Skip to main content

Advertisement

SpringerLink
Log in

Ecological release and directional change in White Sands lizard trophic ecomorphology

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

Abstract

A species’ trophic ecomorphology can change drastically following the colonization of a new environment. Resource shifts may result in dietary change of colonists and therefore, the evolution of ecomorphological adaptations such as changes in bite force, head, and body size. To understand the drivers and dynamics of ecomorphological change after colonization we studied prey availability, diet, performance, and morphology in three lizard species (Aspidoscelis inornata, Holbrookia maculata, and Sceloporus cowlesi) in the ecologically distinct environment of White Sands, New Mexico. White Sands, which formed within the last 6,000 years, was most likely colonized by nearby “dark soils” populations. Therefore, for each species we compared White Sands individuals to conspecific inhabiting the surrounding Chihuahuan Desert habitat. The White Sands habitat had higher prey morphospecies richness, increased breadth of prey orders, and a higher percentage of hard-bodied prey than the dark soils habitat. Differences in prey availability in White Sands and dark soils habitats were reflected in lizard diets. Specifically, morphospecies richness and percentage of hard bodied prey were higher in the diet of White Sands lizards compared to dark soils lizards. These similarities in resource use across the three species in two habitats indicated parallel responses to a shared environment. Although some dietary shifts in the three species were predictable and reflected prey availability, differences in performance and morphology traits indicated different ecological responses in each species. In general, average prey hardness was higher in the two White Sands species that had stronger absolute bite force and larger absolute head size. While White Sands lizards generally also included a larger proportion of hard prey in their diets, had higher absolute bite-force, head size, and body size than dark soils lizards, the magnitude of these differences varied across species.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguirre LF, Herrel A, Van Damme R, Mathyssen E (2003) The implications of food hardness for diet in bats. Funct Ecol 17:201–212

    Article  Google Scholar 

  • Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23:347–361

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Aubret F, Bonnet X, Shine R (2007) The role of adaptive plasticity in a major evolutionary transition: early aquatic experience affects locomotor performance of terrestrial snakes. Funct Ecol 21:1154–1161

    Article  Google Scholar 

  • Bolnick DI, Svanbäck R, Araújo MS, Persson L (2007) Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. PNAS 104:10075–10079

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Calsbeek R, Irschick DJ (2007) The quick and the dead: correlational selection on morphology, performance, and habitat use in island lizards. Evolution 61:2493–2503

    Article  PubMed  Google Scholar 

  • Calsbeek R, Smith TB (2007) Probing the adaptive landscape using experimental islands: density-dependent natural selection on lizard body size. Evolution 61:1052–1061

    Article  PubMed  Google Scholar 

  • Dayan T, Simberloff D (1998) Size patterns among competitors: ecological character displacement and character release in mammals, with special reference to island populations. Mamm Rev 28:99–124

    Article  Google Scholar 

  • Degenhardt WG, Painter CW, Price AH (2005) Amphibians and reptiles of New Mexico. University of New Mexico Press, Albuquerque

    Google Scholar 

  • DeMarco VG, Drenner RW, Ferguson GW (1985) Maximum prey size of an insectivorous lizard, Sceloporus cowlesi garmani. Copeia 1985:1077–1080

  • Des Roches S, Robertson JM, Harmon LJ, Rosenblum EB (2011) Ecological release in White Sands lizards. Ecol Evol 1:571–578

    Article  PubMed Central  PubMed  Google Scholar 

  • Des Roches S, Torresdal J, Morgan TW, Harmon LJ, Rosenblum EB (2014) Beyond black and white: divergent behaviour and performance in three rapidly evolving lizard species at White Sands. Biol J Linnean Soc 111:169–182

    Article  Google Scholar 

  • Dixon JR (1967) Aspects of the biology of the lizards of the White Sands, New Mexico. Los Angeles County Museum of Natural History

