Plio–Pleistocene vicariance across arid Australia in the ‘Spiny Knob-tailed Geckos’ (Nephrurus asper group), with the description of a new species from western Queensland
Paul M. Oliver A * , Stephen C. Donnellan B and Bee F. Gunn CA Centre for Planetary Health and Food Security, Griffith University, 170 Kessels Road, Brisbane, Qld 4121, and Biodiversity and Geosciences Program, Queensland Museum, South Brisbane, Qld 4101, Australia.
B South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
C Royal Botanic Gardens Victoria, Birdwood Avenue, Melbourne, Vic. 3004, Australia.
Australian Journal of Zoology 69(6) 216-228 https://doi.org/10.1071/ZO22008
Submitted: 28 February 2022 Accepted: 1 July 2022 Published: 25 October 2022
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Across Australia’s monsoon tropics and vast arid zone isolated regions or ‘islands’ of upland or rocky habitat are home to disjunct populations of many taxa of plants and animals. Comparative analyses of lineages that occur across these habitat islands provide opportunities to understand when and how environmental change drove isolation and diversification across arid Australia. Here we present an analysis of mitochondrial genetic diversity across disjunct populations of geckos in the Nephrurus asper group. Dating analyses suggest that disjunct and genetically divergent populations spanning the northern half of Australia diverged through the Plio–Pleistocene. Based on the timing of divergence and current habitat associations we hypothesise that species in this lineage were isolated by the expansion of unsuitable arid-zone habitats from the late Pliocene onwards. Across most areas, these barriers appear to be sandy or stony deserts. However, in eastern Australia genetically divergent populations are separated by grassland on flat vertisol-dominated soils (‘blacksoils’), suggesting that these habitats also expanded during the late Pliocene aridification. Finally, we show that western Queensland populations formerly referred to N. asper are genetically divergent and diagnosable on the basis of colour pattern and, herein, recognise these populations as a distinct species. https://zoobank.org/urn:lsid:zoobank.org:pub:9508CAAA-D014-452D-A3DA-325851615FA7
Keywords: aridification, biogeography, blacksoil, Nephrurus eromanga sp. nov, refugia, sandy deserts, stony deserts, vicariance, gecko.
References
Andreone, F, Glaw, F, Nussbaum, RA, Raxworthy, CJ, Vences, M, and Randrianirina, JE (2003). The amphibians and reptiles of Nosy Be (NW Madagascar) and nearby islands: a case study of diversity and conservation of an insular fauna. Journal of Natural History 37, 2119–2149.| The amphibians and reptiles of Nosy Be (NW Madagascar) and nearby islands: a case study of diversity and conservation of an insular fauna.Crossref | GoogleScholarGoogle Scholar |
ASH (2016) Position of the Australian Society of Herpetologists on the increasing proliferation of names for taxa without adequate diagnosis or description and published without the benefits of peer review. (Australian Society of Herpetologists Inc., Position Statement, No. 2) Available at https://static1.squarespace.com/static/5448a9abe4b0ad6dc5e6fe6d/t/577e45a029687fd477a8375a/1467893157321/ASH_taxonomic_position_statement.pdf. [Accessed 5 February 2022]
Ashman, LG, Bragg, JG, Doughty, P, Hutchinson, MN, Bank, S, Matzke, NJ, Oliver, P, and Moritz, C (2018). Diversification across biomes in a continental lizard radiation. Evolution 72, 1553–1569.
| Diversification across biomes in a continental lizard radiation.Crossref | GoogleScholarGoogle Scholar |
Bouckaert, R, Heled, J, Kühnert, D, Vaughan, T, Wu, CH, Xie, D, Suchard, MA, Rambaut, A, and Drummond, AJ (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.
| BEAST 2: a software platform for Bayesian evolutionary analysis.Crossref | GoogleScholarGoogle Scholar |
Byrne, M, Yeates, DK, Joseph, L, Kearney, M, Bowler, J, Williams, MAJ, Cooper, S, Donnellan, SC, Keogh, JS, Leys, R, Melville, J, Murphy, DJ, Porch, N, and Wyrwoll, K-H (2008). Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Molecular Ecology 17, 4398–4417.
| Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota.Crossref | GoogleScholarGoogle Scholar |
Christidis, L, Rheindt, FE, Boles, WE, and Norman, JA (2010). Plumage patterns are good indicators of taxonomic diversity, but not of phylogenetic affinities, in Australian grasswrens Amytornis (Aves: Maluridae). Molecular Phylogenetics and Evolution 57, 868–877.
| Plumage patterns are good indicators of taxonomic diversity, but not of phylogenetic affinities, in Australian grasswrens Amytornis (Aves: Maluridae).Crossref | GoogleScholarGoogle Scholar |
Couper, PJ, and Gregson, RAM (1994). Redescription of Nephrurus asper Gunther, and description of N. amyae sp. nov. and N. sheai sp. nov. Memoirs of the Queensland Museum 37, 67–81.
