Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2024-04-15
Page range: 336-362
Abstract views: 66
PDF downloaded: 2

Morphological and genetic data challenge species and subspecies in the Lerista microtis group (Squamata: Scincidae)

School of Biological Sciences; Monash University; Clayton; Victoria; Australia
Museum of Zoology & Department of Ecology and Evolutionary Biology; University of Michigan; Ann Arbor MI USA
Collections & Research; Western Australian Museum; Welshpool; WA 6106; Australia
Museum of Zoology & Department of Ecology and Evolutionary Biology; University of Michigan; Ann Arbor MI USA
School of Biological Sciences; Monash University; Clayton; Victoria; Australia
Squamata Australia clinal variation colour pattern mitochondrial and nuclear DNA Reptilia south-coast five-toed slider subspecies taxonomy

Abstract

The subspecies rank has been widely applied by taxonomists to capture infraspecific variation within the Linnaean classification system. Many subspecies described throughout the 20th century were recognised largely based on perceived variation in single morphological characters yet have since been found not to correspond to separately evolving population lineages, thus requiring synonymy or elevation to full species under lineage-based views of species. These modern lineage-based taxonomic resolutions have resulted from a combination of new molecular genetic techniques, improved geographical sampling of specimens, and more sophisticated analyses of morphological variation (e.g., statistical assessments rather than solely univariate descriptive ones). Here, we revisit the current taxonomic arrangement of species-level and subspecific taxa in the Lerista microtis (Gray) group, which is distributed along a narrow ~2000 km strip on the southern coast of Australia. From specimens of the L. microtis group, an additional species (Lerista arenicola) and two additional subspecies (L. m. intermedia and L. m. schwaneri) were described. We collected data on mensural, meristic, and colour pattern characters to explore morpho-spatial relationships among these taxa. Although our morphological analyses revealed some distinctiveness among specimens from locations assigned to each taxon, this variation is continuous along Australia’s southern coastline, assuming the form of a geographic cline rather than discrete forms. For many characters, however, spatial patterns were inconsistent with the original descriptions, particularly of the subspecies. Moreover, analysis of genome wide restriction-associated DNA loci revealed multiple instances of paraphyly among taxa, with phylogenetic clustering of specimens assigned to distinct species and subspecies. These emerging patterns provide no support for L. arenicola as a species evolving separately from L. microtis. Additionally, our findings challenge the presumed distinctiveness and coherence of the three subspecies of L. microtis. We thus synonymise L. arenicola and the L. microtis subspecies with L. microtis and provide a redescription of a single yet morphologically variable species—an arrangement that best reflects evolutionary history and the continuous nature of morphological variation across space.

References

  1. Aplin, K.P. & Adams, M. (1998) New species of gekkonid and scincid lizards (Squamata) from the Carnarvon Basin region of Western Australia: morphological and genetic studies of ‘‘cryptic species.’’ Journal of the Royal Society of Western Australia, 81, 201–204.
  2. Battey, C.J., Ralph, P.L. & Kern, A.D. (2020) Space is the place: Effects of continuous spatial structure on analysis of population genetic data. Genetics, 215 (1), 193–214. https://doi.org/10.1534/genetics.120.303143
  3. Braby, M.F., Eastwood, R. & Murray, N. (2012) The subspecies concept in butterflies: Has its application in taxonomy and conservation biology outlived its usefulness? Biological Journal of the Linnean Society, 106, 699–716. https://doi.org/10.1111/j.1095-8312.2012.01909.x
  4. Brenneman, R.A., McLain, A.T., Taylor, J.M., Zaonarivelo, J.R., Lei, R., McGuire, S.M., Andriantompohavana, R., Rylands, A.B., Louis, E.E. Jr. (2016) Genetic analysis of the Indri reveals no evidence of distinct subspecies. International Journal of Primatology, 37, 460–477. https://doi.org/10.1007/s10764-016-9911-3
  5. 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 (7), e9069. https://doi.org/10.1002/ece3.9069
  6. 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
  7. Chang, C., Wu, P., Baker, R.E., Maini, P.K., Alibardi, L. & Chuong, C.-M. (2009) Reptile scale paradigm: evodevo, pattern formation and regeneration. The International Journal of Developmental Biology, 53, 813–826. https://doi.org/10.1387/ijdb.072556cc
  8. Chapple, D., Tingley, R., Mitchell, N., Macdonald, S., Keogh, J., Shea, G., Bowles, P., Cox, N. & Woinarski, J. (2019) Action Plan for Australian Lizards and Snakes 2017. CSIRO Publishing, Clayton South, Victoria, 680 pp. https://doi.org/10.1071/9781486309474
  9. Darwin, C. (1859) On the origin of species by means of natural selection. John Murray, London. Available from: https://darwin-online.org.uk/content/frameset?itemID=F373&viewtype=text&pageseq=1 (accessed 20 March 2024)
  10. de Queiroz, K. (1998) The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. In: Howard, D.J. & Berlocher, S.H. (Eds.), Endless Forms: Species and Speciation. Oxford University Press, Oxford, pp. 57–75.
