Facultative paedomorphosis as a mechanism promoting intraspecific niche differentiation

The paginated published version of this paper is available on Wiley Online Library (see DOI link). The author version is available in open access hereunder.

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

trophic ecology; food web; feeding ecology; resource partitioning; isotopic niche; stable isotope; facultative paedomorphosis; polyphenism; polymorphism; Alps; Lac de la Cabane; alpine lake; alpine newt; Ichthyosaura alpestris; Shannon index; mixing model; biomass; diet; stomach flushing; predation; prey; amphibian; triton alpestre; régime alimentaire; carbon; nitrogen; SIBER; SIAR; heterogeneous environment; open niche; vacant niche; sexual difference; sex; heterochrony; foraging

Abstract :

[en] Organisms with complex life cycles are characterized by a metamorphosis that allows for a major habitat shift and the exploitation of alternative resources. However, metamorphosis can be bypassed in some species through a process called paedomorphosis, resulting in the retention of larval traits at the adult stage and is considered important at both micro- and macroevolutionary scales. In facultatively paedomorphic populations of newts, some individuals retain gills and a fully aquatic life at the adult stage (paedomorphs), while others undergo complete metamorphosis (metamorphs), allowing for a terrestrial life-stage. Because facultative paedomorphosis affects trophic structures and feeding mechanism of newts, one hypothesis is that it may be maintained as a trophic polymorphism, with the advantage to lessen intraspecific competition during the shared aquatic life-stage. Here, we tested this hypothesis combining stomach content data with stable isotope techniques, using carbon and nitrogen stable isotopes, in facultatively paedomorphic alpine newts Ichthyosaura alpestris. Both stomach content and stable isotope analyses showed that paedomorphs had smaller trophic niches and were more reliant on pelagic resources, while metamorphs relied more on littoral resources, corresponding to a polyphenism along the littoral-pelagic axis and the extension of the population's trophic niche to otherwise ‘underused’ pelagic resources by paedomorphs. Interestingly, stable isotopes revealed that the trophic polyphenism was less marked in males than in females and potentially linked to sexual activity. Although paedomorphosis and metamorphosis are primarily seen as results of tradeoffs between the advantages of using aquatic versus terrestrial habitats, this study provides evidence that additional forces, such as intraspecific trophic niche differences between morphs and trophic niche expansion, may play an important role in the persistence of this dimorphism in heterogeneous environments. Moreover, the different patterns found in males and females show the importance of considering sex to understand the evolutionary ecology of trophic polymorphisms.

Research Center/Unit :

AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège

Disciplines :

Aquatic sciences & oceanology
Environmental sciences & ecology

Author, co-author :

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

Sturaro, Nicolas ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique

Lepoint, Gilles ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique

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

Language :

English

Title :

Facultative paedomorphosis as a mechanism promoting intraspecific niche differentiation

Publication date :

March 2018

Journal title :

Oikos

ISSN :

0030-1299

eISSN :

1600-0706

Publisher :

Blackwell Publishing

Volume :

127

Issue :

Pages :

427-439

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

http://www.oikosjournal.org/blog/forever-young-strategy-niche-differentiation

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique
ULg FSR - Université de Liège. Fonds spéciaux pour la recherche

Available on ORBi :

since 17 October 2017

Statistics

Number of views

387 (108 by ULiège)

