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Habitat partitioning and morphological differentiation: the Southeast Asian Draco lizards and Caribbean Anolis lizards compared

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Abstract

Sympatric species that initially overlap in resource use are expected to partition the environment in ways that will minimize interspecific competition. This shift in resource use can in turn prompt evolutionary changes in morphology. A classic example of habitat partitioning and morphological differentiation are the Caribbean Anolis lizards. Less well studied, but nevertheless striking analogues to the Anolis are the Southeast Asian Draco lizards. Draco and Anolis have evolved independently of each other for at least 80 million years. Their comparison subsequently offers a special opportunity to examine mechanisms of phenotypic differentiation between two ecologically diverse, but phylogenetically distinct groups. We tested whether Draco shared ecological axes of differentiation with Anolis (e.g., habitat use), whether this differentiation reflected interspecific competition, and to what extent adaptive change in morphology has occurred along these ecological axes. Using existing data on Anolis, we compared the habitat use and morphology of Draco in a field study of allopatric and sympatric species on the Malay Peninsula, Borneo and in the Philippines. Sympatric Draco lizards partitioned the environment along common resource axes to the Anolis lizards, especially in perch use. Furthermore, the morphology of Draco was correlated with perch use in the same way as it was in Anolis: species that used wider perches exhibited longer limb lengths. These results provide an important illustration of how interspecific competition can occur along common ecological axes in different animal groups, and how natural selection along these axes can generate the same type of adaptive change in morphology.

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References

  • Alfaro ME, Bolnick DI, Wainwright PC (2005) Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. Am Nat 165:E140–E154

    Article  PubMed  Google Scholar 

  • Bickel R, Losos JB (2002) Patterns of morphological variation and correlates of habitat use in Chameleons. Biol J Linn Soc 76:91–103

    Article  Google Scholar 

  • Brown WL, Wilson EO (1956) Character displacement. Syst Zool 5:49–64

    Article  Google Scholar 

  • Cain ML, Bowman WD, Hacker SD (2008) Ecology. Sinauer, Sunderland

    Google Scholar 

  • Campbell NA, Reece JB (2002) Biology, 6th edn. Cummings, Menlo Park

    Google Scholar 

  • Collar DC, Schulte JA II, O’Meara BC, Losos JB (2010) Habitat use affects morphological diversification in dragon lizards. J Evol Biol 23:1033–1049

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Das I (2010) A field guide to the reptiles of South-east Asia. New Holland, London

    Google Scholar 

  • Dayan T, Simberloff D (2005) Ecological and community-wide character displacement: the next generation. Ecol Lett 8:875–894

    Article  Google Scholar 

  • Daza JD, Abdala V, Arias JS, Garcia-Lopez D, Ortiz P (2012) Cladistic analysis of Iguania and a fossil lizard from the late Pliocene of northwestern Argentina. J Herpetol 46:104–119

    Article  Google Scholar 

  • Grant PR (1972) Convergent and divergent character displacement. Biol J Linn Soc 4:39–68

    Article  Google Scholar 

  • Grismer LL (2011) Lizards of peninsular Malaysia, Singapore and their adjacent archipelagos. Chimaira, Frankfurt

    Google Scholar 

  • Hairston NG (1957) Observations on the behaviour of Draco volans in the Philippines. Copeia 1957:262–265

    Article  Google Scholar 

  • Hansen TF (1997) Stabilizing selection and the comparative analysis of adaptation. Evolution 51:1341–1351

    Article  Google Scholar 

  • Hansen TF, Martins EP (1996) Translating between microevolutionary process and macroevolutionary patterns: the correlation structure of interspecific data. Evolution 50:1404–1417

    Article  Google Scholar 

  • Heaney LR (1986) Biogeography of mammals in SE Asia: estimates of rates of colonization, extinction and speciation. Biol J Linn Soc 28:127–165

    Article  Google Scholar 

  • Herrel A, Meyers JJ, Vanhooydonck B (2002) Relations between microhabitat use and limb shape in phrynosomatid lizards. Biol J Linn Soc 77:149–163

    Article  Google Scholar 

  • Higham TE, Davenport MS, Jayne BC (2001) Maneuvering in an arboreal habitat: the effects of turning angle on the locomotion of three sympatric ecomorphs of Anolis lizards. J Exp Biol 204:4141–4155

    CAS  PubMed  Google Scholar 

  • Inger RF (1983) Morphological and ecological variation in the flying lizards (genus Draco). Field Zool 18:1–33

    Google Scholar 

  • Irschick DJ, Losos JB (1999) Do lizards avoid habitats in which performance is submaximal? The relationship between sprinting capabilities and structural habitat use in Caribbean anoles. Am Nat 154:293–305

