Abstract
Litoria rothii is a widespread pelodryadid frog with a charismatic “laughing” advertisement call, distributed across the Australian Monsoon Tropics and southern New Guinea. Given its large distribution spanning well-known biogeographic barriers, variation in male advertisement calls and the prevalence of unresolved species complexes in the Australian frog fauna, we examine the genetic, morphological and acoustic diversity in the species from across its range. Our analyses reveal the presence of a previously unrecognised species in western parts of the range of L. rothii sensu lato, which we describe herein as a new species. Litoria ridibunda sp. nov. is distinguished from L. rothii on the basis of paraphyly of nuclear gene trees with L. everetti from Indonesia, colour patterns on the posterior thigh and male advertisement calls. Compared to L. rothii, the new species has a less contrasting pattern on the posterior thigh and a male advertisement call with a greater number of notes per call and a greater call duration. In particular, the magnitude of call differences between the species is highest where the ranges of the two species are in proximity in north-western Queensland. Our study further emphasises the undiagnosed diversity that remains in Australian frogs, even in relatively large, charismatic, frequently encountered species that often share human dwellings.
References
- Amey, A.P. & Couper, P.J. (2022) Herpetological type specimens held at the Queensland Museum: a catalogue. Memoirs of the Queensland Museum—Nature, 64, 19–259. https://doi.org/10.17082/j.2204-1478.64.2022.2020-12
- Anderson, E.C. & Thompson, E.A. (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics, 160, 1217–1229. https://doi.org/10.1093/genetics/160.3.1217
- Anstis, M.A. (2013) Frogs and tadpoles of Australia. New Holland Publishers, Sydney, 829 pp.
- Anstis, M., Price, L.C., Roberts, J.D., Catalano, S., Doughty, P., Hines, H.B. & Donnellan, S.C. (2016) Revision of the Australian water holding frog (Cyclorana platycephala, Anura: Hylidae), with a description of a new species and subspecies. Zootaxa, 4126, 451–479. https://doi.org/10.11646/zootaxa.4126.4.1
- Boulenger, G.A. (1885) Remarks on Mr. C. W. De Vis’s recent contributions to the herpetology of Australia. Annals and Magazine of Natural History, Series 5, 16, 386–388. https://doi.org/10.1080/00222938509459896
- Boulenger, G.A. (1897) A list of the reptiles and batrachians collected by Mr. Alfred Everett in Lombok, Flores, Sumba, and Savu, with descriptions of new species. Annals and Magazine of Natural History, Series 6, 19, 503–509. https://doi.org/10.1080/00222939708680570
- Bowman, D.M.J.S., Brown, G., Braby, M.F., Brown, J., Cook, L., Crisp, M.D., Ford, F., Haberle, S., Hughes, J.M., Isagi, Y., Joseph, L., McBride, J., Nelson, G. & Ladiges, P.Y. (2010) Biogeography of the Australian monsoon tropics. Journal of Biogeography, 37, 201–216. https://doi.org/10.1111/j.1365-2699.2009.02210.x
- Burbrink, F.T., Crother, B.I., Murray, C.M., Smith, B.T., Ruane, S., Myers, E.A. & Pyron, R.A.. (2022) Empirical and philosophical problems with the subspecies rank. Ecology and Evolution, 12, e9069. https://doi.org/10.1002/ece3.9069
- Bryant, L.M. & Krosch, M.N. (2016) Lines in the land: a review of evidence for eastern Australia’s major biogeographical barriers to closed forest taxa. Biological Journal of the Linnean Society, 119, 238–264. https://doi.org/10.1111/bij.12821
- Byrne, M., Steane, D.A., Joseph, L., Yeates, D.K., Jordan, G.J., Crayn, D., Aplin, K., Cantrill, D.J., Cook, L.G., Crisp, M.D., Keogh, J.S., Melville, J., Moritz, C., Porch, N., Sniderman, J.M.K., Sunnucks, P. & Weston, P.H. (2011) Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota. Journal of Biogeography, 38, 1635–1656. https://doi.org/10.1111/j.1365-2699.2011.02535.x
- Catullo, R.A. Lanfear, R., Doughty, P. & Keogh, J.S. (2014) The biogeographical boundaries of northern Australia: evidence from ecological niche models and a multi-locus phylogeny of Uperoleia toadlets (Anura: Myobatrachidae). Journal of Biogeography, 41, 659–672. https://doi.org/10.1111/jbi.12230
- Chan, K.O. & Grismer, L.L. (2022) GroupStruct: an R Package for allometric size correction. Zootaxa, 5124 (4), 471–482. https://doi.org/10.11646/zootaxa.5124.4.4
- Chifman, J. & Kubatko, L. (2014) Quartet inference from SNP data under the coalescent model. Bioinformatics, 30, 3317–3324. https://doi.org/10.1093/bioinformatics/btu530
- Cogger, H.G., Cameron, E.E. & Cogger, H.M. (1983) Zoological Catalogue of Australia. Vol. 1. Amphibia and Reptilia. Australian Government Publishing Service, Canberra, vi + 313 pp.
