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Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus


Autoři: Polina Yu. Novikova aff001;  Ian G. Brennan aff003;  William Booker aff004;  Michael Mahony aff005;  Paul Doughty aff006;  Alan R. Lemmon aff007;  Emily Moriarty Lemmon aff004;  J. Dale Roberts aff008;  Levi Yant aff009;  Yves Van de Peer aff001;  J. Scott Keogh aff003;  Stephen C. Donnellan aff012
Působiště autorů: VIB-UGent Center for Plant Systems Biology, Ghent, Belgium aff001;  Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium aff002;  Division of Ecology & Evolution, Research School of Biology, The Australian National University, Canberra, Australia aff003;  Department of Biological Science, Florida State University, Tallahassee, Florida, United States of America aff004;  School of Environmental and Life Sciences, University of Newcastle, Callaghan, Australia aff005;  Western Australian Museum, Welshpool, Perth, Australia aff006;  Department of Scientific Computing, Florida State University, Tallahassee, Florida, United States of America aff007;  School of Biological Sciences, and, Centre for Evolutionary Biology, University of Western Australia, Albany, Western Australia, Australia aff008;  School of Life Sciences and Future Food Beacon, University of Nottingham, Nottingham, United Kingdom aff009;  Bioinformatics Institute Ghent, Ghent University, Ghent, Belgium aff010;  Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria, South Africa aff011;  South Australian Museum, North Terrace, Adelaide, Australia aff012;  School of Biological Sciences, University of Adelaide, North Terrace, Adelaide, Australia aff013
Vyšlo v časopise: Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus. PLoS Genet 16(5): e1008769. doi:10.1371/journal.pgen.1008769
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008769

Souhrn

Polyploidy has played an important role in evolution across the tree of life but it is still unclear how polyploid lineages may persist after their initial formation. While both common and well-studied in plants, polyploidy is rare in animals and generally less understood. The Australian burrowing frog genus Neobatrachus is comprised of six diploid and three polyploid species and offers a powerful animal polyploid model system. We generated exome-capture sequence data from 87 individuals representing all nine species of Neobatrachus to investigate species-level relationships, the origin and inheritance mode of polyploid species, and the population genomic effects of polyploidy on genus-wide demography. We describe rapid speciation of diploid Neobatrachus species and show that the three independently originated polyploid species have tetrasomic or mixed inheritance. We document higher genetic diversity in tetraploids, resulting from widespread gene flow between the tetraploids, asymmetric inter-ploidy gene flow directed from sympatric diploids to tetraploids, and isolation of diploid species from each other. We also constructed models of ecologically suitable areas for each species to investigate the impact of climate on differing ploidy levels. These models suggest substantial change in suitable areas compared to past climate, which correspond to population genomic estimates of demographic histories. We propose that Neobatrachus diploids may be suffering the early genomic impacts of climate-induced habitat loss, while tetraploids appear to be avoiding this fate, possibly due to widespread gene flow. Finally, we demonstrate that Neobatrachus is an attractive model to study the effects of ploidy on the evolution of adaptation in animals.

Klíčová slova:

Amphibian genomics – Gene flow – Genetic loci – Phylogenetic analysis – Ploidy – Polyploidy – Sequence alignment – Tetraploidy


Zdroje

1. Soltis DE, Visger CJ, Soltis PS. The polyploidy revolution then. . .and now: Stebbins revisited. Am J Bot. 2014;101(7):1057–78. doi: 10.3732/ajb.1400178 25049267

2. Van de Peer Y, Mizrachi E, Marchal K. The evolutionary significance of polyploidy. Nat Rev Genet. 2017;18(7):411–24. doi: 10.1038/nrg.2017.26 28502977

3. Dehal P, Boore JL. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 2005;3(10):e314. doi: 10.1371/journal.pbio.0030314 16128622

4. Otto SP, Whitton J. Polyploid incidence and evolution. Annu Rev Genet. 2000;34:401–37. doi: 10.1146/annurev.genet.34.1.401 11092833