  11. de Queiroz, K. (2020) An updated concept of subspecies resolves a dispute about the taxonomy of incompletely separated lineages. Herpetological Review, 51, 459–461.
  12. de Queiroz, K. (2021) Response to criticisms of an updated subspecies concept. Herpetological Review, 52 (4), 773–776.
  13. Eaton, D.A.R. & Overcast, I. (2020) ipyrad: Interactive assembly and analysis of RADseq datasets. Bioinformatics, 36, 2592–2594. https://doi.org/10.1093/bioinformatics/btz966
  14. Gray, J.E. (1845) Catalogue of the specimens of lizards in the collection of the British Museum. Trustees of the British Museum/Edward Newman, London, 83 pp.
  15. Greer, A.E. (1967) A new generic arrangement for some Australian scincid lizards. Breviora Museum of Comparative Zoology, 267, 1‒19.
  16. Haig, S.M., Beever, E.A., Chambers, S.M., Draheim, H.M., Dugger, B.D., Dunham, S., Elliott-Smith, E., Fontaine, J.B., Kesler, D.C., Knaus, B.J., Lopes, I.F., Loschl, P., Mullins, T.D. & Sheffield, L.M. (2006) Taxonomic considerations in listing subspecies under the U.S. Endangered Species Act. Conservation Biology, 20, 1584–1594. https://doi.org/10.1111/j.1523-1739.2006.00530.x
  17. Hillis, D.M. (2019) Species delimitation in herpetology. Journal of Herpetology, 53, 3–12. https://doi.org/10.1670/18-123
  18. Hillis, D.M. (2020) The detection and naming of geographic variation within species. Herpetological Review, 51, 52–56.
  19. Hillis, D.M. (2021) Conceptualizations of species and subspecies: A Reply to the ‘It’s Species All the Way Down View’. Herpetological Review, 52, 49–50.
  20. Hillis, D.M. & Wüster, W. (2021) Taxonomy and nomenclature of the Pantherophis obsoletus complex. Herpetological Review, 105, 795–809.
  21. Hillis, D.M. (2022) Distinguishing intraspecific geographic variation from distinct species boundaries. Sonoran Herpetologist, 35 (2), 52–57.
  22. Hutchinson, M., Adams, M. & Fricker, S. (2006) Genetic variation and taxonomy of the Ctenotus brooksi species-complex (Squamata: Scincidae). Transactions of the Royal Society of South Australia, 130, 48–65. https://doi.org/10.1080/3721426.2006.10887047
  23. Hutchinson, M.N. & Rawlinson, P.A. (1995) The water skinks (Lacertilia: Eulamprus) of Victoria and South Australia. Records of the South Australian Museum, 28, 185–207.
