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The evolution of coulour polymorphism in ectothermic vertebrates: a study on asp vipers

Gesuchsteller/in Dubey Sylvain
Nummer 136649
Förderungsinstrument Ambizione
Forschungseinrichtung Département d'Ecologie et d'Evolution Faculté de Biologie et de Médecine Université de Lausanne
Hochschule Universität Lausanne - LA
Hauptdisziplin Oekologie
Beginn/Ende 01.12.2011 - 30.11.2014
Bewilligter Betrag 486'491.00
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Alle Disziplinen (2)

Disziplin
Oekologie
Zoologie

Keywords (11)

Colour polymorphism; Evolution; Genetics; Melanism; Thermoregulation; Adaptation; Climate change; Fitness; Ectotherm; Reptile; Vipera aspis

Lay Summary (Englisch)

Lead
Lay summary
Many factors contribute to a population’s ability to persist in the face of climatic variation. Previous research has emphasised the possible roles of factors such as life-history traits, physiological tolerance to cold, and energy requirements in this respect. My project will focus on another potential contributor to population resilience: the presence of colour polymorphism. An ectotherm’s body colour affects many facets of its existence, including fitness-relevant functions such as thermoregulation, foraging behaviour, metabolic physiology, and prey–predator interactions. Colour polymorphism within a population may thereby expand the range of environmental conditions under which at least some individuals are well-suited to meeting local challenges, even when those challenges vary considerably over small spatial and temporal scales. Body colour is likely to be especially significant for ectothermic animals, because of their reliance upon ambient conditions for thermoregulation. In particular, the relationship between an organism’s colour and the local environment is critical for ambush-foraging ectotherms, that rely upon background colour-matching to evade detection by potential prey. Thus, colour traits in such species will be subject to complex multifunctional optimisation. The ideal model system in which to explore the ecological consequences of colour polymorphism would be a lineage of ectothermic species, widely distributed over Europe and exhibiting discrete colour polymorphism. The genus Vipera fulfils these criteria: (i) It comprises 21 species of medium–sized viviparous snakes distributed in the Palaearctic, and genetic data suggest that these snakes persisted in European refugia more successfully than did most other taxa of reptiles and amphibians; (ii) many viperid taxa exhibit extensive intraspecific color variation: for example, in addition to the “normal” (brown-blotched) form, taxa such as V. aspis, V. berus, and V. seoanei exhibit both melanic morphs and uniformly light–coloured morphs. In fact, V. aspis is one of the most chromatically variable snakes in the world. Its abundance and wide distribution have made this species one of the most intensively studied reptiles in the Northern Hemisphere. It is present over a wide elevational gradient through its range with dorsal colouration varying among as well as within populations. For example, up to 50% of individuals at high elevation are melanistic, probably as an adaptation to enhance rates of heat transfer during basking, whereas “normal” or uniformly light morphs dominate in other populations. The frequency of alternative colour morphs also depends on parameters such as body size and sex; for example, melanic morphs are more common in adult females than in adult males. This system thus is ideally suited to provide a robust understanding of how body colour affects organismal fitness in a population of ectotherms, and how chromatic polymorphism might modify the impact of climate change on population viability. My study centres on the hypothesis that colour polymorphism within vipers allows these taxa to exploit a broader range of environmental conditions, hence increasing their ability to persist despite the challenges imposed by environmental changes such as global warming. I will test this hypothesis using molecular genetic analyses to reveal the phylogenetic history of colour polymorphism within the Vipera clade and to identify genetic determinants of the relevant colour traits. In addition, I will manipulate thermal regimes of captive vipers and conduct field studies to investigate ecological correlates of colour in free-ranging snakes from several sites.

Consequently, my study will clarify the ecological significance of colour variation in a wide-ranging ectotherm species, and provide a direct empirical test of the hypothesis that a population containing individuals of a wide range of dorsal colours is able to exploit a broader range of environmental conditions than could a monomorphic population – and hence, that the evolution of colour polymorphism may have had significant lineage-wide consequences for the ability of viperid snakes to withstand past climatic extremes more successfully than did other taxa. Clearly, understanding how species have dealt with climate change in the past can provide valuable insights into how they are likely to respond in the future, and will shed light on the likely impacts of global warming.

