The role of predation risk in metamorphosis versus behavioural avoidance: a sex-specific study in a facultative paedomorphic amphibian
Evolutionary theory predicts the evolution of metamorphosis over paedomorphosis (the retention of larval traits at the adult stage) in response to life in unfavourable habitats and to the benefits of dispersal. Although many organisms are canalised into obligatory complex or simple life cycles, some species of newts and salamanders can express both processes (facultative paedomorphosis). Previous research highlighted the detrimental effect of fish on both metamorphic and paedomorphic phenotypes, but it remains unknown whether predation risk could induce shifts from paedomorphosis to metamorphosis, whether behavioural avoidance could be an alternative strategy to metamorphosis and whether these responses could be sex-biased. Testing these hypotheses is important because metamorphosed paedomorphs are dispersal individuals which could favour the long-term persistence of the process by breeding subsequently in more favourable waters. Therefore, we quantified the spatial behaviour and timing of the metamorphosis of facultative paedomorphic palmate newts Lissotriton helveticus in response to predation risk. We found that fish induced both male and female paedomorphs to hide more often, but behavioural avoidance was not predictive of metamorphosis. Paedomorphs did not metamorphose more in the presence of fish, yet there was an interaction between sex and predation risk in metamorphosis timing. These results improve our understanding of the lower prevalence of paedomorphs in fish environments and of the female-biased sex ratios in natural populations of paedomorphic newts. Integrating sex-dependent payoffs of polyphenisms and dispersal across habitats is therefore essential to understand the evolution of these processes in response to environmental change.
KeywordsBehavioural avoidance Facultative paedomorphosis Invasive species Metamorphosis Polymorphism
We wish to thank J.L. Soulié for allowing access to the pond and two anonymous reviewers for their constructive comments on our manuscript. MD is a Research Director at the Fonds de la Recherche Scientifique—FNRS, LW was a PhD fellow at FNRS and is now funded by a Fyssen Foundation post-doctoral fellowship and NO was a Marie Curie COFUND post-doctoral fellow. This study was funded by Fonds de la Recherche Scientifique—FNRS grant numbers J.008.13 and J.0112.16.
Author contribution statement
MD and LW conceived and supervised the study. MD, LD and NO collected newts in the field. LD carried out behavioural observations. LD, NO, LW, and MD participated to the logistics of the experiment. LW and MD carried out the statistical analyses. MD wrote the first draft of the manuscript, and MD, LW and NO contributed to the revisions. All authors agreed on the final version of the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable institutional and national guidelines for the care and use of animals were followed. The capture permit was issued by DREAL Languedoc-Roussillon (decree 2013274-0001). All experiments were approved by the University of Liège’s animal ethical committee (authorization 1613).
- Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673. https://doi.org/10.1146/annurev.ecolsys.35.021004.112426 CrossRefGoogle Scholar
- Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
- Denoël M, Ficetola GF, Ćirović R, Radović D, Džukić G, Kalezić ML, Vukov TD (2009) A multi-scale approach to facultative padomorphosis of European newts in the Montenegrin karst: distribution pattern, environmental variables and conservation. Biol Conserv 142:509–517. https://doi.org/10.1016/j.biocon.2008.11.008 CrossRefGoogle Scholar
- Ficetola GF, Siesa ME, Manenti R, Bottoni L, De Bernardi F, Padoa-Schioppa E (2011) Early assessment of the impact of alien species: differential consequences of an invasive crayfish on adult and larval amphibians. Divers Distrib 17:1141–1151. https://doi.org/10.1111/j.1472-4642.2011.00797.x CrossRefGoogle Scholar
- 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, FranceGoogle Scholar
- Gould SJ (1977) Ontogeny and phylogeny. Harvard University Press, CambridgeGoogle Scholar
- Istock CA (1967) The evolution of complex life cycle phenomena: an ecological perspective. Evolution 21:592–605. https://doi.org/10.1111/j.1558-5646.1967.tb03414.x CrossRefGoogle Scholar
- Kalezić ML, Džukić G (1985) Ecological aspects of the smooth newt (Triturus vulgaris) paedomorphosis from Montenegro. Ark Biol Nauka 37:43–50Google Scholar
- Knapp RA, Matthews KR, Sarnelle O (2001) Resistance and resilience of alpine lake fauna to fish introductions. Ecol Monogr 71:401–421. https://doi.org/10.1890/0012-9615(2001)071%5b0401:RAROAL%5d2.0.CO;2 CrossRefGoogle Scholar
- Luiselli L, Filippi E, Capula M (2005) Geographic variation in diet composition of the grass snake (Natrix natrix) along the mainland and an island of Italy: the effects of habitat type and interference with potential competitors. Herpetol J 15:221–230Google Scholar
- McKinney ML, McNamara KJ (1991) Heterochrony. The evolution of ontogeny. Plenum Press, New YorkGoogle Scholar
- Oromi N, Valbuena-Ureña E, Soler-Membrives A, Amat F, Camarasa S, Carranza S, Sanuy D, Denoël M (2019) Genetic structure of lake and stream populations in a Pyrenean amphibian (Calotriton asper) reveals evolutionary significant units associated with paedomorphosis. J Zool Res Evol Syst. https://doi.org/10.1111/jzs.12250 Google Scholar
- Roček Z (1995) Heterochrony: response of amphibia to cooling events. Geolines, Praha 3:55–58Google Scholar
- Semlitsch RD, Wilbur HM (1989) Artificial selection for paedomorphosis in the salamander Ambystoma talpoideum. Evolution 43:105–112. https://doi.org/10.1111/j.1558-5646.1989.tb04210.x CrossRefGoogle Scholar
- Shaffer HB (1984) Evolution in a paedomorphic lineage. I. An electrophoretic analysis of the Mexican ambystomatid salamanders. Evolution 38:1194–1206. https://doi.org/10.1111/j.1558-5646.1984.tb05643.x CrossRefGoogle Scholar
- Sih A, Crowley P, McPeek M, Petranka J, Strohmeier K (1985) Predation, competition, and prey communities: a review of field experiments. Annu Rev Ecol Syst 16:269–311. https://doi.org/10.1146/annurev.es.16.110185.001413 CrossRefGoogle Scholar
- Stoks R, Cordoba-Aguilar A (2012) Evolutionary ecology of Odonata: a complex life cycle perspective. Annu Rev Entomol 57:249–265. https://doi.org/10.1146/annurev-ento-120710-100557 CrossRefGoogle Scholar
- Therneau TM (2017) Package ‘survival’. Version 2.41-2Google Scholar
- Van Buskirk J, Schmidt BR (2000) Predator-induced phenotypic plasticity in larval newts: trade-offs, selection, and variation in nature. Ecology 81:3009–3028. https://doi.org/10.1890/0012-9658(2000)081%5b3009:PIPPIL%5d2.0.CO;2 CrossRefGoogle Scholar
- Whiteman HH (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 CrossRefGoogle Scholar
- Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93. https://doi.org/10.1146/annurev.es.11.110180.000435 CrossRefGoogle Scholar