Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2023-10-10
Page range: 265-275
Abstract views: 225
PDF downloaded: 21

Genetic and morphological concordance and discordance within the Cyrtodactylus brevipalmatus group (Squamata: Gekkonidae)

Herpetology Laboratory; Department of Biology; La Sierra University; 4500 Riverwalk Parkway; Riverside; California 92505; USA.; Department of Herpetology; San Diego Natural History Museum; PO Box 121390; San Diego; California; 92112; USA; Institute for Tropical Biology and Conservation; Universiti Malaysia Sabah; Jalan UMS; 88400; Kota Kinabalu; Sabah; Malaysia
School of Biological Sciences; Universiti Sains Malaysia; 11800 Minden; Penang; Malaysia; Center for Marine and Coastal Studies; Universiti Sains Malaysia; 11800 USM; Pulau Pinang; Malaysia.
Centre for Global Sustainability Studies (CGSS); Level 5; Hamzah Sendut Library; Universiti Sains Malaysia; 11800 USM; Penang
Institute for Environment and Development; (LESTARI); Universiti Kebangsaan Malaysia; 43600 Bangi; Selangor Darul Eshan; Malaysia
Institute for Tropical Biology and Conservation; Universiti Malaysia Sabah; Jalan UMS; 88400; Kota Kinabalu; Sabah; Malaysia.; Lee Kong Chian Natural History Museum; National University of Singapore; 2 Conservatory Drive; 117377; Singapore
Reptilia Crypsis Sample error Bent-toed gecko Thailand Malaysia

Abstract

We use data sets from the Cyrtodactylus brevipalmatus group with limited genetic and morphological sampling to demonstrate that not accounting for sampling error may adversely influence decisions regarding species delimitation and diagnosis. Lack of geographic sampling between the endpoints of a species’ range may recover notable interpopulational genetic differentiation consistent with species-level differentiation. Additionally, small population sample sizes may fail recover statistically different diagnostic morphological differences. Combined, these types of sampling error can produce results seemingly consistent with the recognition of cryptic species—genetically delimited populations lacking diagnostic morphological characters. This is the current situation within some lineages of the C. brevipalmatus group whereas in others, sampling error is less problematic and does not jeopardize their taxonomy. We note the potential negative effects for comparative biology as a whole if sampling error is not taken into consideration prior to constructing taxonomies.

 

References

  1. Bauer, A.M., Masroor, R., T-McQuillan, J., Heinicke. M.P., Daza, J.D. & Jackman, T.R. (2013) A preliminary phylogeny of the Palearctic naked-toed geckos (Reptilia: Squamata: Gekkonidae) with taxonomic implications. Zootaxa, 3599 (4), 301–324. https://doi.org/10.11646/zootaxa.3599.4.1
  2. Bauer, A.M., Heinike, M.P., Jackman, T.R. & Branch, W.R. (2011) Systematics of the Pachydactylus mariquensis group of geckos (Reptilia: Squamata: Gekkonidae): status of P. mariquensis latirostris, P. m. macrolepis and P. amoenus. Navorsinge van die Nasionale Museum Bloemfonten, 27, 85–108.
