Correlated evolution of microhabitat, morphology, and behavior in West Indian Anolis lizards: a test of the habitat matrix model

in Behaviour
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

The habitat matrix model (HMM) explains convergence among arboreal animals as a result of the correlated evolution of morphology, locomotor mode, and habitat use. Although the HMM has generated important insights into the ecology of arboreal species, these tests have left a gap in the habitat-behavior-morphology story by focusing primarily on locomotor performance in lab and field experiments and thus failing to include data on locomotor behavior of undisturbed animals in the wild. We combined data on undisturbed locomotion, habitat use, and morphology for 31 species of arboreal lizard in the genus Anolis and used these data to test nine specific predictions arising from the HMM. We find strong support for nearly all aspects of this model. The addition of data on locomotion by undisturbed wild animals offers a more direct and compelling case for the HMM than most previous tests.

Sections

References

BeuttellK.LososJ.B. (1999). Ecological morphology of Caribbean anoles. — Herpetol. Monogr. 13: 1-28.

BickelR.LososJ.B. (2002). Patterns of morphological variation and correlates of habitat use in chameleons. — Biol. J. Linn. Soc. 76: 91-103.

ButlerM.A.LososJ.B. (2002). Multivariate sexual dimorphism, sexual selection, and adaptation in Greater Antillean Anolis lizards. — Ecol. Monogr. 72: 541-559.

ButlerM.A.SchoenerT.W.LososJ.B. (2000). The relationship between sexual size dimorphism and habitat use in Greater Antillean Anolis lizards. — Evolution 54: 259-272.

Conway MorrisS. (2003). Life’s solution: inevitable humans in a lonely universe. — Cambridge University Press, Cambridge.

CromptonR.H. (1984). Foraging, habitat structure, and locomotion in two species of Galago. — In: Adaptations for foraging in non-human primates ( RodmanP.S.CantJ.G.H., eds). Columbia University Press, New York, NY, p.  73-111.

EssnerR.L. (2007). Morphology, locomotor behavior and microhabitat use in North American squirrels. — J. Zool. 272: 101-109.

FelsensteinJ. (1985). Phylogenies and the comparative method. — Am. Nat. 125: 1-15.

FreckletonR.P.HarveyP.H.PagelM. (2002). Phylogenetic analysis and comparative data: a test and review of evidence. — Am. Nat. 160: 712-726.

FutuymaD.J. (1997). Evolutionary biology. — Sinauer Associates, Sunderland, MA.

GarlandT.Jr.IvesA.R. (2000). Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. — Am. Nat. 155: 346-364.

GillisG.B.BonviniL.A.IrschickD.J. (2009). Losing stability: tail loss and jumping in the arboreal lizard Anolis carolinensis. — J. Exp. Biol. 212: 604-609.

GoodmanB.A.MilesD.B.SchwarzkopfL. (2008). Life on the rocks: habitat use drives morphological and performance evolution in lizards. — Ecology 89: 3462-3471.

HarmonL.J.KolbeJ.J.CheverudJ.M.LososJ.B. (2005). Convergence and the multidimensional niche. — Evolution 59: 409-421.

HarveyP.H.PagelM.D. (1991). The comparative method in evolutionary biology. Oxford series in ecology and evolution, Vol. 1. — Oxford University Press, Oxford.

HerrelA.MeyersJ.J.VanhooydonckB. (2001). Correlations between habitat use and body shape in a phrynosomatid lizard (Urosaurus ornatus): a population-level analysis. — Biol. J. Linn. Soc. 74: 305-314.

IrschickD.J.JayneB.C. (1999). Comparative three-dimensional kinematics of the hindlimb for high-speed bipedal and quadrupedal locomotion of lizards. — J. Exp. Biol. 202: 1047-1065.

IrschickD.J.LososJ.B. (1998). A comparative analysis of the ecological significance of maximal locomotor performance in Caribbean Anolis lizards. — Evolution 52: 219-226.