    Article  PubMed  Google Scholar 

  • Irschick DJ, Vitt LJ, Zani PA, Losos JB (1997) A comparison of evolutionary radiations in mainland and Caribbean Anolis lizards. Ecology 78:2191–2203

    Article  Google Scholar 

  • Jackman TR, Irschick DJ, de Queiroz K, Losos JB, Larson A (2002) Molecular phylogenetic perspective on evolution of lizards of the Anolis grahami series. J Exp Zool 294:1–16

    Article  CAS  PubMed  Google Scholar 

  • Kuo C-Y, Gillis GB, Irschick DJ (2012) Take this broken tail and learn to jump: the ability to recover from reduced in-air stability in tailless green anole lizards [Anolis carolinensis (Squamata: Dactyloidae)]. Biol J Linn Soc 107:583–592

    Article  Google Scholar 

  • Lazell J (1992) New flying lizards and predictive biogeography of two Asian Archipelagos. Bull Mus Comp Zool 152:475–505

    Google Scholar 

  • Lenormand T, Roze D, Rousset F (2009) Stochasticity in evolution. Trends Ecol Evol 24:157–165

    Article  PubMed  Google Scholar 

  • Losos JB (1990a) Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: an evolutionary analysis. Ecol Monogr 60:369–388

    Article  Google Scholar 

  • Losos JB (1990b) A phylogenetic analysis of character displacement in Caribbean Anolis lizards. Evolution 44:558–569

    Article  Google Scholar 

  • Losos JB (1992) A critical comparison of the taxon-cycle and character-displacement models of size evolution of Anolis lizards in the lesser Antilles. Copeia 1992:279–288

    Article  Google Scholar 

  • Losos JB (1994) Integrative approaches to evolutionary ecology: Anolis lizards as model systems. Annu Rev Ecol Syst 25:467–493

    Article  Google Scholar 

  • Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California Press, Berkeley

    Google Scholar 

  • Losos JB, Sinervo B (1989) The effects of morphological and perch diameter on sprint performance of Anolis lizards. J Exp Biol 145:23–30

    Google Scholar 

  • Losos JB, Marks JC, Schoener TW (1993) Habitat use and ecological interactions of an introduced and native species of Anolis lizard on Grand Cayman, with a review of the outcomes of anole introductions. Oecologia 95:525–532

    Google Scholar 

  • Losos JB, Warheit KI, Schoener TW (1997) Adaptive differentiation following experimental island colonization in Anolis lizards. Nature 387:70–72

    Article  CAS  Google Scholar 

  • Losos JB, Jackman TR, Larson A, de Queiroz K, Rodriguez-Schettino L (1998) Contingency and determinism in replicated adaptive radiations of island lizards. Science 279:2115–2118

    Article  CAS  PubMed  Google Scholar 

  • Losos JB, Creer DA, Glossip D, Goellner R, Hampton A, Roberts G, Haskell N, Taylor P, Ettling J (2000) Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution 54:301–305

    CAS  PubMed  Google Scholar 

  • Losos JB, Leal M, Glor RE, de Queiroz K, Hertz PE, Schettino LR, Lara AC, Jackman TR, Larson A (2003) Niche lability in the evolution of a Caribbean lizard community. Nature 424:542–545

    Article  CAS  PubMed  Google Scholar 

  • Losos JB, Schoener TW, Spiller DA (2004) Predator-induced behaviour shifts and natural selection in field-experimental lizard populations. Nature 432:505–508

    Article  CAS  PubMed  Google Scholar 

  • Losos JB, Schoener TW, Langerhans RB, Spiller DA (2006) Rapid temporal reversal in predator-driven natural selection. Science 314:1111

    Article  CAS  PubMed  Google Scholar 

  • Maddison WP, Maddison DR (2010) Mesquite: a modular system for evolutionary analysis. http://mesquiteprogect.org

  • Martins EP (2004) COMPARE 4.6b: statistical analysis of comparative data. http://compare.bio.indiana.edu/

  • May RM, MacArthur RH (1972) Niche overlap as a function of environmental variability. Proc Natl Acad Sci USA 69:1109–1113

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McGuire JA, Alcala AC (2000) A taxonomic revision of the flying lizards (Iguania: Agamidae: Draco) of the Philippine Islands, with a description of a new species. Herpetol Monogr 14:81–138

    Article  Google Scholar 

  • McGuire JA, Dudley R (2005) The cost of living large: comparative gliding performance in flying lizards (Agamidae: Draco). Am Nat 166:93–106

    Article  PubMed  Google Scholar 

  • McGuire JA, Dudley R (2011) The biology of gliding in flying lizards (genus Draco) and their fossil and extant analogs. Integr Comp Biol 51:983–990

