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

  • Chapter
  • First Online:
Population Genomics: Wildlife

Part of the book series: Population Genomics ((POGE))

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
EUR 29.95
Price includes VAT (Germany)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 149.79
Price includes VAT (Germany)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
EUR 192.59
Price includes VAT (Germany)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
EUR 192.59
Price includes VAT (Germany)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Allendorf FW. Genetics and the conservation of natural populations: allozymes to genomes. Mol Ecol. 2017;26:420–30.

    PubMed  CAS  Google Scholar 

  • Allendorf FW, Phelps SR. Use of allelic frequencies to describe population structure. Can J Fish Aquat Sci. 1981;38:1507–14.

    Google Scholar 

  • Allendorf FW, Hohenlohe PA, Luikart G. Genomics and the future of conservation genetics. Nat Rev Genet. 2010;11:697–709.

    PubMed  CAS  Google Scholar 

  • Allendorf FW, Luikart G, Aitken SN. Conservation and the genetics of populations. 2nd ed. Oxford: Wiley-Blackwell; 2013.

    Google Scholar 

  • AmphibiaWeb. University of California, Berkeley, 2018. http://amphibiaweb.org/. Accessed 30 Sept 2018.

  • Anderson E, Stebbins GL. Hybridization as an evolutionary stimulus. Evolution. 1954;8:378–88.

    Google Scholar 

  • Andrés JA, Bogdanowicz SM. Isolating microsatellite loci: looking back, looking ahead. Methods Mol Biol. 2011;772:211–32.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Arnold ML. Natural hybridization and evolution. Oxford: Oxford University Press; 1997.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Bachtrog D. A dynamic view of sex chromosome evolution. Curr Opin Genet Dev. 2006;16:578–85.

    PubMed  CAS  Google Scholar 

  • Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, et al. Rapid SNP discovery and genetic map** using sequenced RAD markers. PLoS One. 2008;3:e3376.

    PubMed  PubMed Central  Google Scholar 

  • Balkenhol N, Cushman SA, Storfer AT, Waits LP. Landscape genetics: concepts, methods, applications. Oxford: Wiley-Blackwell; 2016.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • Barrow LN, Lemmon AR, Lemmon EM. Targeted sampling and target capture: assessing phylogeographic concordance with genome-wide data. Syst Biol. 2018; https://doi.org/10.1093/sysbio/syy021/4948751.

  • Barton N, Bengtsson BO. The barrier to genetic exchange between hybridizing populations. Heredity. 1986;57:357–76.

    PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • Beaumont MA, Balding DJ. Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol. 2004;13:969–80.

    PubMed  CAS  Google Scholar 

  • 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 

  • Beebee TJC. Conservation genetics of amphibians. Heredity. 2005;95:423–7.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Black WC IV, Baer CF, Antolin MF, DuTeau NM. Population genomics: genome-wide sampling of insect populations. Annu Rev Entomol. 2001;46:441–69.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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 

  • Coop G, Witonsky D, Di Rienzo A, Pritchard JK. Using environmental correlations to identify loci underlying local adaptation. Genetics. 2010;185:1411–23.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Crispo E. Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow. J Evol Biol. 2008;21:1460–9.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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; https://doi.org/10.1101/329847.

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • Drummond AJ, Suchard MA, **e D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969–73.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Duellman WE, Trueb L. Biology of amphibians. New York: McGraw-Hill Book; 1986.

    Google Scholar 

  • Eckert CG, Samis KE, Lougheed SC. Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol. 2008;17:1170–88.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • Elinson RP. Inheritance and expression of a sex-linked enzyme in the frog, Rana clamitans. Biochem Genet. 1983;21:435–42.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Endler JA. Natural selection in the wild. Monogr Popul Biol. 1986;21:1–336.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Faith DP. Conservation evaluation and phylogenetic diversity. Biol Conserv. 1992;61:1–10.

    Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ficetola GF, Bonin A. Conserving adaptive genetic diversity in dynamic landscapes. Mol Ecol. 2011;20:1569–71.