Number of downloads

415 (30 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Anderson M. J. 2001. A new method for non-parametric multivariate analysis of variance. – Austral Ecol. 26: 32–46.
Anderson M. J. Walsh D. C. I. 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? – Ecol. Monogr. 83: 557–574.
Anderson M. J. et al. 2008. PERMANOVA+ for PRIMER: a guide to software and statistical methods.
Arntzen A. J. W. et al. 1999. Marking and tissue sampling effects on body condition and survival in the newt Triturus cristatus. – J. Herpetol. 33: 567–576.
Benke A. C. et al. 1999. Length-mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeastern United States. − J. N. Am. Benthol. Soc. 18: 308–343.
Bolnick D. I. 2001. Intraspecific competition favours niche width expansion in Drosophila melanogaster. – Nature 410: 463–466.
Bolnick D. I. Fitzpatrick B. M. 2007. Sympatric speciation: models and empirical evidence. – Annu. Rev. Ecol. Evol. Syst. 38: 459–487.
Bolnick D. I. et al. 2003. The ecology of individuals: incidence and implications of individual specialization. – Am. Nat. 161: 1–28.
Bolnick D. I. et al. 2010. Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. – Proc. R. Soc. B 277: 1789–1797.
Chevin L.-M. Lande R. 2013. Evolution of discrete phenotypes from continuous norms of reaction. – Am. Nat. 182: 13–27.
Clarke K. R. 1993. Non-parametric multivariate analyses of changes in community structure. – Aust. J. Ecol. 18: 117–143.
Clarke K. R. Gorley R. N. 2006. PRIMER v6: User manual/tutorial. – Plymouth Marine Laboratory.
Cloyed C. S. et al. 2015. Trophic discrimination factors and incorporation rates of carbon- and nitrogen-stable isotopes in adult green frogs, Lithobates clamitans. – Physiol. Biochem. Zool. 88: 576–585.
Coplen T. B. 2011. Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. – Rapid Commun. Mass Spectrom. 25: 2538–2560.
Darwin C. 1859. On the origin of species by means of natural selection. – John Murray.
Denoël M. 2002. Paedomorphosis in the alpine newt (Triturus alpestris): decoupling behavioural and morphological change. – Behav. Ecol. Sociobiol. 52: 394–399.
Denoël M. 2004. Feeding performance in heterochronic alpine newts is consistent with trophic niche and maintenance of polymorphism. – Ethology 110: 127–136.
Denoël M. 2017. On the identification of paedomorphic and overwintering larval newts based on cloacal shape: review and guidelines. – Curr. Zool. 63: 165– 173.
Denoël M. Joly P. 2001. Adaptive significance of facultative paedomorphosis in Triturus alpestris (Amphibia, Caudata): resource partitioning in an alpine lake. – Freshwater Biol. 46: 1387–1396.
Denoël M. Ficetola G. F. 2014. Heterochrony in a complex world: disentangling environmental processes of facultative paedomorphosis in an amphibian. – J. Anim. Ecol. 83: 606–615.
Denoël M. Winandy L. 2015. The importance of phenotype diversity in conservation: resilience of palmate newt morphotypes after fish removal in Larzac ponds (France). – Biol. Conserv. 192: 402–408.
Denoël M. et al. 2001a. Biogeography and ecology of paedomorphosis in Triturus alpestris (Amphibia, Caudata). – J. Biogeogr. 28: 1271–1280.
Denoël M. et al. 2001b. Sexual compatibility between two heterochronic morphs in the alpine newt, Triturus alpestris. – Anim. Behav. 62: 559–566.
Denoël M. et al. 2002. Short- and long term advantages of an alternative ontogenetic pathway. – Biol. J. Linn. Soc. 77: 105–112.
Denoël M. et al. 2004. Trophic specialisations in alternative heterochronic morphs. – Naturwissenschaften 91: 81–84.
Denoël M. et al. 2005. Evolutionary ecology of facultative paedomorphosis in newts and salamanders. – Biol. Rev. Camb. Phil. Soc. 80: 663–671.
Denoël M. et al. 2016. Newt life after fish introduction: extirpation of paedomorphosis in a mountain fish lake and newt use of satellite pools. – Curr. Zool. 62: 61–69.
Dumont H. J. et al. 1975. The dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters. − Oecologia 19: 75–97.
