Skip to main content
SpringerLink
Log in

Processes driving male breeding colour and ecomorphological diversification in rainbow skinks: a phylogenetic comparative test

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

We used a phylogenetic comparative approach to investigate the importance of ecological shifts in the diversification of both signalling traits and ecomorphological traits in a diverse group of Australian skinks (Carlia). First, we tested whether divergence in male breeding coloration is associated with shifts in habitat openness. Second, we examined whether the type or location of male breeding coloration changes predictably with habitat openness. Third, we tested the ecomorphological predictions that body size should vary in relation to habitat openness and that limb length, toe length and head depth should vary with substrate use. Divergence in male breeding coloration was positively associated with shifts in habitat openness. Our results also indicate that species occupying more open habitats tend to use male sexual signals located on lateral body regions and not necessarily on body regions that are potentially more concealed from aerial predators (e.g. chest and throat). With regard to ecomorphological traits, habitat openness appears to have no predictable influence on body size at the inter-specific level, contrary to expectations based on intra-specific studies. However, consistent with functional predictions, we found that preference for rocky habitats is associated with relatively longer hind limb length, presumably due to selection for greater speed and jumping ability on these substrates. Overall, results of this study support the hypothesis that ecological shifts play a central role in promoting morphological diversification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arnold EN (1998) Cranial kinesis in lizards—variations, uses, and origins. Evol Biol 30:323–357

    Google Scholar 

  • Blomberg S, Owens IPF, Stuart-Fox D (2001) UV reflectance in the small skink, Carlia pectoralis. Herpetol Rev 32:16–17

    Google Scholar 

  • Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948. doi:10.1038/35082064

    Article  CAS  PubMed  Google Scholar 

  • Boughman JW (2002) How sensory drive can promote speciation. Trends Ecol Evol 17:571–577. doi:10.1016/S0169-5347(02)02595-8

    Article  Google Scholar 

  • Brown RP, Thorpe RS (1991) Within-Island microgeographic variation in body dimensions and scalation of the skink Chalcides sexlineatus, with testing of causal hypotheses. Biol J Linn Soc Lond 44:47–64. doi:10.1111/j.1095-8312.1991.tb00606.x

    Article  Google Scholar 

  • Butler MA, King AA (2004) Phylogenetic comparative analysis: a modeling approach for adaptive evolution. Am Nat 164:683–695. doi:10.1086/426002

    Article  Google Scholar 

  • Charlesworth B (1994) The genetics of adaptation—lessons from mimicry. Am Nat 144:839–847. doi:10.1086/285710

    Article  Google Scholar 

  • Cogger HG (1996) Reptiles and amphibians of Australia. Reed Books Australia, Port Melbourne

    Google Scholar 

  • Cogger HG (2000) Reptiles and amphibians of Australia. Reed New Holland, Sydney

    Google Scholar 

  • Dolman G (2008) Evidence for differential assortative female preference in association with refugial isolation of rainbow skinks in Australia’s tropical rainforests. PLosOne 3:e3499. doi:10.1371/journal.pone.0003499

  • Dolman G, Hugall AF (2008) Combined mitochondrial and nuclear data enhance resolution of a rapid radiation or Australian rainbow skinks (Scincidae: Carlia). Mol Phylogenet Evol 49:782–794. doi:10.1016/j.ympev.2008.09.021

  • Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, Princeton

    Google Scholar 

  • Endler JA (1980) Natural selection on colour patterns in Poecilia reticulata. Evol Int J Org Evol 34:76–91. doi:10.2307/2408316

    Google Scholar 

  • Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153. doi:10.1086/285308

    Article  Google Scholar 

  • Endler JA (1993) Some general comments on the evolution and design of animal communication systems. Philos Trans R Soc Lond B Biol Sci 340:215–225. doi:10.1098/rstb.1993.0060