  • Dixon JR, Medica PA (1966) Summer food of four species of lizards from the vicinity of White Sands, New Mexico. Los Angel Cty Mus Contrib Sci 121:1–6

    Google Scholar 

  • Edwards S, Tolley KA, Vanhooydonck B, Measey GJ, Herrel A (2013) Is dietary niche breadth linked to morphology and performance in Sandveld lizards Nucras (Sauria: Lacertidae)? Biol J Linnean Soc 110:674–688

    Article  Google Scholar 

  • Emerson FW (1935) An ecological reconnaissance in the White Sands, New Mexico. Ecology 16:226–233

    Article  Google Scholar 

  • Galis F (1996) The application of functional morphology to evolutionary studies. Trends Ecol Evolut 11:124–129

    Article  CAS  Google Scholar 

  • Herrel A, O’Reilly JC (2006) Ontogenetic scaling of bite force in lizards and turtles. Physiol Biochem Zool 79:31–42

    Article  PubMed  Google Scholar 

  • Herrel A, Spithoven L, Van Damme R, De Vree F (1999) Sexual dimorphism of head size in Gallotia galloti; testing the niche divergence hypothesis by functional analyses. Funct Ecol 13:289–297

    Article  Google Scholar 

  • Herrel A, Van Damme R, Vanhooydonck B, De Vree F (2001) The implications of bite performance for diet in two species of lacertid lizards. Can J Zool 79:662–670

    Article  Google Scholar 

  • Herrel A, Joachim R, Vanhooydonck B, Irschick DJ (2006) Ecological consequences of ontogenetic changes in head shape and bite performance in the Jamaican lizard Anolis lineatopus. Biol J Linn Soc 89:443–454

    Article  Google Scholar 

  • Herrel A, Huyghe K, Vanhooydonck B, Backeljau T, Breugelmans K, Grbac I, Van Damme R, Irschick DJ (2008) Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. PNAS 105:4792–4795

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hunt J, Breuker CJ, Sadowski JA, Moore AJ (2009) Male–male competition, female mate choice and their interaction: determining total sexual selection. J Evol Biol 22:13–26

    Article  PubMed  Google Scholar 

  • Husak JF, Lappin AK, Fox SF, Lemos-Espinal JA (2006) Bite-force performance predicts dominance in male venerable collared lizards (Crotaphytus antiquus). Copeia 2006:301–306

  • Irschick DJ (2002) Evolutionary approaches for studying functional morphology: examples from studies of performance capacity. Integr Comp Biol 42:278–290

    Article  PubMed  Google Scholar 

  • Irschick DJ, Meyers JJ (2007) An analysis of the relative roles of plasticity and natural selection in the morphology and performance of a lizard (Urosaurus ornatus). Oecologia 153:489–499

    Article  PubMed  Google Scholar 

  • Irschick DJ, Meyers JJ, Husak JF, Le Galliard J (2008) How does selection operate on whole-organism functional performance capacities? A review and synthesis. Evol Ecol Res 10:177

    Google Scholar 

  • Kaliontzopoulou A, Adams DC, van der Meijden A, Perera A, Carretero MA (2012) Relationships between head morphology, bite performance and ecology in two species of Podarcis wall lizards. Evol Ecol 26:825–845

    Article  Google Scholar 

  • Kocurek G, Carr M, Ewing R, Havholm KG, Nagar YC, Singhvi AK (2007) White Sands dune field, New Mexico: age, dune dynamics and recent accumulations. Sediment Geol 197:313–331

    Article  Google Scholar 

  • Lappin AK, Husak JF (2005) Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris). Am Nat 166:426–436

    Article  PubMed  Google Scholar 

  • Legler JM, Sullivan LJ (1979) The application of stomach-flushing to lizards and anurans. Herpetologica 35:107–110

    Google Scholar 

  • Leyte-Manrique A, RamÍrez-Bautista A (2010) Diet of two populations of Sceloporus grammicus (Squamata: Phrynosomatidae) from Hidalgo, Mexico. Southwest Nat 55:98–103

