From micro to macroevolution: drivers of shape variation in an island radiation of Podarcis lizards.
Bite force
diet
geometric morphometrics
head shape
intraspecific variation
island
lizards
sexual competition
Journal
Evolution; international journal of organic evolution
ISSN: 1558-5646
Titre abrégé: Evolution
Pays: United States
ID NLM: 0373224
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
revised:
16
07
2021
received:
12
01
2021
accepted:
21
07
2021
pubmed:
13
8
2021
medline:
21
12
2021
entrez:
12
8
2021
Statut:
ppublish
Résumé
Phenotypictraits have been shown to evolve in response to variation in the environment. However, the evolutionary processes underlying the emergence of phenotypic diversity can typically only be understood at the population level. Consequently, how subtle phenotypic differences at the intraspecific level can give rise to larger-scale changes in performance and ecology remains poorly understood. We here tested for the covariation between ecology, bite force, jaw muscle architecture, and the three-dimensional shape of the cranium and mandible in 16 insular populations of the lizards Podarcis melisellensis and P. sicula. We then compared the patterns observed at the among-population level with those observed at the interspecific level. We found that three-dimensional head shape as well as jaw musculature evolve similarly under similar ecological circumstances. Depending on the type of food consumed or on the level of sexual competition, different muscle groups were more developed and appeared to underlie changes in cranium and mandible shape. Our findings show that the local selective regimes are primary drivers of phenotypic variation resulting in predictable patterns of form and function. Moreover, intraspecific patterns of variation were generally consistent with those at the interspecific level, suggesting that microevolutionary variation may translate into macroevolutionary patterns of ecomorphological diversity.
Banques de données
Dryad
['10.5061/dryad.b5mkkwhdn']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2685-2707Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2021 The Authors. Evolution © 2021 The Society for the Study of Evolution.
Références
Adams, D. C., and E. Otárola-Castillo. 2013. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4:393-399.
Adams, D. C., Rohlf, F. J., and Slice, D. E. 2013. A field comes of age: geometric morphometrics in the 21st century. Hystrix 24(1): 7.
Altshuler, D. L., J. W. Bahlman, R. Dakin, A. H. Gaede, B. Goller, D. Lentink, P. S. Segre, and D. A. Skandalis. 2015. The biophysics of bird flight: functional relationships integrate aerodynamics, morphology, kinematics, muscles, and sensors. Can. J. Zool. 93:961-975.
Baeckens, S., and R. Van Damme. 2020. The island syndrome. Curr. Biol. 30:338-339.
Barel, C. D., G. C. Anker, F. Witte, R. J. Hoogerhoud, and T. Goldschmidt. 1989. Constructional constraint and its ecomorphological implications. Acta Morphol. Neerl. Scand. 27:83-109.
Bergmann, P. J., and E. J. McElroy. 2014. Many-to-many mapping of phenotype to performance: an extension of the F-matrix for studying functional complexity. Evolutionary Biology 41:546-560.
Blount, Z. D., Lenski, R. E., and Losos, J. B. 2018. Contingency and determinism in evolution: Replaying life’s tape. Science 362:6415.
Boag, P. T., and P. R. Grant. 1981. Intense natural selection in a population of Darwin's finches (Geospizinae) in the Galapagos. Science 214:82-85.
Bookstein, F. L. 1997. Morphometric tools for landmark data: geometry and biology Cambridge University Press.
Calsbeek, R., J. H. Knouft, and T. B. Smith. 2006. Variation in scale numbers is consistent with ecologically based natural selection acting within and between lizard species. Evolutionary Ecology 20:377-394.
Campbell-Staton, S. C., Z. A. Cheviron, N. Rochette, J. Catchen, J. B. Losos, and S. V. Edwards. 2017. Winter storms drive rapid phenotypic, regulatory, and genomic shifts in the green anole lizard. Science 357:495-498.
Cardini, A. 2016. Lost in the other half: improving accuracy in geometric morphometric analyses of one side of bilaterally symmetric structures. Syst. Biol. 65:1096-1106.