5. Li Z, Tiley GP, Galuska SR, Reardon CR, Kidder TI, Rundell RJ, et al. Multiple large-scale gene and genome duplications during the evolution of hexapods. Proc Natl Acad Sci U S A. 2018;115(18):4713–8. doi: 10.1073/pnas.1710791115 29674453

6. Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M, Noel B, et al. The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun. 2014;5:3657. doi: 10.1038/ncomms4657 24755649

7. Stenberg P, Saura A. Meiosis and its deviations in polyploid animals. Cytogenet Genome Res. 2013;140(2–4):185–203. doi: 10.1159/000351731 23796636

8. Neiman M, Sharbel TF, Schwander T. Genetic causes of transitions from sexual reproduction to asexuality in plants and animals. J Evol Biol. 2014;27(7):1346–59. doi: 10.1111/jeb.12357 24666600

9. Mable BK, Alexandrou MA, Taylor MI. Genome duplication in amphibians and fish: an extended synthesis: Polyploidy in amphibians and fish. Journal of Zoology. 2011;284:151–82.

10. Evans BJ. Genome evolution and speciation genetics of clawed frogs (Xenopus and Silurana). Front Biosci. 2008;13:4687–706. doi: 10.2741/3033 18508539

11. Session AM, Uno Y, Kwon T, Chapman JA, Toyoda A, Takahashi S, et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature. 2016;538(7625):336–43. doi: 10.1038/nature19840 27762356

12. Schmid M, Evans BJ, Bogart JP. Polyploidy in Amphibia. Cytogenetic and Genome Research. 2015;145:315–30. doi: 10.1159/000431388 26112701

13. Miura I. Sex Determination and Sex Chromosomes in Amphibia. Sex Dev. 2017;11(5–6):298–306. doi: 10.1159/000485270 29241181

14. Schmid M, Steinlein C. Sex chromosomes, sex-linked genes, and sex determination in the vertebrate class amphibia. EXS. 2001(91):143–76. doi: 10.1007/978-3-0348-7781-7_8 11301597

15. Roberts JD. Taxonomic status of the Australian burrowing frogs Neobatrachus sudelli, N. centralis and Neoruinosus and clarification of the type specimen of N. albipes. Records of the Western Australian Museum. 2010;25: 455–8.

16. Frost DR. Amphibian Species of the World: an Online Reference. Version 6.0 (Date of access). Electronic Database accessible at http://research.amnh.org/herpetology/amphibia/index.html. American Museum of Natural History, New York, USA. 2016.

17. Mahony MJ, Robinson ES. Polyploidy in the australian leptodactylid frog genus Neobatrachus. Chromosoma. 1980;81(2):199–212. doi: 10.1007/BF00285949 7192202

18. Shea GM. Emendation of the specific name of the frog Neobatrachus sudelli (Lamb, 1911) (Anura:Myobatrachidae). Memoirs of the Queensland Museum. 2012;56(1):116–7.

19. Mable BKR, Roberts J.D. Mitochondrial DNA evolution of tetraploids in the genus Neobatrachus (Anura: Myobatrachidae). Copeia. 1997;4:680–9.

20. Mahony M, Roberts JD. Two new species of desert burrowing frogs of the genus Neobatrachus (Anura:Myobatrachidae) from Western Australia. Records of the Western Australian Museum. 1986;13:155–70.

21. Roberts JD, Mahony M, Kendrick P, Majors CM. A new species of burrowing frog, Neobatrachus (Anura:Myobatrachidae), from the eastern wheatbelt of Western Australia. Records of the Western Australian Museum. 1991;15:23–32.

22. Mahony M, Donnellan SC, Roberts JD. An Electrophoretic Investigation of Relationships of Diploid and Tetraploid Species of Australian Desert Frogs Neobatrachus (Anura: Myobatrachidae). Australian Journal of Zoology. 1996;44:639–50.

23. Keller MJ, Gerhardt HC. Polyploidy alters advertisement call structure in gray treefrogs. Proc Biol Sci. 2001;268(1465):341–5. doi: 10.1098/rspb.2000.1391 11270429

24. Roberts JD. Call Evolution in Neobatrachus (Anura: Myobatrachidae): Speculations on Tetraploid Origins. Copeia. 1997;1997(4):791–801.