    PubMed  Google Scholar 

  • 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 

  • Fisher RA. The genetical theory of natural selection. Oxford: Clarendon Press; 1930.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Francois O, Martins H, Caye K, Schoville SD. Controlling false discoveries in genome scans for selection. Mol Ecol. 2016;25:454–69.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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 

  • Fuentes-Pardo AP, Ruzzante DE. Whole-genome sequencing approaches for conservation biology: advantages, limitations and practical recommendations. Mol Ecol. 2017;26:5369–406.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Funk WC, Mckay JK, Hohenlohe PA, Allendorf FW. Harnessing genomics for delineating conservation units. Trends Ecol Evol. 2012;27:489–96.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Gamble T, Zarkower D. Identification of sex-specific molecular markers using restriction site-associated DNA sequencing. Mol Ecol Resour. 2014;14:902–13.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • García-R JC, Crawford AJ, Mendoza AM, Ospina O, Cardenas H, Castro F. Comparative phylogeography of direct-develo** frogs (Anura: Craugastoridae: Pristimantis) in the southern Andes of Colombia. PLoS One. 2012;7:e46077.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Glaubitz JC, Rhodes OE, Dewoody JA. Prospects for inferring pairwise relationships with single nucleotide polymorphisms. Mol Ecol. 2003;12:1039–47.

    PubMed  CAS  Google Scholar 

  • Glenn TC. Field guide to next-generation DNA sequencers. Mol Ecol Resour. 2011;11:759–69.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Gompert Z, Fordyce JA, Forister ML, Shapiro AM, Nice CC. Homoploid hybrid speciation in an extreme habitat. Science. 2006;314:1923–5.

    PubMed  CAS  Google Scholar 

  • Grant PR, Grant BR. Hybridization of bird species. Science. 1992;256:193–7.

    PubMed  CAS  Google Scholar 

  • 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 

  • Gregory TR. Animal genome size database. 2011. http://www.genomesize.com/.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Guerrero RF, Kirkpatrick M, Perrin N. Cryptic recombination in the ever-young sex chromosomes of hylid frogs. J Evol Biol. 2012;25:1947–54.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Haldane JBS. A mathematical theory of natural and artificial selection. VI. Isolation. Proc Camb Philos Soc. 1930;26:220–30.

    Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Harding G, Griffiths RA, Pavajeau L. Developments in amphibian captive breeding and reintroduction programs. Conserv Biol. 2016;30:340–9.

    PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • Hayes TB. Sex determination and primary sex differentiation in amphibians: genetic and developmental mechanisms. J Exp Zool. 1998;281:373–99.

    PubMed  CAS  Google Scholar 

  • Heinicke MP, Lemmon AR, Lemmon EM, McGrath K, Hedges SB. Phylogenomic support for evolutionary relationships of New World direct-develo** frogs (Anura: Terraranae). Mol Phylogenet Evol. 2018;118:145–55.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hillis DM, Green DM. Evolutionary changes of heterogametic sex in the phylogenetic history of amphibians. J Evol Biol. 1990;3:49–64.

    Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hughes C. Integrating molecular techniques with field methods in studies of social behavior: a revolution results. Ecology. 1998;79:383–99.

    Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • Isaac NJB, Redding DW, Meredith HM, Safi K. Phylogenetically-informed priorities for amphibian conservation. PLoS One. 2012;7:e43912.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Jockusch EL. An evolutionary correlate of genome size change in plethodontid salamanders. Proc R Soc B Biol Sci. 1997;264(1381):597–604.

    CAS  Google Scholar 

  • Johnson WE, Koepfli K. The role of genomics in conservation and reproductive sciences. Adv Exp Med Biol. 2014;753:71–96.

    PubMed  Google Scholar 

  • Jones MR, Good JM. Targeted capture in evolutionary and ecological genomics. Mol Ecol. 2016;25:185–202.

    PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • Kimura M, Crow JF. The measurement of the effective population number. Evolution. 1963;17:279–88.

    Google Scholar 

  • Kingman JFC. The coalescent. Stoch Process Appl. 1982;13:235–48.

