Evolution; Facultative paedomorphosis; Metamorphosis; Population genetics; Microsatellites; Gene flow; Population structure; Alternative morphs; Heterochrony; Polymorphism; Polyphenism; Lissotriton helveticus; Palmate newt; Amphibian; Larzac
Abstract :
[en] Paedomorphosis and metamorphosis are two major developmental processes that characterize the evolution of complex life cycles in many lineages. Whereas these processes were fixed in some taxa, they remained facultative in others, with alternative phenotypes expressed in the same populations. From a genetic perspective, it is still unknown whether such phenotypes form a single population or whether they show some patterns of isolation in syntopy. This has deep implications for understanding the evolution of the phenotypes, i.e. towards their persistence or their fixation and speciation. Newts and salamanders are excellent models to test this hypothesis because they exhibit both developmental processes in their populations: the aquatic paedomorphs retain gills, whereas the metamorphs are able to colonize land. Using microsatellite data of coexisting paedomorphic and metamorphic palmate newts (Lissotriton helveticus), we found that they formed a panmictic population, which evidences sexual compatibility between the two phenotypes. The high gene flow could be understood as an adaptation to unstable habitats in which phenotypic plasticity is favored over the fixation of developmental alternatives. This makes then possible the persistence of a polyphenism: only metamorphosis could be maintained in case of occasional drying whereas paedomorphosis could offer specific advantages in organisms remaining in water.
Research Center/Unit :
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Disciplines :
Environmental sciences & ecology Genetics & genetic processes Life sciences: Multidisciplinary, general & others Zoology Aquatic sciences & oceanology
Author, co-author :
Oromi Farrús, Neus ; Université de Liège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Michaux, Johan ; Université de Liège > Département des sciences de la vie > Génétique et physiologie des microalgues
Denoël, Mathieu ; Université de Liège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Language :
English
Title :
High gene flow between alternative morphs and the evolutionary persistence of facultative paedomorphosis
Publication date :
August 2016
Journal title :
Scientific Reports
eISSN :
2045-2322
Publisher :
Nature Publishing Group, London, United Kingdom
Volume :
6
Pages :
32046
Peer reviewed :
Peer Reviewed verified by ORBi
European Projects :
FP7 - 600405 - BEIPD - Be International Post-Doc - Euregio and Greater Region
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique Marie-Curie BeIPD COFUND CE - Commission Européenne
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Taborsky, M., Brockmann, H.M., Alternative reproductive tactics and life history phenotypes (2010) Animal Behaviour: Evolution and Mechanisms, pp. 537-586. , Springer ed. Kappeler, P
Bush, G.L., Sympatric speciation in animals: New wine in old bottles (1994) Trends Ecol. Evol, 9, pp. 285-288
Skulason, S., Smith, T.B., Resource polymorphisms in vertebrates (1995) Trends Ecol. Evol, 10, pp. 366-370
Seehausen, O., Process and pattern in cichlid radiations-inferences for understanding unusually high rates of evolutionary diversification (2015) New Phytol, 207, pp. 304-312
Huyghe, K., Genetic divergence among sympatric colour morphs of the Dalmatian wall lizard (Podarcis melisellensis) (2010) Genetica, 138, pp. 387-393
Gordeeva, N.V., Alekseyev, S.S., Matveev, A.N., Samusenok, V.P., Parallel evolutionary divergence in Arctic char Salvelinus alpinus complex from Transbaikalia: Variation in differentiation degree and segregation of genetic diversity sympatric forms (2014) Can. J. Fish. Aquat. Sci, 72, pp. 96-115
Kusche, H., Elmer, K.R., Meyer, A., Sympatric ecological divergence associated with a color polymorphism (2015) BMC Biol, 13, p. 82
Murren, C.J., Constraints on the evolution of phenotypic plasticity: Limits and costs of phenotype and plasticity (2015) Heredity, 115, pp. 293-301