 

Direktlink auf Lay Summary Letzte Aktualisierung: 21.02.2013

Verantw. Gesuchsteller/in und weitere Gesuchstellende

Mitarbeitende

Publikationen

Publikation
Evolutionary and biomedical consequences of internal melanins
Dubey Sylvain, Roulin Alexandre (2014), Evolutionary and biomedical consequences of internal melanins, in Pigment Cell & Melanoma Research , 27, 327-338.
Multiple origins of invasive and « native » water frogs (Pelophylax spp.) in Switzerland
Dubey Sylvain, Leuenberger Julien, Perrin Nicolas (2014), Multiple origins of invasive and « native » water frogs (Pelophylax spp.) in Switzerland, in Biological Journal of the Linnean Society , 112, 442-449.
Role of climate on the presence of colour polymorphism in two montane reptile species
Broennimann Olivier, Ursenbacher Sylvain, Meyer Andreas, Golay Philippe, Monney Jean-Claude, Schmocker Hans, Guisan Antoine, Dubey Sylvain (2014), Role of climate on the presence of colour polymorphism in two montane reptile species, in Biology Letters, 10, 20140638.
The genetic identity of the critically endangered Wimmer’s shrew Crocidura wimmeri
Vogel Peter, Vogel Valerie, Fumagalli Luca, Kadjo Blaise, Kouadio Roger Y, Dubey Sylvain (2014), The genetic identity of the critically endangered Wimmer’s shrew Crocidura wimmeri, in Biological Journal of the Linnean Society , 111, 224-229.
The proopiomelanocortin POMC gene and melanin-based colour polymorphism in a snake
Ducrest Anne-Lyse, Ursenbacher Sylvain, Golay Philippe, Monney Jean-Claude, Mebert Konrad, Roulin Alexandre, Dubey Sylvain (2014), The proopiomelanocortin POMC gene and melanin-based colour polymorphism in a snake, in Biological Journal of the Linnean Society, (111), 160-168.
Amphibians in the diet of European Barn Owls
Roulin Alexandre, Dubey Sylvain (2013), Amphibians in the diet of European Barn Owls, in Bird study, (60), 264-269.
Assessment of terrestrial small mammals with records of the critically endangered shrew Crocidura wimmeri in the Banco National Park (Côte d’Ivoire)
Kadjo Blaise, Kouadio Roger Y, Vogel Valerie, Dubey Sylvain, Vogel Peter (2013), Assessment of terrestrial small mammals with records of the critically endangered shrew Crocidura wimmeri in the Banco National Park (Côte d’Ivoire), in Mammalia , 4, 439-446.
Colour polymorphism and body condition in the Asp viper
Castella Briseïs, Golay Joaquim, Monney Jean-Claude, Golay Philippe, Mebert Konrad, Dubey Sylvain (2013), Colour polymorphism and body condition in the Asp viper, in Journal of Zoology , 290, 273-280.
Effects of season, sex and body size on the feeding ecology of turtle-headed seasnakes (Emydocephalus annulatus) on IndoPacific inshore coral reefs
Goiran Claire, Dubey Sylvain, Shine Richard (2013), Effects of season, sex and body size on the feeding ecology of turtle-headed seasnakes (Emydocephalus annulatus) on IndoPacific inshore coral reefs, in Coral Reefs , 32, 527-538.
Homologous sex chromosomes in three deeply divergent anuran species
Brelsford Alan, Stöck Matthias, Betto-Colliard Caroline, Dubey Sylvain, Dufresnes Christophe, Jourdan-Pineau Helene, Rodrigues Nicolas, Savary Romain, Sermier Roberto, Perrin Nicolas (2013), Homologous sex chromosomes in three deeply divergent anuran species, in Evolution, 67, 2434-2440.
Multiple Paternity in Polyandrous Barn Owls (Tyto alba)
Henry Isabelle, Antoniazza Sylvain, Dubey S, Simon Celine, Waldvogel Celine, Burri Reto, Roulin Alexandre (2013), Multiple Paternity in Polyandrous Barn Owls (Tyto alba), in PLoS ONE , 8, e80112-e80112.
New record of Crocidura zarudnyi from Zabol, Iran
Mohammadi Saeed, Dubey Sylvain, Sabbaghzadeh Ali (2013), New record of Crocidura zarudnyi from Zabol, Iran, in Zoology and Ecology , 23, 162-164.
Population demography of an endangered lizard, the Blue Mountains Water Skink (Eulamprus leuraensis)