  3. Baxter, S.W., Papa, R., Chamberlain, N., Humphray, S., Joron, M., Morrison, C., Ffrench-Constant, R.H., McMillan, W.O. & Jiggins, C.D. (2008) Convergent evolution in the genetic basis of Müllerian mimicry in Heliconius butterflies. Genetics, 180, 1567–1577. https://doi.org/10.1534/genetics.107.082982
  4. Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2006) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution, 22, 148–155. https://doi.org/10.1016/j.tree.2006.11.004
  5. 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
  6. Chan, Y.F., Marks, M.E., Jones, F.C., Villareal Jr., G., Shapiro, M., Brady, S.D., Southwick, A.M., Absher, D.M., Grimwood, J., Schmutz, J., Myers, R.M., Petrov, D., Jónsson, B., Schluter, D., Bell, M.A. & Kingsley, D.M. (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science, 327, 302–305. https://doi.org/10.1126/science.1182213
  7. Chiba, S. (2004) Ecological and morphological patterns in communities of land snails of the genus Mandarina from the Bonin Islands. Journal of Evolutionary Biology, 17, 131–43. https://doi.org/10.1046/j.1420-9101.2004.00639.x
  8. Chomdej, S., Suwannapoom, C., Pradit, W., Phupanbai, A. & Grismer, L.L. (2023) A new species of the Cyrtodactylus brevipalmatus group (Squamata, Gekkonidae) from Tak Province, northwestern Thailand. ZooKeys, 1164, 63–88. https://doi.org/10.3897/zookeys.1164.101263
  9. Daza, J.D., Pinto, B.J, Thomas, R., Herrera-Martinez, A., Scantlebury, D.P., García, L.F.P, Balaraman, R.P., Perry, G. & Gamble T. (2019) The sprightly little sphaerodactyl: Systematics and biogeography of the Puerto Rican dwarf geckos Sphaerodactylus (Gekkota, Sphaerodactylidae) Zootaxa, 4712 (2), 151–201. https://doi.org/10.11646/zootaxa.4712.2.1
  10. Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A (2012) Bayesian phylogenetics with BEAUti and BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973. https://doi.org/10.1093/molbev/mss075
  11. Gillespie, R. (2004). Community assembly through adaptive radiation in Hawaiian spiders. Science, 303, 356–359. https://doi.org/10.1126/science.1091875
  12. Gorin, V.A., Solovyeva, E.N., Hasan, M., Okamiya, H., Karunarathna, D.M.S.S., Pawangkhanant, P., de Silva, A., Juthong, W., Milto, K.D., Nguyen, L.T., Suwannapoom, C., Haas, A., Bickford, D.P., Das, I. & Poyarkov, N.A. (2020) A little frog leaps a long way: compounded colonizations of the Indian Subcontinent discovered in the tiny Oriental frog genus Microhyla (Amphibia: Microhylidae). PeerJ, 8, e9411. https://doi.org/10.7717/peerj.9411
  13. Grismer, L.L. (2008) On the distribution and identification of Cyrtodactylus brevipalmatus Smith, 1923 and Cyrtodactylus elok Dring, 1979. The Raffles Bulletin of Zoology, 56 (1), 177–179.
  14. Grismer, L.L. (2021) Comparative ecomorphology of the sandstone night lizard (Xantusia gracilis) and the granite night lizard (Xantusia henshawi). Vertebrate Zoology, 7, 425–437. https://doi.org/10.3897/vz.71.e69214
  15. Grismer, L.L., Aowphol, A., Yodthong, S., Ampai, N., Termprayoon, K., Aksornneam, A. & Rujirawan, A (2022b) Integrative taxonomy delimits and diagnoses cryptic arboreal species of the Cyrtodactylus brevipalmatus group Squamata, Gekkonidae) with descriptions of four new species from Thailand. ZooKeys, 1129, 109–162. https://doi.org/10.3897/zookeys.1129.90535
  16. Grismer, L.L., Chan, K.O., Oaks, J.R., Neang, T., Sokun, L., Murdoch, M.L., Stuart, B.L. & Grismer, J.L. (2020b) A new insular species of the Cyrtodactylus intermedius (Squamata: Gekkonidae) group from Cambodia with a discussion of habitat preference and ecomorphology. Zootaxa, 4830 (1), 75–102. https://doi.org/10.11646/zootaxa.4830.1.3
