[en] Tetrapod limbs are serially homologous structures that represent a particularly interesting model for studies on morphological integration, i.e. the tendency of developmental systems to produce correlated variation. In newts, limbs develop at an early larval stage and grow continuously, including after the habitat transition from water to land following metamorphosis. However, aquatic and terrestrial environments impose different constraints and locomotor modes that could affect patterns of morphological integration and evolvability. We hypothesize that this would be the case for alternative heterochronic morphs in newts, i.e. aquatic paedomorphs that keep gills at the adult stage and adult metamorphs that are able to disperse on land. To this end, we analysed patterns and strengths of correlations between homologous skeletal elements of the fore- and hindlimbs as well as among skeletal elements within limbs in both phenotypes in the alpine newt, Ichthyosaura alpestris. Our results showed that metamorphs and paedomorphs had similar, general patterns of limb integration. Partial correlations between homologous limb elements and within limb elements were higher in paedomorphs when compared to metamorphs. Decrease in partial correlation between homologous limb elements in metamorphs is accompanied with a higher evolvability of the terrestrial morph. All these results indicate that environmental demands shaped the patterns of morphological integration of alpine newt limbs and that the observed diversity in correlation structure could be related to a qualitative difference in the modes of locomotion between the morphs.
Research Center/Unit :
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Disciplines :
Zoology
Author, co-author :
Tomašević, Natasa; University of Belgrade
Cvijanović, Milena; University of Belgrade
Denoël, Mathieu ; Université de Liège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Ivanović, Ana; University of Belgrade
Language :
English
Title :
Morphological integration and alternative life history strategies: a case study in a facultatively paedomorphic newt
Publication date :
2017
Journal title :
Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution
Arntzen JW, Beukema W, Galis F, Ivanović A. 2015. Vertebral number is highly evolvable in salamanders and newts (family Salamandridae) and variably associated with climatic parameters. Contr Zool 84:85–113.
Ashley-Ross MA, Bechtel BF. 2004. Kinematics of the transition between aquatic and terrestrial locomotion in the newt Taricha torosa. J Exp Biol 207:461–474.
Azizi E, Horton JM. 2004. Patterns of axial and appendicular movements during aquatic walking in the salamander Siren lacertina. Zoology 107:111–120.
Bell E, Andres B, Goswami A. 2011. Integration and dissociation of limb elements in flying vertebrates: a comparison of pterosaurs, birds and bats. J Evol Biol 24:2586–2599.
Biewener AA. 1990. Biomechanics of mammalian terrestrial locomotion. Science 250:1097.
Bininda-Emonds ORP, Jeffery JE, Sánchez-Villagra MR, et al. 2007. Forelimb-hindlimb developmental timing changes across tetrapod phylogeny. BMC Evol Biol 7:182.
Blanco JJ, Alberch P. 1992. Caenogenesis, developmental variability, and evolution in the carpus and tarsus of the marbled newt, Triturus marmoratus. Evolution 46:677–687.
Blob RW, Biewener AA. 1999. In vivo locomotor strain in the hindlimb bones of Alligator mississippiensis and Iguana iguana: implications for the evolution of limb bone safety factor and non-sprawling limb posture. J Exp Biol 202:1023–1046.
Cheverud JM. 1982. Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution 36:499–516.
Cheverud JM. 1988. A comparison of genetic and phenotypic correlations. Evolution 42:958–968.
Deban SM, Schilling N. 2009. Activity of trunk muscles during aquatic and terrestrial locomotion in Ambystoma maculatum. J Exp Biol 212:2949–2959.
Denoël M, Joly P. 2001. Adaptive significance of facultative paedomorphosis in Triturus alpestris (Amphibia, Caudata): resource partitioning in an alpine lake. Freshw Biol 46:1387–1396.
Denoël M, Schabetsberger R. 2003. Resource partitioning in two heterochronic populations of Greek Alpine newts, Triturus alpestris veluchiensis. Acta Oecol 24:55–64.