25. Roberts JD, Edwards D. The Evolution, Physiology and Ecology of the Australian Arid-Zone Frog Fauna. On the Ecology of Australia’s Arid Zone 2018. p. 149–80.

26. Wasserman AO. Polyploidy in the common tree toad Hyla versicolor Le Conte. Science. 1970;167(3917):385–6. doi: 10.1126/science.167.3917.385 5409740

27. Bogart J. Evolutionary implications of polyploidy in amphibians and reptiles. In: Lewis WH ed Polyploidy: Biological relevance. Plenum Press: New York. pp 341–378. 1980.

28. Holloway AK, Cannatella DC, Gerhardt HC, Hillis DM. Polyploids with different origins and ancestors form a single sexual polyploid species. Am Nat. 2006;167(4):E88–101. doi: 10.1086/501079 16670990

29. Comai L. The advantages and disadvantages of being polyploid. Nat Rev Genet. 2005;6(11):836–46. doi: 10.1038/nrg1711 16304599

30. Mason AS, Pires JC. Unreduced gametes: meiotic mishap or evolutionary mechanism? Trends Genet. 2015;31(1):5–10. doi: 10.1016/j.tig.2014.09.011 25445549

31. Pandian TJK, R. Ploidy induction and sex control in fish. Hydrobiologia. 1998;384(1–3):167–243.

32. Parisod C, Holderegger R, Brochmann C. Evolutionary consequences of autopolyploidy. New Phytol. 2010;186(1):5–17. doi: 10.1111/j.1469-8137.2009.03142.x 20070540

33. Becak ML, Becak W, Rabello MN. Cytological evidence of constant tetraploidy in the bisexual South American frog Odontophrynus americanus. Chromosoma. 1966;19(2):188–93. doi: 10.1007/BF00293683 5959682

34. Bogart JP. Chromosomes of the South American amphibian family Ceratophridae with a reconsideration of the taxonomic status of Odontophrynus americanus. Can J Genet Cytol. 1967;9(3):531–42. doi: 10.1139/g67-057 6079738

35. Martino AL, Sinsch U. Speciation by polyploidy in Odontophrynus americanus. Journal of Zoology. 2002;257(1):67–81.

36. Pollo FE, Grenat PR, Otero MA, Babini S, Salas NE, Martino AL. Evaluation in situ of genotoxic and cytotoxic response in the diploid/polyploid complex Odontophrynus (Anura: Odontophrynidae) inhabiting agroecosystems. Chemosphere. 2019;216:306–12. doi: 10.1016/j.chemosphere.2018.10.149 30384299

37. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues AS, Fischman DL, et al. Status and trends of amphibian declines and extinctions worldwide. Science. 2004;306(5702):1783–6. doi: 10.1126/science.1103538 15486254

38. Collins JP. Amphibian decline and extinction: what we know and what we need to learn. Dis Aquat Organ. 2010;92(2–3):93–9. doi: 10.3354/dao02307 21268970

39. Hudson MA, Young RP, D'Urban Jackson J, Orozco-terWengel P, Martin L, James A, et al. Dynamics and genetics of a disease-driven species decline to near extinction: lessons for conservation. Sci Rep. 2016;6:30772. doi: 10.1038/srep30772 27485994

40. O'Hanlon SJ, Rieux A, Farrer RA, Rosa GM, Waldman B, Bataille A, et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Science. 2018;360(6389):621–7. doi: 10.1126/science.aar1965 29748278

41. Lemmon AR, Emme SA, Lemmon EM. Anchored hybrid enrichment for massively high-throughput phylogenomics. Syst Biol. 2012;61(5):727–44. doi: 10.1093/sysbio/sys049 22605266

42. Barrow LN, Lemmon AR, Lemmon EM. Targeted Sampling and Target Capture: Assessing Phylogeographic Concordance with Genome-wide Data. Syst Biol. 2018;67(6):979–96. doi: 10.1093/sysbio/syy021 30339251

43. 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. doi: 10.1016/j.ympev.2017.09.021 28963082

44. Yuan Z-Y, Zhang B-L, Raxworthy CJ, Weisrock DW, Hime PM, Jin J-Q, et al. Natatanuran frogs used the Indian Plate to step-stone disperse and radiate across the Indian Ocean. National Science Review. 2018:nwy092–nwy.