  17. Grismer, L.L. & Grismer, J.L. (2017) A re-evaluation of the phylogenetic relationships of the Cyrtodactylus condorensis group (Squamata; Gekkonidae) and a suggested protocol for the characterization of rock-dwelling ecomorphology in Cyrtodactylus. Zootaxa, 4300 (4), 486–504. https://doi.org/10.11646/zootaxa.4300.4.2
  18. Grismer, L.L., Nazarov, R.A., Bobrov, V.V. & Poyarkov, N.A. (2020c) A new species of Sphenomorphus (Squamata: Scincidae) from Phu Quoc Island,Vietnam with a discussion of biogeography and character state evolution in the S. stellatus group. Zootaxa, 4801 (3), 461–487. https://doi.org/10.11646/zootaxa.4801.3.3
  19. Grismer, L.L., Poyarkov, N.A., Quah, E.S.H., Grismer, J.L. & Wood Jr., P.L. (2022d) The biogeography of bent-toed geckos, Cyrtodactylus (Squamata: Gekkonidae). PeerJ, 10, e13153. http://doi.org/10.7717/peerj.13153
  20. Grismer, L.L. & Quah, E.S.H. (2019) An annotated and updated checklist of the lzards of Peninsualr Malaysia, Singapore, and their adjacent archipelagos. Zootaxa, 4545 (2), 230–248. https://doi.org/10.11646/zootaxa.4545.2.4
  21. Grismer, L.L., Rujirawan, A., Yodthong, S., Stuart, B.L., Le, M.D., Le, D.T., Chuaynkern, Y., Wood Jr., P.L. & Aowphol, A. (2022a) The taxonomy and phylogeny of the Cyrtodactylus brevipalmatus group (Squamata: Gekkonidae) with emphasis on C. interdigitalis and C. ngati. Vertebrate Zoology, 72, 245–269. https://doi.org/10.3897/vz.72.e80615
  22. Grismer, L.L., Rujirawan, A., Chomdej, S., Suwannapoom, C., Yodthong, S., Aksornneam, A. & Aowphol, A. (2023) A new species of the Cyrtodactylus brevipalmatus group (Squamata; Gekkonidae) from the uplands of western Thailand ZooKeys, 1141, 93–118. https://doi.org/10.3897/zookeys.1141.97624
  23. Grismer, L.L., Wood Jr., P.L., Le, M.D., Quah, E.S.H. & Grismer, J.L. (2020a) Evolution of habitat preference in 243 species of Bent‐toed geckos (Genus Cyrtodactylus Gray, 1827) with a discussion of karst habitat conservation. Ecology and Evolution, 10, 13717–13730. https://doi.org/10.1002/ece3.6961
  24. Grismer, L.L., Wood Jr., P.L., Poyarkov, N.A., Le, M.D., Kraus, F., Agarwal, I., Oliver, P.M., Nguyen, S.N., Nguyen, T.Q., Karunarathna ,S., Welton, L.J., Stuart, B.L., Luu, V.Q., Bauer, A.M., O’Connell, K.A., Quah, E.S.H., Chan, K.O., Ziegler, T., Ngo, H., Nazarov, R.A., Aowphol, A., Chomdej, S., Suwannapoom, C., Siler, C.D., Anuar, S,. Tri, N.V. & Grismer, J.L. (2021a) Phylogenetic partitioning of the third-largest vertebrate genus in the world, Cyrtodactylus Gray, 1827 (Reptilia; Squamata; Gekkonidae) and its relevance to taxonomy and conservation. Vertebrate Zoology, 71, 101–154. https://doi.org/10.3897/vertebrate-zoology.71.e59307
  25. Grismer, L.L., Wood Jr., P.L., Poyarkov, N.A., Le, M.D., Karunarathna, S., Chomdej, S., Suwannapoom, C., Qi, S., Liu, S., Che, J., Quah, E.S.H., Kraus, F., Oliver, P.M., Riyanto, A., Pauwels, O.S.G. & Grismer, J.L. (2021b) Karstic landscapes are foci of species diversity in the World’s Third-Largest Vertebrate genus Cyrtodactylus Gray, 1827 (Reptilia: Squamata; Gekkonidae). Diversity, 13, 183. https://doi.org/10.3390/d13050183
  26. Grismer, L.L., Suwannapoom, C., Pawangkhanant, P., Nazarov, R.A., Yushchenko, P.V., Naiduangchan, M., Le, M.D., Luu, V.Q. & Poyarkov, N.A. (2021c) A new cryptic arboreal species of the Cyrtodactylus brevipalmatus group (Squamata: Gekkonidae) from the uplands of western Thailand. Vertebrate Zoology, 71, 723–746. https://doi.org/10.3897/vz.71.e76069
  27. Grismer, L.L., Wood Jr., P.P., Quah, E.S.H., Anuar, S., Ngadi, E.B., Izam, N.A.M. & Ahmad, N. (2018) Systematics, ecomorphology, cryptic speciation and biogeography of the lizard genus Tytthoscincus Linkem, Diesmos & Brown (Squamata: Scincidae) from the sky-island archipelago of Peninsular Malaysia. Zoological Journal of the Linnean Society, 183, 635–671. https://doi.org/10.1093/zoolinnean/zlx067