- Condit, J.M. (1964) A list of the types of hylid frogs in the collection of the British Museum (Natural History). Journal of the Ohio Herpetological Society, 4, 85–98. https://doi.org/10.2307/1562641
- Cutajar, T.P., Portway, C., Gillard, G.L. & Rowley, J.J.L. (2022) Australian frog atlas: Species’ distribution maps informed by the FrogID dataset. Technical Reports of the Australian Museum Online. Sydney, 36, 1–48. https://doi.org/10.3853/j.1835-4211.36.2022.1789
- de Queiroz, K. (1998) The general lineage concept of species, species criteria and the process of speciation. In: Howard, D.J. & Berlocher, S.H. (Eds.), Endless Forms, Species and Speciation. Oxford University Press, Oxford, pp. 57–75.
- de Queiroz, K. (2011) Branches in the lines of descent: Charles Darwin and the evolution of the species concept. Biological Journal of the Linnean Society, 103, 19–35. https://doi.org/10.1111/j.1095-8312.2011.01634.x
- de Queiroz, K. (2020) An updated concept of subspecies resolves a dispute about the taxonomy of incompletely separated lineages. Herpetological Review, 51, 459–461
- De Vis, C.W. (1884) On some new batrachians from Queensland. Proceedings of the Linnean Society of New South Wales, 9, 65–67. https://doi.org/10.5962/bhl.part.29923
- Donnellan, S.C., Tyler, M.J., Monis, P., Barclay, A. & Medlin, A. (2000) Do skin peptide profiles reflect speciation in the Australian treefrog Litoria caerulea (Anura: Hylidae)? Australian Journal of Zoology, 48, 33–46. https://doi.org/10.1071/ZO99068
- Donnellan, S.C., Catalano, S., Pederson, S., Mitchell, K., Suhendran, A., Price, L.C., Doughty, P. & Richards, S.J. (2021) Revision of the Litoria watjulumensis (Anura: Pelodryadidae) group from the Australian monsoonal tropics, including the resurrection of L. spaldingi. Zootaxa, 4933 (2), 211–240. https://doi.org/10.11646/zootaxa.4933.2.3
- Duellman, W.E. (1970) The hylid frogs of Middle America. 2 Vols. Monograph. Museum of Natural History, University of Kansas, Lawrence, 753 pp. https://doi.org/10.5962/bhl.title.2835
- Earl, D.A. & vonHoldt, B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7
- Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. https://doi.org/10.1093/nar/gkh340
- Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
- Forcart, L. (1953) Die Amphibien und Reptilien von Sumba ihre zoogeographischen Beziehungen und Revision der Unterarten von Typhlops polygrammicus. Verhandlungen der Naturforschenden Gesellschaft in Basel, 64, 356–388.
- Gaikhorst, G. & Foster, J. (2022) Green Tree Frogs (Litoria caerulea) on the hop: observations on established populations in the Pilbara. Western Australian Naturalist, 32, 197–210.