Gould, S.J., (1977) Ontogeny and Phylogeny, , Harvard University Press
McNamara, K.J., (1997) Shapes of Time. The Evolution of Growth and Development, , John Hopkins University Press
McNamara, K.J., Heterochrony: The evolution of development (2012) Evol. Educ. Outreach, 5, pp. 203-218
Holstein, T.W., Laudet, V., Life-history evolution: At the origins of metamorphosis (2014) Curr. Biol, 24, pp. R159-R161
Laudet, V., The origins and evolution of vertebrate metamorphosis (2011) Curr. Biol, 21, pp. R726-R737
Fusco, G., Minelli, A., Phenotypic plasticity in development and evolution: Facts and concepts (2010) Philos. Trans. R. Soc. B Biol. Sci, 365, pp. 547-556
Deno, M., Joly, P., Whiteman, H.H., Evolutionary ecology of facultative paedomorphosis in newts and salamanders (2005) Biol. Rev. Camb. Philos. Soc, 80, p. 663
Wilbur, H.M., Collins, J.P., Ecological aspects of amphibian metamorphosis: Nonnormal distributions of competitive ability reflect selection for facultative metamorphosis (1973) Science, 182, pp. 1305-1314
Voss, S.R., Shaffer, H.B., Adaptive evolution via a major gene effect: Paedomorphosis in the Mexican axolotl (1997) Proc. Natl. Acad. Sci. USA, 94, pp. 14185-14189
Bonett, R.M., Steffen, M.A., Lambert, S.M., Wiens, J.J., Evolution of paedomorphosis in plethodontid salamanders: Ecological correlates and re-evolution of metamorphosis (2014) Evolution, 68, pp. 466-482
Semlitsch, R.D., Wilbur, H.M., Artificial selection for paedomorphosis in the salamander Ambystoma talpoideum (1989) Evolution, 43, pp. 105-112
Semlitsch, R.D., Harris, R.N., Wilbur, H.M., Paedomorphosis in Ambystoma talpoideum: Maintenance of population variation and alternative life-history pathways (1990) Evolution, 44, pp. 1604-1613
Deno, M., Poncin, P., Ruwet, J.C., Sexual compatibility between two heterochronic morphs in the Alpine newt, Triturus alpestris (2001) Anim. Behav, 62, pp. 559-566
Krenz, J.D., Sever, D.M., Mating and oviposition in paedomorphic Ambystoma talpoideum precedes the arrival of terrestrial males (1995) Herpetologica, 51, pp. 387-393
Whiteman, H.H., Krenz, J.D., Semlitsch, R.D., Intermorph breeding and the potential for reproductive isolation in polymorphic mole salamanders (Ambystoma talpoideum) (2006) Behav. Ecol. Sociobiol, 60, pp. 52-61
Winandy, L., Deno, M., Expression of sexual ornaments in a polymorphic species: Phenotypic variation in response to environmental risk (2015) J. Evol. Biol, 28, pp. 1049-1056
Deno, M., Ficetola, G.F., Heterochrony in a complex world: Disentangling environmental processes of facultative paedomorphosis in an amphibian (2014) J. Anim. Ecol, 83, pp. 606-615
Whiteman, H.H., Evolution of facultative paedomorphosis in salamanders (1994) Q. Rev. Biol, 69, pp. 205-221
Deno, M., Joly, P., Neoteny and progenesis as two heterochronic processes involved in paedomorphosis in Triturus alpestris (Amphibia: Caudata) (2000) Proc. R. Soc. B, 267, pp. 1481-1485
Deno, M., Winandy, L., The importance of phenotypic diversity in conservation: Resilience of palmate newt morphotypes after fish removal in Larzac ponds (France) (2015) Biol. Conserv, 192, pp. 402-408
Evanno, G., Regnaut, S., Goudet, J., Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study (2005) Mol. Ecol, 14, pp. 2611-2620
Svanbk, R., Ekl, P., Fransson, R., Holmgren, K., Intraspecific competition drives multiple species resource polymorphism in fish communities (2008) Oikos, 117, pp. 114-124
Chevin, L.-M., Lande, R., Evolution of discrete phenotypes from continuous norms of reaction (2013) Am. Nat, 182, pp. 13-27
Roff, D., (2002) Life History Evolution, , Sinauer Associates, Sunderland, MA
Deno, M., Ficetola, G.F., Using kernels and ecological niche modeling to delineate conservation areas in an endangered patchbreeding phenotype (2015) Ecol. Appl, 25, pp. 1922-1931
Shaffer, H.B., Voss, S.R., Phylogenetic and mechanistic analysis of a developmentally integrated character complex: Alternate life history modes in ambystomatid salamanders (1996) Am. Zool, 36, pp. 24-35