Cardini, A. 2017. Left, right or both? Estimating and improving accuracy of one-side-only geometric morphometric analyses of cranial variation. Journal of Zoological Systematics and Evolutionary Research 55:1-10.
Cornette, R., A. Tresset, and A. Herrel. 2015. The shrew tamed by Wolff's law: Do functional constraints shape the skull through muscle and bone covariation? J. Morphol. 276:301-309.
Currey, J. D. 2002. The structure of bone tissue. In: J. D. Currey, ed. Bones: Structure and mechanics. Princeton University Press, New Jersey, USA, 3-26.
Cheverud, J. M. 1982. Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution 36:499-516.
Da Silva, F. O., A. C. Fabre, Y. Savriama, J. Ollonen, K. Mahlow, A. Herrel, J. Müller, and N. Di-Poï. 2018. The ecological origins of snakes as revealed by skull evolution. Nat. Commun. 9:1-11.
D'Arcy, T. 1942. On growth and form. Cambridge University Press.
Donihue, C. M., K. M. Brock, J. Foufopoulos, and A. Herrel. 2016. Feed or fight: testing the impact of food availability and intraspecific aggression on the functional ecology of an island lizard. Functional Ecology 30:566-575. https://doi.org/10.1111/1365-2435.12550
Donihue, C. M., A. Herrel, A. C. Fabre, A. Kmath, A. J. Geneva, T. W. Schoener, J. J. Kolbe, and J. B. Losos. 2018. Hurricane-induced selection on the morphology of an island lizard. Nature 560:88-92.
Ellner, S., N. G. Hairstone, C. M. Kearns, and D. Babaï. 1999. The roles of fluctuating selection and long-term diapause in microevolution of diapause timing in a fresh-water copepod. Evolution 53:111-122.
Fabre, A. C., D. V. Andrade, K. Huyghe, R. Cornette, and A. Herrel. 2014a. Interrelationships between bones, muscles, and performance: biting in the lizard Tupinambis merianae. Evolutionary Biology 41:518-527.
Fabre, A. C., C. Bardua, M. Bon, J. Clavel, R. N. Felice, J. W. Streicher, J. Bonnel, E. L. Stanley, D. C. Blackburn, and A. Goswami. 2020. Metamorphosis shapes cranial diversity and rate of evolution in salamanders. Nature Ecology and Evolution 4:1129-1140.
Fabre, A. C., R. Cornette, K. Huyghe, D. V. Andrade, and A. Herrel. 2014b. Linear versus geometric morphometric approaches for the analysis of head shape dimorphism in lizards. J. Morphol. 275:1016-1026.
Fabre, A. C., C. Dowling, R. Portela Miguez, V. Fernandez, E. Noirault, and A. Goswami. 2021. Functional constraints during development limit jaw shape evolution in marsupials. Proceedings of the Royal Society B 288:20210319.
Fabre, A. C., J. M. Perry, A. Hartstone-Rose, A. Lowie, A. Boens, and M. Dumont. 2018. Do muscles constrain skull shape evolution in Strepsirrhines? Anat. Rec. 301:291-310.
Felsenstein, J. 1985. Phylogenies and the Comparative Method. The American Naturalist 125(1):1-15.
Fish, F. E. 1998. Comparative kinematics and hydrodynamics of odontocete cetaceans: morphological and ecological correlates with swimming performance. J. Exp. Biol. 201:2867-2877.
Fish, F. E., L. E. Howle, and M. M. Murray. 2008. Hydrodynamic flow control in marine mammals. Integr. Comp. Biol. 48:788-800.
Gibbs, H. L., and P. R. Grant. 1987. Oscillating selection on Darwin's finches. Nature 327:511-513.
Goodwin, B. C., and L. E. H. Trainor. 1980. A field description of the cleavage process in embryogenesis. J. Theor. Biol. 85:757-770.
Gould, S. J. 1989. In: “A wonderful life: The Burgess Shale and the Nature of History”. WW Norton and Company, USA.
Gould, S. J., and R. C. Lewontin. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the royal society of London Series B Biological Sciences 205:581-598.
Grant, P. R., and B. R. Grant. 2006. Evolution of character displacement in Darwin's finches. Science 313:224-226.