  24. Hutchinson, M.N., Doughty, P. & Oliver, P.M. (2009) Taxonomic revision of the stone geckos (Squamata: Diplodactylidae: Diplodactylus) of southern Australia, Zootaxa, 2167 91), 25–46. https://doi.org/10.11646/zootaxa.2167.1.2
  25. IUCN (2022) The Guidelines for Using the IUCN Red List Categories and Criteria. Version 15.1. July 2022. Available from: https://www.iucnredlist.org/resources/redlistguidelines (accessed 11 May 2023)
  26. Jackson, N.D., Carstens, B.C., Morales, A.E. & O’Meara, B.C. (2017) Species delimitation with gene flow. Systematic Biology, 66, 799–812.
  27. Jörger, K.M. & Schrödl, M. (2013) How to describe a cryptic species? Practical challenges of molecular taxonomy. Frontiers in Zoology, 10 (1), 1–27. https://doi.org/10.1186/1742-9994-10-59
  28. Kaiser, H.F. (1960) The application of electronic computers to factor analysis. Educational and Psychological Measurement, 20 (1), 141–151. https://doi.org/10.1177/001316446002000116
  29. Kassambara, A. & Mundt, F. (2020) Factoextra: Extract and visualize the results of multivariate data analyses. R Package Version 1.0.7. Available from: https://CRAN.R-project.org/package=factoextra (accesed 20 March 2024)
  30. Kealley, L., Doughty, P., Edwards, D. & Brennan, I.G. (2020) Taxonomic assessment of two pygopodoid gecko subspecies from Western Australia. Israel Journal of Ecology and Evolution, 66 (3–4), 126–141. https://doi.org/10.1163/22244662-20191078
  31. Keogh, J.S., Scott, I.A. & Hayes, C. (2005) Rapid and repeated origin of insular gigantism and dwarfism in Australian tiger snakes. Evolution, 59 (1), 226–233. https://doi.org/10.1111/j.0014-3820.2005.tb00909.x
  32. Kleiber, C. & Zeileis, A. (2022) AER: Applied Econometrics with R. R package Version 1.2–10. Available from: https://CRAN.R-project.org/package=AER (accessed 20 March 2024)
  33. Lê, S., Josse, J. & Husson, F. (2008) FactoMineR: an R package for multivariate analysis. Journal of Statistical Software, 25, 1–18. https://doi.org/10.18637/jss.v025.i01
  34. Lleonart, J., Salat, J. & Torres, G.J. (2000) Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology, 205 (1), 85–93. https://doi.org/10.1006/jtbi.2000.2043
  35. Maryan, B., Brennan, I.G., Hutchinson, M.N. & Geidans, L.S. (2020) What’s under the hood? Phylogeny and taxonomy of the snake genera Parasuta Worrell and Suta Worrell (Squamata: Elapidae), with a description of a new species from the Pilbara, Western Australia. Zootaxa, 4778 (1), 1–47. https://doi.org/10.11646/zootaxa.4778.1.1
  36. Martinez Arbizu, P. (2017) pairwiseAdonis: Pairwise multilevel comparison using adonis. R Package Version 0.4. Available from: https://github.com/pmartinezarbizu/pairwiseAdonis (accessed 20 March 2024)
  37. Mayr, E. (1963) Animal species and evolution. Harvard University Press, Cambridge, XVI + 797 pp. https://doi.org/10.4159/harvard.9780674865327
  38. Mayr, E. (1982) Of what use are subspecies? The Auk, 99, 593–595.
  39. McCoy, M.W., Bolker, B.M., Osenberg, C.W., Miner, B.G. & Vonesh, J.R. (2006) Size correction: Comparing morphological traits among populations and environments. Oecologia, 148, 547–554. https://doi.org/10.1007/s00442-006-0403-6
  40. Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop, 2010, 1–8. [https://ieeexplore.ieee.org/document/5676129] https://doi.org/10.1109/GCE.2010.5676129
  41. Nankivell, J.H., Maryan, B., Bush, B.G. & Hutchinson, M.N. (2023) Whip it into shape: Revision of the Demansia psammophis (Schlegel, 1837) complex (Squamata: Elapidae), with a description of a new species from central Australia. Zootaxa, 5311 (3), 301–339. https://doi.org/10.11646/zootaxa.5311.3.1
  42. Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Stevens, M.H.H., Oksanen, M.J. & Suggests, M.A.S.S. (2007) The vegan package. Community ecology package, 10(631–637), 719.