    Article  CAS  PubMed  Google Scholar 

  • Endler JA, Basolo AL (1998) Sensory ecology, receiver biases and sexual selection. Trends Ecol Evol 13:415–420. doi:10.1016/S0169-5347(98)01471-2

    Article  Google Scholar 

  • Fuller RC, Houle D, Travis J (2005) Sensory bias as an explanation for the evolution of mate preferences. Am Nat 166:437–446. doi:10.1086/444443

    Article  PubMed  Google Scholar 

  • Garland TJ, Losos JB (1994) Ecological morphology of locomotor performance in Squamate reptiles. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, pp 240–302

    Google Scholar 

  • Gifford ME, Herrel A, Mahler DL (2008) The evolution of locomotor morphology, performance, and anti-predator behaviour among populations of Leiocephalus lizards from the Dominican Republic. Biol J Linn Soc Lond 93:445–456. doi:10.1111/j.1095-8312.2007.00909.x

    Article  Google Scholar 

  • Goodman BA, Isaac JL (2008) Convergent body flattening in a clade of tropical rock-using lizards (Scincidae: Lygosominae). Biol J Linn Soc Lond 94:399–411. doi:10.1111/j.1095-8312.2008.00988.x

    Article  Google Scholar 

  • Greer AE (1989) The biology and evolution of Australian skinks. Surrey Beatty, Sydney

    Google Scholar 

  • Hansen TF (1997) Stabilizing selection and the comparative analysis of adaptation. Evol Int J Org Evol 51:1341–1351. doi:10.2307/2411186

    Google Scholar 

  • Hansen TF, Orzack SH (2005) Assessing current adaptation and phylogenetic inertia as explanations of trait evolution: the need for controlled comparisons. Evol Int J Org Evol 59:2063–2072

    Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. doi:10.1093/bioinformatics/17.8.754

    Article  CAS  PubMed  Google Scholar 

  • Ingram G, Covacevich JA (1988) Revision of the genus Lygisaurus de Vis (Scincidae: Reptilia) in Australia. Mem Queensl Mus 25:335–354

    Google Scholar 

  • Ingram G, Covacevich JA (1989) Revision of the genus Carlia (Reptilia, Scincidae) in Australia and comments on Carlia bicarinata of New Guinea. Mem Queensl Mus 27:443–490

    Google Scholar 

  • Jackson JF (1973) Distribution and population phenetics of the Florida scrub lizard, Sceloporus woodi. Copeia 1973:746–761. doi:10.2307/1443075

    Article  Google Scholar 

  • Jaksic FM, Núñez H (1979) Escaping behavior and morphological correlates in two Liolaemus species of central Chile (Lacertilia: Iguanidae). Oecologia 42:119–122

    Google Scholar 

  • Jaksic FM, Nunez H, Ojeda FP (1980) Body proportions, microhabitat selection, and adaptive radiation of Liolaemus lizards in Central Chile. Oecologia 45:178–181. doi:10.1007/BF00346457

    Article  Google Scholar 

  • Kraus F (2007) Taxonomic partitioning within Papuan members of the Carlia novaeguineae complex (Squamata : Scincidae). J Herpetol 41:410–423. doi:10.1670/0022-1511(2007)41[410:TPWPMO]2.0.CO;2

    Article  Google Scholar 

  • Langerhans RB, Gifford ME, Joseph EO (2007) Ecological speciation in Gambusia fishes. Evol Int J Org Evol 61:2056–2074. doi:10.1111/j.1558-5646.2007.00171.x

    CAS  Google Scholar 

  • Langkilde T, Schwartzkopf L, Alford R (2003) An ethogram for adult male rainbow skinks, Carlia jarnoldae. Herpetol J 13:141–148

    Google Scholar 

  • Langkilde T, Schwarzkoff L, Alford RA (2005) The function of tail displays in male rainbow skinks (Carlia jarnoldae). J Herpetol 39:325–328. doi:10.1670/0022-1511(2005)039[0325:TFOTDI]2.0.CO;2