Gunz, P., and P. Mitteroecker. 2013. Semilandmarks: a method for quantifying curves and surfaces. Hystrix, the Italian journal of mammalogy 24:103-109.
Gunz, P., P. Mitteroecker, and F. L. Bookstein. 2005. Semilandmarks in three dimensions. In D. E. Slice, ed. Modern morphometrics in physical anthropology, Springer, Boston, MA, 73-98.
Haines, R. W.. 1969. Epiphyses and sesamoids. Biology of the Reptilia, 1, 3:81-115.
Hairstone, N. G., and T. A. Dillon. 1990. Fluctuating selection and response in a population of freshwater copepods. Evolution 44:1796-1805.
Hall, J. M., and Warner, D. A. 2017. Body size and reproduction of a non-native lizard are enhanced in an urban environment. Biological Journal of the Linnean Society 122(4):860-871.
Hedenström, A. 2002. Aerodynamics, evolution and ecology of avian flight. Trends Ecol. Evol. 17:415-422.
Hedenström, A., and L. C. Johansson. 2015. Bat flight: aerodynamics, kinematics and flight morphology. J. Exp. Biol. 218:653-663.
Herrel, A., P. Aerts, and F. De Vree. 1998. Static biting in lizards: functional morphology of the temporal ligaments. J. Zool. 244:135-143.
Herrel, A., L. Spithoven, R. Van Damme, and F. De Vree. 1999a. Sexual dimorphism of head size in Gallotia galloti: testing the niche divergence hypothesis by functional analyses. Functional Ecology 13:289-297.
Herrel, A., E. D. De Grauw, and J. A. Lemos-Espinal. 2001. Head shape and bite performance in Xenosaurid lizards. J. Exp. Zool. 290:101-107.
Herrel, A., R. Joachim, B. Vanhooydonck, and D. J. Irschick. 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.
Herrel, A., L. D. McBrayer, and P. M. Larson. 2007. Functional basis for sexual differences in bite force in the lizard Anolis carolinensis. Biol. J. Linn. Soc. 91:111-119.
Herrel, A., J. Podos, B. Vanhooydonck, and A. P. Hendry. 2009. Force-velocity trade-off in Darwin's finch jaw function: a biomechanical basis for ecological speciation? Functional Ecology 23:119-125.
Herrel, A., J. A. Moore, E. M. Bredeweg, and N. J. Nelson. 2010. Sexual dimorphism, body size, bite force and male mating success in Tuatara. Biol. J. Linn. Soc. 100:287-292.
Herrel, A., M. Verstappen, and F. De Vree. 1999b. Modulatory complexity of the feeding repertoire in scincid lizards. Journal of Comparative Physiology A 184:501-518.
Huyghe, K., A. Herrel, D. Adriaens, Z. Tadić, and R. Van Damme. 2009. 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.
Itescu, Y., Foufopoulos, J., Pafilis, P., and Meiri, S. 2019. The diverse nature of island isolation and its effect on land bridge insular faunas. Global Ecology and Biogeography 29(2):262-280.
Kaliontzopoulou, A. 2011. Geometric morphometrics in herpetology: modern tools for enhancing the study of morphological variation in amphibians and reptiles. Basic and Applied Herpetology 25:5-32.
Kaliontzopoulou, A., M. A. Carretero, and G. A. Llorente. 2010. Intraspecific ecomorphological variation: linear and geometric morphometrics reveal habitat-related patterns within Podarcis bocagei wall lizards. Journal Evolutionary Biology 23:1234-1244.
Kaliontzopoulou, A., C. Pinho, and F. Martinez-Freiria. 2018. Where does diversity come from? Linking geographical patterns of morphological, genetic, and environmental variation in wall lizards. BMC Evol. Biol. 18:124-136.
Klingenberg, C. P. 2002. Morphometrics and the role of the phenotype in studies of the evolution of developmental mechanisms. Gene 287:3-10.
Klingenberg, C. P. 2011. MorphoJ: an integrated software package for geometric morphometrics. Mol. Ecol. Resour. 11:353-357.