  43. Owen, D.F. (1963a) Screech owl polymorphism. Wilson Bulletin, 75, 183–189.
  44. Owen, D.F. (1963b) Variation in North American screech owls and the subspecies concept. Systematic Zoology, 12, 8–14. https://doi.org/10.2307/2411890
  45. Padial, J.M. & De la Riva, I. (2021) A paradigm shift in our view of species drives current trends in biological classification. Biological Reviews, 96, 731–751. https://doi.org/10.1111/brv.12676
  46. Patten, M.A. (2015) Subspecies and the philosophy of science. The Auk, 132, 481–485. https://doi.org/10.1642/AUK-15-1.1
  47. Patton, J.L. & Conroy, C.J. (2017) The conundrum of subspecies: morphological diversity among desert populations of the California vole (Microtus californicus, Cricetidae). Journal of Mammalogy, 98 (4), 1010–1026. https://doi.org/10.1093/jmammal/gyx074
  48. Pepper, M., Sumner, J., Brennan, I.G., Hodges, K., Lemmon, A.R., Lemmon, E.M., Peterson, G., Rabosky, D.L., Schwarzkopf, L., Scott, I.A., Shea, G. & Keogh, S. (2018) Speciation in the mountains and dispersal by rivers: Molecular phylogeny of Eulamprus water skinks and the biogeography of Eastern Australia. Journal of Biogeography, 45 (9), 2040–2052. https://doi.org/10.1111/jbi.13385
  49. Peterson, M. & Metcalfe, C. (2005) Herpetofaunal assemblages utilising abandoned stick-nest ant (Iridomyrmex conifer) nests as refugia. Herpetofauna, 35 (1), 7–10.
  50. Pulido‐Santacruz, P., Aleixo, A. & Weir, J.T. (2020) Genomic data reveal a protracted window of introgression during the diversification of a neotropical woodcreeper radiation. Evolution, 74 (5), 842–858. https://doi.org/10.1111/evo.13902
  51. Prates, I., Doughty, P. & Rabosky, D.L. (2023) Subspecies at crossroads: the evolutionary significance of genomic and phenotypic variation in a wide-ranging Australian lizard (Ctenotus pantherinus). Zoological Journal of the Linnean Society, 197 (3), 768–786. https://doi.org/10.1093/zoolinnean/zlac076
  52. R Core Team (2022) R: a language and environment for statistical computing. Version 4.1.2. R Foundation for Statistical Computing, Vienna. [program]
  53. Rabosky, D.L., Talaba, A.L., Donnellan, S.C. & Lovette, I.J. (2009) Molecular evidence for hybridization between two Australian desert skinks, Ctenotus leonhardii and Ctenotus quattuordecimlineatus (Scincidae: Squamata). Molecular Phylogenetics and Evolution, 53, 368–377. https://doi.org/10.1016/j.ympev.2009.06.020
  54. Rabosky, D.L., Hutchinson, M.N., Donnellan, S.C., Talaba, A.L. & Lovette, I.J. (2014) Phylogenetic disassembly of species boundaries in a widespread group of Australian skinks (Scincidae: Ctenotus). Molecular Phylogenetics and Evolution, 77, 71–82. https://doi.org/10.1016/j.ympev.2014.03.026
  55. Reist, J.D. (1985) An empirical evaluation of several univariate methods that adjust for size variation in morphometric data. Canadian Journal of Zoology, 63, 1429–1439. https://doi.org/10.1139/z85-213
  56. Remsen, J.V. (2010) Chapter 6: Subspecies as a meaningful taxonomic rank in avian classification. Ornithological Monographs, 67, 62–78. https://doi.org/10.1525/om.2010.67.1.62
  57. Singhal, S., Huang, H., Grundler, M.R., Marchaìn-Rivadeneira, M.R., Holmes, I., Title, P.O., Donnellan, S.C. & Rabosky, D.L. (2018) Does population structure predict the rate of speciation? A comparative test across Australia’s most diverse vertebrate radiation. The American Naturalist, 192, 432–447. https://doi.org/10.1086/699515
  58. Singhal, S., Huang, H., Title, P.O., Donnellan, S.C., Holmes, I. & Rabosky, D.L. (2017) Genetic diversity is largely unpredictable but scales with museum occurrences in a species-rich clade of Australian lizards. Proceedings of the Royal Society B: Biological Sciences, 284, 20162588. https://doi.org/10.1098/rspb.2016.2588
  59. Smith, H.M. & White, F.N. (1956) A case for the trinomen. Systematic Zoology, 5 (4), 183–190. https://doi.org/10.2307/2411920
