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Island colonisation leads to rapid behavioural and morphological divergence in Anolis lizards

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Abstract

Islands are hotspots of endemism and often function as engines of adaptive radiation. Nevertheless, we lack a deep understanding of the processes that generate phenotypic divergence when populations first colonise islands. Important questions include: (1) Do populations experience shifts in habitat use and behaviour with reduced competition and predation, and how fast do these changes occur? (2) Do shifts in niche occupancy result in morphological divergence from mainland populations? To investigate these questions, we transplanted 210 slender anole lizards (Anolis apletophallus) from mainland Panama to three islands in the Panama Canal that are likely species-poor compared to the mainland. We compared habitat use, flight initiation distance, and morphology among populations across two generations of divergence. We found that island lizards changed their behaviour immediately after colonisation, perching on lower and broader surfaces and allowing observers to approach more closely before fleeing. Although we found only weak evidence for an association between survival and morphological trait variation, trait means in the second generation often shifted in the direction expected if selection had acted on the founders. Our results indicate that colonising individuals can change their behaviour rapidly to exploit new structural niches, and that substantial shifts in morphology can occur after only a single generation. These changes, which are probably facilitated by ecological release, may represent the first steps in adaptive radiation of island lineages.

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References

  • Andrews RM (1979) Reproductive effort of female Anolis limifrons (Sauria: Iguanidae). Copeia 620–626

  • Andrews RM (1991) Population stability of a tropical lizard. Ecology 72:1204–1217

    Article  Google Scholar 

  • Andrews RM, Nichols JD (1990) Temporal and spatial variation in survival rates of the tropical lizard Anolis limifrons. Oikos 57:215–221

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker BM, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  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 

  • Broeckhoven C, le Mouton P (2014) Under pressure: morphological and ecological correlates of bite force in the rock-dwelling lizards Ouroborus cataphractus and Karusasaurus polyzonus (Squamata: Cordylidae). Biol J Linn Soc 111:823–833

    Article  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 

  • Cooper WE, Pyron RA, Garland T (2014) Island tameness: living on islands reduces flight initiation distance. Proc Royal Soc B Biol Sci 281:20133019

    Article  Google Scholar 

  • Cox CL, Alexander S, Casement B, Chung AK, Curlis JD, Degon Z, Dubois M et al (2020) Ectoparasite extinction in simplified lizard assemblages during experimental island invasion. Biol Lett 16:20200474

    Article  PubMed  PubMed Central  Google Scholar 

  • Crandell KE, Herrel A, Sasa M, Losos JB, Autumn K (2014) Stick or grip? Co-evolution of adhesive toepads and claws in Anolis lizards. Zoology 117:363–369

    Article  PubMed  Google Scholar 

  • De Meyer J, Irschick DJ, Vanhooydonck B, Losos JB, Adriaens D, Herrel A (2019) The role of bite force in the evolution of head shape and head shape dimorphism in Anolis lizards. Funct Ecol 33:2191–2202

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Des Roches S, Brinkmeyer MS, Harmon LJ, Rosenblum EB (2015) Ecological release and directional change in White Sands lizard trophic ecomorphology. Evol Ecol 29:1–16

    Article  Google Scholar 

  • Eloy de Amorim M, Schoener TW, Santoro GRCC, Lins ACR, Piovia-Scott J, Brandão RA (2017) Lizards on newly created islands independently and rapidly adapt in morphology and diet. Proc Nat Acad Sci 114:8812–8816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fey SB, Vasseur DA, Alujević K, Kroeker KJ, Logan ML, O’Connor MI, Rudolf VHW et al (2019) Opportunities for behavioral rescue under rapid environmental change. Glob Change Biol 25:3110–3120

    Article  Google Scholar 

  • Giles Leigh E Jr, Wright SJ, Herre A, Putz FE (1993) The decline of tree diversity on newly isolated tropical islands: a test of a null hypothesis and some implications. Evol Ecol 7:76–102

    Article  Google Scholar 

  • Gillespie R (2004) Community assembly through adaptive radiation in hawaiian spiders. Science 303:356–359

    Article  CAS  PubMed  Google Scholar 

  • Grant BR, Grant PR (2003) What Darwin’s finches can teach us about the evolutionary origin and regulation of biodiversity. Bioscience 53:965

    Article  Google Scholar 

  • Gross K, Pasinelli G, Kunc HP (2010) Behavioral plasticity allows short-term adjustment to a novel environment. Am Nat 176:456–464