Dubey Sylvain, Sinsch Ulrich, Dehling Maximilian, Chevalley Maya, Shine Richard (2013), Population demography of an endangered lizard, the Blue Mountains Water Skink (Eulamprus leuraensis), in BMC Ecology, 13, 4-4.
Phylogeography and dispersal in the velvet gecko (Oedura lesueurii), and potential implications for conservation of an endangered snake (Hoplocephalus bungaroides)
Dubey Sylvain, Croak Benjamin, Pike David A, Webb Jonathan, Shine Richard (2012), Phylogeography and dispersal in the velvet gecko (Oedura lesueurii), and potential implications for conservation of an endangered snake (Hoplocephalus bungaroides), in BMC Evolutionary Biology, 12, 67-86.
Are reptile and amphibian species younger in the Northern Hemisphere than the Southern Hemisphere?
Dubey Sylvain, Shine Richard (2012), Are reptile and amphibian species younger in the Northern Hemisphere than the Southern Hemisphere?, in Journal of Evolutionary Biology , 25, 220-226.
Colour-polymorphic snake species are older
Pizzato Ligia, Dubey Sylvain (2012), Colour-polymorphic snake species are older, in Biological Journal of the Linnean Society, 107(1), 210-218.
Disparity in the timing of vertebrate diversification events between the Northern and Southern Hemispheres
Tingley Reid, Dubey Sylvain (2012), Disparity in the timing of vertebrate diversification events between the Northern and Southern Hemispheres, in BMC Evolutionary Biology, 12, 244.
Host-parasite relationships during a biologic invasion: 75 years postinvasion, cane toads and sympatric Australian frogs retain separate lungworm faunas.
Pizzato Ligia, Kelehear Crystal, Dubey Sylvain, Barton Di, Shine Richard (2012), Host-parasite relationships during a biologic invasion: 75 years postinvasion, cane toads and sympatric Australian frogs retain separate lungworm faunas., in Journal of Wildlife Diseases, 48(4), 951-961.
Multiple refugia and barriers explain the phylogeography of the Valais shrew, Sorex antinorii
Yannic G, Pellissier L, Dubey S, Vega R, Basset P, Mazzoti S, Pecchioli E, Vernesi C, Hauffe HC, Searle JB, Hausser J (2012), Multiple refugia and barriers explain the phylogeography of the Valais shrew, Sorex antinorii, in Biological Journal of the Linnean Society , 105, 864-880.
The occurrence of reptiles in European Barn Owl diet
Roulin Alexandre, Dubey Sylvain (2012), The occurrence of reptiles in European Barn Owl diet, in Bird Study, (iFirst), 1-5.
Evolutionary and biomedical consequences of internal melanins
Dubey Sylvain, Roulin Alexandre, Evolutionary and biomedical consequences of internal melanins, in Pigment Cell & Melanoma Research.
Interpopulation differences in parental care expression
Huang Wen.San, Lin Si-Min, Dubey Sylvain, Pike David A, Interpopulation differences in parental care expression, in Journal of Animal Ecology.
Introduced freshwater blenny influences the diet and body condition of the invasive dice snake in Lake Geneva
Dubey Sylvain, Christe Philippe, Formenti Vanessa, Staub Emilie, Schuerch Johan, Glaizot Olivier, Ursenbacher Sylvain, Introduced freshwater blenny influences the diet and body condition of the invasive dice snake in Lake Geneva, in Journal of Wildlife Management.
Invader immunology: invasion history alters immune-system function in cane toads (Rhinella marina) in tropical Australia
Brown Gregory, Phillips Ben, Dubey Sylvain, Shine Richard, Invader immunology: invasion history alters immune-system function in cane toads (Rhinella marina) in tropical Australia, in Ecology Letters.
Predicting the impacts of climate change on genetic diversity in an endangered lizard species
Dubey Sylvain, Pike David, Shine Richard, Predicting the impacts of climate change on genetic diversity in an endangered lizard species, in Climatic Change.