Voss, S.R., Kump, D.K., Walker, J.A., Shaffer, H.B., Voss, G.J., Thyroid hormone responsive QTL and the evolution of paedomorphic salamanders (2012) Heredity, 109, pp. 293-298
Johnson, C.K., Voss, S.R., Salamander paedomorphosis: Linking thyroid hormone to life history and life cycle evolution (2013) Curr. Top. Dev. Biol, 103, pp. 229-258
Paris, M., Laudet, V., The history of a developmental stage: Metamorphosis in chordates (2008) Genesis, 46, pp. 657-672
Canestrelli, D., Caputo, F.P., Bagnoli, C., Nascetti, G., Integrating genetic, demographic and ecological issues for the conservation of the Alpine newt in central Italy (2006) Ann. Zool. Fennici, 43, pp. 322-334
Whiteman, H.H., Larval growth in polyphenic salamanders: Making the best of a bad lot (2012) Oecologia, 168, pp. 109-118
Deno, M., Džukić, G., Kalezić, M.L., Effects of widespread fish introductions on paedomorphic newts in Europe (2005) Conserv. Biol, 19, pp. 162-170
Andersen, L.W., Fog, K., Damgaard, C., Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea) (2004) Proc. R. Soc. B, 271, pp. 1293-1302
Kraaijeveld-Smit, F.J.L., Beebee, T.J.C., Griffiths, R.A., Moore, R.D., Schley, L., Low gene flow but high genetic diversity in the threatened Mallorcan midwife toad Alytes muletensis (2005) Mol. Ecol, 14, pp. 3307-3315
Garant, D., Forde, S.E., Hendry, A.P., The multifarious effects of dispersal and gene flow on contemporary adaptation (2007) Funct. Ecol, 21, pp. 434-443
Keller, L.F., Immigration and the ephemerality of a natural population bottleneck: Evidence from molecular markers (2001) Proc. R. Soc. B, 268, pp. 1387-1394
Deno, M., Seasonal variation of morph ratio in facultatively paedomorphic populations of the palmate newt Triturus helveticus (2006) Acta Oecologica, 29, pp. 165-170
Garner, T.W.J., Schmidt, B.R., Relatedness, body size and paternity in the alpine newt, Triturus alpestris (2003) Proc. R. Soc. B, 270, pp. 619-624
Miaud, C., (1990) La Dynamique des Populations Subdivisons: Ude Comparative Chez Trois Amphibiens Urodes (Triturus Alpestris T. Helveticus et T. Cristatus), , PhD thesis (Claude Bernard University, Lyon, France
Arntzen, J.W., Smithson, A., Oldham, R.S., Marking and tissue sampling effects on body condition and survival in the newt Triturus cristatus (1999) J. Herpetol, 33, pp. 567-576
Drechsler, A., Geller, D., Freund, K., What remains from a 454 run: Estimation of success rates of microsatellite loci development in selected newt species (Calotriton asper, Lissotriton helveticus, Triturus cristatus) (2013) Ecol. Evol, 3, pp. 3947-3957
Van Oosterhout, C., Hutchinson, W.F., MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data (2004) Mol. Ecol, 4, pp. 535-538
Goudet, J., (2001) FSTAT A Program to Estimate and Test Gene Diversities and Fixation Indices (Version 2.9.3)
Raymond, M., Rousset, F., GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism (1995) J. Hered, 86, pp. 248-249
Guo, S.W., Thompson, E.A., Performing the exact test of Hardy-Weinberg proportion for multiple alleles (1992) Biometrics, 48, pp. 361-372
Antao, T., Lopes, A., Lopes, R.J., Beja-Pereira, A., Luikart, G., LOSITAN: A workbench to detect molecular adaptation based on a Fst-outlier method (2008) BMC Bioinformatics, 9, pp. 1-5
Excoffier, L., Laval, G., Schneider, S., (2006) ARLEQUIN Version 3.01 An Integrated Software Package for Population Genetics
Pritchard, J.K., Stephens, M., Donnelly, P., Inference of population structure using multilocus genotype data (2000) Genetics, 155, pp. 945-959
Earl, D.A., VonHoldt, B.M., STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method (2012) Conserv. Genet. Resour, 4, pp. 359-361
Kopelman, N.M., Mayzel, J., Jakobsson, M., Rosenberg, N.A., Mayrose, I., Clumpak: A program for identifying clustering modes and packaging population structure inferences across K (2015) Mol. Ecol. Resour, 15, pp. 1179-1191
Comps, B., Gomoy, D., Letouzey, J., Thiaut, B., Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European beech (2001) Genetics, 157, pp. 389-397
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.