  28. Grismer, L.L., Wood Jr., P.P., Quah, E.S.H., Anuar, S., Ngadi, E.B. & Ahmad, N. (2015) A new insular species of Rock Gecko (Cnemaspis Boulenger) from Pulau Langkawi, Kedah, Peninsular Malaysia. Zootaxa, 3985 (1), 203–218. https://doi.org/10.11646/zootaxa.3985.2.2
  29. Grismer, L.L., Wood Jr., P.P., Anuar, S. Muin, M.A., Quah, E.S.H., Mcguire, M.A., Brown, R.A., Ngo, V.T. & Thai, P.H. (2013) Integrative taxonomy uncovers high levels of cryptic species diversity in Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) and the description of a new species from Peninsular Malaysia. Zoological Journal of the Linnean Society, 2013, 849–880. https://doi.org/10.1111/zoj.12064
  30. Grismer, L.L., Wood Jr., P.L., Quah, E.S.H., Shahrul, A., Muin, M.A., Sumontha, M., Ahmad, N., Bauer, A.M., Wangkulangkul, S., Grismer, J.L. & Pauwels, O.S.G. (2012) A phylogeny and taxonomy of the Thai-Malay Peninsula Bent-toed Geckos of the Cyrtodactylus pulchellus complex (Squamata: Gekkonidae): combined morphological and molecular analyses with descriptions of seven new species. Zootaxa, 3520 (1), 1–55. https://doi.org/10.11646/zootaxa.3520.1.1
  31. Gross, J.B., Borowsky, R. & Tabin, C.J. (2009) A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genetics, 5 (1), e1000326. https://doi.org/10.1371/journal.pgen.1000326
  32. Harvey, P.H. & Pagel, M.D. (1991) The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford, 344 pp.
  33. Heinicke, M.P., Adderly, L.M., Bauer, A.M. & Jackman, T.R. (2011a) A long-known new species of gecko allied to Pachydactylus bicolor (Squamata: Gekkonidae) from the central Namibian coast. African Journal of Herpetology, 60, 113–129. https://doi.org/10.1080/21564574.2011.613952
  34. Heinicke, M.P., Greenbaum, E., Jackman, T.R. & Bauer, AM. (2011b) Phylogeny of a trans-Wallacean radiation (Squamata, Gekkonidae, Gehyra) supports a single early colonization of Australia. Zoologica Scripta, 40, 584–602. https://doi.org/10.1111/j.1463-6409.2011.00495.x
  35. Husson, F., Josse, J., Le, S. & Mazet, J. (2017) FactoMine R: explortory data analysis and data mining. R package, version 1.36. [program]
  36. Jöger, K.M. & Schrödl, M. (2013) How to describe a cryptic species? Practical challenges of molecular taxonomy. Frontiers in Zoology, 10, 59–86. https://doi.org/10.1186/1742-9994-10-59
  37. Johnson, C.B., Quah, E.S.H., Shahrul, A., Muin, M.A., Wood Jr., P.L., Grismer, J.L., Greer, L.F., Chan, K.O., Ahad, N., Bauer, A.M. & Grismer, L.L. (2012) Phylogeography, geographic variation, and taxonomy of the Bent-toed Gecko Cyrtodactylus quadrivirgatus Taylor, 1962 from Peninsular Malaysia with the description of a new swamp dwelling species. Zootaxa, 3406 (1), 39–58. https://doi.org/10.11646/zootaxa.3406.1.3
  38. Kaatz, A., Grismer, J.L. & Grismer, L.L. (2021) Convergent evolution of karst habitat preference and its ecomorphological correlation in three species of Bent-toed Geckos (Cyrtodactylus) from Peninsular Malaysia. Vertebrate Zoology, 71, 367–386. https://doi.org/10.3897/vz.71.e66871
  39. Kassambara, A. & Mundt, F. (2017) Factoextra: extract and visualize the result of multivariate data analyses. R package, Version 1.0.5.999. [program]
  40. Landry, L., Vincent, W.F. & Bernatchez, L. (2007) Parallel evolution of lake whitefish dwarf ecotypes in association with limnological features of their adaptive landscape. European Society for Evolutionary Biology, 20, 971–984. https://doi.org/10.1111/j.1420-9101.2007.01304.x