45. Mirarab S, Warnow T. ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics. 2015;31(12):i44–52. doi: 10.1093/bioinformatics/btv234 26072508

46. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–3. doi: 10.1093/bioinformatics/btu033 24451623

47. Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Research. 2009;19:1655–64. doi: 10.1101/gr.094052.109 19648217

48. 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(29):E5864–E70. doi: 10.1073/pnas.1704632114 28673970

49. Hollister JD, Arnold BJ, Svedin E, Xue KS, Dilkes BP, Bomblies K. Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genet. 2012;8(12):e1003093. doi: 10.1371/journal.pgen.1003093 23284289

50. Arnold B, Kim ST, Bomblies K. Single Geographic Origin of a Widespread Autotetraploid Arabidopsis arenosa Lineage Followed by Interploidy Admixture. Mol Biol Evol. 2015;32(6):1382–95. doi: 10.1093/molbev/msv089 25862142

51. Pickrell JK, Pritchard JK. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 2012;8(11):e1002967. doi: 10.1371/journal.pgen.1002967 23166502

52. Solis-Lemus C, Ane C. Inferring Phylogenetic Networks with Maximum Pseudolikelihood under Incomplete Lineage Sorting. PLoS Genet. 2016;12(3):e1005896. doi: 10.1371/journal.pgen.1005896 26950302

53. Solis-Lemus C, Bastide P, Ane C. PhyloNetworks: A Package for Phylogenetic Networks. Mol Biol Evol. 2017;34(12):3292–8. doi: 10.1093/molbev/msx235 28961984

54. AmphibiaWeb. Information on amphibian biology and conservation. Berkeley, California: AmphibiaWeb Available: http://amphibiaweborg/. 2016.

55. Hijmans RJ, Cameron S. E., Parra J. L., Jones P. G. and Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005;25:1965–78.

56. Phillips SJ, Anderson RP, Schapire RE. Maximum entropy modeling of species geographic distributions. Ecological Modelling. 2006;190(3):231–59.

57. Novikova PY, Hohmann N, Nizhynska V, Tsuchimatsu T, Ali J, Muir G, et al. Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism. Nat Genet. 2016;48(9):1077–82. doi: 10.1038/ng.3617 27428747

58. Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, et al. A Draft Sequence of the Neandertal Genome. Science. 2010;328:710–22. doi: 10.1126/science.1188021 20448178

59. Nishihara H, Maruyama S, Okada N. Retroposon analysis and recent geological data suggest near-simultaneous divergence of the three superorders of mammals. Proc Natl Acad Sci U S A. 2009;106(13):5235–40. doi: 10.1073/pnas.0809297106 19286970

60. Hallstrom BM, Janke A. Mammalian evolution may not be strictly bifurcating. Mol Biol Evol. 2010;27(12):2804–16. doi: 10.1093/molbev/msq166 20591845

61. Garrigan D, Kingan SB, Geneva AJ, Andolfatto P, Clark AG, Thornton KR, et al. Genome sequencing reveals complex speciation in the Drosophila simulans clade. Genome Res. 2012;22(8):1499–511. doi: 10.1101/gr.130922.111 22534282

62. Martin SH, Dasmahapatra KK, Nadeau NJ, Salazar C, Walters JR, Simpson F, et al. Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Research. 2013;23:1817–28. doi: 10.1101/gr.159426.113 24045163

63. Jonsson H, Schubert M, Seguin-Orlando A, Ginolhac A, Petersen L, Fumagalli M, et al. Speciation with gene flow in equids despite extensive chromosomal plasticity. Proc Natl Acad Sci U S A. 2014;111(52):18655–60. doi: 10.1073/pnas.1412627111 25453089

64. Fontaine MC, Pease JB, Steele A, Waterhouse RM, Neafsey DE, Sharakhov IV, et al. Mosquito genomics. Extensive introgression in a malaria vector species complex revealed by phylogenomics. Science. 2015;347(6217):1258524. doi: 10.1126/science.1258524 25431491