- Georges, A., Gruber, B., Pauly, G.B., White, D., Adams, M., Young, M.J., Kilian, A., Zhang, X., Shaffer, H.B. & Unmack, P.J. (2018) Genome wide SNP markers breathe new life into phylogeography and species delimitation for the problematic short‐necked turtles (Chelidae: Emydura) of eastern Australia. Molecular Ecology, 27, 5195–5213. https://doi.org/10.1111/mec.14925
- Gruber, B., Unmack, P.J., Berry, O.F. & Georges, A. (2018) dartr: An R package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Molecular Ecology Resources, 18, 691–699. https://doi.org/10.1111/1755-0998.12745
- Häupl, M. & Tiedemann, F. (1978) Vertebrata 1. Typenkatalog der Herpetologischen Sammlung. Kataloge der Wissenschaftlichen Sammlungen des Naturhistorischen Museums in Wien, 2, 7–34.
- Häupl, M., Tiedemann, F. & Grillitsch, H. (1994) 3—Vertebrata, I—Amphibia. Katalog der Typen der Herpetologischen Sammlung nach dem Stand vom 1. Jänner 1994. Kataloge der Wissenschaftlichen Sammlungen des Naturhistorischen Museums in Wien, 9, 1–42.
- Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology Evolution, 35, 518–522. https://doi.org/10.1093/molbev/msx281
- Hoskin, C., Grigg, G., Stewart, D. & McDonald, S. (2015) Frogs of Australia—a complete electronic field guide to Australian frogs. Ug Media, Birmingham. [electronic book]
- Jombart, T. (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403–1405. https://doi.org/10.1093/bioinformatics/btn129
- Kaiser, H., O’Shea, M. & Kaiser, C.M. (2014) Amphibians of Timor-Leste: A Small Fauna under Pressure Chapter 21. In: Heatwole, H. & Das, I. (Eds.), Conservation Biology of Amphibians of Asia: Status of Conservation and decline of Amphibians: Eastern Hemisphere. Natural History Publications, Borneo, pp. 361–370.
- Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
- Kassambara, A. & Mundt, F. (2017) factoextra: Extract and visualize the results of multivariate data analyses. Retrieved from: https://cran.r-project.org/package=factoextra (accessed 3 September 2023)
- Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S. & Duran, C. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
- Kilian, A., Wenzl, P., Huttner, E., Carling, J., Xia, L., Blois, H., Caig, V., Heller-Uszynska, K., Jaccoud, D., Hopper, C., Aschenbrenner-Kilian, M., Evers, M., Peng, K., Cayla, C., Hok, P. & Uszynski, G. (2012) Diversity arrays technology: A generic genome profiling technology on open platforms. In: Data Production and Analysis in Population Genomics. Methods in Molecular Biology, 888, pp. 67–89. https://doi.org/10.1007/978-1-61779-870-2_5
- Köhler, J., Jansen, M., Rodriguez, A., Kok, P.J., Toledo, L.F., Emmrich, M., Glaw, F., Haddad, C.F., Roedel, M.O. & Vences, M. (2017) The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa, 4251 (1), 1–124. https://doi.org/10.11646/zootaxa.4251.1.1
- Kopelman, N.M., Mayzel, J., Jakobsson, M., Rosenberg, N.A. & Mayrose, I. (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources, 15, 1179–1191. https://doi.org/10.1111/1755-0998.12387
- Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, 772–773. https://doi.org/10.1093/molbev/msw260
- Leaché, A.D., Banbury, B.L., Felsenstein, J., de Oca, A.N. & Stamatakis, A. (2015) Short tree, long tree, right tree, wrong tree: new acquisition bias corrections for inferring SNP phylogenies. Systematic Biology, 64, 1032–1047. https://doi.org/10.1093/sysbio/syv053
- Lleonart, J., Salat, J. & Torres, G.J. (2000) Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology, 205, 85–93. https://doi.org/10.1006/jtbi.2000.2043
- Luedeling, E. (2019) chillR: statistical methods for phenology analysis in temperate fruit trees. R package version 0.70.21
- Mahony, M.J., Moses, B., Mahony, S., Lemckert, F. & Donnellan, S.C. (2020) A new species of frog in the Litoria ewingii species group (Anura: Pelodryadidae) from south-eastern Australia. Zootaxa, 4858 (2), 201–230. https://doi.org/10.11646/zootaxa.4858.2.3
- Martin, A.A., Watson, G.F., Gartside, D.F., Littlejohn, M.J. & Loftus-Hills, J.J. (1979) A new species of the Litoria peronii complex (Anura: Hylidae) from eastern Australia. Proceedings of the Linnean Society of New South Wales, 103, 23–35.
