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Whole-organism studies of adhesion in pad-bearing lizards: creative evolutionary solutions to functional problems

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Abstract

Understanding the evolution of complex functional traits is a challenge for evolutionary physiology. Here we investigate the evolution of subdigital toepads in lizards, which have arisen independently at least three times, although with subtle anatomical differences. Some designs (anole, gecko) appear functionally equivalent, whereas other designs (skink) are inferior. The functional equivalence of geckos and anoles highlights the creative aspect of the evolutionary process in that these two groups have arrived at the same functional endpoint along very different trajectories. However, this functional equivalence does not result in equivalence for performance at whole-organism tasks (e.g., running uphill), as the evolution of behavior (e.g., toe-furling) has enabled geckos to be superior climbers than anoles. We also show that adaptive increases in the toepad size within a closely related lizard genus (Anolis) has resulted in concomitant evolution of enhanced clinging ability and increased perch heights. A third insight is that pad-bearing geckos are capable of carrying tremendous loads (up to 250% of body weight) up smooth surfaces, and that the toepad itself does not appear limiting. This comparative and whole-organism approach to lizard toepads underscores how organisms can evolve multiple solutions to evolutionary problems.

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References

  • Aerts P (1990) Mathematical biomechanics and the “what!”, “how?” and “why” in functional morphology.Neth J Zool 40:153–172

    Article  Google Scholar 

  • Aerts P (1998) Vertical jumping in Galago senegalensis: the quest for a hidden power amplifier. Phil Trans R Soc B 353:1607–1620

    Article  Google Scholar 

  • Arzt E, Gorb S, Spolenak R (2003) From micro and nano contacts in biological attachment devices. Proc Natl Acad Sci USA 100:10603–10606

    Article  PubMed  CAS  Google Scholar 

  • Austin CC (1995) Molecular and morphological evolution in South Pacific scincid lizards: morphological conservatism and phylogenetic relationships of Papuan Lipinia (Scincidae). Herpetologica 51:291–300

    Google Scholar 

  • Austin CC, Jessing KW (1994) Green-blood pigmentation in lizards. Comp Biochem Physiol 109A:619–626

    Article  CAS  Google Scholar 

  • Autumn K, YA Liang, Hsieh ST, Zesch W, Chan WP, Kenny TW, Fearing R, Full RJ (2000) Adhesive force of a single gecko foot-hair. Nature 405:681–685

    Article  PubMed  CAS  Google Scholar 

  • Autumn K, Sitti M, Liang YCA, Peattie PA, Hansen WR, Sponberg S, Kenny TW, Fearing R, Israelachvili JN, Full RJ (2002) Evidence for van der Waals adhesion in gecko setae. Proc Natl Acad Sci USA 99:12252–12256

    Article  PubMed  CAS  Google Scholar 

  • Bauer AM, Good DA (1986) Scaling of scansorial surface area in the genus Gekko. In: Rocek Z (ed) Studies in herpetology, Charles University, Prague

    Google Scholar 

  • Bauer AM, Russell AP (1988) Morphology of gekkonoid cutaneous sensilla, with comments on function and phylogeny in the Carphodactylini (Reptilia: Gekkonidae). Can J Zool 66:1583–1588

    Article  Google Scholar 

  • Baum AM, Larson A (1991) Adaptation reviewed: A phylogenetic methodology for studying character macroevolution. Syst Zool 40:1–18

    Article  Google Scholar 

  • Bauwens D, Thoen C (1981) Escape tactics and vulnerability to predation associated with reproduction in the lizard Lacerta vivipara. J Anim Ecol 50:733–743

    Article  Google Scholar 

  • Bennett AF, Huey RB (1990) Studying the evolution of physiological performance. Oxford Surv Evol Biol 7:251–284

    Google Scholar 

  • Bergmann P, Irschick DJ (2005) Effects of temperature on maximum clinging ability in a diurnal gecko: evidence for a passive clinging mechanism? J Exp Zool 303A:785–791

    Article  Google Scholar 

  • Bloch N, Irschick DJ (2005) Toe-clipping dramatically reduces clinging performance in a pad-bearing lizard (Anolis carolinensis). J Herp 39:288–293

    Article  Google Scholar 

  • Brown WC, Fehlman A (1958) A new genus and species of arboreal scincid lizards from the Palau Islands. Occ Pap Nat Hist Mus Stanford 6:1–7

