Neoteny and progenesis as two heterochronic processes involved in paedomorphosis in Triturus alpestris (Amphibia: Caudata)

Denoël, Mathieu; Joly, Pierre

doi:10.1098/rspb.2000.1168

Article (Scientific journals)

Neoteny and progenesis as two heterochronic processes involved in paedomorphosis in Triturus alpestris (Amphibia: Caudata)

Denoël, Mathieu; Joly, Pierre

2000 • In Proceedings of the Royal Society. Biological Sciences, 267 (1451), p. 1481-1485

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/1588

DOI
10.1098/rspb.2000.1168

PubMed
10983835

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Keywords :

Heterochrony; Paedomorphosis; Neoteny; Progenesis; Development; Evolution; Amphibian; Salamandridae; Mesotriton alpestris; Alpine newt; Age structure; Size structure; Processes; Demography; Skeletochronology; First reproduction; Early maturity; Population size; Ichthyosaura alpestris; Lac de la cabane; Apennines; Growth; Ichthyosaura alpestris alpestris; Ichthyosaura alpestris apuanus; France; Italy

Abstract :

[en] Current theories on the evolution of paedomorphosis suppose that several ontogenetic pathways have appeared according to different selective pressures. The aim of this study was to find out whether two distinct processes can lead to paedomorphosis in the Alpine newt, Triturus alpestris. In this respect, we compared age structures of paedomorphic and metamorphic individuals in two newt populations where the two forms lived syntopically. Whereas paedomorphosis resulted in a slower rate of somatic development in one population, it resulted in an acceleration of sexual maturation in the other population. These processes correspond to neoteny and progenesis, respectively. These results suggest that phenotypic plasticity can result from contrasted ontogenetic pathways between two populations of the same species. They give support to models that consider gonadic development as the target of selection under different environmental pressures.

Disciplines :

Zoology
Life sciences: Multidisciplinary, general & others
Environmental sciences & ecology

Author, co-author :

Denoël, Mathieu ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale

Joly, Pierre; Université Claude Bernard - Lyon 1 - UCLB - France

Language :

English

Title :

Neoteny and progenesis as two heterochronic processes involved in paedomorphosis in Triturus alpestris (Amphibia: Caudata)

Publication date :

2000

Journal title :

Proceedings of the Royal Society. Biological Sciences

ISSN :

0962-8452

eISSN :

1471-2954

Publisher :

The Royal Society, United Kingdom

Volume :

267

Issue :

1451

Pages :

1481-1485

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique

Available on ORBi :