    Article  Google Scholar 

  • Lister BC (1976a) The nature of niche expansion in West Indian Anolis lizards I: ecological consequences of reduced competition. Evolution 30:659–676

    Article  Google Scholar 

  • Lister BC (1976b) The nature of niche expansion in West Indian Anolis lizards II: evolutionary components. Evolution 30:677–692

    Article  Google Scholar 

  • Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evolut 8:133–137

    Article  CAS  Google Scholar 

  • Losos JB, De Queiroz K (1997) Evolutionary consequences of ecological release in Caribbean Anolis lizards. Biol J Linnean Soc 61:459–483

    Google Scholar 

  • Losos JB, Mahler DL (2010) Adaptive radiation: the interaction of ecological opportunity, adaptation, and speciation. Evol Since Darwin First 150:381–420

    Google Scholar 

  • McPhail JD (1993) Ecology and evolution of sympatric sticklebacks (Gasterosteus): origin of the species pairs. Can J Zool 71:515–523

    Article  Google Scholar 

  • Meyers JJ, Herrel A, Birch J (2002) Scaling of morphology, bite force and feeding kinematics in an iguanian and a scleroglossan lizard. In: Aerts P, Daout K, Herrel A, Van Damme R (eds) Topics in functional and ecological vertebrate morphology. Shaker Publishing, Maastricht, pp 47–62

    Google Scholar 

  • Mosimann JE (1970) Size allometry: size and shape variables with characterizations of the lognormal and generalized gamma distributions. J Am Stat Assoc 65:930–945

    Article  Google Scholar 

  • Newbold TS, MacMahon JA (2009) Spatial and seasonal dietary patterns of the desert horned lizard (Phrynosoma platyrhinos): harvester ant specialist or generalist ant feeder? Can J Zool 87:112–123

    Article  Google Scholar 

  • Parsons PA (1982) Adaptive strategies of colonizing animal species. Biol Rev 57:117–148

    Article  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reznick DN, Ghalambor CK (2001) The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112:183–198

    Article  PubMed  Google Scholar 

  • Robbins TR, Langkilde T (2012) The consequences of lifetime and evolutionary exposure to toxic prey: changes in avoidance behaviour through ontogeny. J Evol Biol 25:1937–1946

    Article  CAS  PubMed  Google Scholar 

  • Robbins TR, Freidenfelds NA, Langkilde T (2013) Native predator eats invasive toxic prey: evidence for increased incidence of consumption rather than aversion learning. Biol Invasions 15:407–415

    Article  Google Scholar 

  • Robertson JM, Rosenblum EB (2009) Rapid divergence of social signal coloration across the White Sands ecotone for three lizard species under strong natural selection. Biol J Linnean Soc 98:243–255

    Article  Google Scholar 

  • Robertson JM, Rosenblum EB (2010) Male territoriality and ‘sex confusion’ in recently adapted lizards at White Sands. J Evol Biol 23:1928–1936

    Article  CAS  PubMed  Google Scholar 

  • Robertson JM, Hoversten K, Grundler M, Poorten TJ, Hews DK, Rosenblum EB (2011) Colonization of novel White Sands habitat is associated with changes in lizard anti-predator behaviour. Biol J Linnean Soc 103:657–667

    Article  Google Scholar 

  • Robinson BW, Wilson DS (1998) Optimal foraging, specialization, and a solution to Liem’s paradox. Am Nat 151:223–235

    Article  CAS  PubMed  Google Scholar 

  • Rosenblum EB (2006) Convergent evolution and divergent selection: lizards at the White Sands ecotone. Am Nat 167:1–15

    Article  PubMed  Google Scholar 

  • Rosenblum EB, Harmon LJ (2011) “Same same but different”: replicated ecological speciation at White Sands. Evolution 65:946–960