65. Lamichhaney S, Berglund J, Almen MS, Maqbool K, Grabherr M, Martinez-Barrio A, et al. Evolution of Darwin's finches and their beaks revealed by genome sequencing. Nature. 2015;518(7539):371–5. doi: 10.1038/nature14181 25686609

66. Suh A, Smeds L, Ellegren H. The Dynamics of Incomplete Lineage Sorting across the Ancient Adaptive Radiation of Neoavian Birds. PLoS Biol. 2015;13(8):e1002224. doi: 10.1371/journal.pbio.1002224 26284513

67. Pease JB, Haak DC, Hahn MW, Moyle LC. Phylogenomics Reveals Three Sources of Adaptive Variation during a Rapid Radiation. PLoS Biol. 2016;14(2):e1002379. doi: 10.1371/journal.pbio.1002379 26871574

68. Becak ML, Becak W. Further studies on polyploid amphibians (Ceratophrydidae). 3. Meiotic aspects of the interspecific triploid hybrid: Odontophrynus cultripes (2n = 22) x O. americanus (4n = 44). Chromosoma. 1970;31(4):377–85. doi: 10.1007/BF00285829 5490304

69. Main AR. Comparisons of breeding biology and isolating mechanisms in Western Australian frogs. (ed.) G WL, editor. Melbourne, Victoria, Australia: Melbourne Univ. Press 1962. 370–9 p.

70. Nishioka M, Ueda H. Studies on polyploidy in Japanese frogs. Sci Rep Lab Amphibian Biol Hiroshima Univ. 1983;6:207–52.

71. Bogart JP, Bi K. Genetic and genomic interactions of animals with different ploidy levels. Cytogenet Genome Res. 2013;140(2–4):117–36. doi: 10.1159/000351593 23751376

72. Shimada M, Hase K. Female polyandry and size-assortative mating in isolated local populations of the Japanese common toad Bufo japonicus. Biological Journal of the Linnean Society. 2014;113(1):236–42.

73. Geach TJ, Stemple DL, Zimmerman LB. Genetic analysis of Xenopus tropicalis. Methods Mol Biol. 2012;917:69–110. doi: 10.1007/978-1-61779-992-1_5 22956083

74. Lafon-Placette C, Johannessen IM, Hornslien KS, Ali MF, Bjerkan KN, Bramsiepe J, et al. Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe. Proc Natl Acad Sci U S A. 2017;114(6):E1027–E35. doi: 10.1073/pnas.1615123114 28115687

75. Lafon-Placette C, Kohler C. Endosperm-based postzygotic hybridization barriers: developmental mechanisms and evolutionary drivers. Mol Ecol. 2016;25(11):2620–9. doi: 10.1111/mec.13552 26818717

76. Marburger S, Monnahan P, Seear PJ, Martin SH, Koch J, Paajanen P, et al. Interspecific introgression mediates adaptation to whole genome duplication. Nature Communications. 2019;10(1):5218. doi: 10.1038/s41467-019-13159-5 31740675

77. Schmickl R, Marburger S, Bray S, Yant L. Hybrids and horizontal transfer: introgression allows adaptive allele discovery. J Exp Bot. 2017;68(20):5453–70. doi: 10.1093/jxb/erx297 29096001

78. McCartney-Melstad E, Shaffer HB. Amphibian molecular ecology and how it has informed conservation. Mol Ecol. 2015;24(20):5084–109. doi: 10.1111/mec.13391 26437125

79. McCartney-Melstad E, Gidis M, Shaffer HB. Population genomic data reveal extreme geographic subdivision and novel conservation actions for the declining foothill yellow-legged frog. Heredity (Edinb). 2018;121(2):112–25. doi: 10.1038/s41437-018-0097-7 29941996

80. Callaghan CT, Rowley JJL, Cornwell WK, Poore AGB, Major RE. Improving big citizen science data: Moving beyond haphazard sampling. PLoS Biol. 2019;17(6):e3000357. doi: 10.1371/journal.pbio.3000357 31246950

81. Rowley JJL, Callaghan CT, Cutajar T, Portway C, Potter K, Mahony S, et al. FrogID: Citizen scientists provide validated biodiversity data on frogs of Australia. Herpetological Conservation and Biology. 2019;14(1):155–70.