Fukumori K. et al. 2008. Stable isotopes reveal life history polymorphism in the coastal fish Apogon notatus. − Mar. Ecol. Prog. Ser. 362: 279–289.
Gabor C. R. Halliday T. R. 1997. Sequential mate choice by multiply mating smooth newts: females become more choosy. – Behav. Ecol. 8: 162–166.
Gillespie J. H. 2013. Application of stable isotope analysis to study temporal changes in foraging ecology in a highly endangered amphibian. – PLoS One 8: e53041.
Hayden B. et al. 2014. Lake morphometry and resource polymorphism determine niche segregation between cool-and cold-water-adapted fish. – Ecology 95: 538–552.
Jackson A. L. et al. 2011. Comparing isotopic niche widths among and within communities: SIBER - Stable isotope bayesian ellipses in R. – J. Anim. Ecol. 80: 595–602.
Jackson M. C. et al. 2012. Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. – PLoS One 7: 1–12.
Jakob E. M. et al. 1996. Estimating fitness: A comparison of body condition indices. – Oikos 77: 61–67.
Joly P. 1981. Le comportement prédateur du triton alpestre (Triturus alpestris). I. Etude descriptive. – Biol. Behav. 6: 339–355.
Joly P. 1987. Le régime alimentaire des amphibiens méthodes d’étude. – Alytes 6: 11–17.
Kornfield I. L. et al. 1982. The cichlid fish of Cuatro Cienegas, Mexico: direct evidence of conspecificity among distinct trophic morphs. – Evolution 36: 658–664.
Lauder G. V. Shaffer B. H. 1993. Design of feeding systems in aquatic vertebrates: major patterns and their evolutionary interpretations. – In: Hanken J. and Hall B. K. (eds), The skull, Vol. 3. Functional and evolutionary mechanisms. Chicago Univ. Press, pp. 113–149.
Lauder G. V. Reilly S. M. 1994. Amphibian feeding behavior: comparative biomechanics and evolution. – In: Bels V. et al. (eds), Advances in comparative and environmental physiology, Vol. 18. Springer-Verlag, pp. 163–195.
Laudet V. 2011. The origins and evolution of vertebrate metamorphosis. – Curr. Biol. 21: R726–R737.
Layman C. A. et al. 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? – Ecology 88: 42–48.
Lejeune B. et al. 2017. Data from: Facultative paedomorphosis as a mechanism promoting intraspecific niche differentiation. – Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.7m3dq.
Malmquist H. J. 1992. Phenotype-specific feeding behaviour of two arctic charr Salvelinus alpinus morphs. – Oecologia 92: 354–361.
Malmquist H. J. et al. 1992. Diet differentiation in polymorphic arctic charr in Thingvallavatn, Iceland. – J. Anim. Ecol. 61: 21–35.
Mantel S. K. et al. 2004. Foodweb structure in a tropical Asian forest stream. – J. N. Am. Benthol. Soc. 23: 728–755.
McKinney M. L. McNamara K. J. 1991. Heterochrony: the evolution of ontogeny. – Plenum Press.
Meyer A. 1990. Ecological and evolutionary consequences of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae). – Biol. J. Linn. Soc. 39: 279–299.
Miaud C. 1993. Predation of newt eggs (Triturus alpestris and T. helveticus) – identification of predators and protective role of oviposition behavior. – J. Zool. 231: 575–582.
Murren C. J. et al. 2015. Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. – Heredity 115: 293–301.
Newsome S. D. et al. 2007. A niche for isotope ecology. – Front. Ecol. Environ. 5: 429–436.
Oromi N. et al. 2016. High gene flow between alternative morphs and the evolutionary persistence of facultative paedomorphosis. – Sci. Rep. 6: 32046.
Parnell A. et al. 2010. Source partitioning using stable isotopes: coping with too much variation. – PLoS One 5: e9672.
Pfennig D. W. 1992. Proximate and functional causes of polyphenism in an anuran tadpole. – Funct. Ecol. 6: 167–174.
Pfennig D. W. McGee M. 2010. Resource polyphenism increases species richness: a test of the hypothesis. – Phil. Trans. R. Soc. B 365: 577–591.
Pfennig D. W. Pfennig K. S. 2010. Character displacement and the origins of diversity. – Am. Nat. 176: S26–S44.
Proulx R. Magnan P. 2004. Contribution of phenotypic plasticity and heredity to the trophic polymorphism of lacustrine brook charr (Salvelinus fontinalis M.). – Evol. Ecol. Res. 6: 503–522.