    Article  PubMed  Google Scholar 

  • McGuire JA, Heang KB (2001) Phylogenetic systematics of Southeast Asian flying lizards (Iguania: Agamidae: Draco) as inferred from mitochondrial DNA sequence data. Biol J Linn Soc 72:203–229

    Google Scholar 

  • Mori A, Hikida T (1994) Field observations on the social behavior of the flying lizard, Draco volans sumatranus, in Borneo. Copeia 1994:124–130

    Article  Google Scholar 

  • Mulcahy DG, Noonan BP, Moss T, Townsend TM, Reeder TW, Sites JW Jr, Wiens JJ (2012) Estimating divergence dates and evaluating dating methods using phylogenomic and mitochondrial data in squamate reptiles. Mol Phyl Evol 65:974–991

    Article  Google Scholar 

  • Nicholson KE, Glor RE, Kolbe JJ, Larson A, Hedges SB, Losos JB (2005) Mainland colonization by island lizards. J Biogeogr 32:929–938

    Article  Google Scholar 

  • Ord TJ (2008) Dawn and dusk ‘chorus’ in visually communicating Jamaican anole lizards. Am Nat 172:585–592

    Article  PubMed  Google Scholar 

  • Ord TJ, Martins EP (2006) Tracing the origins of signal diversity in anole lizards: phylogenetic approaches to inferring the evolution of complex behaviour. Anim Behav 71:1411–1429

    Article  Google Scholar 

  • Ord TJ, Stamps JA (2009) Species identity cues in animal communication. Am Nat 174:585–593

    Article  PubMed  Google Scholar 

  • Ord TJ, Charles GK, Hoffer RK (2011) The evolution of alternative adaptive strategies for effective communication in noisy environments. Am Nat 177:54–64

    Article  PubMed  Google Scholar 

  • Pacala S, Roughgarden J (1982) Resource partitioning and interspecific competition in two two-species insular Anolis lizard communities. Science 217:444–446

    Article  CAS  PubMed  Google Scholar 

  • Pacala S, Roughgarden J (1985) Population experiments with the Anolis lizards of St. Maarten and St. Eustatus. Ecology 66:129–141

    Article  Google Scholar 

  • Pfennig DW, Pfennig KS (2012) Evolution’s wedge: competition and the origins of diversity. University of California Press, Berkeley

    Book  Google Scholar 

  • Pianka ER (1974) Niche overlap and diffuse competition. Proc Natl Acad Sci USA 71:2141–2145

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pinto G, Mahler DL, Harmon LJ, Losos JB (2008) Testing the island effect in adaptive radiation: rates and patterns of morphological diversification in Caribbean and mainland Anolis lizards. Proc R Soc Lond B 275:2749–2757

    Article  Google Scholar 

  • Pyron RA, Burbrink FT (2014) Early origin of viviparity and multiple reversions to oviparity in squamate reptiles. Ecol Letters 17:13–21

    Google Scholar 

  • Rand AS (1964) Inverse relationship between temperature and shyness in the lizard Anolis lineatopus. Ecology 45:863–864

    Article  Google Scholar 

  • Rand AS (1967) Ecology and social organization in the iguanid lizard Anolis lineatopus. Proc US Natl Mus 122:1–77

    Article  Google Scholar 

  • Rummel J, Roughgarden J (1985) Effects of reduced perch-height separation on competition between two Anolis lizards. Ecology 66:430–444

    Article  Google Scholar 

  • Schaad EW, Poe S (2010) Patterns of ecomorphological convergence among mainland and island Anolis lizards. Biol J Linn Soc 101:852–859

    Article  Google Scholar 

  • Schluter D, McPhail JD (1992) Ecological character displacement and speciation in sticklebacks. Am Nat 140:85–108

    Article  CAS  PubMed  Google Scholar 

  • Schoener TW (1968) The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schulte JA II, Losos JB, Cruz FB, Nunez H (2004) The relationship between morphology, escape behaviour and microhabitat occupation in the lizard clade Liolaemus (Iguanidae: Tropidurinae*: Liolaemini). J Evol Biol 17:408–420

    Article  PubMed  Google Scholar 

  • Schwartz A, Henderson RW (1991) Amphibians and reptiles of the West Indies: descriptions, distributions and natural history. University of Florida Press, Gainesville

    Google Scholar 

  • Shine R, Keogh S, Doughty P, Giragossyan H (1998) Costs of reproduction and the evolution of sexual dimorphism in a ‘flying lizard’ Draco melanopogon (Agamidae). J Zool 246:203–213

    Google Scholar 

  • Strong DR Jr, Szyska LA, Simberloff DS (1979) Test of community-wide character displacement against null hypotheses. Evolution 33:897–913