82. Prum RO, Berv JS, Dornburg A, Field DJ, Townsend JP, Lemmon EM, et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature. 2015;526:569. doi: 10.1038/nature15697 26444237

83. Rokyta DR, Lemmon AR, Margres MJ, Aronow K. The venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus). BMC Genomics. 2012;13:312. doi: 10.1186/1471-2164-13-312 23025625

84. Hamilton CA, Lemmon AR, Lemmon EM, Bond JE. Expanding anchored hybrid enrichment to resolve both deep and shallow relationships within the spider tree of life. BMC Evol Biol. 2016;16(1):212. doi: 10.1186/s12862-016-0769-y 27733110

85. Pyron RA, Hsieh FW, Lemmon AR, Lemmon EM, Hendry CR. Integrating phylogenomic and morphological data to assess candidate species-delimitation models in brown and red-bellied snakes (Storeria). Zoological Journal of the Linnean Society. 2016;177(4):937–49.

86. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–80. doi: 10.1093/molbev/mst010 23329690

87. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28(12):1647–9. doi: 10.1093/bioinformatics/bts199 22543367

88. Weiss CL, Pais M, Cano LM, Kamoun S, Burbano HA. nQuire: a statistical framework for ploidy estimation using next generation sequencing. BMC Bioinformatics. 2018;19(1):122. doi: 10.1186/s12859-018-2128-z 29618319

89. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics (Oxford, England). 2009;25:1754–60.

90. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics (Oxford, England). 2009;25:2078–9.

91. Roberts JD. Geographic Variation in Calls of Males and Determination of Species Boundaries in Tetraploid Frogs of the Australian Genus Neobatrachus (Myobatrachidae). Australian Journal of Zoology 1997;45(2):95–112.

92. Mahony M. Cytogenetic studies on Australian frogs of the family Myobatrachidae. Ph.D. thesis, Macquarie University, Sydney, Australia. 1986.

93. Choleva L, Janko K. Rise and persistence of animal polyploidy: evolutionary constraints and potential. Cytogenet Genome Res. 2013;140(2–4):151–70. doi: 10.1159/000353464 23838539

94. Okamoto T, Ohnishi Y, Toda E. Development of polyspermic zygote and possible contribution of polyspermy to polyploid formation in angiosperms. J Plant Res. 2017;130(3):485–90. doi: 10.1007/s10265-017-0913-9 28275885

95. Hillis DM, Heath TA, St John K. Analysis and visualization of tree space. Syst Biol. 2005;54(3):471–82. doi: 10.1080/10635150590946961 16012112

96. Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics (Oxford, England). 2004;20:289–90.

97. Maechler M, Rousseeuw P, Struyf A, Hubert M. cluster: Cluster Analysis Basics and Extension. 2018.

98. Ogilvie HA, Bouckaert RR, Drummond AJ. StarBEAST2 Brings Faster Species Tree Inference and Accurate Estimates of Substitution Rates. Mol Biol Evol. 2017;34(8):2101–14. doi: 10.1093/molbev/msx126 28431121

99. Borowiec ML. AMAS: a fast tool for alignment manipulation and computing of summary statistics. PeerJ. 2016;4:e1660. doi: 10.7717/peerj.1660 26835189

100. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Syst Biol. 2018;67(5):901–4. doi: 10.1093/sysbio/syy032 29718447

101. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74. doi: 10.1093/molbev/msu300 25371430

102. Ramsey J, Schemske DW. Neopolyploidy in Flowering Plants. Annual Review of Ecology and Systematics. 2002;33(1):589–639.

103. Pfeifer B, Wittelsburger U, Ramos-Onsins SE, Lercher MJ. PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol Biol Evol. 2014;31(7):1929–36. doi: 10.1093/molbev/msu136 24739305

104. Hijmans RJ, van Etten J. raster: Geographic analysis and modeling with raster data. R package version 2.0–12. 2012.


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