Zusammenarbeit

Gruppe / Person Land
Formen der Zusammenarbeit
Dr Fabien Aubret (Laboratoire d'Ecologie Expérimentale, CNRS Moulis) Frankreich (Europa)
- vertiefter/weiterführender Austausch von Ansätzen, Methoden oder Resultaten
Prof. Alexandre Roulin (University of Lausanne) Schweiz (Europa)
- vertiefter/weiterführender Austausch von Ansätzen, Methoden oder Resultaten
- Publikation
Dr Sylvain Ursenbacher (Section of Conservation Biology, University of Basel) Schweiz (Europa)
- vertiefter/weiterführender Austausch von Ansätzen, Methoden oder Resultaten
- Publikation

Wissenschaftliche Veranstaltungen

Aktiver Beitrag

Titel Art des Beitrags Titel des Artikels oder Beitrages Datum Ort Beteiligte Personen
4th Biology of the vipers conference Vortrag im Rahmen einer Tagung Impact of colour polymorphism and thermal conditions on thermoregulation, reproductive success, and development in Vipera aspis 10.10.2014 Athens, Griechenland Dubey Sylvain;
Colloque herpétologique du Karch Vortrag im Rahmen einer Tagung Origines multiples des grenouilles vertes en Suisse 07.12.2013 Goldau, Schweiz Dubey Sylvain;
17th European Congress of Herpetology Vortrag im Rahmen einer Tagung Impact of colour polymorphism in interaction with thermal conditions on reproductive success in asp viper (Vipera aspis) 22.08.2013 Veszprém, Ungarn Dubey Sylvain;
7th World Congress of Herpetology Vortrag im Rahmen einer Tagung Are reptile and amphibian species younger in the Northern Hemisphere than in the Southern Hemisphere? 08.08.2012 Vancouver, Kanada Dubey Sylvain;
RESAL (Réseau des animaleries lémaniques) meeting Vortrag im Rahmen einer Tagung Conservation of the Blue Mountains water skink (Eulamprus leuraensis) 02.12.2011 University of Geneva, Schweiz Dubey Sylvain;


Auszeichnungen

Titel Jahr
Prix de la Faculté de Biologie et de Médecine de l'Université de Lausanne pour l'excellence de son travail de Master 2013

Verbundene Projekte

Nummer Titel Start Förderungsinstrument
157244 Evolution of melanin-based colour polymorphism in the asp viper 01.12.2014 Ambizione