    Google Scholar 

  • Koepfli KP, Paten B, O’Brien SJ, Scientists GKC. The Genome 10K Project: a way forward. Annu Rev Anim Biosci. 2015;3:57–111.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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 

  • Lemmon EM, Juenger TE. Geographic variation in hybridization across a reinforcement contact zone of chorus frogs (Pseudacris). Ecol Evol. 2017;7:9485–502.

    PubMed  PubMed Central  Google Scholar 

  • Lemmon AR, Emme SA, Lemmon EM. Anchored hybrid enrichment for massively high-throughput phylogenomics. Syst Biol. 2012;61:727–44.

    PubMed  CAS  Google Scholar 

  • 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. https://doi.org/10.1038/s41559-018-0674-4.

    Article  PubMed  Google Scholar 

  • Longcore JE, Pessier AP, Nichols DK. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia. 1999;91:219–27.

    Google Scholar 

  • Longo AV, Burrowes PA, Zamudio KR. Genomic studies of disease-outcome in host-pathogen dynamics. Integr Comp Biol. 2014;54:427–38.

    PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Luikart G, England PR, Tallmon D, Jordan S, Taberlet P. The power and promise of population genomics: from genoty** to genome ty**. Nat Rev Genet. 2003;4:981–94.

    PubMed  CAS  Google Scholar 

  • Mallet J. Hybridization as an invasion of the genome. Trends Ecol Evol. 2005;20:229–37.

    PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mavárez J, Salazar CA, Bermingham E, Salcedo C, Jiggins CD, Linares M. Speciation by hybridization in Heliconius butterflies. Nature. 2006;441:868–71.

    PubMed  Google Scholar 

  • McCartney-Melstad E, Shaffer HB. Amphibian molecular ecology and how it has informed conservation. Mol Ecol. 2015;24:5084–109.

    PubMed  Google Scholar 

  • McCartney-Melstad E, Mount GG, Shaffer HB. Exon capture optimization in amphibians with large genomes. Mol Ecol Resour. 2016;16:1084–94.

    PubMed  CAS  Google Scholar 

  • McCormack JE, Faircloth BC. Next-generation phylogenetics takes root. Mol Ecol. 2013;22:19–21.

    PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • McKay JK, Latta RG. Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol. 2002;17:285–91.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Nakamura M. Sex determination in amphibians. Semin Cell Dev Biol. 2009;20(3):271–82.

    PubMed  Google Scholar 

  • 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 

  • Newman CE, Austin CC. Sequence capture and next-generation sequencing of ultraconserved elements in a large-genome salamander. Mol Ecol. 2016;25:6162–74.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, et al. Map** the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS One. 2013;8:e56802.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Pennell MW, Mank JE, Peichel CL. Transitions in sex determination and sex chromosomes across vertebrate species. Mol Ecol. 2018;27:3950–63. https://doi.org/10.1111/mec.14540.

    Article  PubMed  PubMed Central  Google Scholar 

  • Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. Double digest RADseq: an inexpensive method for de novo SNP discovery and genoty** in model and non-model species. PLoS One. 2012;7:e37135.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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; https://doi.org/10.1073/pnas.1809326115.

  • 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.

    PubMed  CAS  Google Scholar 

  • Pritchard JK. Whole-genome sequencing data offer insights into human demography. Nat Genet. 2011;43:923–5.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Rhymer JM, Simberloff D. Extinction by hybridization and introgression. Annu Rev Ecol Syst. 1996;27:83–109.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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; https://doi.org/10.1093/molbev/msy185.

  • Rokas A, Abbot P. Harnessing genomics for evolutionary insights. Trends Ecol Evol. 2009;24:192–200.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • Schmid M, Evans B, Bogart JP. Polyploidy in Amphibia. Cytogenet Genome Res. 2015;145:315–30.

    PubMed  Google Scholar 

  • Seigel RA, Dodd CK Jr. Translocation of amphibians: proven management method or experimental technique? Conserv Biol. 2002;16:552–4.

    Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Slatkin M. Estimating levels of gene flow in natural populations. Genetics. 1981;99:323–35.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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. https://doi.org/10.1101/373548.

  • Soltis DE, Morris AB, McLachlan JS, Manos PS, Soltis PS. Comparative phylogeography of unglaciated eastern North America. Mol Ecol. 2006;15:4261–93.

    PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Steiner CC, Putnam AS, Hoeck PEA, Ryder OA. Conservation genomics of threatened animal species. Annu Rev Anim Biosci. 2013;1:261–81.

    PubMed  Google Scholar 

  • Stinchcombe JR, Hoekstra HE. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity. 2008;100:158–70.

    PubMed  CAS  Google Scholar 

  • 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 

  • Storfer A, Eastman JM, Spear SF. Modern molecular methods for amphibian conservation. Bioscience. 2009;59:559–71.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • Sun YB, **ong ZJ, **ang 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Taberlet P, Coissac E, Hajibabaei M, Rieseberg LH. Environmental DNA. Mol Ecol. 2012;21:1789–93.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Trenham PC, Marsh DM. Amphibian translocation programs: reply to Seigel and Dodd. Conserv Biol. 2002;16:555–6.

    Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Vinogradov AE. Genome size and GC-percent in vertebrates as determined by flow cytometry: the triangular relationship. Cytometry. 1998;31:100–9.

    PubMed  CAS  Google Scholar 

  • Vorburger C, Reyer HU. A genetic mechanism of species replacement in European waterfrogs? Conserv Genet. 2003;4:141–55.

    CAS  Google Scholar 

  • Wang Z, Gerstein M, Snyder M. RNA-seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009;10:57–63.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wang G-D, Zhang B-L, Zhou W-W, Li Y-X, ** 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ward RD, Skibinski DOF, Woodwark M. Protein heterozygosity, protein-structure, and taxonomic differentiation. Evol Biol. 1992;26:73–159.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Weir BS, Anderson AD, Hepler AB. Genetic relatedness analysis: modern data and new challenges. Nat Rev Genet. 2006;7:771–80.

    PubMed  CAS  Google Scholar 

  • Welch AM, Semlitsch RD, Gerhardt HC. Call duration as an indicator of genetic quality in male gray tree frogs. Science. 1998;280:1928–30.

    PubMed  CAS  Google Scholar 

  • Wells KD. The ecology and behavior of amphibians. Chicago: University of Chicago Press; 2007.

    Google Scholar 

  • Wilhelm J, **oud A, Hahn M. Real-time PCR-based method for the estimation of genome sizes. Nucleic Acids Res. 2003;31:e56.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Wright S. Evolution in Mendelian populations. Genetics. 1931;16:97–159.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wright S. The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution. 1965;19:395–420.

    Google Scholar 

  • Yandell M, Ence D. A beginner’s guide to eukaryotic genome annotation. Nat Rev Genet. 2012;13:329–42.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Zeisset I, Beebee TJC. Amphibian phylogeography: a model for understanding historical aspects of species distributions. Heredity. 2008;101:109–19.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Zhang P, Wake DB. Higher-level salamander relationships and divergence dates inferred from complete mitochondrial genomes. Mol Phylogenet Evol. 2009;53:492–508.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhen Y, Aardema ML, Medina EM, Schumer M, Andolfatto P. Parallel molecular evolution in an herbivore community. Science. 2012;337:1634–7.

    PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to W. Chris Funk .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Funk, W.C., Zamudio, K.R., Crawford, A.J. (2018). Advancing Understanding of Amphibian Evolution, Ecology, Behavior, and Conservation with Massively Parallel Sequencing. In: Hohenlohe, P.A., Rajora, O.P. (eds) Population Genomics: Wildlife. Population Genomics. Springer, Cham. https://doi.org/10.1007/13836_2018_61

Download citation

  • DOI: https://doi.org/10.1007/13836_2018_61

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-030-63488-9

  • Online ISBN: 978-3-030-63489-6

  • eBook Packages: Computer ScienceComputer Science (R0)

Publish with us

Policies and ethics

Navigation