IrschickD.J.LososJ.B. (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.

JohnsonM.A.LealM.Rodríguez SchettinoL.Chamizo LaraA.RevellL.J.LososJ.B. (2008). A phylogenetic perspective on foraging mode evolution in West Indian Anolis lizards. — Anim. Behav. 75: 555-563.

KohlsdorfT.GarlandT.Jr.NavasC.A. (2001). Limb and tail lengths in relation to substrate usage in Tropidurus lizards. — J. Morphol. 248: 151-164.

LegreneurP.LaurinM.MonteilK.M.BelsV. (2012). Convergent exaptation of leap up for escape in distantly related arboreal amniotes. — Adapt. Behav. 20: 67-77.

LososJ.B. (1990a). Concordant evolution of locomotor behavior, display rate, and morphology in West Indian Anolis lizards. — Anim. Behav. 39: 879-890.

LososJ.B. (1990b). Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: an evolutionary analysis. — Ecol. Monogr. 60: 369-388.

LososJ.B. (1990c). A phylogenetic analysis of character displacement in Caribbean Anolis lizards. — Evolution 44: 558-569.

LososJ.B. (1990d). The evolution of form and function: morphology and locomotor performance in West Indian Anolis lizards. — Evolution 44: 1189-1203.

LososJ.B. (2009). Lizards in an evolutionary tree: ecology and adaptive radiation of anoles, Vol. 10. — University of California Press, Berkeley, CA.

LososJ.B. (2011). Convergence, adaptation, and constraint. — Evolution 65: 1827-1840.

LososJ.B.IrschickD.J. (1996). The effect of perch diameter on escape behavior of Anolis lizards: laboratory predictions and field tests. — Anim. Behav. 51: 593-602.

LososJ.B.JackmanT.R.LarsonA.de QueirozK.Rodríguez-SchettinoL. (1998). Contingency and determinism in replicated adaptive radiations of island lizards. — Science 279: 2115-2118.

LososJ.B.SinervoB. (1989). The effect of morphology and perch diameter on sprint performance of Anolis lizards. — J. Exp. Biol. 145: 23-30.

MartinsE.P.HansenT.F. (1997). Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. — Am. Nat. 149: 646-667.

MattinglyW.B.JayneB.C. (2004). Resource use in arboreal habitats: structure affects locomotion of four ecomorphs of Anolis lizards. — Ecology 85: 1111-1124.

MayerG.C. (1989). Deterministic patterns of community structure in West Indian reptiles and amphibians. — PhD dissertation, Harvard University, Cambridge, MA.

MilesD.B.RicklefsR. (1984). The correlation between ecology and morphology in deciduous forest passerine birds. — Ecology 65: 629-1640.

MoermondT.C. (1979a). The influence of habitat structure on Anolis foraging behavior. — Behaviour 70: 147-167.

MoermondT.C. (1979b). Habitat constraints on the behavior, morphology, and community structure of Anolis lizards. — Ecology 60: 152-164.

MoffettM.W. (2000). What’s “up”? A critical look at the basic terms of canopy biology. — Biotropica 32: 569-596.

MoffettM.W. (2001). The nature and limits of canopy biology. — Selbyana 22: 155-179.

MorenoE.CarrascalL.M. (1993). Leg morphology and feeding postures in four Parus species: an experimental ecomorphological approach. — Ecology 74: 2037-2044.

NicholsonK.E.GlorR.E.KolbeJ.J.LarsonA.HedgesS.B.LososJ.B. (2005). Mainland colonization by island lizards. — J. Biogeography 32: 929-938.

PagelM. (1999). Inferring the historical patterns of biological evolution. — Nature 401: 877-884.

ParadisE.ClaudeJ.StrimmerK. (2004). APE: analyses of phylogenetics and evolution in R language. — Bioinformatics 20: 289-290.