Quevedo M. et al. 2009. Intrapopulation niche partitioning in a generalist predator limits food web connectivity. – Ecology 90: 2263–2274.
Recuero E. et al. 2014. Evolutionary history of Ichthyosaura alpestris (Caudata, Salamandridae) inferred from the combined analysis of nuclear and mitochondrial markers. – Mol. Phylogenet. Evol. 81: 207–220.
Robinson B. W. Parsons K. J. 2002. Changing times, spaces, and faces: tests and implications of adaptive morphological plasticity in the fishes of northern postglacial lakes. – Can. J. Fish. Aquat. Sci. 59: 1819–1833.
Rohde K. 1991. Intra- and interspecific interactions in low density populations in resource-rich habitats. – Oikos 60: 91–104.
Sage R. D. Selander R. K. 1975. Trophic radiation through polymorphism in cichlid fishes. – Proc. Natl Acad. Sci. USA 72: 4669–4673.
Schabetsberger R. 1994. Gastric evacuation rates of adult and larval alpine newts (Triturus alpestris) under laboratory and field conditions. – Freshwater. Biol. 31: 143–151.
Schluter D. 2000. The ecology of adaptive radiation. – Oxford Univ. Press.
Schluter D. Rambaut A. 1996. Ecological speciation in postglacial fishes. – Phil. Trans. R. Soc. B 351: 807–814.
Schmidt P. S. et al. 2000. Environmental heterogeneity and balancing selection in the acorn barnacle Semibalanus balanoides. – Proc. R. Soc. B 267: 379–384.
Schoener T. W. 1968. The Anolis lizards of Bimini: resource partitioning in a complex fauna. – Ecology 49: 704–726.
Seliskar A. Pehani H. 1935. Limnologische Beiträge zum Problem der Amphibienneotenie (Beobachtungen an Tritonen der Triglavseen). – Verh. Int. Ver. Theor. Angew. Limnol. 7: 263–294.
Semlitsch R. D. 1987. Paedomorphosis in Ambystoma talpoideum: effects of density, food and pond drying. – Ecology 68: 994–1002.
Shannon C. E. 1948. A mathematical theory of communication. – Bell Syst. Tech. J. 27: 379–423.
Shedd K. R. et al. 2015. Ecological release leads to novel ontogenetic diet shift in kokanee (Oncorhynchus nerka). – Can. J. Fish. Aquat. Sci. 72: 1718–1730.
Smith J. M. 1966. Sympatric speciation. – Am. Nat. 100: 637–650.
Smith T. B. Skúlason S. 1996. Evolutionary significance of resource polymorphisms in fishes, amphibians and birds. – Annu. Rev. Ecol. Syst. 27: 111–133.
Svanbäck R. Eklöv P. 2003. Morphology dependent foraging efficiency in perch: a tradeoff for ecological specialization? – Oikos 102: 273–284.
Svanbäck R. et al. 2008. Intraspecific competition drives multiple species resource polymorphism in fish communities. – Oikos 117: 114–124.
Swanson B. O. et al. 2003. Trophic polymorphism and behavioral differences decrease intraspecific competition in a cichlid, Herichthys minckleyi. – Ecology 84: 1441–1446.
Van Valen L. 1965. Morphological variation and width of ecological niche. – Am. Nat. 99: 377–390.
West-Eberhard M. J. 1989. Phenotypic plasticity and the origins of diversity. – Annu. Rev. Ecol. Syst. 20: 249–278.
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. Semlitsch R. D. 2005. Asymmetric reproductive isolation among polymorphic salamanders. – Biol. J. Linn. Soc. 86: 265–281.
Whiteman H. H. et al. 1996. Growth and foraging consequences of facultative paedomorphosis in the tiger salamander Ambystoma tigrinum nebulosum. – Evol. Ecol. 10: 433–446.
Whiteman H. H. et al. 2012. Larval growth in polyphenic salamanders: making the best of a bad lot. – Oecologia 168: 109–118.
Wilbur H. M. Collins J. P. 1973. Ecological aspects of amphibian metamorphosis. – Science 182: 1305–1314.
Wimberger P. H. 1994. Trophic polymorphisms, plasticity and speciation in vertebrates. – In: Stouder D. J. et al. (eds), Theory and application in fish feeding ecology. Univ. of South Carolina Press, pp. 19–43.
Winandy L. Denoël M. 2015. Expression of sexual ornaments in a polymorphic species: phenotypic variation in response to environmental risk. – J. Evol. Biol. 28: 1049–1056.
Woods P. J. et al. 2013. Resource polymorphism and diversity of arctic charr Salvelinus alpinus in a series of isolated lakes. – J. Fish Biol. 82: 569–587.