Skip to main content
Log in

Island Tiger Snakes (Notechis scutatus) Gain a ‘Head Start’ in Life: How Both Phenotypic Plasticity and Evolution Underlie Skull Shape Differences

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript


Repeated island colonisation by Australian tiger snakes (Notechis scutatus) has become a model system demonstrating how prey size on islands influences a snake’s body and jaw size. Tiger snakes on islands with large prey have relatively longer jaws compared to their mainland counterparts, due to diet-induced phenotypic plasticity followed by assimilation of favourable traits. We present the first examination of the effects of diet on all skull elements that are involved in feeding, by analysing shape and size differences using CT imaging and a combination of linear measurements and three dimensional geometric morphometrics. We compared two populations of tiger snakes, one from Carnac Island, where the snakes were first introduced approximately 100 years ago, and another from Herdsman Lake on the mainland (a putative source population). Each population was divided into two groups, one was fed small prey and the other large prey. While snakes from the island exhibited relatively longer trophic bones at birth, they also had slightly slower growth rates for these elements regardless of diet. The island forms showed diet-induced plasticity within specific trophic elements, the mandible and palatopterygoid, which grew longer when the snakes were fed larger prey. Importantly, skull plasticity was expressed only after prolonged dietary stress, and was not clearly observable until the snakes approached adulthood. We hypothesize that this plastic response resulting in increased gape may be adaptive, allowing ingestion of large prey items available to adult tiger snakes on Carnac Island. In contrast, no plastic response was observed in the mainland population.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

All specimen data and analysis code are included in the submission as supplementary data, available at


  • Abdi, H., & Williams, L. J. (2010). Principal component analysis. Wiley Interdisciplinary Reviews: Computational Statistics, 2, 433–459.

    Google Scholar 

  • Adams, D. C., Collyer, M. L., Kaliontzopoulou A., & Baken E. K. (2021). Geomorph: Software for geometric morphometric analyses. R package version 4.0.

  • Aubret, F. (2012). Body-size evolution on islands: Are adult size variations in tiger snakes a nonadaptive consequence of selection on birth size? The American Naturalist, 179, 756–767.

    PubMed  Google Scholar 

  • Aubret, F. (2015). Island colonisation and the evolutionary rates of body size in insular neonate snakes. Heredity, 115, 349–356.

    CAS  PubMed  Google Scholar 

  • Aubret, F., Burghardt, G. M., Maumelat, S., Bonnet, X., & Bradshaw, D. (2006). Feeding preferences in 2 disjunct populations of tiger snakes, Notechis scutatus (Elapidae). Behavioral Ecology, 17, 716–725.

    Google Scholar 

  • Aubret, F., & Shine, R. (2007). Rapid prey-induced shift in body size in an isolated snake population (Notechis scutatus, Elapidae). Austral Ecology, 32, 889–899.

    Google Scholar 

  • Aubret, F., & Shine, R. (2009). Genetic assimilation and the postcolonization erosion of phenotypic plasticity in island tiger snakes. Current Biology, 19, 1932–1936.

    CAS  PubMed  Google Scholar 

  • Aubret, F., & Shine, R. (2010). Fitness costs may explain the post-colonisation erosion of phenotypic plasticity. Journal of Experimental Biology, 213, 735–739.

    CAS  PubMed  Google Scholar 

  • Aubret, F., Shine, R., & Bonnet, X. (2004). Adaptive developmental plasticity in snakes. Nature, 431, 261–262.

    CAS  PubMed  Google Scholar 

  • Behera, N., & Nanjundiah, V. (2004). Phenotypic plasticity can potentiate rapid evolutionary change. Journal of Theoretical Biology, 226, 177–184.

    PubMed  Google Scholar 

  • Bonnet, X., Bradshaw, D., Shine, R., & Pearson, D. (1999). Why do snakes have eyes? The (non-) effect of blindness in island tiger snakes (Notechis scutatus). Behavioral Ecology and Sociobiology, 46, 267–272.

    Google Scholar 

  • Bonnet, T., Morrissey, M. B., de Villemereuil, P., Alberts, S. C., Arcese, P., Bailey, L. D., Boutin, S., Brekke, P., Brent, L. J., Camenisch, G., & Charmantier, A. (2022). Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals. Science, 376, 1012–1016.

    CAS  PubMed  Google Scholar 

  • Campbell-Staton, S. C., Arnold, B. J., Gonçalves, D., Granli, P., Poole, J., Long, R. A., & Pringle, R. M. (2021). Ivory poaching and the rapid evolution of tusklessness in African elephants. Science, 374, 483–487.

    CAS  PubMed  Google Scholar 

  • Clarke, C. A., Mani, G. S., & Wynne, G. (1985). Evolution in reverse: Clean air and the peppered moth. Biological Journal of the Linnean Society, 26, 189–199.

    Google Scholar 

  • Cundall, D. (1983). Activity of head muscles during feeding by snakes: A comparative study. American Zoologist, 23, 383–396.