Denoël M, Schabetsberger R, Joly P. 2004. Trophic specialisations in alternative heterochronic morphs. Naturwissenschaften 91:81–84.
Denoël M, Joly P, Whiteman HH. 2005. Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biol Rev Camb Philos Soc 80:663–671.
Denoël M, Ivanović A, Džukić G, Kalezić ML. 2009. Sexual size dimorphism in the evolutionary context of facultative paedomorphosis: insights from European newts. BMC Evol Biol 9:278.
Denoël M. 2017. On the identification of paedomorphic and overwintering larval newts based on cloacal shape: review and guidelines. Curr Zool 63:165–173.
Dingerkus G, Uhler LD. 1977. Enzyme clearing of alcian blue stained whole small vertebrates for demonstration of cartilage. Stain Tech 52:229–232.
Diogo R, Linde-Medina M, Abdala V, Ashley-Ross MA. 2013. New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma. Biol Rev 88:196–214.
Diogo R, Ziermann JM. 2014. Development of fore-and hindlimb muscles in frogs: morphogenesis, homeotic transformations, digit reduction, and the forelimb–hindlimb enigma. J Exp Zool B 322:86–105.
Džukić G, Kalezić ML, Tvrtković N, Djorović A. 1990. An overview of the occurrence of paedomorphosis in Yugoslav newt (Triturus, Salamandridae) populations. Brit Herp Soc Bull 34:16–22.
Džukić G, Cvijanović M, Urošević A, et al. 2015. The Batrachological collection of the Institute for Biological research “Siniša Stanković”, University of Belgrade. Bull Nat Hist Mus 8:118–167.
Fischer-Rousseau L, Cloutier R, Zelditch ML. 2009. Morphological integration and developmental progress during fish ontogeny in two contrasting habitats. Evol Dev 11:740–753.
Frolich LM, Biewener AA. 1992. Kinematic and electromyographic analysis of the functional role of the body axis during terrestrial and aquatic locomotion in the salamander Ambystoma tigrinum. J Exp Biol 162:107–130.
Frost H. 1988. Vital biomechanics: proposed general concepts for skeletal adaptations to mechanical usage. Calcif Tissue Int 42:145–156.
Glücksohn S. 1932. Aussere Entwicklung der Extremitaten und Stadien einteilung der Larvenperiode von Triton taeniatus Leyd. und Triton cristatus Laur. Wilhelm Roux Arch Entwickl Org 125:341–405.
Goswami A. 2006. Morphological integration in the carnivoran skull. Evolution 60:169–183.
Goswami A, Polly PD. 2010. Methods for studying morphological integration and modularity. In: Alroy J, Hunt G, editors. Quantitative methods in paleobiology. Ithaca, NY: Paleontological Society. p. 213–243.
Gould SJ. 1977. Ontogeny and phylogeny. Cambridge, MA: Harvard University Press.
Gvoždik L, Van Damme R. 2006. Triturus newts defy the running-swimming dilemma. Evolution 60:2110–2121.
Hall BK. 1995. Homology and embryonic development. In: Hecht M, Macintyre RJ, Clegg MT, editors. Evolutionary biology. New York: Springer. p. 1–37.
Hall BK. 2005. Bones and cartilage: developmental and evolutionary skeletal biology. San Diego, CA: Academic Press.
Hallgrímsson B, Willmore K, Hall BK. 2002. Canalization, developmental stability, and morphological integration in primate limbs. Am J Phys Anthropol 119:131–158.
Hallgrímsson B, Jamniczky H, Young NM, et al., 2009. Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol Biol 36:355–376.
Hansen TF, Houle D. 2008. Measuring and comparing evolvability and constraint in multivariate characters. J Evol Biol 21:1201–1219.
Hood G. 2004. Poptools, ver. 2.62. CSIRO, Canberra, Australia. http://www.poptools.org (Accessed on 25 February 2004).
Ivanović A, Kalezić ML, Aleksić I. 2005. Morphological integration of cranium and postcranial skeleton during ontogeny of facultative paedomorphic European newts (Triturus vulgaris and alpestris). Amphibia-Reptilia 26:485–495.
Kalezić ML, Džukić G. 1986. The frequent occurrence of paedomorphosis in the smooth newt (Triturus vulgaris) population from the submediterranean area of Yugoslavia. Amphibia-Reptilia 7:86–89.
Kalezić ML, Cvetković D, Djorović A, Džukić G. 1996. Alternative life-history pathways: paedomorphosis and adult fitness in European newts (Triturus vulgaris and T. alpestris). J Zool Syst Evol Res 34:1–7.
Kelly EM, Sears KE. 2011. Reduced phenotypic covariation in marsupial limbs and the implications for mammalian evolution. Biol J Linn Soc 102:22–36.
Knight FCE. 1938. Die Entwicklung von Triton alpestris bei verschiedenen Temperaturen mit Normentafel. Wilhem Roux Archiv Entwickl Org 137:461–473.
Klingenberg CP. 2008. Morphological integration and developmental modularity. Annu Rev Ecol Evol S 39:115–132.
Klingenberg CP. 2014. Studying morphological integration and modularity at multiple levels: concepts and analysis. Phil Trans R Soc B 369:20130249.
Labonne G, Navarro N, Laffont R, Chateau-Smith C, Montuire S. 2014. Developmental integration in a functional unit: deciphering processes from adult dental morphology. Evol Dev 16:224–232.
Lande R. 1979. Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution 33:402–416.
Laudet V. 2011. The origins and evolution of vertebrate metamorphosis. Curr Biol 21:R726–R737.
Lawler RR. 2008. Morphological integration and natural selection in the postcranium of wild Verreaux's sifaka (Propithecus verreauxi verreauxi). Am J Phys Anthropol 136:204–213.
Lebedkina NS. 2004. Evolution of the amphibian skull. In: Kuzmin SL, editor. Advances in amphibian research in the former Soviet Union. vol. 9. Sofia, Bulgaria: Pensoft Publishers. p 1–239.
Lewton KL. 2012. Evolvability of the primate pelvic girdle. Evol Biol 39:126–139.
Lleonart J, Salat J, Torres GJ. 2000. Removing allometric effects of body size in morphological analysis. J Theor Biol 205:85–93.
Magwene PM. 2001. New tools for studying integration and modularity. Evolution 55:1734–1745.
Manly B. 1991. Randomization and Monte Carlo methods in biology. London: Chapman & Hall.
Margulies EH, Kardia SL, Innis JW. 2001. A comparative molecular analysis of developing mouse forelimbs and hindlimbs using serial analysis of gene expression (SAGE). Genome Res 11:1686-1698.
Marroig G, Cheverud JM. 2001. A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology and ontogeny during cranial evolution of new world monkeys. Evolution 55:2576–2600.
Marroig G, Cheverud JM. 2004. Cranial evolution in sakis (Pithecia, Platyrrhini) I: interspecific differentiation and allometric patterns. Am J Phys Anthropol 125:266–278.
Marroig G, Cheverud JM. 2005. Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World monkeys. Evolution 59:1128–1142.
Martin-Serra A, Figueirido B, Pérez-Claros JA, Palmqvist P. 2015. Patterns of morphological integration in the appendicular skeleton of mammalian carnivores. Evolution 69:321–340.
McNamara JM. 2012. Heterochrony: the evolution of development. Evo Edu Outreach 5:203–218.
Olson E, Miller R. 1958. Morphological integration. Chicago: University Chicago Press.
Oromi N, Michaux J, Denoël M. 2016. High gene flow between alternative morphs and the evolutionary persistence of facultative paedomorphosis. Sci Rep 6:32046.
Pavlicev M, Cheverud JM, Wagner GP. 2009. Measuring morphological integration using eigenvalue variance. Evol Biol 36:157–170.
Petit F, Sears KE, Ahituv N. 2017. Limb development: a paradigm of gene regulation. Nat Rev Genet 18:245–258.