PoundsJ.A. (1988). Ecomorphology, locomotion, and microhabitat structure: patterns in a tropical mainland Anolis community. — Ecol. Monogr. 58: 299-320.

R Core Team (2013). R: a language and environment for statistical computing. — R Foundation for Statistical Computing, Vienna. Available online at http://www.R-project.org/.

RevellL.J. (2008). On the analysis of evolutionary change along single branches in a phylogeny. — Am. Nat. 172: 140-147.

RevellL.J. (2009). Size-correction and principal components for interspecific comparative studies. — Evolution 63: 3258-3268.

RevellL.J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). — Methods Ecol. Evol. 3: 217-223.

RevellL.J.HarmonL.J. (2008). Testing quantitative genetic hypotheses about the evolutionary rate matrix for continuous characters. — Evol. Ecol. Res. 10: 311-321.

RevellL.J.HarrisonA.S. (2008). PCCA: a program for phylogenetic canonical correlation analysis. — Bioinformatics 24: 1018-1020.

RohlfF.J. (2001). Comparative methods for the analysis of continuous variables: geometric interpretations. — Evolution 55: 2143-2160.

SchmittD.LemelinP. (2002). Origins of primate locomotion: gait mechanics of the woolly opossum. — Am. J. Phys. Anthropol. 118: 231-238.

SpezzanoL.C.JayneB.C. (2004). The effects of surface diameter and incline on the hindlimb kinematics of an arboreal lizard (Anolis sagrei). — J. Exp. Biol. 207: 2115-2131.

ToroE.HerrelA.IrschickD. (2004). The evolution of jumping performance in Caribbean Anolis lizards: solutions to biomechanical trade-offs. — Am. Nat. 163: 844-856.

ToroE.HerrelA.IrschickD.J. (2006). Movement control strategies during jumping in a lizard (Anolis valencienni). — J. Biomech. 39: 2014-2019.

VanhooydonckB.HerrelA.Van DammeR.IrschickD.J. (2006). The quick and the fast: the evolution of acceleration capacity in Anolis lizards. — Evolution 60: 2137-2147.

VanhooydonckB.Van DammeR.AertsP. (2000). Ecomorphological correlates of habitat partitioning in Corsican lacertid lizards. — Funct. Ecol. 14: 358-368.

WilliamsE.E. (1972). Evolution of lizard congeners in a complex island fauna: a trial analysis. — Evol. Biol. 6: 47-89.

WilliamsE.E. (1983). Ecomorphs, faunas, island size, and diverse end points in island radiations of Anolis. — In: Lizard ecology: studies of a model organism ( HueyR.B.PiankaE.R.SchoenerT.W., eds). Harvard University Press, Cambridge, MA, p.  326-370.

Figures

  • (a) In the first canonical correlation between habitat and behavior, species found on narrow perches tend to walk, as outlined in Prediction 4, while species found on broad perches tend to run (Prediction 7). (b) In the second canonical correlation between habitat and behavior, species living on dense, low perches, have a tendency to jump (Prediction 1).

    View in gallery
  • (a) In the first canonical correlation between behavior and morphology, species that walk frequently have shorter forelimbs and hindlimbs, consistent with Prediction 5 of the HMM. Walking species also have more lamellae. (b) In the second canonical correlation between behavior and morphology, species that jump and move infrequently have shorter forelimbs and longer tails, consistent with Prediction 2.

    View in gallery
  • (a) In the first canonical correlation between habitat and morphology, species that use narrow perches have shorter limbs (Prediction 6). (b) In the second canonical correlation between habitat and morphology, species that use dense, low perches tend to have longer hindlimbs and tails (Prediction 3), although this relationship is not significant in our dataset. This is true whether the unusual Anolis chamaeleolis is included or excluded from the analysis.

    View in gallery

Information

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 15 15 7
Full Text Views 4 4 4
PDF Downloads 2 2 2
EPUB Downloads 0 0 0