since 29 November 2008

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Bibliography

Alberch P., Gould S.J., Oster G.F., Wake D.B. (1979) Size and shape in ontogeny and phylogeny. Pateobiology 5:296-317.
Bizer J.R. (1978) Growth rates and size at metamorphosis of high elevation populations of Ambystoma tigrinum. Oecologia 34:175-184.
Breuil M., Biologie et differenciation genetique des population du triton alpestre (Triturus alpestris) (Amphibia Caudata) dans le sud-est de la France et en Italie. PhD theis, Universite Paris-Sud Orsay, Paris, France; 1986.
Breuil M. (1992) La neotenie dans le genre Triturus: Mythes et realites. Bull. Soc. Herpetol. Fr. 61:11-44.
Bruce R.C. (1979) Evolution of paedomorphosis in salamanders of the genus Gyrinophilus. Evolution 33:998-1000.
Duellman W.E., Trueb L., Biology of amphibians. New York: McGraw-Hill; 1986.
Emerson S.B. (1986) Heterochrony and frogs: The relationship of a life history trait to morphological form. Am. Nat. 127:167-183.
Fasola M. (1993) Resource partitioning by three species of newts during their aquatic phase. Ecography 16:73-81.
Fiorello C.V., German R.Z. (1997) Heterochrony within species: Craniofacial growth in giant, standard, and dwarf rabbits. Evolution 51:205-261.
Gabrion J., Sentein P., Gabrion C. (1978) Les populations neoteniques de Triturus helveticus Raz. des Causses et du Bas-Languedoc. II. Ecologie. La Terre et la Vie 32:577-610.
Gilbert S.F., Development biology. Sunderland, MA: Sinauer Associates, Inc.; 1994.
Gould S.J., Ontogeny and phylogeny. Cambridge, UK: Belknap Press.; 1977.
Greenwood J.J.D., Basic techniques. Ecological census techniques (ed W. J. Sutherland), Cambridge University Press.; 1999, 11-110.
Harris R.N. (1987) Density-dependent paedomorphosis in the salamander Notophthalmus viridescens dorsalis. Ecology 68:705-712.
Harris R.N., Semlitsch R.D., Wilbur H.M., Fauth J.E. (1990) Local variation in the genetic basis of paedomorphosis in the salamander Ambystoma talpoideum. Evolution 44:1588-1603.
Harvell C.D. (1994) The evolution of polymorphism in colonial invertebrates and social insects. Q. Rev. Biol. 69:155-185.
Healy W.R. (1974) Population consequences of alternative life histories in Notophthalmus v. viridescens. Copeia 1974:221-229.
Jackson M.E., Semlitsch R.D. (1993) Paedomorphosis in the salamander Ambystoma talpoideum: Effects of a fish predator. Evolution 74:342-350.
Joly P., Miaud C. (1989) Tattooing as an individual marking techniques in urodeles. Alytes 8:11-16.
Joly P., Miaud C. (1989) Fidelity to the breeding site in the Alpine newt Triturus alpestris. Behav. Process. 19:47-56.
Kalezic M.L., Cvetkovic D., Djorovic A., Dzukic G. (1996) Alternative life-history pathways: Paedomorphosis and adult fitness in European newt. J. Zool. Syst. Evol. Res. , (Triturus vulgaris and T. alpestris); 34:1-7.
Krenz J.D., Sever D.M. (1995) Mating and oviposition in paedomorphosis Ambystoma talpoideum precedes the arrival of terrestrial males. Herpetologica 51:387-393.
Livezey B.C. (1992) Flightlessness in the Galapagos cormorant (Compsobalieus [Nannopterum] harrisi): Heterochrony, giantism, and specialization. Zool. J. Linn. Soc. 105:155-224.
McKinney M.L., McNamara K.J., Heterochrony. The evolution of ontogeny. New York: Plenum Press; 1991.
McNamara K.J., Shapesof time. The evolution of growth and development. Baltimore, MA: Johns Hopkins University Press.; 1997.
Meyer A. (1987) Phenotypic plasticity and heretochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implication for speciation in cichlid fishes. Evolution 41:1357-1369.
Miaud C., Joly P., Castanet J. (1993) Variation in age structures in a subdivided population of Triturus cristatus. Can. J. Zool. 71:1874-1879.
Miaud C., Guyetant R., Faber H., Age, size, and growth of the Alpine newt, Triturus alpestris (Urodela: Salamandridae), at high altitude and a review of life-history trait variation throughout its range. Herpetologica (In the press); 2000, 56.
Raff R.A., The shape of life. Genes, development, and the evolution of animal form. University of Chicago Press; 1996.
Reilly S.M., Lauder G.V. (1988) Ontogeny of aquatic feeding performance in the Eastern newt, Notophthalmus viridescens (Salamandridae). Copeia 1988:87-91.
Reilly S.M., Wiley E.O., Meinhardt D.J. (1997) An integrative approach to heterochrony: The distinction between interspecific and intranspecific phenomena. Biol. J. Linn. Soc. 60:119-143.
Ridley M., Evolution. Oxford University Press; 1996.
Roff D.A., The evolution of life histories. Theory and analysis. New York: Chapman and Hall; 1992.
Ryan T.J., Semlitsch R.D. (1998) Intranspecific heterochrony and life history evolution: Decoupling somatic and sexual development in a facultatively paedomorphic salamander. Proc. Natl Acad. Sci. USA 95:5643-5648.
Scheiner S.M. (1993) Genesis and evolution of phenotypic plasticity. A. Rev. Ecol. Syst. 24:35-68.
Schlichting C.D., Pigliucci M. (1995) Gene regulation, quantitative genetics, and the evolution of reaction norms. Ecol. Ecol. 9:154-168.
Semlitsch R.D. (1987) Paedomorphosis in Ambystoma talpoideum. Effects of density, food and pond drying. Ecology 68:994-1002.
Semlitsch R.D., Wilbur H.M. (1989) Artificial selection for paedomorphosis in the salamander Ambystoma talpoideum. Evolution 43:105-112.
Semlitsch R.D., Harris R.N., Wilbur H.M. (1990) Paedomorphosis in ambystoma talpoideum: Maintenance of population variation and alternative life-history pathways. Evolution 44:1604-1613.
Shaffer H.B., Voss S.R. (1996) Phylogenetic and mechanistic analysis of a developmentally integrated character complex: Alternative life history models in ambystomatid salamanders. Am. Zool. 36:24-35.
Siegel S., Castellan N.J., Nonparametric statistics for the behavioral sciences. New York: McgGraw-Hill; 1988.
Smith T.B., Skulason S. (1996) Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. A. Rev. Ecol. Syst. 27:111-133.
Sprules W.G. (1974) The adaptive significance of paedogenesis in North American species of Ambystoma (Amphibia: Caudata): An hypothesis. Can. J. Zool. 52:393-400.
.
Stearns S. C., The evalution of life histories. Oxford University Press; 1992.
Svob M. (1965) Neurosekretion in Triturus alpestris montenegrinus Radov. und ihre korrelation mit der neotenie. Bull. Sci. Acad. R. S. F. Yougoslavie A 10:379-381.
Voss S.R. (1995) Genetic basis of paedomorphosis in the axolotl, Ambystoma mexicanum: A test of the single-gene hypothesis. J. Hered. 86:441-447.
Voss S.R., Shaffer H.B. (1997) Adaptative evolution via a major gene effect: Paedomorphosis in the Mexican axolotl. Proc. Natl Acad. Sci. USA 94:14185-14189.
Wake D.B., Castanet J. (1995) A skeletochronological sutdy of growth and age in relation to adult size in Batrachoseps attenuatus. J. Herpetol. 29:60-65.
Whiteman H.H. (1994) Evolution of facultative paedomorphosis in salamanders. Q. Rev. Biol. 69:205-221.
Whiteman H.H. (1997) Maintenance of polymorphism promoted by sex-specific fitness payoffs. Evolution 51:2039-2044.
Whiteman H.H., Wissinger S.A., Brown W.S. (1996) Growth and foraging consequences of facultative paedomorphosis in the tiger salamander, Ambystoma tigrinum nebulosum. Evol. Ecol. 10:433-446.
Wilbur H.M., Collins J.P. (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305-1314.