Kueffer, C., D. R. Drake, and J. M. Fernández-Palacios. 2014. Island biology: looking towards the future. Biol. Lett. 10:20140719.
Lande, R. 1976. Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314-334.
Lappin, A. K., P. S. Hamilton, and B. K. Sullivan. 2006. Bite-force performance and head shape in a sexually dimorphic crevice-dwelling lizard, the common chuckwalla [Sauromalus ater ( = obesus)]. Biol. J. Linn. Soc. 88:215-222.
Lappin, A. K., and J. F. Husak. 2005. Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris). Am. Nat. 166:426-436.
Lomolino, M. V. 2005. Body size evolution in insular vertebrates: generality of the island rule. Journal of Biogeography 32(10):1683-1699.
Lopez-Darias, M., B. Vanhooydonck, R. Cornette, and A. Herrel. 2015. Sex-specific differences in ecomorphological relationships in lizards of the genus Gallotia. Functional Ecology 29:506-514.
Losos, J. B. 1990. Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: an evolutionary analysis. Ecological Monographs 60:369-388.
Losos, J. B. 2009. Lizards in an evolutionary tree. Ecology and Adaptive radiation of Anoles. University of California Press, CA.
Losos, J. B., and R. E. Ricklefs. 2009. Adaptation and diversification on islands. Nature 457:830-836.
Marroig, G., and J. M. Cheverud. 2005. Size as a line of least evolutionary resistance: diet and adapative morphological radiation in New World Monkeys. Evolution 59:1128-1142.
Martin, R. D., and C. F. Ross. 2005. The evolutionary and ecological context of primate vision. In J. Kremers, ed. The primate visual system: A comparative approach, John Wiley & Sons, Ltd 1-36.
McGlothlin, J. W., M. E. Kobiela, H. V. Wright, D. L. Mahler, J. J. Kolbe, J. B. Losos, and E. D. Brodie III. 2018. Adaptive radiation along a deeply conserved genetic line of least resistance in Anolis lizards. Evolution Letters 4:310-322.
Meiri, S. 2008. Evolution and ecology of lizard body sizes. Global Ecol. Biogeogr. 17:724-734.
Mendez, J., A. Keys, J. T. Anderson, and F. Grande. 1960. Density of fat and bone mineral of the mammalian body. Metabolism 9:472-477.
Novosolov, M., and Meiri, S. 2013. The effect of island type on lizard reproductive traits. Journal of Biogeography 40(12):2385-2395.
Novosolov, M., Rodda, G. H., Feldman, A., Kadison, A. E., Dor, R., and Meiri, S. 2016. Power in numbers. Drivers of high population density in insular lizards. Global Ecology and Biogeography 25(1):87-95.
Pigliucci, M., and J. Kaplan. 2000. The fall and rise of Dr Pangloss: adaptationism and the Spandrels paper 20 years later. Trends Ecol. Evol. 15:66-70.
R Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: https://www.R-project.org/.
Rieppel, O., and R. W. Gronowski. 1981. The loss of the lower temporal arcade in diapsid reptiles. Zoological Journal of the Linnean Society 72:203-217.
Reilly, S. M., D. B. Miles, and L. D. McBrayer. 2007. The evolution of foraging mode paradigm in lizard ecology. In S. M. Reilly, L. D. McBrayer, D. B. Miles, eds. In Lizard Ecology, The evolutionary consequences of foraging mode, 17, Cambridge University Press.
Renaud, S., J. C. Auffray, and S. De la Porte. 2010. Epigenetic effects on the mouse mandible: common features and discrepancies in remodelling due to muscular dystrophy and response to food consistency. BMC Evol. Biol. 10:28.
Renaud, S., S. Pantalacci, and J. C. Auffray. 2011. Differential evolvability along lines of least resistance of upper and lower molars in island house mice. PlosOne 6:e18951.
Rodrigues, H. G., R. Šumbera, and L. Hautier. 2015. Life in burrows channeled the morphological evolution of the skull in rodents: the case of African Mole-Rats (Bathyergidae, Rodentia). Journal of Mammalian Evolution 23:175-189.