Porto A, de Oliveira FB, Shirai LT, De Conto V, Marroig G. 2009. The evolution of modularity in the mammalian skull I: morphological integration patterns and magnitudes. Evol Biol 36:118–135.
Recuero E, Buckley D, García-París M, Arntzen JW, Cogălniceanu D, Martínez-Solano I. 2014. Evolutionary history of Ichthyosaura alpestris (Caudata, Salamandridae) inferred from the combined analysis of nuclear and mitochondrial markers. Mol Phylogenet Evol 81:207–220.
Rohlf FJ. 2005. TpsDig program, version 2.04, Ecology and Evolution, SUNY at Stony Brook. Available online at: http://life.bio.sunysb.edu/morph/. (Accessed on 7 February 2010).
Rolian C. 2009. Integration and evolvability in primate hands and feet. Evol Biol 36:100–117.
Schluter D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50:1766–1774.
Schmidt M, Fischer MS. 2009. Morphological integration in mammalian limb proportions: dissociation between function and development. Evolution 63:749–766.
Semlitsch RD, Wilbur HM. 1989. Artificial selection for paedomorphosis in the salamander Ambystoma talpoideum. Evolution 43:105–112.
Sheets HD. 2000. Integrated Morphometrics Package (IMP). http://www3.canisius.edu/sheets/morphsoft.html. (Accessed on 6 January 2010).
Sheffield KM, Blob RW. 2011. Loading mechanics of the femur in tiger salamanders (Ambystoma tigrinum) during terrestrial locomotion. J Exp Biol 214:2603–2615.
Shou S, Scott V, Reed C, Hitzemann R, Stadler HS. 2005. Transcriptome analysis of the murine forelimb and hindlimb autopod. Dev Dynam 234:74–89.
Shubin N, Alberch P. 1986. A morphogenetic approach to the origin and basic organization of the tetrapod limb. Evol Biol 20:319-387.
Steinfartz S, Vicario S, Arntzen JW, Caccone A. 2007. A Bayesian approach on molecules and behavior: reconsidering phylogenetic and evolutionary patterns of the Salamandridae with emphasis on Triturus newts. J Exp Zool B 308:139–162.
Smirnov SV, Vassilieva AB. 2003. Skeletal and dental ontogeny in the smooth newt, Triturus vulgaris (Urodela: Salamandridae): role of thyroid hormone in its regulation. Russ J Herpetol 10:93–110.
Tomašević Kolarov N, Ivanović A, Kalezić ML. 2011. Morphological integration and ontogenetic niche shift: a study of crested newt limbs. J Exp Zool B 316:296–305.
Vorobyeva EI, Hinchliffe JR. 1996. Developmental pattern and morphology of Salamandrella keyserlingii limbs (Amphibia, Hynobiidae) including some evolutionary aspects. Russ J Herpetol 3:68–81.
Wagner GP. 1984. On the eigenvalue distribution of genetic and phenotypic dispersion matrices - evidence for a nonrandom organization of quantitative character variation. J Math Biol 21:77–95.
Whitaker J. 1990. Graphical models in applied mathematical multivariate statistics. New York: Wiley
Whiteman HH. 1994. Evolution of facultative paedomorphosis in salamanders. Q Rev Biol 69:205–221.
Willis JH, Coyne JA, Kirkpatrick M. 1991. Can one predict the evolution of quantitative characters without genetics? Evolution 45:441–444.
Young NM, Hallgrímsson B. 2005. Serial homology and the evolution of mammalian limb covariation structure. Evolution 59:2691–2704.
Young NM, Hallgrímsson B, Garland T. 2009. Epigenetic effects on integration of limb lengths in a mouse model: selective breeding for high voluntary locomotor activity. Evol Biol 36:88.
Young NM, Wagner GP, Hallgrímsson B. 2010. Development and the evolvability of human limbs. Proc Natl Acad Sci U S A 107:3401–3405.
Zelditch ML, Lundrigan BL, Garland T. 2004. Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evol Dev 6:194–206.
