et al. Selection and environmental adaptation along a path to speciation in the Tibetan frog Nanorana parkeri. Proc Natl Acad Sci U S A. 2018;115:E5056–E65.Google Scholar
  233. Ward RD, Skibinski DOF, Woodwark M. Protein heterozygosity, protein-structure, and taxonomic differentiation. Evol Biol. 1992;26:73–159.Google Scholar
  234. Weinman LR, Solomon JW, Rubenstein DR. A comparison of single nucleotide polymorphism and microsatellite markers for analysis of parentage and kinship in a cooperatively breeding bird. Mol Ecol Resour. 2015;15:502–11.Google Scholar
  235. Weir BS, Anderson AD, Hepler AB. Genetic relatedness analysis: modern data and new challenges. Nat Rev Genet. 2006;7:771–80.Google Scholar
  236. Welch AM, Semlitsch RD, Gerhardt HC. Call duration as an indicator of genetic quality in male gray tree frogs. Science. 1998;280:1928–30.Google Scholar
  237. Wells KD. The ecology and behavior of amphibians. Chicago: University of Chicago Press; 2007.Google Scholar
  238. Wilhelm J, Pingoud A, Hahn M. Real-time PCR-based method for the estimation of genome sizes. Nucleic Acids Res. 2003;31:e56.Google Scholar
  239. Wong PBY, Wiley EO, Johnson WE, Ryder OA, O’Brien SJ, Haussler D, et al. Tissue sampling methods and standards for vertebrate genomics. Gigascience. 2012;1:8.Google Scholar
  240. Woodhams DC, Alford RA, Briggs CJ, Johnson M, Rollins-Smith LA. Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogens. Ecology. 2008;89:1627–39.Google Scholar
  241. Wright S. Evolution in Mendelian populations. Genetics. 1931;16:97–159.Google Scholar
  242. Wright S. The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution. 1965;19:395–420.Google Scholar
  243. Yandell M, Ence D. A beginner’s guide to eukaryotic genome annotation. Nat Rev Genet. 2012;13:329–42.Google Scholar
  244. Yang WZ, Qi Y, Bi K, Fu JZ. Toward understanding the genetic basis of adaptation to high-elevation life in poikilothermic species: a comparative transcriptomic analysis of two ranid frogs, Rana chensinensis and R. kukunoris. BMC Genomics. 2012;13:588.Google Scholar
  245. Zamudio KR, Savage WK. Historical isolation, range expansion, and secondary contact of two highly divergent mitochondrial lineages in spotted salamanders (Ambystoma maculatum). Evolution. 2003;57:1631–52.Google Scholar
  246. Zamudio KR, Harrison RG, Matocq M. Hybridization in threatened and endangered animal taxa: implications for conservation and management of biodiversity. In: DeWoody A, Bickham J, Michler C, Nichols K, Rhodes G, Woeste K, editors. Molecular approaches in natural resource conservation and management. Cambridge: Cambridge University Press; 2010. p. 169–89.Google Scholar
  247. Zamudio KR, Bell RC, Mason NA. Phenotypes in phylogeography: species’ traits, environmental variation, and vertebrate diversification. Proc Natl Acad Sci U S A. 2016a;113:8041–8.Google Scholar
  248. Zamudio KR, Bell RC, Nali RC, Haddad CFB, Prado CPA. Polyandry, predation, and the evolution of frog reproductive modes. Am Nat. 2016b;188:S41–61.Google Scholar
  249. Zeisset I, Beebee TJC. Amphibian phylogeography: a model for understanding historical aspects of species distributions. Heredity. 2008;101:109–19.Google Scholar
  250. Zhai WW, Nielsen R, Slatkin M. An investigation of the statistical power of neutrality tests based on comparative and population genetic data. Mol Biol Evol. 2009;26:273–83.Google Scholar
  251. Zhang P, Wake DB. Higher-level salamander relationships and divergence dates inferred from complete mitochondrial genomes. Mol Phylogenet Evol. 2009;53:492–508.Google Scholar
  252. Zhang GJ, Li C, Li QY, Li B, Larkin DM, Lee C, et al. Comparative genomics reveals insights into avian genome evolution and adaptation. Science. 2014;346(6215):1311–20.Google Scholar
  253. Zhen Y, Aardema ML, Medina EM, Schumer M, Andolfatto P. Parallel molecular evolution in an herbivore community. Science. 2012;337:1634–7.Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • W. Chris Funk
    • 1
    Email author
  • Kelly R. Zamudio
    • 2
  • Andrew J. Crawford
    • 3
  1. 1.Department of Biology, Graduate Degree Program in EcologyColorado State UniversityFort CollinsUSA
  2. 2.Ecology and Evolutionary BiologyCornell UniversityIthacaUSA
  3. 3.Department of Biological SciencesUniversidad de Los AndesBogotáColombia

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