    Article  Google Scholar 

  • Maddison WP, Maddison DR (2008) Mesquite: a modular system for evolutionary analysis

  • Malhotra A, Thorpe RS (1997) Size and shape variation in a Lesser Antillean anole, Anolis oculatus (Sauria: Iguanidae) in relation to habitat. Biol J Linn Soc Lond 60:53–72

    Google Scholar 

  • Marchetti K (1993) Dark habitats and bright birds illustrate the role of the environment in species divergence. Nature 362:149–152. doi:10.1038/362149a0

    Article  Google Scholar 

  • Martins EP (1994) Estimating the rate of phenotypic evolution from comparative data. Am Nat 144:193–209. doi:10.1086/285670

    Article  Google Scholar 

  • Martins EP (2004) COMPARE, version 4.6b. Computer programs for the statistical analysis of comparative data. Distributed by the author at http://compare.bio.indiana.edu/. Department of Biology, Indiana University, Bloomington

  • Martins EP, Hansen TF (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149:646–667. doi:10.1086/286013

    Article  Google Scholar 

  • Martins EP, Diniz JAF, Housworth EA (2002) Adaptive constraints and the phylogenetic comparative method: a computer simulation test. Evol Int J Org Evol 56:1–13

    Google Scholar 

  • Martins EP, Labra A, Halloy M, Thompson JT (2004) Large-scale patterns of signal evolution: an interspecific study of Liolaemus lizard headbob displays. Anim Behav 68:453–463. doi:10.1016/j.anbehav.2003.08.026

    Article  Google Scholar 

  • Mayr E (1947) Ecological factors in speciation. Evol Int J Org Evol 1:263–288. doi:10.2307/2405327

    Google Scholar 

  • Miles DB (1994) Covariation between morphology and locomotory performance in sceloporine lizards. In: Vitt LJ, Pianka ER (eds) Lizard ecology. Princeton University Press, Princeton New Jersey, pp 207–235

    Google Scholar 

  • Muller HJ (1942) Isolating mechanisms, evolution, and temperature. Biol Symp 6:71–125

    Google Scholar 

  • Ord TJ, Stuart-Fox D (2006) Ornament evolution in dragon lizards: multiple gains and widespread losses reveal a complex history of evolutionary change. J Evol Biol 19:797–808. doi:10.1111/j.1420-9101.2005.01050.x

    Article  CAS  PubMed  Google Scholar 

  • Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia. Ecology 50:1012–1030. doi:10.2307/1936893

    Article  Google Scholar 

  • Revell LJ, Johnson MA, Schulte JA, Kolbe JJ, Losos JB (2007) A phylogenetic test for adaptive convergence in rock-dwelling lizards. Evol Int J Org Evol 61:2898–2912. doi:10.1111/j.1558-5646.2007.00225.x

    Google Scholar 

  • Reznick DN, Butler MJ, Rodd FH, Ross P (1996) Life-history evolution in guppies (Poecilia reticulata). 6. Differential mortality as a mechanism for natural selection. Evol Int J Org Evol 50:1651–1660. doi:10.2307/2410901

    Google Scholar 

  • Sanderson MJ (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol 19:101–109

    CAS  PubMed  Google Scholar 

  • Sanderson M (2004) r8s. Section of ecology and evolution. University of California, Davis

    Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  • Schneider CJ, Smith TB, Larison B, Moritz C (1999) A test of alternative models of diversification in tropical rainforests: ecological gradients vs. rainforest refugia. Proc Natl Acad Sci 96:13869–13873. doi:10.1073/pnas.96.24.13869

    Article  CAS  PubMed  Google Scholar 

  • Shine R (1980) Ecology of eastern Australian whipsnakes of the genus Demansia. J Herpetol 14:381–389. doi:10.2307/1563694

    Article  Google Scholar 

  • Sillman AJ, Govardovskii VI, Rohlich P, Southard JA, Loew ER (1997) The photoreceptors and visual pigments of the garter snake (Thamnophis sirtalis): a microspectrophotometric, scanning electron microscopic and immunocytochemical study. J Comparative Physiol Sensory Neural Behav Physiol 181:89–101

    Article  CAS  Google Scholar 

  • Smith TB, Schneider CJ, Holder K (2001) Refugial isolation versus ecological gradients. Genetica 112:383–398. doi:10.1023/A:1013312510860

    Article  PubMed  Google Scholar 

  • Storr GM (1974) The genus Carlia (Lacertilia, Scincidae) in Western Australia and the Northern Territory. Rec West Aust Mus 3:151–165

    Google Scholar 

  • Stuart-Fox DM, Ord TJ (2004) Sexual selection, natural selection and the evolution of dimorphic coloration and ornamentation in agamid lizards. Proc R Soc Lond B Biol Sci 271:2249–2255. doi:10.1098/rspb.2004.2802

    Article  Google Scholar 

  • Van Damme R, Vanhooydonck B (2001) Origins of interspecific variation in lizard sprint capacity. Funct Ecol 15:186–202. doi:10.1046/j.1365-2435.2001.00513.x

    Article  Google Scholar 

  • Vitt LJ (1991) An introduction to the ecology of Cerrado lizards. J Herpetol 25:79–90. doi:10.2307/1564798

    Article  Google Scholar 

  • Vitt LJ, Caldwell JP, Zani PA, Titus TA (1997) The role of habitat shift in the evolution of Lizard morphology: evidence from tropical Tropidurus. Proc Natl Acad Sci USA 94:3828–3832. doi:10.1073/pnas.94.8.3828

    Article  CAS  PubMed  Google Scholar 

  • Wainwright PC, Reilly SM (1994) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago

    Google Scholar 

  • Whittier JM (1993) Ecological notes on Carlia rostralis in rainforest and associated habitat in the southern Wet Tropics. Mem Queensl Mus 34:125–129

    Google Scholar 

  • Zug GR (2004) Systematics of the Carlia “fusca” lizards (Squamata: Scincidae) of New Guinea and nearby islands. Bishop Museum Press, Honolulu

    Google Scholar 

Download references

Acknowledgments

We thank Craig Moritz for guidance and partial funding. We are grateful to Adnan Moussalli for constructive comments and Craig Moritz, Sandie Degnan, Jeremy Austin and John Endler for helpful comments on drafts of an earlier manuscript. We are very grateful to Patrick Couper and Andrew Amey (Queensland Museum), Paul Horner (Northern Territory Museum), Ross Sadlier (Australian Museum), Steve Donnellan (South Australian Museum) and Laurie Smith (West Australian Museum) for access to collections and insight into the biology of Carlia. GD was supported by an F. G. Meade Scholarship and a CSIRO OCE Postdoctoral Fellowship and DSF was supported by the Australian Research Council.

Author information

Authors and Affiliations

  1. School of Integrative Biology, University of Queensland, St Lucia, QLD, 4072, Australia

    Gaynor Dolman

  2. Australian National Wildlife Collection, CSIRO Sustainable Ecosystems, Canberra, ACT, 2601, Australia

    Gaynor Dolman

  3. Department of Zoology, University of Melbourne, Melbourne, 3010, Australia

    Devi Stuart-Fox

  4. Australian National Wildlife Collection, c/o School of Earth and Environmental Sciences, University of Adelaide, Darling Building, DX 650 418, North Terrace Campus, Adelaide, SA, 5005, Australia

    Gaynor Dolman

Authors
  1. Gaynor Dolman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Devi Stuart-Fox
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gaynor Dolman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dolman, G., Stuart-Fox, D. Processes driving male breeding colour and ecomorphological diversification in rainbow skinks: a phylogenetic comparative test. Evol Ecol 24, 97–113 (2010). https://doi.org/10.1007/s10682-009-9293-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-009-9293-5

Keywords

Search

Navigation