    Google Scholar 

  • Dai Z, Gorb SN, Schwarz U (2002) Roughness-dependent friction force of the tarsal claw system in the beetle Pachnoda marginata (Coleoptera, Scarabaeidae). J Exp Biol 205:2479–2488

    PubMed  Google Scholar 

  • Dodd CK (1993) The effects of toe-clipping on the sprint performance of the lizard Cnemidophorus sexlineatus. J Herp 27:209–213

    Article  Google Scholar 

  • Dunham AE, Morin PJ, Wilbur HM (1994) Methods for the study of reptile populations. In: Gans C, Huey RB (eds) Biology of reptilia, Branta Brooks, Ann Harbor

    Google Scholar 

  • Elstrott J, Irschick DJ (2004) Evolutionary correlations among morphology, habitat use and clinging performance in Caribbean Anolis lizards. Biol J Linn Soc 83:389–398

    Article  Google Scholar 

  • Ernst VV, Ruibal R (1967) The structure and development of the digital lamellae of lizards. J Morph 120:233–266

    Article  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Garland T Jr, Arnold SJ (1983) Effects of a full stomach on locomotory performance of juvenile garter snakes (Thamnophis elegans). Copeia 1983:1092–1096

    Article  Google Scholar 

  • Garland T Jr, Dickerman AW Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292

    Article  Google Scholar 

  • Garland T Jr, Losos JB (1994) Ecological morphology of locomotor performance in reptiles. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. Chicago University Press, Chicago

    Google Scholar 

  • Hecht MK (1952) Natural selection in the lizard genus Aristelliger. Evolution 6:112–124

    Article  Google Scholar 

  • Hiller U (1976a) Comparative studies on the functional morphology of two gekkonid lizards. J Bombay Nat Hist Soc 73:278–282

    Google Scholar 

  • Hiller U (1976b) Elektronenmikroskopische Untersuchungen zur funktionellen Morphologie der borstenfhrenden Hautsinnesorgane bei Tarentola mauritanica L. (Reptilia, Gekkonidae). Zoomorphologie 84:211–221

    Article  Google Scholar 

  • Hudson S (1996) Natural toe loss in the southern Australian skinks: implications for marking by toe-clipping. J Herp 30:106–110

    Article  Google Scholar 

  • Huey RB, Bennett AF (1987) Phylogenetic studies of coadaptation—preferred temperatures versus optimal performance temperatures of lizards. Evolution 41:1098–1115

    Article  Google Scholar 

  • Irschick DJ (2003) Studying performance in nature: implications for fitness variation within populations. Int Comp Biol 43:36–47

    Google Scholar 

  • Irschick DJ, Garland T Jr (2001) Integrating function and ecology in studies of adaptation: studies of locomotor capacity as a model system. Annu Rev Ecol Syst 32:367–396

    Article  Google Scholar 

  • Irschick DJ, Bocchi S, Full RJ (2002) Does power limit climbing performance? Loading small climbing lizards. Am Zool 41:15.1

    Google Scholar 

  • Irschick DJ, Vanhooydonck B, Herrel A, Androsceu A (2003) Effects of loading and size on maximum power output and kinematics in geckos. J Exp Biol 206:3923–3934

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Irschick DJ, Austin CC, Petren K, Fisher RN, Losos JB, Ellers O (1996) A comparative analysis of clinging ability among pad-bearing lizards. Biol J Linn Soc 59:21–35

    Article  Google Scholar 

  • Lauder GV (1990) Functional morphology and systematics: studying functional patterns in a historical context. Annu Rev Ecol Syst 21:317–340

    Article  Google Scholar 

  • Lauder GV, Reilly SM (1996) The mechanistic basis of behavioral evolution: comparative analysis of muscoskeletal function. In Martins E (ed). Phylogenies and the comparative method in animal behavior. Oxford University Press, Oxford

  • Leal MA, Knox K, Losos JB (2002) Lack of convergence in aquatic Anolis lizards. Evolution 56:785–791

    Article  PubMed  Google Scholar 

  • Losos JB (1990a) Thermal sensitivity of sprinting and clinging performance in the Tokay gecko (Gekko gecko). Asiatic Herp Res 3:54–59

    Google Scholar 

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

    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, Miles DB (1994) Adaptation, constraint, and the comparative method: phylogenetic issues and methods. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. Chicago University Press, Chicago