- Melville, J., Ritchie, E.G. Chapple, S.N.J., Glor, R.E. & Schulte, J.A. (2011) Evolutionary origins and diversification of dragon lizards in Australia’s tropical savannas. Molecular Phylogenetics and Evolution, 58, 257–270. https://doi.org/10.1016/j.ympev.2010.11.025
- Menzies, J.I. (2006) The Frogs of New Guinea and the Solomon Islands. Moscow: Pensoft.
- Mitchell, B.A., Callaghan, C.T. & Rowley, J.J.L. (2020) Continental-scale citizen science data reveal no changes in acoustic responses of a widespread treefrog to an urbanisation gradient. Journal of Urban Ecology, 2020, 1–12. https://doi.org/10.1093/jue/juaa002
- Moritz, C.C., Pratt, R.C., Bank, S., Bourke, G., Bragg, J.G. Doughty, P., Keogh, S.J., Laver, R.J., Potter, S., Teasdale, L.C., Tedeschi, L.G. & Oliver, P.M. (2018) Cryptic lineage diversity, body size divergence, and sympatry in a species complex of Australian lizards (Gehyra). Evolution, 72, 54–66. https://doi.org/10.1111/evo.13380
- Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300
- Nyári, A.S. & Joseph, L. (2013) Comparative phylogeography of Australo-Papuan mangrove-restricted and mangrove-associated avifaunas. Biological Journal of the Linnean Society, 109, 574–598. https://doi.org/10.1111/bij.12082
- Oliver, P.M., Rittmeyer, E.N., Torkkola, J., Donnellan, S.C., Dahl, C. & Richards, S.J. (2021) Multiple trans-Torres Strait colonisations by tree frogs in the Litoria caerulea group, with the description of a new species from New Guinea. Australian Journal of Zoology, 68, 25–39. https://doi.org/10.1071/ZO20071
- Pepper, M., Hamilton, D.G., Merkling, T., Svedin, N., Cser, B., Catullo, R.A., Pryke, S.R. & Keogh, J.S. (2017) Phylogeographic structure across one of the largest intact tropical savannahs: Molecular and morphological analysis of Australia’s iconic frilled lizard Chlamydosaurus kingii. Molecular Phylogenetics and Evolution, 106, 217–227. https://doi.org/10.1016/j.ympev.2016.09.002
- Potter, S., Eldridge, M.D.B., Taggart, D.A. & Cooper, S.J.B. (2012) Multiple biogeographic barriers identified across the monsoon tropics of northern Australia: phylogeo-graphic analysis of the brachyotis group of rock-wallabies. Molecular Ecology, 21, 2254–2269. https://doi.org/10.1111/j.1365-294X.2012.05523.x
- Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959. https://doi.org/10.1093/genetics/155.2.945
- Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901–904. https://doi.org/10.1093/sysbio/syy032
- Renner, S.S. (2016) Return to Linnaeus’s focus on diagnosis, not description: the use of DNA characters in the formal naming of species. Systematic Biology, 65, 1085–1095. https://doi.org/10.1093/sysbio/syw032
- Richards, S.J. & Donnellan, S.C. (2023) Two new species of green treefrogs (Pelodryadidae: Litoria) from the northern slopes of Papua New Guinea’s central cordillera. Zootaxa, 5271 (3), 477–502. https://doi.org/10.11646/zootaxa.5271.3.3
- Richards, S.J., Donnellan, S.C. & Oliver, P.M. (2023) Five new species of the pelodryadid genus Litoria Tschudi from the southern versant of Papua New Guinea’s Central Cordillera, with observations on the diversification of reproductive strategies in Melanesian treefrogs. Zootaxa, 5263 (2), 151–190. https://doi.org/10.11646/zootaxa.5263.2.1
- Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MRBAYES 3.2: efficient Bayesian phylogenetic inference and model selection across a large model space. Systematic Biology, 61, 539–542. https://doi.org/10.1093/sysbio/sys029
- Rosauer, D., Laffan, S.W., Crisp, M.D., Donnellan, S.C. & Cook, L.G. (2009) Phylogenetic endemism: a new approach for identifying geographical concentrations of evolutionary history. Molecular Ecology, 18, 4061–72. https://doi.org/10.1111/j.1365-294X.2009.04311.x
- Rowley, J.J.L., Callaghan, C.T., Cutajar, T., Portway, C., Potter, K., Mahony, S., Trembath, D.F., Flemons, P. & Woods, A. (2019) FrogID: Citizen scientists provide validated biodiversity data on frogs of Australia. Herpetological Conservation and Biology, 14, 155–170.
