Genetic structure of lake and stream populations in a Pyrenean amphibian (Calotriton asper) reveals evolutionary significant units associated with paedomorphosis
[en] Differences in environmental conditions such as those between lakes and streams can produce phenotypic variation and ultimately promote evolutionary diversification. Some species of newts and salamanders can occupy these habitats and express alternative phenotypes: metamorphs that lose gills at metamorphosis and paedomorphs that retain them at the adult stage. Whereas this process is facultative in some species, it is obligatory in others, thus suggesting that isolation and environmental pressures may have canalized developmental pathways. In this study, we focused our research on the Pyrenean brook newt, Calotriton asper which is present in both lakes and streams, but whose fully aquatic paedomorphic individuals are only present in lakes. We aimed to determine the genetic structure and differentiation of two paedomorphic populations, including their surrounding stream and lake metamorphic populations, to test whether populations of paedomorphs can constitute evolutionary significant units. Although gene flow was identified between lakes and nearby stream populations, there was a low percentage of dispersers, and the paedomorphic populations were genetically differentiated from the populations of metamorphs. It is likely that the studied lakes have offered peculiar conditions that have allowed the development of a paedomorphic phenotype. These populations and phenotypes therefore constitute good models to understand local adaptations. As each of these populations of paedomorphs can be considered evolutionary significant units that cannot be replaced by other nearby populations in case of a population crash, conservation actions should be focused directly on them.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Oromi Farrús, Neus ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Valbuena-Ureña, Emilio; Universitat Autònoma de Barcelona
Soler-Membrives, Anna; Soler-Membrives
Amat, Felix; Museu de Granollers
Camarasa, Sebastià; CSIC-Universitat Pompeu Fabra
Carranza, Salvador; CSIC-Universitat Pompeu Fabra
Sanuy, Delfi; Universitat de Lleida
Denoël, Mathieu ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Language :
English
Title :
Genetic structure of lake and stream populations in a Pyrenean amphibian (Calotriton asper) reveals evolutionary significant units associated with paedomorphosis
Publication date :
May 2019
Journal title :
Journal of Zoological Systematics and Evolutionary Research
ISSN :
0947-5745
eISSN :
1439-0469
Publisher :
Wiley, Oxford, United Kingdom
Volume :
57
Issue :
2
Pages :
418-430
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique Marie curie COFUND
Allentoft, M. E., & O'Brien, J. (2010). Global amphibian declines, loss of genetic diversity and fitness: A review. Diversity, 2, 47–71. https://doi.org/10.3390/d2010047
Arntzen, A. J. W., Smithson, A., & Oldham, R. S. (1999). Marking and tissue sampling effects on body condition and survival in the newt Triturus cristatus. Journal of Herpetology, 33, 567–576. https://doi.org/10.2307/1565573
Bates, K. A., Clare, F. C., O'Hanlon, S., Bosch, J., Brookes, L., Hopkins, K., … Harrison, X. A. (2018). Amphibian chytridiomycosis outbreak dynamics are linked with host skin bacterial community structure. Nature Communications, 9, 693. https://doi.org/10.1038/s41467-018-02967-w
Bonett, R. M., Phillips, J. G., Ledbetter, N. M., Martin, S. D., & Lehman, L. (2018). Rapid phenotypic evolution following shifts in life cycle complexity. Proceedings of the Royal Society B: Biological Sciences, 285, 20172304. https://doi.org/10.1098/rspb.2017.2304
Bonett, R. M., Steffen, M. A., Lambert, S. M., Wiens, J. J., & Chippindale, P. T. (2014). Evolution of paedomorphosis in plethodontid salamanders: Ecological correlates and re-evolution of metamorphosis. Evolution, 68, 466–482. https://doi.org/10.1111/evo.12274
Campbell Grant, E. H., Nichols, J. D., Lowe, W. H., & Fagan, W. F. (2010). Use of multiple dispersal pathways facilitates amphibian persistence in stream networks. Proceedings of the National Academy of Sciences, 107, 6936–6940. https://doi.org/10.1073/pnas.1000266107
Campeny, R., Montori, A., & Llorente, G. A. (1986). Nuevos datos sobre la permanencia de caracteres larvarios en individuos adultos de una población de tritón pirenaico (Euproctus asper) en el Valle de Arán. Acta Vertebrata, 17, 170–174.
Carranza, S., & Amat, F. (2005). Taxonomy, biogeography and evolution of Euproctus (Amphibia: Salamandridae), with the resurrection of the genus Calotriton and the description of a new endemic species from the Iberian Peninsula. Zoological Journal of the Linnean Society, 145, 555–582. https://doi.org/10.1111/j.1096-3642.2005.00197.x
Caspers, B. A., Krause, E. T., Hendrix, R., Kopp, M., Rupp, O., Rosentreter, K., & Steinfartz, S. (2014). The more the better – Polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra). Molecular Ecology, 23, 239–250. https://doi.org/10.1111/mec.12577
Chapuis, M.-P., & Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24, 621–631. https://doi.org/10.1093/molbev/msl191
Contreras, V., Martínez-Meyer, E., Valiente, E., & Zambrano, L. (2009). Recent decline and potential distribution in the last remnant area of the microendemic Mexican axolotl (Ambystoma mexicanum). Biological Conservation, 142, 2881–2885. https://doi.org/10.1016/j.biocon.2009.07.008
Crandall, K. A., Bininda-Emonds, O. R. R., Mace, G. M., & Wayne, R. K. (2000). Considering evolutionary processes in conservation biology. Trends in Ecology and Evolution, 15, 290–295. https://doi.org/10.1016/S0169-5347(00)01876-0
Cushman, S. A., McKelvey, K. S., Hayden, J., & Schwartz, M. K. (2006). Gene flow in complex landscapes: Testing multiple hypotheses with causal modeling. The American Naturalist, 168, 486–499. https://doi.org/10.1086/506976
Cushman, S. A., Wasserman, T. N., Landguth, E. L., & Shirk, A. J. (2013). Re-evaluating causal modeling with Mantel tests in landscape genetics. Diversity, 5, 51–72. https://doi.org/10.3390/d5010051
Dalongeville, A., Andrello, M., Mouillot, D., Albouy, C., & Manel, S. (2016). Ecological traits shape genetic diversity patterns across the Mediterranean Sea: A quantitative review on fishes. Journal of Biogeography, 43, 845–857. https://doi.org/10.1111/jbi.12669
Denoël, M., Dalleur, S., Langrand, E., Besnard, A., & Cayuela, H. (2018). Dispersal and alternative pond fidelity strategies in an amphibian. Ecography, 41, 1543–1555. https://doi.org/10.1111/ecog.03296
Denoël, M., & Ficetola, G. F. (2014). Heterochrony in a complex world: Disentangling environmental processes of facultative paedomorphosis in an amphibian. Journal of Animal Ecology, 83, 606–615. https://doi.org/10.1111/1365-2656.12173
Denoël, M., Ficetola, G. F., Ćirović, R., Radović, D., Džukić, G., Kalezić, M. L., & Vukov, T. D. (2009). A multi-scale approach to facultative paedomorphosis of European newts (Salamandridae) in the Montenegrin karst: Distribution pattern, environmental variables, and conservation. Biological Conservation, 142, 509–517. https://doi.org/10.1016/j.biocon.2008.11.008
Denoël, M., Joly, P., & Whiteman, H. H. (2005). Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biological Reviews of the Cambridge Philosophical Society, 80, 663–671. https://doi.org/10.1017/S1464793105006858
Denoël, M., Džukić, G., & Kalezić, M. L. (2005). Effect of widespread fish introductions on paedomorphic newts in Europe. Conservation Biology, 19, 162–170. https://doi.org/10.1111/j.1523-1739.2005.00001.x
Denoël, M., Lena, J. P., & Joly, P. (2007). Morph switching in a dimorphic population of Triturus alpestris (Amphibia, Caudata). Evolutionary Ecology, 21, 325–335. https://doi.org/10.1007/s10682-006-9103-2
Denoël, M., Poncin, P., & Ruwet, J.-C. (2001). Sexual compatibility between two heterochronic morphs in the alpine newt, Triturus alpestris. Animal Behaviour, 62, 559–566. https://doi.org/10.1006/anbe.2001.1793
Denoël, M., Scimè, P., & Zambelli, N. (2016). Newt life after fish introduction: Extirpation of paedomorphosis in a mountain fish lake and newt use of satellite pools. Current Zoology, 62, 61–69. https://doi.org/10.1093/cz/zov003
Denoël, M., Whiteman, H. H., & Wissinger, S. A. (2007). Foraging tactics in alternative heterochronic salamander morphs: Trophic quality of ponds matters more than water permanency. Freshwater Biology, 52, 1667–1676. https://doi.org/10.1111/j.1365-2427.2007.01793.x
Denoël, M., & Winandy, L. (2015). The importance of phenotypic diversity in conservation: Resilience of palmate newt morphotypes after fish removal in Larzac ponds (France). Biological Conservation, 192, 402–408. https://doi.org/10.1016/j.biocon.2015.10.018
Drechsler, A., Geller, D., Freund, K., Schmeller, D. S., Künzel, S., Rupp, O., … Steinfartz, S. (2013). What remains from a 454 run: Estimation of success rates of microsatellite loci development in selected newt species (Calotriton asper, Lissotriton helveticus, and Triturus cristatus) and comparison with Illumina-based approaches. Ecology and Evolution, 3, 3947–3957. https://doi.org/10.1002/ece3.764
Earl, D. A., & vonHoldt, B. M. (2012). STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7
Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14, 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Ferchaud, A. L., & Hansen, M. M. (2016). The impact of selection, gene flow and demographic history on heterogeneous genomic divergence: Three-spine sticklebacks in divergent environments. Molecular Ecology, 25, 238–259. https://doi.org/10.1111/mec.13399
Fouquet, A., Courtois, E. A., Baudain, D., Lima, J. D., Souza, S. M., Noonan, B. P., & Rodrigues, M. T. (2015). The trans-riverine genetic structure of 28 Amazonian frog species is dependent on life history. Journal of Tropical Ecology, 31, 361–373. https://doi.org/10.1017/S0266467415000206
Fraser, D. J., & Bernatchez, L. (2001). Adaptive evolutionary conservation: Towards a unified concept for defining conservation units. Molecular Ecology, 10, 2741–2752. https://doi.org/10.1046/j.0962-1083.2001.01411.x
Fusco, G., & Minelli, A. (2010). Phenotypic plasticity in development and evolution: Facts and concepts. Introduction. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 365, 547–556. https://doi.org/10.1098/rstb.2009.0267
Garcia-Dorado, A. (1986). The effect of niche preference on polymorphism protection in a heterogeneous environment. Evolution, 40, 936–945. https://doi.org/10.1111/j.1558-5646.1986.tb00562.x
Goedbloed, D. J., Czypionka, T., Altmüller, J., Rodriguez, A., Küpfer, E., Segev, O., … Steinfartz, S. (2017). Parallel habitat acclimatization is realized by the expression of different genes in two closely related salamander species (genus Salamandra). Heredity, 119, 429–437. https://doi.org/10.1038/hdy.2017.55
Goudet, J. (1995). FSTAT (Version 1.2): A computer program to calculate F-statistics. Journal of Heredity, 86, 485–486. https://doi.org/10.1093/oxfordjournals.jhered.a111627
Gould, S. J. (1977). Ontogeny and phylogeny. Cambridge, MA: Harvard University Press.
Gross, M. R. (1991). Salmon breeding behavior and life history evolution in changing environments. Ecology, 72, 1180–1186. https://doi.org/10.2307/1941091
Guillot, G., Mortier, F., & Estoup, A. (2005). GENELAND: A computer package for landscape genetics. Molecular Ecology Notes, 5, 712–715. https://doi.org/10.1111/j.1471-8286.2005.01031.x
Guo, S. W., & Thompson, E. (1992). Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics, 48, 361–372. https://doi.org/10.2307/2532296
Hendrix, R., Schmidt, B. R., Schaub, M., Krause, E. T., & Steinfartz, S. (2017). Differentiation of movement behaviour in an adaptively diverging salamander population. Molecular Ecology, 26, 6400–6413. https://doi.org/10.1111/mec.14345
Isselin-Nondedeu, F., Trochet, A., Joubin, T., Picard, D., Etienne, R., Chevalier, H. Le, & Ribéron, A. (2017). Spatial genetic structure of Lissotriton helveticus L. following the restoration of a forest ponds network. Conservation Genetics, 18, 853–866. https://doi.org/10.1007/s10592-017-0932-z
Izen, R., Stuart, Y. E., Jiang, Y., & Bolnick, D. I. (2016). Coarse- and fine-grained phenotypic divergence among threespine stickleback from alternating lake and stream habitats. Evolutionary Ecology Research, 17, 437–457.
Jensen, J. L., Bohonak, A. J., & Kelley, S. T. (2005). Isolation by distance, web service. BMC Genetics, 6, 13. https://doi.org/10.1186/1471-2156-6-13
Jombart, T. (2008). Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403–1405.
Jombart, T., Devillard, S., & Balloux, F. (2010). Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genetics, 11, 94. https://doi.org/10.1186/1471-2156-11-94
Jones, J. S., & Probert, R. F. (1980). Habitat selection maintains a deleterious allele in a heterogeneous environment. Nature, 287, 632–633. https://doi.org/10.1038/287632a0
Jones, O. R., & Wang, J. (2010). COLONY: A program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources, 10, 551–555. https://doi.org/10.1111/j.1755-0998.2009.02787.x
Kaya, C. M., & Jeanes, E. D. (1995). Notes: Retention of adaptive rheotactic behavior by F1 fluvial Arctic grayling. Transactions of the American Fisheries Society, 124, 453–457. https://doi.org/10.1577/1548-8659(1995)124<0453:NROARB>2.3.CO;2
Keinath, M. C., Voss, S. R., Tsonis, P. A., & Smith, J. J. (2017). A linkage map for the Newt Notophthalmus viridescens: Insights in vertebrate genome and chromosome evolution. Developmental Biology, 426, 211–218. https://doi.org/10.1016/j.ydbio.2016.05.027
Kopelman, N. M., Mayzel, J., Jakobsson, M., Rosenberg, N. A., & Mayrose, I. (2015). Clumpak: A program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources, 15, 1179–1191. https://doi.org/10.1111/1755-0998.12387
Laudet, V. (2011). The origins and evolution of vertebrate metamorphosis. Current Biology, 21, R726–R737. https://doi.org/10.1016/j.cub.2011.07.030
Lejeune, B., Sturaro, N., Lepoint, G., & Denoël, M. (2018). Facultative paedomorphosis as a mechanism promoting intraspecific niche differentiation. Oikos, 127, 427–439. https://doi.org/10.1111/oik.04714
Lowe, W. H., Mcpeek, M. A., Likens, G. E., & Cosentino, B. J. (2008). Linking movement behaviour to dispersal and divergence in plethodontid salamanders. Molecular Ecology, 17, 4459–4469. https://doi.org/10.1111/j.1365-294X.2008.03928.x
Mantel, N. (1967). The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209–220.
Mathiron, A. G. E., Lena, J.-P., Baouch, S., & Denoël, M. (2017). The “male escape hypothesis”: Sex-biased metamorphosis in response to climatic drivers in a facultatively paedomorphic amphibian. Proceedings of the Royal Society B: Biological Sciences, 284, 20170176. https://doi.org/10.1098/rspb.2017.0176
de Meeûs, T., Michalakis, Y., Renaud, F., & Olivieri, I. (1993). Polymorphism in heterogeneous environments, evolution of habitat selection and sympatric speciation: Soft and hard selection models. Evolutionary Ecology, 7, 175–198. https://doi.org/10.1007/BF01239387
Milá, B., Carranza, S., Guillaume, O., & Clobert, J. (2010). Marked genetic structuring and extreme dispersal limitation in the Pyrenean brook newt Calotriton asper (Amphibia: Salamandridae) revealed by genome-wide AFLP but not mtDNA. Molecular Ecology, 19, 108–120. https://doi.org/10.1111/j.1365-294X.2009.04441.x
Miró, A., Sabás, I., & Ventura, M. (2018). Large negative effect of non-native trout and minnows on Pyrenean lake amphibians. Biological Conservation, 218, 144–153. https://doi.org/10.1016/j.biocon.2017.12.030
Miró, A., & Ventura, M. (2014). Evidence of exotic trout mediated minnow invasion in Pyrenean high mountain lakes. Biological Invasions, 17, 791–803. https://doi.org/10.1007/s10530-014-0769-z
Montori, A., & Llorente, G.A. (2014). Tritón pirenaico – Calotriton asper (Dugès, 1852). In: A. Salvador & I. Martínez-Solano, (Eds.), Enciclopedia virtual de los vertebrados (pp. 28). Versión 2-10-2014. Madrid, Spain: Museo Nacional de Ciencias Naturales.
Montori, A., Llorente, G., & Richter-Boix, À. (2008). Habitat features affecting the small-scale distribution and longitudinal migration patterns of Calotriton asper in a Pre-Pyrenean population. Amphibia-Reptilia, 29, 371–381. https://doi.org/10.1163/156853808785112048
Oromi, N., Amat, F., Sanuy, D., & Carranza, S. (2014). Life history trait differences between a lake and a stream-dwelling population of the Pyrenean brook newt (Calotriton asper). Amphibia-Reptilia, 35, 53–62. https://doi.org/10.1163/15685381-00002921
Oromi, N., Michaux, J., & Denoël, M. (2016). High gene flow between alternative morphs and the evolutionary persistence of facultative paedomorphosis. Scientific Reports, 6, 32046. https://doi.org/10.1038/srep32046
Paetkau, D., Slade, R., Burden, M., & Estoup, A. (2004). Genetic assignment methods for the direct, real-time estimation of migration rate: A simulation-based exploration of accuracy and power. Molecular Ecology, 13, 55–65. https://doi.org/10.1046/j.1365-294X.2004.02008.x
Page, R. B., Boley, M. A., Smith, J. J., Putta, S., & Voss, S. R. (2010). Microarray analysis of a salamander hopeful monster reveals transcriptional signatures of paedomorphic brain development. BMC Evolutionary Biology, 10, 199. https://doi.org/10.1186/1471-2148-10-199
Paz, A., Ibáñez, R., Lips, K. R., & Crawford, A. J. (2015). Testing the role of ecology and life history in structuring genetic variation across a landscape: A trait-based phylogeographic approach. Molecular Ecology, 24, 3723–3737. https://doi.org/10.1111/mec.13275
Percino-Daniel, R., Recuero, E., Vázquez-Domínguez, E., Zamudio, K. R., & Parra-Olea, G. (2016). All grown-up and nowhere to go: Paedomorphosis and local adaptation in Ambystoma salamanders in the Cuenca Oriental of Mexico. Biological Journal of the Linnean Society, 118, 582–597. https://doi.org/10.1111/bij.12750
Piry, S., Alapetite, A., Cornuet, J. M., Paetkau, D., Baudouin, L., & Estoup, A. (2004). GENECLASS2: A software for genetic assignment and first-generation migrant detection. Journal of Heredity, 95, 536–539. https://doi.org/10.1093/jhered/esh074
Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.
Rannala, B., & Mountain, J. L. (1997). Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences of the United States of America, 94, 9197–9201. https://doi.org/10.1073/pnas.94.17.9197
Ravigné, V., Olivieri, I., & Dieckmann, U. (2004). Implications of habitat choice for protected polymorphisms. Evolutionary Ecology Research, 6, 125–145.
RCoreTeam (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution, 43, 223–225. https://doi.org/10.1111/j.1558-5646.1989.tb04220.x
Rousset, F. (1997). Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145, 1219–1228.
Schlichting, C. D., & Pigliucci, M. (1998). Phenotypic evolution: A reaction norm perspective. Sunderland, MA: Sinauer Associates.
Schluter, D. (2000). The ecology of adaptive radiation. Oxford, UK: Oxford University Press.
Seehausen, O. (2015). Process and pattern in cichlid radiations - inferences for understanding unusually high rates of evolutionary diversification. New Phytologist, 207, 304–312. https://doi.org/10.1111/nph.13450
Semlitsch, R. D. (1987). Paedomorphosis in Ambystoma talpoideum: effects of density, food and pond drying. Ecology, 68, 994–1002. https://doi.org/10.2307/1938370
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. https://doi.org/10.1111/j.1558-5646.1990.tb03849.x
Semlitsch, R. D., & Wilbur, H. M. (1989). Artificial selection for paedomorphosis in the salamander Ambystoma talpoideum. Evolution, 43, 105–112. https://doi.org/10.1111/j.1558-5646.1990.tb03849.x
Sillero, N., Campos, J., Bonardi, A., Corti, C., Creemers, R., Crochet, P.-A., … Vences, M. (2014). Updated distribution and biogeography of amphibians and reptiles of Europe. Amphibia Reptilia, 35, 418–31. https://doi.org/10.1163/15685381-00002935
Skulason, S., & Smith, T. B. (1995). Resource polymorphisms in vertebrates. Trends in Ecology & Evolution, 10, 366–370. https://doi.org/10.1016/S0169-5347(00)89135-1
Sprules, W. (1974). Environmental factors and the incidence of neoteny in Ambystoma gracile (Baird) (Amphibia: Caudata). Canadian Journal of Zoology, 52, 1545–1552. https://doi.org/10.1139/z74-200
Valbuena-Ureña, E., Oromi, N., Soler-Membrives, A., Carranza, S., Amat, F., Camarasa, S., … Steinfartz, S. (2018). Jailed in the mountains: Genetic diversity and structure of an endemic newt species across the Pyrenees. PLoS ONE, 13, e0200214. https://doi.org/10.1371/journal.pone.0200214
Valbuena-Urena, E., Soler-Membrives, A., Steinfartz, S., Orozco-terWengel, P., & Carranza, S. (2017). No signs of inbreeding despite long-term isolation and habitat fragmentation in the critically endangered Montseny brook newt (Calotriton arnoldi). Heredity, 118, 424–435. https://doi.org/10.1038/hdy.2016.123
Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., & Shipley, P. (2004). MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Ventura, M., Tiberti, R., Buchaca, T., Buñay, D., Sabás, I., & Miró, A. (2017). Why should we preserve fishless high mountain lakes? In J. Catalan, J. M. Ninot & M. M. Aniz (Eds), High mountain conservation in a changing world (pp. 181–205). Advances in Global Change Research 62. Cham, Switzerland: Springer. https://doi.org/10.1007/978-3-319-55982-7
Vörös, J., Ursenbacher, S., Kiss, I., Jelić, D., Schweiger, S., & Szabó, K. (2017). Increased genetic structuring of isolated Salamandra salamandra populations (Caudata: Salamandridae) at the margins of the Carpathian Mountains. Journal of Zoological Systematics and Evolutionary Research, 55, 138–149. https://doi.org/10.1111/jzs.12157
Voss, S. R., & Shaffer, H. B. (1997). Adaptive evolution via a major gene effect: Paedomorphosis in the Mexican axolotl. Population Biology, 94, 14185–14189. https://doi.org/10.1073/pnas.94.25.14185
Weber, J. N., Bradburd, G. S., Stuart, Y. E., Stutz, W. E., & Bolnick, D. I. (2017). Partitioning the effects of isolation by distance, environment, and physical barriers on genomic divergence between parapatric threespine stickleback. Evolution, 71, 342–356. https://doi.org/10.1111/evo.13110
West-Eberhard, M. J. (1989). Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics, 20, 249–278. https://doi.org/10.1146/annurev.es.20.110189.001341
Whiteman, H. H. (1994). Evolution of facultative paedomorphosis in salamanders. The Quarterly Review of Biology, 69, 205–221. https://doi.org/10.1086/418540
Whiteman, H. H., & Semlitsch, R. D. (2005). Asymmetric reproductive isolation among polymorphic salamanders. Biological Journal of the Linnean Society, 86, 265–281. https://doi.org/10.1111/j.1095-8312.2005.00537.x
Whiteman, H. H., Wissinger, S. A., Denoël, M., Mecklin, C. J., Gerlanc, N. M., & Gutrich, J. J. (2012). Larval growth in polyphenic salamanders: Making the best of a bad lot. Oecologia, 168, 109–118. https://doi.org/10.1007/s00442-011-2076-z