Couper, P, and Hoskin, C (2008). Litho-refugia: the importance of rock landscapes for the long-term persistence of Australian rainforest fauna. Australian Zoologist 34, 554–560.
| Litho-refugia: the importance of rock landscapes for the long-term persistence of Australian rainforest fauna.Crossref | GoogleScholarGoogle Scholar |
Cracraft, J (1991). Patterns of diversification within continental biotas: hierarchical congruence among the areas of endemism of Australian vertebrates. Australian Systematic Botany 4, 211–227.
| Patterns of diversification within continental biotas: hierarchical congruence among the areas of endemism of Australian vertebrates.Crossref | GoogleScholarGoogle Scholar |
Edgar, RC (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1–15.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar |
Esquerré, D, Donnellan, SC, Pavón-Vázquez, CJ, Fenker, J, and Keogh, JS (2021). Phylogeography, historical demography and systematics of the world’s smallest pythons (Pythonidae, Antaresia). Molecular Phylogenetics and Evolution 161, 107181.
| Phylogeography, historical demography and systematics of the world’s smallest pythons (Pythonidae, Antaresia).Crossref | GoogleScholarGoogle Scholar |
Ford F (2022) Tropical and subtropical grasslands, savannas and shrublands: northeastern Australia. Available at https://www.worldwildlife.org/ecoregions/aa0707
Fujioka, T, Chappell, J, Honda, M, Yatsevich, I, Fifield, K, and Fabel, D (2005). Global cooling initiated stony deserts in central Australia 2–4 Ma, dated by cosmogenic 21Ne-10Be. Geology 33, 993–996.
| Global cooling initiated stony deserts in central Australia 2–4 Ma, dated by cosmogenic 21Ne-10Be.Crossref | GoogleScholarGoogle Scholar |
Fujita, MK, McGuire, JA, Donnellan, SC, and Moritz, C (2010). Diversification and persistence at the arid–monsoonal interface: Australia-wide biogeography of the Bynoe’s gecko (Heteronotia binoei; Gekkonidae). Evolution 64, 2293–2314.
| Diversification and persistence at the arid–monsoonal interface: Australia-wide biogeography of the Bynoe’s gecko (Heteronotia binoei; Gekkonidae).Crossref | GoogleScholarGoogle Scholar |
Huson, DH, and Bryant, D (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23, 254–267.
| Application of phylogenetic networks in evolutionary studies.Crossref | GoogleScholarGoogle Scholar |
Kaiser, H, Crother, BI, Kelly, CMR, Luiselli, L, O’Shea, M, Ota, H, Passos, P, Schleip, WD, and Wüster, W (2013). Best practices: In the 21st Century, taxonomic decisions in herpetology are acceptable only when supported by a body of evidence and published via peer-review. Herptological Review 44, 8–23.
Kealley, L, Doughty, P, Pepper, M, Keogh, JS, Hillyer, M, and Huey, J (2018). Conspicuously concealed: revision of the arid clade of the Gehyra variegata (Gekkonidae) group in Western Australia using an integrative molecular and morphological approach, with the description of five cryptic species. PeerJ 6, e5334.
| Conspicuously concealed: revision of the arid clade of the Gehyra variegata (Gekkonidae) group in Western Australia using an integrative molecular and morphological approach, with the description of five cryptic species.Crossref | GoogleScholarGoogle Scholar |
Kealley, L, Doughty, P, Edwards, D, and Brennan, IG (2020). Taxonomic assessment of two pygopodoid gecko subspecies from Western Australia. Israel Journal of Ecology and Evolution 66, 126–141.
| Taxonomic assessment of two pygopodoid gecko subspecies from Western Australia.Crossref | GoogleScholarGoogle Scholar |
Kumar, S, Stecher, G, Li, M, Knyaz, C, and Tamura, K (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.