    Article  PubMed  Google Scholar 

  • Hagey TJ, Harte S, Vickers M, Harmon LJ, Schwarzkopf L (2017) There’s more than one way to climb a tree: Limb length and microhabitat use in lizards with toe pads. PLOS ONE 12:e0184641

    Article  PubMed  PubMed Central  Google Scholar 

  • Hagey TJ, Uyeda JC, Crandell KE, Cheney JA, Autumn K, Harmon LJ (2017) Tempo and mode of performance evolution across multiple independent origins of adhesive toe pads in lizards. Evolution 71:2344–2358

    Article  PubMed  Google Scholar 

  • Herrel A, Castilla AM, Al-Sulaiti MK, Wessels JJ (2014) Does large body size relax constraints on bite-force generation in lizards of the genus Uromastyx? J Zool 292:170–174

    Article  Google Scholar 

  • Herrmann NC, Stroud JT, Losos JB (2021) The evolution of ‘Ecological release’ into the 21st Century. Trends Ecol Evol 36:206–215

    Article  PubMed  Google Scholar 

  • Hover EL, Jenssen A (1976) Displays of Anolis limifrons (Sauria, Iguanidae). Behaviour 58:173–191

    Article  Google Scholar 

  • Hu J, Askary AM, Thurman TJ, Spiller DA, Palmer TM, Pringle RM, Barrett RDH (2019) The epigenetic signature of colonizing new environments in Anolis lizards. Mol Biol Evol 36:2165–2170

    Article  CAS  PubMed  Google Scholar 

  • Huey RB, Hertz PE, Sinervo B (2003) Behavioral drive versus behavioral inertia in evolution: a null model approach. Am Nat 161:357–366

    Article  PubMed  Google Scholar 

  • Huyghe K, Herrel A, Adriaens D, Tadić Z, Van Damme R (2008) It is all in the head: morphological basis for differences in bite force among colour morphs of the Dalmatian wall lizard. Biol J Linn Soc 96:13–22

    Article  Google Scholar 

  • Jenssen T, Hover HL (1974) Display repertoire of Anolis limifrons. Am Zool 14:1278–1278

    Google Scholar 

  • Kambysellis MP, Ho K-F, Craddock EM, Piano F, Parisi M, Cohen J (1995) Pattern of ecological shifts in the diversification of Hawaiian Drosophila inferred from a molecular phylogeny. Curr Biol 5:1129–1139

    Article  CAS  PubMed  Google Scholar 

  • Kier G, Kreft H, Lee TM, Jetz W, Ibisch PL, Nowicki C, Mutke J et al (2009) A global assessment of endemism and species richness across island and mainland regions. Proc Nat Acad Sci 106:9322–9327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolbe JJ, Losos JB (2005) Hind-limb length plasticity in Anolis carolinensis. J Herpetology 39:674–678

    Article  Google Scholar 

  • Kolbe JJ, Leal M, Schoener TW, Spiller DA, Losos JB (2012) Founder effects persist despite adaptive differentiation: a field experiment with lizards. Science 335:1086–1089

    Article  CAS  PubMed  Google Scholar 

  • Laake JL (2013) RMark: an R interface for analysis of capture-recapture data with MARK (No. 2013– 01). AFSC Processed Rep. Alaska Fish. Sci. Cent, Seattle WA

    Google Scholar 

  • Lailvaux SP, Irschick DJ (2007) The evolution of performance-based male fighting ability in Caribbean Anolis Lizards. Am Nat 170:573–586

    Article  PubMed  Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    Article  PubMed  Google Scholar 

  • Langkilde T (2006) How much stress do researchers inflict on their study animals? A case study using a scincid lizard, Eulamprus heatwolei. J Exp Biol 209:1035–1043

    Article  PubMed  Google Scholar 

  • Lapiedra O, Sol D, Carranza S, Beaulieu JM (2013) Behavioural changes and the adaptive diversification of pigeons and doves. Proc Royal Soc B Biol Sci 280:20122893

    Article  Google Scholar 

  • Lerner HR, L M, Meyer HF, James M, Hofreiter, Fleischer RC (2011) Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Curr Biol 21:1838–1844

    Article  CAS  PubMed  Google Scholar 

  • Logan ML, Montgomery CE, Boback SM, Reed RN, Campbell JA (2012) Divergence in morphology, but not habitat use, despite low genetic differentiation among insular populations of the lizard Anolis lemurinus in Honduras. J Trop Ecol 28:215–222

    Article  Google Scholar 

  • Logan ML, van Berkel J, Clusella-Trullas S (2019) The Bogert Effect and environmental heterogeneity. Oecologia 191:817–827