  41. Le, D.T., Sitthivong, S., Tran, T.T., Grismer, L.L., Nguyen, T.Q., Le, M.D., Ziegler. T. & Luu. V.Q. (2021) First record of the Cyrtodactylus brevipalmatus group (Squamata: Gekkonidae) from Vietnam with description of a new species. Zootaxa, 4969 (3), 492–510. https://doi.org/10.11646/zootaxa.4969.3.3
  42. Losos, J.B. (2010) Adaptive radiation, ecological opportunity, and evolutionary determinism. American Naturalist, 175, 623–639. https://doi.org/10.1086/652433
  43. Mahler, D.L., Ingram, T., Revell, L.J. & Losos, L.B. (2013) Exceptional convergence on the macroevolutionary landscape in island lizard radiations. Science, 341, 292–295. https://doi.org/10.1126/science.1232392
  44. Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E. & Wagner, H. (2020) Package ‘vegan’. Version 2.5-7. Available from: https://cran.r-project.org/web/packages/vegan/ (accessed 21 August 2023)
  45. Pagès, J. (2015) Multiple Factor Analysis by Example Using R. CRC Press, New York, New York, 272 pp. https://doi.org/10.1201/b17700
  46. Pincheira-Donoso, D., Harvey, L.P. & Ruta, M. (2015) What defines an adaptive radiation? Macroevolutionary diversification dynamics of an exceptionally species-rich continental lizard radiation. BMC Evolutionary Biology, 15, 1–13. https://doi.org/10.1186/s12862-015-0435-9
  47. Pincheira-Donoso, D. & Meiri, S. (2013) An intercontinental analysis of climate-driven body size clines in reptiles: no support for patterns, no signals of processes. Evolutionary Biology, 40, 562–578. https://doi.org/10.1007/s11692-013-9232-9
  48. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. 2018. Available from: http://www.R-project.org (accessed 1 June 2022)
  49. Skalski, J.R., Richins, S.M. & Townsend, R. (2018) A statistical test and sample size recommendations for comparing community composition following PCA. PLoS ONE, 13 (10), e0206003. https://doi.org/10.1371/journal.pone.0206033
  50. Skinner, A., Lee, M.S.Y. & Hutchinson, MN. (2008). Rapid and repeated limb loss in a clade of scincid lizards. BMC Evolutionary Biolology, 8, 310. https://doi.org/10.1186/1471-2148-8-310
  51. Slatkin, M. (1993) Isolation by distance in equilibrium and non-equilib­rium populations. Evolution, 47, 264–279. https://doi.org/10.2307/2410134
  52. Toyama, K.S. (2017) Interaction between morphology and habitat use: a large-scale approach in tropidurine lizards. Breviora, 554, 1–20. https://doi.org/10.3099/0006-9698-554.1.1
  53. Williams, E.E. (1983) Ecomorphs, faunas, island size, and diverse end points in island radiations of Anolis. In: Huey, R.B., Pianka, E.R. & Schoener, T.W. (Eds.), Lizard Ecology: Studies of a Model Organism. Harvard University Press, Cambridge, Massachusetts, pp. 326–370. https://doi.org/10.4159/harvard.9780674183384.c18
  54. Yoder, J.B., Clancey, E., Des Roches, S., Eastman, J.M., Gentry, L., Godsoe, W., Hagey, T.J., Jochimsen, D., Oswald, B.P., Robertson, J., Sarver, B.A.J., Schenk, J.J., Spear, S.F. & Harmon, L.J. (2010) Ecological opportunity and the origin of adaptive radiations. Journal of Evolutionary Biology, 23, 1581–1596. https://doi.org/10.1111/j.1420-9101.2010.02029.x
  55. Yousefkhani, S.S.H., Nabizadeh, H. & Grismer, L.L. (2022) Ecomorphological differences among forest and rock dwelling species of Darevskia Arribas, 1999 (Squamata, Lacertide) in the Elburz Mountains, Iran. Herpetozoa, 35, 245–256. https://doi.org/10.3897/herpetozoa.35.e95257
  56. Zakaria, N., Senawi, J., Musa, F.H., Belabut, D., Chan, K.O., Nor, S.M. & Ahmad, N. (2014) Species composition of amphibians and reptiles in Krau Wildlife Reserve, Pahang, Peninsular Malaysia. Check List, 10 (2), 335–343. https://doi.org/10.15560/10.2.335