Roscito, J. G., and M. T. Rodrigues. 2010. Comparative cranial osteology of fossorial lizards from the tribe Gymnophthalmini (Squamata, Gymnophthalmidae). J. Morphol. 271:1352-1365.
Sagnes, P., P. Gaudin, and B. Statzner. 1997. Shifts in morphometrics and their relation to hydrodynamic potential and habitat use during grayling ontogenesis. J. Fish Biol. 50:846-858.
Sagonas, K., P. Pafilis, P. Lymberakis, C. M. Donihue, A. Herrel, and E. D. Valakos. 2014. Insularity affects head morphology, bite force and diet in a Mediterranean lizard. Biol. J. Linn. Soc. 112:469-484. https://doi.org/10.1111/bij.12290
Schoener, T. W.. 1967. The ecological significance of sexual dimorphism in size in the lizard Anolis conspersus. Science 155:474-477.
Schlager, S. 2013. Morpho: Calculations and visualisations related to Geometric Morphometrics. R package version 0.23 3:195-220.
Schluter, D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50:1766-1774.
Schluter, D. 2000. The ecology of adaptive radiation. Oxford Univ. Press, Oxford, U.K.
Segall, M., A. Herrel, and R. Godoy-Diana. 2019. Hydrodynamics of frontal striking in aquatic snakes: drag, added mass, and the possible consequences for prey capture success. Bioinspiration Biomimetics 14:036005.
Segall, M., R. Cornette, R. Godoy-Diana, and A. Herrel. 2020. Exploring the functional meaning of head shape disparity in aquatic snakes. BioRxiv (preprint).
Stuart, Y. E., T. S. Campbell, P. A. Hohenlohe, R. G. Reynolds, L. J. Revell, and J. B. Losos. 2014. Rapid evolution of a native species following invasion by a congener. Science 346:463-466.
Taverne, M., A. C. Fabre, N. King-Gillies, L. D. Krajnović, L. Martin, L. Michal, D. Petricioli, A. Štambuk, Z. Tadić, C. Vigliotti, et al. 2019. Diet variability among insular populations of Podarcis lizards reveals diverse strategies to face resource-limited environments. Ecology and Evolution 9:12408-12420.
Taverne, M., N. King-Gillies, L. D. Krajnović, O. Mira, D. Petricioli, I. Sabolić, A. Štambuk, Z. Tadić, C. Vigliotti, B. A. Wehrle, et al. 2020. Proximate and ultimate drivers of variation in bite force in the insular lizards Podarcis melisellensis and Podarcis sicula. Biol. J. Linn. Soc. 131:88-108.
Urošević, A., K. Ljubisavljević, D. Jelić, and A. Ivanović. 2012. Variation in the cranium shape of wall lizards (Podarcis spp.): effects of phylogenetic constraints, allometric constraints and ecology. Zoology 115:207-216.
Vanhooydonck, B., F. B. Cruz, C. S. Abdala, D. B. Moreno Azocar, M. F. Bonino, and A. Herrel. 2010. Sex-specific evolution of bite performance in Liolaemus lizards (Iguania: Liolaemidae): the battle of the sexes. Biol. J. Linn. Soc. 101:461-475.
Verwaijen, D., R. Van Damme, and A. Herrel. 2002. Relationships between head size, bite force, prey handling efficiency and diet in two sympatric lacertid lizards. Functional Ecology 16:842-850.
Wake, M. H. 2003. The skull as a locomotor organ. In J. Hanken & B. K. Hall, eds. The skull. University of Chicago Press.
Wake, D. B., G. Roth. 1989. In D. B. Wake, G. Roth, eds. Complex organismal functions: integration and evolution in vertebrates. John Wiley & Sons, Chichester, UK.
Wittorski, A., J. B. Losos, and A. Herrel. 2016. Proximate determinants of bite force in Anolis lizards. J. Anat. 228:85-95.
Whittaker, R. J., Fernandez-Palacios, J. M., Matthews, T. J., Borregaard, M. K., and Triantis, K. A. 2017. Island biogeography: taking the long view of nature's laboratories. Science 357:885.
Zweers, G. A. 1979. Explanation of structure by optimization and systematization. Netherlands Journal of Zoology 29:418-440.