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Losos JB, Queiroz KD (1997) Evolutionary consequences of ecological release in caribbean Anolis lizards. Biol J Linn Soc 61:459–483

    Google Scholar 

  • Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457:830–836

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Losos JB, Warheit KI, Schoener TW (1997) Adaptive differentiation following experimental colonization in Anolis lizards. Nature 387:70–73

    Article  CAS  Google Scholar 

  • Losos JB, Creer DA, Glossip D, Goellner R, Hampton A, Roberts G, Haskell N et al (2000) Evolutionary implications of phenotypic plasticity in the Hindlimb of the Lizard Anolis sagrei. Evolution 54:301–305

    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 314:1111–1111

    Article  CAS  PubMed  Google Scholar 

  • Marais E, Chown SL (2008) Beneficial acclimation and the Bogert effect. Ecol Lett 11:1027–1036

    Article  PubMed  Google Scholar 

  • Muñoz MM, Bodensteiner BL (2019) Janzen’s hypothesis meets the Bogert effect: connecting climate variation, thermoregulatory behavior, and rates of physiological evolution. Integr Organismal Biol 1–12

  • Muñoz MM, Stimola MA, Algar AC, Conover A, Rodriguez AJ, Landestoy MA, Bakken GS et al (2014) Evolutionary stasis and lability in thermal physiology in a group of tropical lizards. Proc Royal Soc B Biol Sci 281:20132433

    Article  Google Scholar 

  • Nicholson DJ, Hassall C, Frazier JA (2015) Comparison of a native and a non-native insular reptile species. J Trop Ecol 31:563–566

    Article  Google Scholar 

  • Nicholson DJ, Knell RJ, McCrea RS, Neel LK, Curlis JD, Williams CE, Chung AK et al (2022) Climate anomalies and competition reduce establishment success during island colonization. Ecol Evol 12

  • Ord TJ, Klomp DA (2014) Habitat partitioning and morphological differentiation: the southeast asian Draco lizards and caribbean Anolis lizards compared. Oecologia 175:651–666

    Article  PubMed  Google Scholar 

  • Ozgul A, Tuljapurkar S, Benton TG, Pemberton JM, Clutton-Brock TH, Coulson T (2009) The dynamics of phenotypic change and the shrinking sheep of St. Kilda. Science 325:464–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petren K, Grant PR, Grant BR, Keller LF (2005) Comparative landscape genetics and the adaptive radiation of Darwin’s finches: the role of peripheral isolation. Mol Ecol 14:2943–2957

    Article  CAS  PubMed  Google Scholar 

  • Pringle RM, Kartzinel TR, Palmer TM, Thurman TJ, Fox-Dobbs K, Xu CCY, Hutchinson MC et al (2019) Predator-induced collapse of niche structure and species coexistence. Nature 570:58–64

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Reznick DN, Losos JB, Travis J (2018) From low to high gear: there has been a paradigm shift in our understanding of evolution. Ecol Lett 22:233–244

    Article  PubMed  Google Scholar 

  • Román-Palacios C, Wiens JJ (2018) The tortoise and the Finch: testing for island effects on diversification using two iconic Galápagos radiations. J Biogeogr 45:1701–1712

    Article  Google Scholar 

  • Sagonas K, Pafilis P, Lymberakis P, Donihue CM, Herrel A, Valakos ED (2014) Insularity affects head morphology, bite force and diet in a Mediterranean lizard:  head morphology in Lacerta trilineata. Biol J Linn Soc 112:469–484

    Article  Google Scholar 

  • Salazar JC, Castañeda MdelR, Londoño GA, Bodensteiner BL, Muñoz MM (2019) Physiological evolution during adaptive radiation: a test of the island effect in Anolis lizards. Evolution 73:1241–1252

    Article  PubMed  PubMed Central  Google Scholar 

  • Schluter D (1993) Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency. Ecology 74:699–709

    Article  Google Scholar 

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

    Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoener TW, Spiller DA (1992) Stabilimenta characteristics of the spider Argiope argentata on small islands: support of the predator-defense hypothesis. Behav Ecol Sociobiol 31:309–318

    Article  Google Scholar 

  • Sexton OJ, Bauman J, Ortleb E (1972) Seasonal food habits of Anolis limifrons. Ecology 53:182–186

    Article  Google Scholar 

  • Stuart YE, Campbell TS, Hohenlohe PA, Reynolds RG, Revell LJ, Losos JB (2014) Rapid evolution of a native species following invasion by a congener. Science 346:463–466

    Article  CAS  PubMed  Google Scholar 

  • Tebbich S, Sterelny K, Teschke I (2010) The tale of the finch: adaptive radiation and behavioural flexibility. Philosophical Trans Royal Soc B: Biol Sci 365:1099–1109