    Article  Google Scholar 

  • Stuart YE, Losos JB (2013) Ecological character displacement: glass half full or half empty? Trends Ecol Evol 28:402–408

    Article  PubMed  Google Scholar 

  • Toro E, Herrel A, Irschick DJ (2004) The evolution of jumping performance in Caribbean Anolis lizards: solutions to biomechanical trade-offs. Am Nat 163:844–856

    Article  PubMed  Google Scholar 

  • Townsend TM, Mulcahy DG, Noonan BP, Sites JW Jr, Kuczynski CA, Wiens JJ, Reeder TW (2011) Phylogeny of iguanian lizards inferred from 29 nuclear loci, and a comparison of concatenated and species-tree approaches for an ancient, rapid radiation. Mol Phyl Evol 61:363–380

    Article  Google Scholar 

  • Vanhooydonck B, van Damme R (1999) Evolutionary relationships between body shape and habitat use in lacertid lizards. Evol Ecol Res 1:785–805

    Google Scholar 

  • Warheit KI, Forman JD, Losos JB, Miles DB (1999) Morphological diversification and adaptive radiation: a comparison of two diverse lizard clades. Evolution 53:1226–1234

    Article  Google Scholar 

  • Wiens JJ, Ackerly DD, Allen AP, Anacker BL, Buckley LB, Cornell HV, Damschen EI, Davies TJ, Grytnes J-A, Harrison SP, Hawkins BA, Holt RD, McCain CM, Stephens PR (2010) Niche conservatism as an emerging principle in ecology and conservation biology. Ecol Lett 13:1310–1324

    Article  PubMed  Google Scholar 

  • Williams EE (1983) Ecomorphs, faunas, island size, and diverse end points in island radiations of Anolis. In: Huey RB, Pianka ER, Schoener TW (eds) Lizard ecology: studies of a model organism. Harvard University Press, Cambridge, pp 326–370

    Google Scholar 

  • Wood TE, Burke JM, Rieseberg LH (2005) Parallel genotypic adaptation: when evolution repeats itself. Genetica 123:157–170

    Article  PubMed Central  PubMed  Google Scholar 

  • Zaaf A, van Damme R (2001) Limb proportions in climbing and ground-dwelling geckos (Lepidosauria, Gekkonidae): a phylogenetically informated analysis. Zoomorphology 121:45–53

    Article  Google Scholar 

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Acknowledgments

We are especially grateful to Indraneil Das, Norhayati Ahmad, Arvin Diesmos and Pan Khang Aun for logistical support in the field and facilitating permits. Jim McGuire, Rafe Brown and Lee Grismer provided advice on potential field sites and focal species. We also thank Devi Stuart-Fox, Adnan Moussalli, Anna de Castro, Kenneth Calabia, Jia Cortes, Bea Javillonar and Saun Mabunay for assistance in the field, and Jonathan Losos for providing access to his data on Anolis and Dave Collar for providing his full supertree of the Agamidae. Jonathan Losos, Yoel Stuart, Jerry Husak, Jim McGuire, Luke Mahler, Lin Schwarzkopf and an anonymous reviewer also provided detailed comments on a previous version of this manuscript that greatly improved this article. This work was conducted under research permits from the Malaysian Economic Planning Unit, Sarawak State Planning Unit, Sarawak Forestry Department, Sarawak National Parks and Nature Reserves, and the Government of the Philippines through the Philippine Natural History Museum. This study was covered by the University of New South Wales (UNSW) Animal Care and Ethical Committee protocol no. 11/33b initially approved on 8 March 2011 and most recently reviewed on 28 February 2013. This work was financially supported by Evolution and Ecology Research Centre start-up funds and a UNSW SFRGP grant to T. J. O., a National Geographic Society grant to Devi Stuart-Fox, and an Australian Postgraduate Award and postgraduate research grant from the School of Biological, Earth and Environmental Sciences to D. A. K. All Draco data from this publication have been archived in the Dryad Digital Repository (http://www.dx.doi.org/10.5061/dryad.q1vf1).

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  1. Evolution and Ecology Research Centre, and the School of Biological, Earth and Environmental Sciences, University of New South Wales, Kensington, NSW, 2052, Australia

    Terry J. Ord & Danielle A. Klomp

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Correspondence to Terry J. Ord.

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Communicated by Lin Schwarzkopf.

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Ord, T.J., Klomp, D.A. Habitat partitioning and morphological differentiation: the Southeast Asian Draco lizards and Caribbean Anolis lizards compared. Oecologia 175, 651–666 (2014). https://doi.org/10.1007/s00442-014-2921-y

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