| MEGA X: molecular evolutionary genetics analysis across computing platforms.Crossref | GoogleScholarGoogle Scholar |
Laver, RJ, Doughty, P, and Oliver, PM (2018). Origins and patterns of endemic diversity in two specialized lizard lineages from the Australian Monsoonal Tropics (Oedura spp.). Journal of Biogeography 45, 142–153.
| Origins and patterns of endemic diversity in two specialized lizard lineages from the Australian Monsoonal Tropics (Oedura spp.).Crossref | GoogleScholarGoogle Scholar |
McDonald, PJ, Jobson, P, Köhler, F, Nano, CEM, and Oliver, PM (2021). The living heart: climate gradients predict desert mountain endemism. Ecology and Evolution 11, 4366–4378.
| The living heart: climate gradients predict desert mountain endemism.Crossref | GoogleScholarGoogle Scholar |
Moritz, CC, Pratt, RC, Bank, S, Bourke, G, Bragg, JG, Doughty, P, Keogh, JS, Laver, RJ, Potter, S, Teasdale, LC, Tedeschi, LG, and Oliver, PM (2018). Cryptic lineage diversity, body size divergence, and sympatry in a species complex of Australian lizards (Gehyra). Evolution 72, 54–66.
| Cryptic lineage diversity, body size divergence, and sympatry in a species complex of Australian lizards (Gehyra).Crossref | GoogleScholarGoogle Scholar |
Nguyen, L-T, Schmidt, HA, von Haeseler, A, and Minh, BQ (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268–274.
| IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies.Crossref | GoogleScholarGoogle Scholar |
Noble, C, Laver, RJ, Rosauer, DF, Ferrier, S, and Moritz, C (2018). Phylogeographic evidence for evolutionary refugia in the Gulf sandstone ranges of northern Australia. Australian Journal of Zoology 65, 408–416.
| Phylogeographic evidence for evolutionary refugia in the Gulf sandstone ranges of northern Australia.Crossref | GoogleScholarGoogle Scholar |
Oliver, PM, and Bauer, AM (2011). Systematics and evolution of the Australian knob-tail geckos (Nephrurus, Carphodactylidae, Gekkota): plesiomorphic grades and biome shifts through the Miocene. Molecular Phylogenetics and Evolution 59, 664–674.
| Systematics and evolution of the Australian knob-tail geckos (Nephrurus, Carphodactylidae, Gekkota): plesiomorphic grades and biome shifts through the Miocene.Crossref | GoogleScholarGoogle Scholar |
Oliver, PM, and McDonald, PJ (2016). Young relicts and old relicts: a novel palaeoendemic vertebrate from the Australian Central Uplands. Royal Society Open Science 3, 160018.
| Young relicts and old relicts: a novel palaeoendemic vertebrate from the Australian Central Uplands.Crossref | GoogleScholarGoogle Scholar |
Oliver, PM, Laver, RJ, Smith, KL, and Bauer, AM (2014). Long-term persistence and vicariance within the Australian Monsoonal Tropics: the case of the giant cave and tree geckos (Pseudothecadactylus). Australian Journal of Zoology 61, 462–468.
| Long-term persistence and vicariance within the Australian Monsoonal Tropics: the case of the giant cave and tree geckos (Pseudothecadactylus).Crossref | GoogleScholarGoogle Scholar |
Oliver, PM, Laver, RJ, De Mello Martins, F, Pratt, RC, Hunjan, S, and Moritz, CC (2017). A novel hotspot of vertebrate endemism and an evolutionary refugium in tropical Australia. Diversity and Distributions 23, 53–66.
| A novel hotspot of vertebrate endemism and an evolutionary refugium in tropical Australia.Crossref | GoogleScholarGoogle Scholar |
Oliver, PM, Ashman, LG, Bank, S, Pratt, RC, Tedeschi, LG, Laver, RJ, Pratt, RC, Tedeschi, LG, and Moritz, CC (2019). On and off the rocks: persistence and ecological diversification in a tropical Australian lizard radiation. BMC Evolutionary Biology 19, 81.
| On and off the rocks: persistence and ecological diversification in a tropical Australian lizard radiation.Crossref | GoogleScholarGoogle Scholar |
Pepper, M, and Keogh, JS (2021). Life in the “dead heart” of Australia: the geohistory of the Australian deserts and its impact on genetic diversity of arid zone lizards. Journal of Biogeography 48, 716–746.