    Google Scholar 

  • Cundall, D., & Irish, F. (2008). The snake skull. In C. Gans, A. S. Gaunt, & K. Adler (Eds.), Biology of the reptilia (Vol. 20, pp. 349–692). Society for the Study of Amphibians and Reptiles.

    Google Scholar 

  • DeWitt, T. J., Sih, A., & Wilson, D. S. (1998). Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution, 13, 77–81.

    CAS  Google Scholar 

  • Donihue, C. M., Herrel, A., Fabre, A. C., et al. (2018). Hurricane-induced selection on the morphology of an island lizard. Nature, 560, 88–91.

    CAS  PubMed  Google Scholar 

  • Fusco, G., & Minelli, A. (2010). Phenotypic plasticity in development and evolution: Facts and concepts. Philosophical Transactions of the Royal Society b: Biological Sciences, 365, 547–556.

    Google Scholar 

  • Gunter, H. M., Fan, S., Xiong, F., Franchini, P., Fruciano, C., & Meyer, A. (2013). Shaping development through mechanical strain: The transcriptional basis of diet-induced phenotypic plasticity in a cichlid fish. Molecular Ecology, 22, 4516–4531.

    PubMed  Google Scholar 

  • Hallgrímsson, B., Willmore, K., & Hall, B. K. (2002). Canalization, developmental stability, and morphological integration in primate limbs. American Journal of Physical Anthropology, 119, 131–158.

    Google Scholar 

  • Keogh, J. S., Scott, I. A., & Hayes, C. (2005). Rapid and repeated origin of insular gigantism and dwarfism in Australian tiger snakes. Evolution, 59, 226–233.

    PubMed  Google Scholar 

  • Ladyman, M., Seubert, E., & Bradshaw, D. (2020). The origin of tiger snakes on Carnac Island. Journal of the Royal Society of Western Australia, 103, 39–42.

    Google Scholar 

  • Levis, N. A., & Pfennig, D. W. (2021). Innovation and diversification via plasticity-led evolution. In D. W. Pfenning (Ed.), Phenotypic plasticity & evolution: Causes, consequences, controversies (pp. 211–240). CRC Press.

    Google Scholar 

  • Losos, J., Warheitt, K., & Schoener, T. (1997). Adaptive differentiation following experimental island colonization in Anolis lizards. Nature, 387, 70–73.

    CAS  Google Scholar 

  • Matsunami, M., Kitano, J., Kishida, O., Michimae, H., Miura, T., & Nishimura, K. (2015). Transcriptome analysis of predator-and prey-induced phenotypic plasticity in the Hokkaido salamander (Hynobius retardatus). Molecular Ecology, 24, 3064–3076.

    CAS  PubMed  Google Scholar 

  • McNamara, K. J. (2012). Heterochrony: the evolution of development. Evolution: Education and Outreach, 5, 203–218.

    Google Scholar 

  • Oksanen, F. J., Blanchet, G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Henry, M., Stevens, H., Szoecs, E., & Wagner, H. (2020). Vegan: Community Ecology Package. R package version 2.5–7.

  • Palci, A., Lee, M. S., & Hutchinson, M. N. (2016). Patterns of postnatal ontogeny of the skull and lower jaw of snakes as revealed by micro-CT scan data and three-dimensional geometric morphometrics. Journal of Anatomy, 229, 723–754.

    PubMed  PubMed Central  Google Scholar 

  • Peter, B. M., & Slatkin, M. (2015). The effective founder effect in a spatially expanding population. Evolution, 69, 721–734.

    PubMed  PubMed Central  Google Scholar 

  • Pfenning, D. W. (2021). Phenotypic plasticity & evolution: Causes, consequences, controversies. CRC Press.

    Google Scholar 

  • Pigliucci, M., Murren, C. J., & Schlichting, C. D. (2006). Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology, 209, 2362–2367.

    PubMed  Google Scholar 

  • R Core Team. (2021). R: a language and environment for statistical computing. R Foundation for Statistical Computing.

  • Relyea, R. A. (2002). Costs of phenotypic plasticity. The American Naturalist, 159, 272–282.

    PubMed  Google Scholar 

  • Rhoda, D., Segall, M., Larouche, O., Evans, K., & Angielczyk, K. D. (2021). Local superimpositions facilitate morphometric analysis of complex articulating structures. Integrative and Comparative Biology, 61, 1892–1904.

    PubMed  PubMed Central  Google Scholar 

  • Rohlf, F. J., & Slice, D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Biology, 39, 40–59.

    Google Scholar 

  • Rollins, L. A., Richardson, M. F., & Shine, R. (2015). A genetic perspective on rapid evolution in cane toads (Rhinella marina). Molecular Ecology, 24, 2264–2276.

    PubMed  Google Scholar 

  • Schlichting, C. D. (2021). Plasticity and evolutionary theory: Where we are and where we should be going. In D. W. Pfenning (Ed.), Phenotypic plasticity & evolution: Causes, consequences, controversies (pp. 367–394). CRC Press.