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Macrini TE, Irschick DJ, Losos JB (2003) Ecomorphological differences in toepad characteristics between mainland and island anoles. J Herp 37:52–58

    Article  Google Scholar 

  • Peterson JA, Williams EE (1981) A case of retrograde evolution: the onca lineage in anoline lizards II. Subdigital fine structure. Bull Mus Comp Zool 149:215–268

    Google Scholar 

  • Pough FH (1989) Organismal performance and Darwinian fitness: approaches and interpretations. Phys Zool 62:199–236

    Google Scholar 

  • Roughgarden J (1995) Anolis lizards of the Caribbean: ecology, evolution, and plate tectonics. Oxford University Press, New York

    Google Scholar 

  • Ruibal R, Ernst V (1965) The structure of digital setae of lizards. J Morph 117:271–294

    Article  PubMed  CAS  Google Scholar 

  • Russell AP (1975) A contribution to the functional analysis of the foot of the Tokay, Gekko gecko (Reptilia: Gekkonidae). J Zool Lond 176:437–476

    Article  Google Scholar 

  • Russell AP (1979) Parallelism and integrated design in the foot structure of gekkonine and diplodactyline geckos. Copeia 1979:1–21

    Article  Google Scholar 

  • Russell AP, Bauer AM (1989) The morphology of the digits of the golden gecko, Calodactylus aureus and its implications for the occupation of rupicolous habitats. Amphib Reptil 10:125–140

    Google Scholar 

  • Russell AP, Bels V (2001) Digital hyperextension in Anolis sagrei. Herpetologica 57:58–65

    Google Scholar 

  • Schluter D, Ricklefs RE (1993) Species diversity in ecological communities. Chicago University Press, Chicago

    Google Scholar 

  • Smith R.J (1999) Statistics of sexual dimorphism. J Hum Evol 36:423–459

    Article  PubMed  CAS  Google Scholar 

  • Spoonberg S, Hansen W, Peattie A, Autumn K (2001) Dynamics of isolated gecko setal arrays. Am Zool 41:1594

    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 

  • Vanhooydonck B, Andronescu A, Herrel A, Irschick DJ (2005) Effects of substrate structure on speed and acceleration capacity in climbing geckos. Biol J Linn Soc 85:385–393

    Article  Google Scholar 

  • Vitt LJ, Congdon JD (1978) Body shape, reproductive effort, and relative clutch mass in lizards: resolution of a paradox. Am Nat 112:595–608

    Article  Google Scholar 

  • Wainwright PC (1994) Functional morphology as a tool in ecological research. In: Wainwright PC, Reilly SM (eds). Ecological morphology: integrative organismal biology. Chicago University Press, Chicago

    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

    Google Scholar 

  • Williams EE, Peterson JA (1982) Convergent and alternative designs in the digital adhesive pads of scincid lizards. Science 215:1509–1511

    Article  PubMed  Google Scholar 

  • Williams TM, Haun JE, Friedl WA (1999) The diving physiology of bottlenose dolphins (Tursiops truncates). I. Balancing the demands of exercise for energy conservation at depth. J Exp Biol 202:2739–2748

    PubMed  CAS  Google Scholar 

  • Zani PA (2000) The comparative evolution of lizard claw and toe morphology and clinging performance. J Evol Biol 13:316–325

    Article  Google Scholar 

  • Zani PA (2001) Clinging performance of the western fence lizard, Sceloporus occidentalis. Herpetologica 57:423–432

    Google Scholar 

Download references

Acknowledgements

We thank Jon Barnes for inviting us to participate in this symposium on adhesion at the International Congress of Vertebrate Morphology. Two reviewers made helpful comments on previous versions of this manuscript. This work was supported by NSF grants to D. Irschick (IBN 9983003 and IOB 0421917). AH and BVH are postdoctoral fellows of the fund for scientific research, Flanders, Belgium (FWO-Vl). All experiments were carried out in accordance with an approved animal use protocol (IACUC 0189-2-16-0301).

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Correspondence to Duncan J. Irschick.

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Irschick, D.J., Herrel, A. & Vanhooydonck, B. Whole-organism studies of adhesion in pad-bearing lizards: creative evolutionary solutions to functional problems. J Comp Physiol A 192, 1169–1177 (2006). https://doi.org/10.1007/s00359-006-0145-2

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