| Life in the “dead heart” of Australia: the geohistory of the Australian deserts and its impact on genetic diversity of arid zone lizards.Crossref | GoogleScholarGoogle Scholar |
Pepper, M, Ho, SYW, Fujita, MK, and Scott Keogh, J (2011). The genetic legacy of aridification: climate cycling fostered lizard diversification in Australian montane refugia and left low-lying deserts genetically depauperate. Molecular Phylogenetics and Evolution 61, 750–759.
| The genetic legacy of aridification: climate cycling fostered lizard diversification in Australian montane refugia and left low-lying deserts genetically depauperate.Crossref | GoogleScholarGoogle Scholar |
Pepper, M, Doughty, P, Fujita, MK, Moritz, C, and Keogh, JS (2013). Speciation on the rocks: integrated systematics of the Heteronotia spelea species complex (Gekkota; Reptilia) from western and central Australia. PLoS One 8, e78110.
| Speciation on the rocks: integrated systematics of the Heteronotia spelea species complex (Gekkota; Reptilia) from western and central Australia.Crossref | GoogleScholarGoogle Scholar |
Porter R (2008) ‘Keeping Australian Geckos.’ (ABK Publications: Burleigh BC, Qld, Australia)
Rabosky, DL, Hutchinson, MN, Donnellan, SC, Talaba, AL, and Lovette, IJ (2014). Phylogenetic disassembly of species boundaries in a widespread group of Australian skinks (Scincidae: Ctenotus). Molecular Phylogenetics and Evolution 77, 71–82.
| Phylogenetic disassembly of species boundaries in a widespread group of Australian skinks (Scincidae: Ctenotus).Crossref | GoogleScholarGoogle Scholar |
Rosauer, DF, Blom, MPK, Bourke, G, Catalano, S, Donnellan, S, Gillespie, G, Mulder, E, Oliver, PM, Potter, S, Pratt, RC, Rabosky, DL, Skipwith, PL, and Moritz, C (2016). Phylogeography, hotspots and conservation priorities: an example from the Top End of Australia. Biological Conservation 204, 83–93.
| Phylogeography, hotspots and conservation priorities: an example from the Top End of Australia.Crossref | GoogleScholarGoogle Scholar |
Shoo, LP, Rose, R, Doughty, P, Austin, JJ, and Melville, J (2008). Diversification patterns of pebble-mimic dragons are consistent with historical disruption of important habitat corridors in arid Australia. Molecular Phylogenetics and Evolution 48, 528–542.
| Diversification patterns of pebble-mimic dragons are consistent with historical disruption of important habitat corridors in arid Australia.Crossref | GoogleScholarGoogle Scholar |
Simó-Riudalbas, M, de Pous, P, Els, J, Jayasinghe, S, Péntek-Zakar, E, Wilms, T, Al-Saadi, S, and Carranza, S (2017). Cryptic diversity in Ptyodactylus (Reptilia: Gekkonidae) from the northern Hajar Mountains of Oman and the United Arab Emirates uncovered by an integrative taxonomic approach. PLoS One 12, e0180397.
| Cryptic diversity in Ptyodactylus (Reptilia: Gekkonidae) from the northern Hajar Mountains of Oman and the United Arab Emirates uncovered by an integrative taxonomic approach.Crossref | GoogleScholarGoogle Scholar |
Skipwith, PL, Bi, K, and Oliver, PM (2019). Relicts and radiations: phylogenomics of an Australasian lizard clade with east Gondwanan origins (Gekkota: Diplodactyloidea). Molecular Phylogenetics and Evolution 140, 106589.
| Relicts and radiations: phylogenomics of an Australasian lizard clade with east Gondwanan origins (Gekkota: Diplodactyloidea).Crossref | GoogleScholarGoogle Scholar |
Sniderman, JMK, Woodhead, JD, Hellstrom, J, Jordan, GJ, Drysdale, RN, Tyler, JJ, and Porch, N (2016). Pliocene reversal of late Neogene aridification. Proceedings of the National Academy of Sciences of the United States of America 113, 1999–2004.
| Pliocene reversal of late Neogene aridification.Crossref | GoogleScholarGoogle Scholar |
Wüster, W, Thomson, SA, O’Shea, M, and Kaiser, H (2021). Confronting taxonomic vandalism in biology: conscientious community self-organization can preserve nomenclatural stability. Biological Journal of the Linnean Society 133, 645–670.
| Confronting taxonomic vandalism in biology: conscientious community self-organization can preserve nomenclatural stability.Crossref | GoogleScholarGoogle Scholar |