    Google Scholar 

  • Schneider, R. F., Li, Y., Meyer, A., & Gunter, H. M. (2014). Regulatory gene networks that shape the development of adaptive phenotypic plasticity in a cichlid fish. Molecular Ecology, 23, 4511–4526.

    PubMed  Google Scholar 

  • Schwaner, T. D., & Sarre, S. D. (1990). Body size and sexual dimorphism in mainland and island tiger snakes. Journal of Herpetology, 24, 320–322.

    Google Scholar 

  • Stearns, S. C. (1989). The evolutionary significance of phenotypic plasticity. BioScience, 39, 436–445.

    Google Scholar 

  • Stratovan Corporation 2020, Stratovan Checkpoint [Software]. Version 2020.10.13.0859. URL:

  • Tchigossou, G. M., Atoyebi, S. M., Akoton, R., Tossou, E., Innocent, D., Riveron, J., Irving, H., Yessoufou, A., Wondji, C., & Djouaka, R. (2020). Investigation of DDT resistance mechanisms in Anopheles funestus populations from northern and southern Benin reveals a key role of the GSTe2 gene. Malaria Journal, 19, 1–12.

    Google Scholar 

  • Thompson, D. B. (1992). Consumption rates and the evolution of diet-induced plasticity in the head morphology of Melanoplus femurrubrum (Orthoptera: Acrididae). Oecologia, 89, 204–213.

    PubMed  Google Scholar 

  • Waddington, C. H. (1942). Canalization of development and the inheritance of acquired characters. Nature, 150, 563–565.

    Google Scholar 

  • Whitman, D. W., & Agrawal, A. A. (2009). What is phenotypic plasticity and why it is important. In D. W. Whitman & T. N. Ananthakrishnan (Eds.), Phenotypic plasticity of insects: Mechanisms and consequences (pp. 1–63). Science Publishers Inc.

    Google Scholar 

  • Wirgin, I., Roy, N. K., Loftus, M., Chambers, R. C., Franks, D. G., & Hahn, M. E. (2011). Mechanistic basis of resistance to PCBs in Atlantic tomcod from the Hudson River. Science, 331, 1322–1325.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wold, S., Esbensen, K., & Geladi, P. (1987). Principal component analysis. Chemometrics and Intelligent Laboratory Systems, 2, 37–52.

    CAS  Google Scholar 

  • Zelditch, M. L., Swiderski, D. L., & Sheets, H. D. (2012). Geometric morphometrics for biologists: A primer. Academic Press.

    Google Scholar 

Download references


We thank Dr Agatha Labridinis, from Adelaide Microscopy, University of Adelaide, South Australia, for assistance provided with the Skyscan 1276 microCT scanner. We are deeply grateful to Dr. Fabien Aubret for his generous assistance in the collection of the tiger snakes used in this experiment. We also thank D. Silva Fernandes and an anonymous reviewer for their useful comments that helped improve this manuscript.


This study was funded by the Australian Research Council as part of VT’s DECRA Fellowship DE180100624, a Linkage grant LP160100189 and a Discovery grant DP200102328.

Author information

Authors and Affiliations



VAT designed the study and collected the snakes, ND, JA, LA took care of their husbandry at Venom Supplies, and VAT, ND, LA, JA undertook the feeding experiment. Ammresh collected and analysed the data. Ammresh and AP, with input from all other authors, interpreted the results, prepared the figures, and wrote the first draft of the manuscript. AP and ES supervised the collection of data and analytical aspects. All authors read, edited, and approved the final version of the manuscript.

Corresponding author

Correspondence to Alessandro Palci.

Ethics declarations

Competing interest

The authors declare that they have no conflict of interest.

Ethical approval

The experiments described below have been approved by the Animal Ethics Committee at the University of Adelaide, Adelaide, South Australia (under UofA AEC Project Approval No’s S-2016–111 and S-2019–002); the collection of the tiger snakes were permitted under a ‘Fauna taking (scientific or other purposes) licence’ #FO25000008 and #FO25000008-2 from the Department of Biodiversity, Conservation and Attractions (DBCA) of Western Australia (WA); the export of the tiger snakes from WA was conducted under ‘Fauna Exporting Licence’ #EF41000039 and #EF41000231 from DBCA of WA; the import of the tiger snakes into South Australia (SA) was conducted under a ‘Permit to undertake Scientific Research’ #E26703-4 and #E26703-5 from the Department of Environment and Water of SA; all Australian legal requirements and guidelines for the care and use of animals have been followed.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 2987 kb)

Supplementary file2 (ZIP 100 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ammresh, Sherratt, E., Thomson, V.A. et al. Island Tiger Snakes (Notechis scutatus) Gain a ‘Head Start’ in Life: How Both Phenotypic Plasticity and Evolution Underlie Skull Shape Differences. Evol Biol 50, 111–126 (2023).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: