The paginated published version of this paper is also available on Wiley Online Library (see DOI link). The Open Access version can be downloaded hereunder. The cover can also be accessed on Wiley website at: https://onlinelibrary.wiley.com/doi/epdf/10.1111/jeb.13328
All documents in ORBi are protected by a user license.
amphibians; facultative paedomorphosis; fitness; heterochrony; metamorphosis; newt; predation; progenesis; reproduction; sex ratio; behaviour; behavior; fecundity; egg laying; size; sexual dimorphism; maturation; courtship; Lissotriton helveticus; palmate newt; cost; benefit; sex biases; small size; sexual selection; Larzac
Abstract :
[en] Progenesis is considered to have an important role in evolution because it allows the retention of both a larval body size and shape in an adult morphology. However, the cost caused by the adoption of a progenetic process in both males and females remains to be explored to explain the success of progenesis and particularly its biased prevalence across the sexes and environments. Here, through an experimental approach, we used a facultative progenetic species, the palmate newt (Lissotriton helveticus) that can either mature at a small size and retain gills or mature after metamorphosis, to test three hypotheses for sex-specific payoffs of progenesis in safe versus risky habitats. Goldfish were used because they caused a higher decline in progenetic than metamorphic newts. We determined that progenetic newts have a lower reproductive fitness than metamorphic newts. We also found that, when compared to metamorphs, progenetic males have lower reproductive activity than progenetic females and that predatory risk affects more progenetic than metamorphic newts. By identifying ultimate causes of the female-biased sex ratios found in nature, these results support the male escape hypothesis, i.e. the higher metamorphosis rate of progenetic males. They also highlight that although progenesis is advantageous in advancing the age at first reproduction, it also brings an immediate fitness cost and this, particularly, in hostile predatory environments. This means that whereas some environmental constraints could favour facultative progenesis, some others, such as predation, can ultimately counter-select progenesis. Altogether, these results improve our understanding of how developmental processes can affect the sexes differently and how species invasions can impair the success of alternative developmental phenotypes.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Denoël, Mathieu ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire d'Écologie et de Conservation des Amphibiens
Drapeau, Laura; Université de Liège - ULiège > Laboratoire d'Ecologie et de Conservation des Amphibiens
Winandy, Laurane ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire d'Écologie et de Conservation des Amphibiens
Language :
English
Title :
Reproductive fitness consequences of progenesis: sex-specific payoffs in safe and risky environments
Adamson, M. L. (1990). Haplodiploidy in the Oxyurida: Decoupling the evolutionary processes of adaptation and speciation. Annales de Parasitologie Humaine et Comparée, 65, 31–35. https://doi.org/10.1051/parasite/1990651031
Alberch, P., Gould, S. J., Oster, G. F., & Wake, D. B. (1979). Size and shape in ontogeny and phylogeny. Paleobiology, 5, 296–317. https://doi.org/10.1017/S0094837300006588
Bonett, R. M. (2016). An integrative endocrine model for the evolution of developmental timing and life history of plethodontids and other salamanders. Copeia, 104, 209–221. https://doi.org/10.1643/OT-15-269
Bonett, R. M., & Blair, A. L. (2017). Evidence for complex life cycle constraints on salamander body form diversification. Proceedings of the National Academy of Sciences of the United States of America, 114, 9936–9941. https://doi.org/10.1073/pnas.1703877114
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
Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretic approach. New York, NY: Springer Verlag.
Cabrera-Guzmán, E., Díaz-Paniagua, C., & Gomez-Mestre, I. (2017). Competitive and predatory interactions between invasive mosquitofish and native larval newts. Biological Invasions, 19, 1449–1460. https://doi.org/10.1007/s10530-017-1369-5
Cabrera-Guzmán, E., Díaz-Paniagua, C., & Gomez-Mestre, I. (2019). Invasive mosquitofish (Gambusia holbrooki) affect egg-laying and behaviour of Spanish pygmy newts (Triturus pygmaeus). Amphibia-Reptilia, 40, 103–112. https://doi.org/10.1163/15685381-20181019
Clarkson, P. M., & Beachy, C. K. (2015). Induction of metamorphosis causes differences in sex-specific allocation patterns in axolotls (Ambystoma mexicanum) that have different growth histories. Journal of Herpetology, 49, 621–626. https://doi.org/10.1670/14-141
Cohen, J. E., Pimm, S. L., Yodzis, P., & Saldaña, J. (1993). Body sizes of animal predators and animal prey in food webs. Journal of Animal Ecology, 62, 67–78. https://doi.org/10.2307/5483
Cornuau, J. H., Rat, M., Schmeller, D. S., & Loyau, A. (2012). Multiple signals in the palmate newt: Ornaments help when courting. Behavioral Ecology Sociobiology, 66, 1045–1055. https://doi.org/10.1007/s00265-012-1355-y
Denoël, M. (2017). On the identification of paedomorphic and overwintering larval newts based on cloacal shape: Review and guidelines. Current Zoology, 63, 165–173. https://doi.org/10.1093/cz/zow054
Denoël, M., Drapeau, L., Oromi, N., & Winandy, L. (2019). The role of predation risk in metamorphosis versus behavioural avoidance: A sex-specific study in a facultative paedomorphic amphibian. Oecologia, 189, 637–645. https://doi.org/10.1007/s00442-019-04362-8
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. (2015). Using kernels and ecological niche modeling to delineate conservation areas in an endangered patch-breeding phenotype. Ecological Applications, 25, 1922–1931. https://doi.org/10.1890/14-1041.1
Denoël, M., Ficetola, G. F., Sillero, N., Džukić, G., Kalezić, M. L., Vukov, T. D., … Lejeune, B. (2019). Traditionally managed landscapes do not prevent amphibian decline and the extinction of paedomorphosis. Ecological Monographs, 89. in press. https://doi.org/10.1002/ecm.1347
Denoël, M., Ivanović, A., Džukić, G., & Kalezić, M. L. (2009). Sexual size dimorphism in the evolutionary context of facultative paedomorphosis: Insights from European newts. BMC Evolutionary Biology, 9, 278. https://doi.org/10.1186/1471-2148-9-278
Denoël, M., & Joly, P. (2000). Neoteny and progenesis as two heterochronic processes involved in paedomorphosis in Triturus alpestris (Amphibia: Caudata). Proceedings of the Royal Society B-Biological Sciences, 267, 1481–1485. https://doi.org/10.1098/rspb.2000.1168
Denoël, M., & Winandy, L. (2015). The importance of phenotype 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
Ebenman, B. (1992). Evolution in organisms that change their niches during the life cycle. The American Naturalist, 139, 990–1021. https://doi.org/10.1086/285370
Edward, D. A., & Chapman, T. (2011). The evolution and significance of male mate choice. Trends in Ecology and Evolution, 26, 647–654. https://doi.org/10.1016/j.tree.2011.07.012
Gabrion, J. (1976). La néoténie chez Triturus helveticus Raz. Etude morphofonctionnelle de la fonction thyroidienne. PhD Thesis, Université des Sciences et Techniques du Languedoc, Montpellier, France.
Galloy, V., & Denoël, M. (2010). Detrimental effect of temperature increase on the fitness of an amphibian (Lissotriton helveticus). Acta Oecologica, 36, 179–183. https://doi.org/10.1016/j.actao.2009.12.002
Garstang, W. (1922). The theory of recapitulation: A critical re-statement of the biogenetic law. The Journal of the Linnean Society, Zoology, 35, 81–101. https://doi.org/10.1111/j.1096-3642.1922.tb00464.x
Garstang, W. (1928). The morphology of Tunicata, and its bearings on the phylogeny of the Chordata. The Quarterly Journal of Microscopical Science, 72, 51–187.
Garstang, W. (1954). Larval forms and other zoological verses. Oxford, UK: Basil Blackwell.
Giard, A. (1887). La castration parasitaire et son influence sur les caractères extérieurs du sexe mâle chez les crustacés décapodes. Bulletin Scientifique du Département du Nord, 18, 629–28.
Gill, D. E. (1978). Effective population size and interdemic migration rates in a metapopulation of the red-spotted newt, Notophthalmus viridescens (Rafinesque). Evolution, 32, 839–849. https://doi.org/10.1111/j.1558-5646.1978.tb04638.x
Gould, S. J. (1977). Ontogeny and phylogeny. Cambridge, MA: Harvard University Press.
Gould, S. J. (1982). Change in developmental timing as a mechanism of macroevolution. In J. T. Bonner (Ed.), Evolution and development (pp. 333–346). Berlin, Heidelberg: Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-642-45532-2
Griffiths, R. A. (1987). Microhabitat and seasonal niche dynamics of smooth and palmate newts, Triturus vulgaris and T. helveticus, at a pond in mid-wales. Journal of Animal Ecology, 56, 441–451. https://doi.org/10.2307/5059
Halliday, T. R. (1975). On the biological significance of certain morphological characters in males of the smooth newt Triturus vulgaris and of the palmate newt Triturus helveticus (Urodela: Salamandridae). Zoological Journal of the Linnean Society, 56, 291–300. https://doi.org/10.1111/j.1096-3642.1975.tb00271.x
Halliday, T. R. (1977). The courtship of European newts: An evolutionary perspective. In D. H. Taylor, & S. I. Guttman (Eds.), The reproductive biology of amphibians (pp. 185–232). New York, NY: Plenum Press. https://doi.org/10.1007/978-1-4757-6781-0
Hanken, J., & Wake, D. B. (1993). Miniaturization of body size: Organismal consequences and evolutionary significance. Annual Review of Ecology and Systematics, 24, 501–519. https://doi.org/10.1146/annurev.es.24.110193.002441
Kalezić, M. L., Cvetković, D., Djorović, A., & Džukić, G. (1996). Alternative life-history pathways: Paedomorphosis and adult fitness in European newts (Triturus vulgaris and T. alpestris). Journal of Zoological Systematics and Evolutionary Research, 34, 629–7. https://doi.org/10.1111/j.1439-0469.1996.tb00804.x
Kalezić, M. L., & 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. https://doi.org/10.1163/156853886X00299
Kon, T., & Yoshino, T. J. I. R. (2002). Extremely early maturity found in Okinawan gobioid fishes. Ichthyological Research, 49, 224–228. https://doi.org/10.1007/s102280200031
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
Lefebvre, F., & Poulin, R. (2005). Progenesis in digenean trematodes: A taxonomic and synthetic overview of species reproducing in their second intermediate hosts. Parasitology, 130, 587–605. https://doi.org/10.1017/S0031182004007103
Long, J. A. (1990). Heterochrony and the origin of tetrapods. Lethaia, 23, 157–166. https://doi.org/10.1111/j.1502-3931.1990.tb01357.x
Magnhagen, C. (1991). Predation risk as a cost of reproduction. Trends in Ecology and Evolution, 6, 183–186. https://doi.org/10.1016/0169-5347(91)90210-O
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
McKinney, M. L., & McNamara, K. J. (1991). Heterochrony. The evolution of ontogeny. New York, NY: Plenum Press.
McNamara, K. J. (1988). Patterns of heterochrony in the fossil record. Trends in Ecology and Evolution, 3, 176–180. https://doi.org/10.1016/0169-5347(88)90036-5
McNamara, K. J. (1990). Echinoids. In K. J. McNamara (Ed.), Evolutionary trends (pp. 205–231). London, UK: Behaven Press.
McNamara, K. J. (2012). Heterochrony: The evolution of development. Evolution: Education and Outreach, 5, 203–218. https://doi.org/10.1007/s12052-012-0420-3
Miaud, C. (1991). La squelettochronologie chez les Triturus (amphibiens, urodèles) à partir d'une étude de T. alpestris, T. helveticus et T. cristatus du sud-est de la France. In J. L. Bagnilières, J. Castanet, F. Conand & F. J. Meunier (Eds.), Tissus durs et âge individuel des vertébrés (pp. 363–384). Paris, France: ORSTIOM-INRA.
Miaud, C. (1993). Predation of newt eggs (Triturus alpestris and T. helveticus) – Identification of predators and protective role of oviposition behavior. Journal of Zoology, 231, 575–582. https://doi.org/10.1111/j.1469-7998.1993.tb01939.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
Orizaola, G., & Braña, F. (2006). Effect of salmonid introduction and other environmental characteristics on amphibian distribution and abundance in mountain lakes of northern Spain. Animal Conservation, 9, 171–178. https://doi.org/10.1111/j.1469-1795.2006.00023.x
Pincheira-Donoso, D., & Hunt, J. (2017). Fecundity selection theory: Concepts and evidence. Biological Reviews, 92, 341–356. https://doi.org/10.1111/brv.12232
Roff, D. A., & Fairbairn, D. J. (1993). The evolution of alternate morphologies: Fitness and wing morphology in male sand crickets. Evolution, 47, 1572–1584. https://doi.org/10.1111/j.1558-5646.1993.tb02176.x
Ryan, T. J., & Hopkins, W. A. (2000). Interaction of sex and size and the standard metabolic rate of paedomorphic Ambystoma talpoideum: Size does matter. Copeia, 2000, 808–812. https://doi.org/10.1643/0045-8511(2000)000[0808:IOSASA]2.0.CO;2
Ryan, T. J., & Semlitsch, R. D. (1998). Intraspecific heterochrony and life history evolution: Decoupling somatic and sexual development in a facultatively paedomorphic salamander. Proceedings of the National Academy of Sciences of the United States of America, 95, 5643–5648. https://doi.org/10.1073/pnas.95.10.5643
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
Snyder, J., & Bretsky, P. (1971). Life habits of diminutive bivalve molluscs in the Maquoketa Formation (Upper Ordovician). American Journal of Science, 271, 227–251. https://doi.org/10.2475/ajs.271.3.227
Sparreboom, M. (2014). Salamanders of the old world. Zeist, The Netherlands: KNVV Publishing. https://doi.org/10.1163/9789004285620
Stearns, S. C. (1992). The evolution of life histories. Oxford, UK: Oxford University Press.
Struck, T. H., Golombek, A., Weigert, A., Franke, F. A., Westheide, W., Purschke, G., … Halanych, K. M. (2015). The evolution of annelids reveals two adaptive routes to the interstitial realm. Current Biology, 25, 1993–1999. https://doi.org/10.1016/j.cub.2015.06.007
Stunkard, H. D. (1959). The morphology and life-history of the digenetic trematode, Asymphylodora amnicolae n. sp.; The possible significance of progenesis for the phylogeny of the Digenea. The Biological Bulletin, 117, 562–581. https://doi.org/10.2307/1538867
Turvey, S. T., Chen, S., Tapley, B., Wei, G., Xie, F., Yan, F., … Cunningham, A. A. (2018). Imminent extinction in the wild of the world's largest amphibian. Current Biology, 28, R592–R594. https://doi.org/10.1016/j.cub.2018.04.005
Verrell, P., & McCabe, N. (1988). Field observations of the sexual behavior of the smooth newt, Triturus vulgaris vulgaris (Amphibia, Salamandridae). Journal of Zoology, 214, 533–545. https://doi.org/10.1111/j.1469-7998.1988.tb03758.x
Voss, S. R., Woodcock, M. R., & Zambrano, L. (2015). A tale of two axolotls. BioScience, 65, 1134–1140. https://doi.org/10.1093/biosci/biv153
Wake, M. H. (1986). The morphology of Idiocranium russeli (Amphibia: Gymnophiona), with comments on miniaturization through heterochrony. Journal of Morphology, 189, 629–16. https://doi.org/10.1002/jmor.1051890102
Walls, S. C., Barichivich, W. J., Brown, M. E., Scott, D. E., & Hossack, B. R. (2013). Influence of drought on salamander occupancy of isolated wetlands on the southeastern coastal plain of the United States. Wetlands, 33, 345–354. https://doi.org/10.1007/s13157-013-0391-3
Wambreuse, P., & Bels, V. (1984). Analyse qualitative et quantitative de la parade sexuelle du triton palmé Triturus helveticus (Razoumowsky 1798). Cahiers d'Ethologie Appliquée, 4, 193–218.
Werner, E. E. (1986). Amphibian metamorphosis: Growth rate, predation risk, and the optimal size at transformation. The American Naturalist, 128, 319–341. https://doi.org/10.1086/284565
West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford, UK: Oxford University Press.
Westheide, W. (1987). Progenesis as a principle in meiofauna evolution. Journal of Natural History, 21, 843–854. https://doi.org/10.1080/00222938700770501
Whiteman, H. H. (1994). Evolution of facultative paedomorphosis in salamanders. Quarterly Review of Biology, 69, 205–221. https://doi.org/10.1086/418540
Whiteman, H. H. (1997). Maintenance of polymorphism promoted by sex-specific fitness payoffs. Evolution, 51, 2039–2044. https://doi.org/10.1111/j.1558-5646.1997.tb05127.x
Whiteman, H. H., Krenz, J. D., & Semlitsch, R. D. (2006). Intermorph breeding and the potential for reproductive isolation in polymorphic mole salamanders (Ambystoma maculatum). Behavioral Ecology and Sociobiology, 60, 52–61. https://doi.org/10.1007/s00265-005-0139-z
Whiteman, H. H., Wissinger, S., Denoël, M., Mecklin, C., Gerlanc, N., & Gutrich, 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
Wilbur, H. M., & Collins, J. P. (1973). Ecological aspects of amphibian metamorphosis. Science, 182, 1305–1314. https://doi.org/10.1126/science.182.4119.1305
Wilson, D. S. (1975). The adequacy of body size as a niche difference. The American Naturalist, 109, 769–784. https://doi.org/10.1086/283042
Winandy, L., Darnet, E., & Denoël, M. (2015). Amphibians forgo aquatic life in response to alien fish introduction. Animal Behaviour, 109, 209–216. https://doi.org/10.1016/j.anbehav.2015.08.018
Winandy, L., & Denoël, M. (2013). Introduced goldfish affect amphibians through inhibition of sexual behaviour in risky habitats: An experimental approach. PLoS One, 8, e82736. https://doi.org/10.1371%2Fjournal.pone.0082736
Winandy, L., & Denoël, M. (2015a). The aggressive personality of an introduced fish affects foraging behavior in a polymorphic newt. Behavioral Ecology, 26, 1528–1536. https://doi.org/10.1093/beheco/arv101
Winandy, L., & Denoël, M. (2015b). Expression of sexual ornaments in a polymorphic species: Phenotypic variation in response to environmental risk. Journal of Evolutionary Biology, 28, 1049–1056. https://doi.org/10.1111/jeb.12636