    Article  PubMed  Google Scholar 

  • Roughgarden J (1972) Evolution of niche width. Am Nat 106:683–718

    Article  Google Scholar 

  • Sales RFD, Ribeiro LB, Jorge JS, Freire EMX (2012) Feeding habits and predator-prey size relationships in the whiptail lizard Cnemidophorus ocellifer (Teiidae) in the semiarid region of Brazil. S Am J Herp 7:149–156

    Article  Google Scholar 

  • Schluter D, Grant PR (1984) Determinants of morphological patterns in communities of Darwin’s finches. Am Nat 123:175–196

    Article  Google Scholar 

  • Schoener TW (1969) Models of optimal size for solitary predators. Am Nat 103:277–313

    Article  Google Scholar 

  • Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39

    Article  CAS  PubMed  Google Scholar 

  • Simberloff D (1978) Using island biogeographic distributions to determine if colonization is stochastic. Am Nat 112:713–726

    Article  Google Scholar 

  • Stebbins RC (1985) A field guide to western reptiles and amphibians, 2nd edn. Houghton Mifflin, Boston

    Google Scholar 

  • Thompson JN (1998) Rapid evolution as an ecological process. Trends Ecol Evol 13:329–332

    Article  CAS  PubMed  Google Scholar 

  • Van Valen L (1965) Morphological variation and width of ecological niche. Am Nat 99:377–390

    Article  Google Scholar 

  • Verwaijen D, Van Damme R, Herrel A (2002) Relationships between head size, bite force, prey handling efficiency and diet in two sympatric lacertid lizards. Funct Ecol 16:842–850

    Article  Google Scholar 

  • Wiens JJ, Kuczynski CA, Arif S, Reeder TW (2010) Phylogenetic relationships of phrynosomatid lizards based on nuclear and mitochondrial data, and a revised phylogeny for Sceloporus. Mol Phylogenet Evol 54:150–161

    Article  PubMed  Google Scholar 

  • Wilson DS (1975) The adequacy of body size as a niche difference. Am Nat 109:769–784

    Article  Google Scholar 

  • Yoder JB, Clancey E, Des Roches S, Eastman JM, Gentry L, Godsoe W, Hagey TJ, Jochimsen D, Oswald BP, Robertson JM, Sarver BAJ, Schenk JJ, Spear SF, Harmon LJ (2010) Ecological opportunity and the origin of adaptive radiations. J Evol Biol 23:1581–1596

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank White Sands National Monument, White Sands Missile Range, Jornada Long-term Ecological Research Station and New Mexico Department of Game and Fish for providing field permits. We thank J. Torresdal, K. Hardwick, J. Robertson, A. Krohn, D. Burkett, P. Culter, and D. Bustos for field help and the Rosenblum and Harmon labs for manuscript feedback. We thank A. Herrel and D. Irschick for feedback on methodology and reviews of the manuscript. We also thank the anonymous reviewers for their helpful feedback. Funding was provided through a National Science Foundation CAREER grant to EBR (DEB-1054062), a Natural Science and Engineering Research Council of Canada PGS-D fellowship, an American Society of Ichthyologists and Herpetologists Gaige grant, and an University of Idaho Student Grant Program grant to SD. All live animal work was conducted with relevant Animal Care and Use Committee permits (University of Idaho, Protocol #2010-48).

Author information

Authors and Affiliations

  1. Department of Environmental Science, Policy, and Management, University of California, Berkeley, Berkeley, CA, USA

    S. Des Roches & E. B. Rosenblum

  2. Department of Biological Sciences, University of Idaho, Moscow, ID, USA

    M. S. Brinkmeyer & L. J. Harmon

Authors
  1. S. Des Roches
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. S. Brinkmeyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. J. Harmon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. B. Rosenblum
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. Des Roches.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Des Roches, S., Brinkmeyer, M.S., Harmon, L.J. et al. Ecological release and directional change in White Sands lizard trophic ecomorphology. Evol Ecol 29, 1–16 (2015). https://doi.org/10.1007/s10682-014-9740-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-014-9740-9

Keywords

Search

Navigation