- Rowley, J., Mahony, M.J., Hines, H.B., Myers, S., Aplin, K.P., Price, L. & Donnellan, S.C. (2021) Two new species from the Litoria rubella species group from eastern Australia. Zootaxa, 5071 (1), 1–41. https://doi.org/10.11646/zootaxa.5071.1.1
- Simpson, G.G. (1951) The species concept. Evolution, 5, 285–298. https://doi.org/10.2307/2405675
- Smith, M.A. (1927) Contributions to the herpetology of the Indo-Australian region. Proceedings of the Zoological Society of London, 1927, 199–225. https://doi.org/10.1111/j.1096-3642.1927.tb02255.x
- Sparks, A.H., Padgham, M., Parsonage, H. & Pembleton, K. (2017) bomrang: Fetch Australian Government Bureau of Meteorology Weather Data. The Journal of Open Source Software, 2, 411. https://doi.org/10.21105/joss.00411
- Sparks, A.H., Carroll, J., Goldie, J., Marchiori, D., Melloy, P., Padgham, M., Parsonage, H. & Pembleton, K. (2020) bomrang: Australian Government Bureau of Meteorology (BOM) Data Client. R package version 0.7.1. Available from: https://CRAN.R-project.org/package=bomrang (accessed 4 September 2023)
- Swofford, D.L. (2003) PAUP*: phylogenetic analysis using parsimony. Version 4.0 b10. Sinauer Associates, Sunderland. [program]
- Tamura, K., Stecher, G. & Kumar, S. (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38, 3022–3027. https://doi.org/10.1093/molbev/msab120
- Thorpe, R.S. (1976) Biometric analysis of geographic variation and racial affinities. Biological Reviews, 51, 407–452. https://doi.org/10.1111/j.1469-185x.1976.tb01063.x
- Toon, A., Hughes, J.M. & Joseph, L. (2010) Multilocus analysis of honeyeaters (Aves: Meliphagidae) highlights spatio-temporal heterogeneity in the influence of biogeographic barriers in the Australian monsoonal zone. Molecular Ecology, 19, 2980–2994. https://doi.org/10.1111/j.1365-294X.2010.04730.x
- Trifinopoulos, J., Nguyen, L.T., von Haeseler A. & Minh, B.Q. (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44 (W1), W232–W235. https://doi.org/10.1093/nar/gkw256
- Tyler, M.J. (1968) Papuan frogs of the genus Hyla. Zoologische Verhandelingen Leiden, 96, 1–203.
- Tyler, M.J. & Davies, M.M. (1978) Species-groups within the Australopapuan hylid frog genus Litoria Tschudi. Australian Journal of Zoology, Supplemental Series 27, 1–47. https://doi.org/10.1071/AJZS063
- Tyler, M.J., Crook, G.A. & Davies, M. (1983) Reproductive biology of the frogs of the Magela Creek System, Northern Territory. Records of the South Australian Museum, 18, 415–440.
- Tyler, M.J., Smith, L.A. & Johnstone, R.E. (1984) Frogs of Western Australia. Western Australia Museum, Perth, 108 pp.
- Venables, W.N. & Ripley, B.D. (2002) Modern applied statistics with S. 4th Edition. Springer, New York, New York. Available from: http://www.stats.ox.ac.uk/pub/MASS4 (accessed 4 Septembere 2023)
- Vörös, J., Wassens, S., Price, L., Hunter, D., Myers, S., Armstrong, K., Mahony, M. & Donnellan, S.C. (2023) Molecular systematic analyses demonstrate that the threatened southern bell frog, Litoria raniformis (Anura: Pelodryadidae), comprises two sub-species. Zootaxa, 5228 (1), 1–43. https://doi.org/10.11646/zootaxa.5228.1.1