  60. Smith, L.A. (1991) Obituary: Glen Milton Storr 1921–1990. Copeia, 1991 (2), 550–552.
  61. Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
  62. Storr, G.M. (1970) The genus Ctenotus (Lacertilia: Scincidae) in the Northern Territory. Journal of the Royal Society of Western Australia, 52 (4), 97–108.
  63. Storr, G.M. (1971) The genus Lerista (Lacertilia, Scincidae) in Western Australia. Journal of the Royal Society of Western Australia, 54 (3), 59–75.
  64. Storr, G.M. (1978) Taxonomic notes on the reptiles of the Shark Bay region, Western Australia. Records of the Western Australian Museum, 6 (3), 303‒318.
  65. Storr, G.M. (1981) Ten new Ctenotus (Lacertilia: Scincidae) from Australia. Records of the Western Australian Museum, 9 (2), 125–146
  66. Storr, G.M. (1991a) Revision of Lerista microtis (Lacertilia: Scincidae). Records of the Western Australian Museum, 15 (2), 469‒476.
  67. Storr, G.M. (1991b) Partial revision of the Lerista macropisthopus group (Lacertilia: Scincidae). Records of the Western Australian Museum, 15 (1) 149‒161.
  68. Storr, G.M. (1991c) A new subspecies of Lerista planiventralis (Lacertilia: Scincidae) from Western Australia. Records of the Western Australian Museum, 15 (2) 483‒485.
  69. Thorpe, R.S. (1983) A review of the numerical methods for recognising and analysing racial differentiation. In: Felsenstein, J. (Ed.), Numerical Taxonomy. NATO ASI Series. Vol. 1. Springer, Berlin/Heidelberg, pp. 404–423. https://doi.org/10.1007/978-3-642-69024-2_43
  70. Thorpe, R.S. (1975) Quantitative handling of characters useful in snake systematics with particular reference to intraspecific variation in the ringed snake Natrix natrix (L.). Biological Journal of the Linnean Society, 7 (1), 27–43. https://doi.org/10.1111/j.1095-8312.1975.tb00732.x
  71. Uetz, P. & Stylianou, A. (2018) The original descriptions of reptiles and their subspecies. Zootaxa, 4375 (2), 257–264. https://doi.org/10.11646/zootaxa.4375.2.5
  72. Uetz, P., Freed, P. & Hošek, J. (2022) The Reptile Database. Available from: http://www.reptile-database.org/db-info/SpeciesStat.html (accessed 8 May 2023)
  73. Wallis, E.J. (2006) Online Zoological Collections of Australian Museums (OZCAM): a national approach to making zoological data available on the web. Integrative Zoology, 1, 78–79. https://doi.org/10.1111/j.1749-4877.2006.00018.x
  74. Wang, X., He, Z., Shi, S. & Wu, C.-I. (2019) Genes and speciation: Is it time to abandon the biological species concept? National Science Review, 7, 1387–1397. https://doi.org/10.1093/nsr/nwz220
  75. Wilson, E.O. & Brown, W.L. (1953) The subspecies concept and its taxonomic application. Systematic Zoology, 2, 97–111. https://doi.org/10.2307/2411818
  76. Wilson, S. & Swan, G. (2021) A Complete Guide to Reptiles of Australia. 6th Edition. Reed New Holland, Wahroonga, New South Wales, 572 pp.
  77. Zink, R.M. (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proceeding of the Royal Society B, 271, 561–564. https://doi.org/10.1098/rspb.2003.2617