Abstract

Many factors contribute to a population’s ability to persist in the face of climatic variation. Previous research has emphasised the possible roles of factors such as life-history traits, physiological tolerance to cold, and energy requirements in this respect. My project will focus on another potential contributor to population resilience: the presence of colour polymorphism. An ectotherm’s body colour affects many facets of its existence, including fitness-relevant functions such as thermoregulation, foraging behaviour, metabolic physiology, and prey-predator interactions. Colour polymorphism within a population may thereby expand the range of environmental conditions under which at least some individuals are well-suited to meeting local challenges, even when those challenges vary considerably over small spatial and temporal scales. Body colour is likely to be especially significant for ectothermic animals, because of their reliance upon ambient conditions for thermoregulation. In particular, the relationship between an organism’s colour and the local environment is critical for ambush-foraging ectotherms, that rely upon background colour-matching to evade detection by potential prey. Thus, colour traits in such species will be subject to complex multifunctional optimisation. The ideal model system in which to explore the ecological consequences of colour polymorphism would be a lineage of ectothermic ambush-foragers, widely distributed over Europe (in present days as well as during historical climatic fluctuations), and exhibiting discrete colour polymorphism. The genus Vipera fulfils these criteria: (i) It comprises 21 species of medium-sized viviparous snakes distributed in the Palaearctic, and genetic data suggest that these snakes persisted in European refugia more successfully than did most other taxa of reptiles and amphibians; (ii) many viperid taxa exhibit extensive intraspecific color variation: for example, in addition to the “normal” (brown-blotched) form, taxa such as V. aspis, V. berus, and V. seoanei exhibit both melanic morphs and uniformly light-coloured morphs. In fact, the asp viper (V. aspis) is one of the most chromatically variable snakes in the world. Its abundance and wide distribution have made this species one of the most intensively studied reptiles in the Northern Hemisphere. It is present over a wide elevational gradient through its range (as in Switzerland) with dorsal colouration varying among as well as within populations. For example, up to 50% of individuals at high elevation are melanistic, probably as an adaptation to enhance rates of heat transfer during basking, whereas “normal” or uniformly light (concolor) morphs dominate in other populations. The frequency of alternative colour morphs also depends on parameters such as body size and sex; for example, melanic morphs are more common in adult females than in adult males. This system thus is ideally suited to provide a robust understanding of how body colour affects organismal fitness in a population of ectotherms, and how chromatic polymorphism might modify the impact of climate change on population viability. My study centres on the hypothesis that colour polymorphism within vipers allows these taxa to exploit a broader range of environmental conditions, hence increasing their ability to persist despite the challenges imposed by environmental changes such as global warming. I will test this hypothesis using molecular genetic analyses to reveal the phylogenetic history of colour polymorphism within the Vipera clade and to identify genetic determinants of the relevant colour traits. In addition, I will manipulate thermal regimes of captive vipers (to explore behavioural responses to environmental conditions for various colour morphs) and conduct field studies to investigate ecological correlates of colour in free-ranging snakes from several sites. More specifically, my research will: (a) identify the gene(s) responsible for the melanin-based colour polymorphism in three viper species (V. aspis, V. berus, V. seoanei) by sequencing candidate genes (e.g. MC1R, TYRP1) and by comparative analysis of full transcriptomes via next-generation sequencing technology (454/Roche, Solexa) in melanic, concolor, and “normal” individuals from multiple populations, (b) determine the number of independent origins of colour polymorphism within this lineage, by performing phylogenetic analyses of the gene(s) identified in point a) (multiple independent evolutionary origins of polymorphism would strongly support the hypothesis that colour polymorphism offers a significant selective advantage), (c) quantify the fitness consequences of the interaction between thermal conditions and snake colour, by manipulating basking opportunities for gravid V. aspis and their offspring in the laboratory (i.e., identify morph-specific thermal optima for ecological traits such as feeding rate, body conditions, fecundity, and growth rate), and (d) evaluate how a snake’s body colour influences fitness-relevant traits in the field and/or in the laboratory, by quantifying aspects of behaviour: antipredator responses, thermoregulatory tactics, heating and cooling rates, habitat selection (especially, background colour-matching in selection of ambush sites), organismal performance (sprint speed, endurance, strike speed and accuracy) of snakes of different colour morphs. My study will clarify the ecological significance of colour variation in a wide-ranging ectotherm species, and provide a direct empirical test of the hypothesis that a population containing individuals of a wide range of dorsal colours is able to exploit a broader range of environmental conditions than could a monomorphic population - and hence, that the evolution of colour polymorphism may have had significant lineage-wide consequences for the ability of viperid snakes to withstand past climatic extremes (e.g. Pleistocene glaciations) more successfully than did other (monomorphic) taxa. Clearly, understanding how species have dealt with climate change in the past can provide valuable insights into how they are likely to respond in the future, and will shed light on the likely impacts of global warming.
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