    Article  Google Scholar 

  • Vanhooydonck B, Herrel A, Damme RV, Irschick DJ (2006) The quick and the fast: the evolution of acceleration capacity in Anolis lizards. Evolution 60:2137–2147

    PubMed  Google Scholar 

  • Wegener JE, Mulder KP, Pringle RM, Losos JB, Kolbe JJ (2019) Head size of male and female lizards increases with population density across island populations in the Bahamas. Breviora 566:1

    Article  Google Scholar 

  • Whittaker RJ (2007) Island Biogeography: Ecology, Evolution, and Conservation. Oxford University Press, Oxford; UK

    Google Scholar 

  • Witter MS, Carr GD (1988) Adaptive radiation and genetic differentiation in the hawaiian Silversword Alliance (Compositae: Madiinae). Evolution 42:1278–1287

    Article  PubMed  Google Scholar 

  • Wittorski A, Losos JB, Herrel A (2016) Proximate determinants of bite force in Anolis lizards. J Anat 228:85–95

    Article  PubMed  Google Scholar 

  • Zeffer A, Johansson LC, Marmebro à (2003) Functional correlation between habitat use and leg morphology in birds (Aves). Biol J Linn Soc 79:461–484

    Article  Google Scholar 

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Acknowledgements

We would like to thank S. Alvarez-Carretero, M. Stevens, J. Dinner, Z. Graham, P. Jervis, and M. Nicholson for help with the analysis and improving the manuscript. We would also like to thank A. Bilgray, P. Gomez, L. Camacho, C. Leon, R. Liones, R. Urriola and M. Cano for logistical support.

Funding

This project was supported by a NERC studentship (NE/L002485/1) and a Smithsonian Pre-Doctoral Fellowship awarded to DJN, US National Science Foundation awards to MLL (DEB-2024157), CLC (DEB-024179), and WOM (DEB-2024109), a Smithsonian Institution Biodiversity Genomics Postdoctoral Fellowship and a Smithsonian Tropical Research Institute Earl S. Tupper Postdoctoral Fellowship awarded to MLL, and American Museum of Natural History Theodore Roosevelt Memorial Research Grants and Georgia Southern University Graduate Student Professional Development grants awarded to AKC and JDC. AKC was also supported by a Smithsonian Tropical Research Institute Short-term Fellowship.

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Authors and Affiliations

  1. Queen Mary University of London, London, UK

    Daniel J. Nicholson & Robert J. Knell

  2. Institute of Zoology, Zoological Society of London, London, UK

    Daniel J. Nicholson & Trenton W. J. Garner

  3. Smithsonian Tropical Research Institute, Panama City, Republic of Panama

    Daniel J. Nicholson, Timothy J. Thurman, W. Owen McMillan, Christian L. Cox & Michael L. Logan

  4. University of Texas Arlington, Arlington, USA

    Daniel J. Nicholson & Edita Folfas

  5. University of Hull, Hull, UK

    Robert J. Knell

  6. Arizona State University, Tempe, USA

    Lauren K. Neel

  7. University of Central Arkansas, Conway, USA

    Zachariah Degon

  8. The Land Institute, Salina, USA

    Madeline DuBois

  9. University of California, Los Angeles, USA

    Xochitl Ortiz-Ross

  10. Princeton University, Princeton, USA

    Albert K. Chung

  11. University of Michigan, Ann Arbor, USA

    John David Curlis

  12. Florida International University, Miami, USA

    Christian L. Cox

  13. University of Nevada, Reno, USA

    Michael L. Logan

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  1. Daniel J. Nicholson
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Contributions

DJN, WOM, TJT, CLC and MLL designed research; DJN, EF, LKN, ZD, MD, XO, AKC, JDC, CLC and MLL performed research; DJN and RJK analyzed data; DJN, RJK, TWJG, LKN, CLC and MLL wrote the paper.

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Correspondence to Daniel J. Nicholson.

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This research was conducted under scientific collecting permits (SE/A-37-19, SE/A-18-18 and SE/A-39-17) from the Ministerio de Ambiente in Panama, permission from the Autoridad del Canal de Panamá, and the Smithsonian Tropical Research Institute Animal Care and Use protocol # 2017-0308-2020.

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Nicholson, D.J., Knell, R.J., Folfas, E. et al. Island colonisation leads to rapid behavioural and morphological divergence in Anolis lizards. Evol Ecol 37, 779–795 (2023). https://doi.org/10.1007/s10682-023-10248-2

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