Barred, blotched or intermediate? A photographic-based survey on the spatial distribution of <em>Vipera aspis</em> phenotypes from central-southern Italy
DOI:
https://doi.org/10.11160/bah.288Keywords:
admixture, asp viper, francisciredi, hybridization, hugyi, transitionAbstract
Variation in animal colouration, which holds ecological and evolutionary significance, is evident in snakes, including the polytypic and highly polymorphic asp viper Vipera aspis. This species, currently acknowledged with four subspecies, features three of them (V. a. aspis, V. a. francisciredi and V. a. hugyi) within the Italian territory, each displaying distinct dorsal patterns. Analysing 143 georeferenced photos from personal surveys and citizen science, the present study explores transition areas between V. a. francisciredi and V. a. hugyi, revealing the coexistence of three dorsal pattern phenotypes (i.e. francisciredi, hugyi, and intermediate) across central-southern Italy. The outcome of the work reveals occurrences of francisciredi phenotypes considerably beyond the southern limit indicated in recent literature. Remarkably, intermediate phenotypes cover a significant portion of southern Italy, including Apulia (three records), Basilicata (six records) and Campania (three records) regions, and overlapping with both hugyi and francisciredi ranges. These findings suggest asymmetrical gene flow from northern to southern populations, resembling patterns observed in other reptiles. The intricate distribution of colour phenotypes underscores the necessity for molecular investigations to comprehend the genetic context and evolutionary history of V. aspis populations from central-southern Italy.
References
Andrén, C. & Nilson, G. (1981). Reproductive success and risk of predation in normal and melanistic colour morphs of the adder, Vipera berus. Biological Journal of the Linnean Society 15: 235-246.
Asztalos, M.; Schultze, N.; Ihlow, F.; Geniez, P.; Berroneau, M.; Delmas, C.; Guiller, G.; Legentilhomme, J.; Kindler, C. & Fritz, U. (2020). How often do they do it? An in-depth analysis of the hybrid zone of two grass snake species (Natrix astreptophora and Natrix helvetica). Biological Journal of the Linnean Society 131: 756-773.
Barbanera, F.; Zuffi, M.A.L.; Guerrini, M.; Gentilli, A.; Tofanelli, S.; Fasola, M. & Dini, F. (2009). Molecular phylogeography of the asp viper Vipera aspis (Linnaeus, 1758) in Italy: Evidence for introgressive hybridization and mitochondrial DNA capture. Molecular Phylogenetics and Evolution 52: 103-114.
Bechtel, H.B. (1978). Color and pattern in snakes (Reptilia, Serpentes). Journal of Herpetology 12: 521-532.
Bisconti, R.; Porretta, D.; Arduino, P.; Nascetti, G. & Canestrelli, D. (2018). Hybridization and extensive mitochondrial introgression among fire salamanders in peninsular Italy. Scientific Reports 8: 13187.
Bruno, S. (1985). Le Vipere d’Italia e d’Europa. Edagricole, Bologna, Italy.
Castella, B.; Golay, J.; Monney, J.‐C.; Golay, P.; Mebert, K. & Dubey, S. (2013). Melanism, body condition and elevational distribution in the asp viper. Journal of Zoology 290: 273-280.
Cattaneo, A. (1985). Il Colubro Ferro di cavallo dell’isola di Pantelleria: Coluber hippocrepis nigrescens subsp. nova. Atti della Società Italiana di Scienze Naturali e del Museo Civico di Storia Naturale in Milano 126: 165-184.
Clusella-Trullas, S.; Van Wyk, J.H. & Spotila, J.R. (2007). Thermal melanism in ectotherms. Journal of Thermal Biology 32: 235-245.
Cope, E.D. (1900). The Crocodilians, Lizards, and Snakes of North America. US Government Printing Office, Washington, DC, USA.
Derryberry, E.P.; Claramunt, S.; Derryberry, G.; Chesser, R.T.; Cracraft, J.; Aleixo, A.; Pérez‐Emán, J.; Remsen, J.V. & Brumfield, R.T. (2011). Lineage diversification and morphological evolution in a large‐scale continental radiation: the Neotropical ovenbirds and woodcreepers (Aves: Furnariidae). Evolution 65: 2973-2986.
De Smedt, J. (2006). The Vipers of Europe. JDS-Verlag, Füssen, Germany.
Di Nicola, M.R. (2019). A revised dichotomous key to the snakes of Italy (Reptilia, Squamata, Serpentes), according to recent systematic updates. Zootaxa: 4686.
Di Nicola, M.R. & Faraone, F.P. (2020). Vipera aspis hugyi (Southern Italian Asp). Coloration. Herpetological Review 51: 631.
Di Nicola, M.R. & Meier, G.J. (2013). Vipera aspis hugyi (Southern Italian asp). Melanism. Herpetological Review 44: 698.
Di Nicola, M.R.; Cavigioli, L.; Luiselli, L. & Andreone, F. (2021). Anfibi & Rettili d’Italia - Edizione Aggiornata. Edizioni Belvedere, Latina, Italy.
Di Nicola, M.R.; Melfi, R.; Faraone, F.P.; Iversen, D.L.N.; Giacalone, G.; Paolino, G. & Lo Valvo, M. (2022). Preliminary genetic characterisation of Southern Smooth Snake Coronella girondica (Serpentes, Colubridae) populations in Italy, with some considerations on their alpine distribution. Acta Herpetologica 17: 115-124.
Di Nicola, M.R.; Pozzi, A.V.; Mezzadri, S.; Faraone, F.P.; Russo, G.; Dorne, J.L.M.C. & Minuti, G. (2023). The endangered Sardinian grass snake: distribution update, bioclimatic niche modelling, dorsal pattern characterisation, and literature review. Life 13: 1867.
Di Nicola, M.R.; Faraone, F.P.; Pozzi, A.V.; Borgianni, N.; Laddaga, L.; Dorne, J.L.C.M. & Minuti, G. (2024). The tale of the black viper: distribution and bioclimatic niche modelling of melanistic Vipera aspis in Italy. Acta Herpetologica 19: https://10.36253/a_h-15271.
Duarte, M.D.O.; Freitas, T.M.D.S. & Prudente, A.L.D.C. (2015). Polychromatism of populations of Corallus hortulanus (Squamata: Boidae) from the southern Amazon Basin, Brazil. Acta Amazonica 45: 373-382.
Dubey, S.; Zwahlen, V.; Mebert, K.; Monney, J.-C.; Golay, P.; Ott, T.; Durand, T.; Thiery, G.; Kaiser, L.; Geser, S.N. & Ursenbacher, S. (2015). Diversifying selection and color-biased dispersal in the asp viper. BMC Evolutionary Biology 15: 99.
Faraone, F.P.; Giacalone, G.; Canale, D.E.; D’Angelo, S.; Favaccio, G.; Garozzo, V.; Giancontieri, G.L.; Isgrò, C.; Melfi, R.; Morello, B.; Navarria, F.; Russo, G.; Tinnirello, V.; Torre, A.; Torre, D.; Torre, G.; Urso, G.; Vinci, P.; Zizzo, M.G. & Marrone, F. (2017). Tracking the invasion of the red swamp crayfish Procambarus clarkii (Girard, 1852) (Decapoda Cambaridae) in Sicily: a “citizen science” approach. Biogeographia – The Journal of Integrative Biogeography 32: 25-29.
Faraone, F.P.; Melfi, R.; Di Nicola, M.R.; Giacalone, G. & Lo Valvo, M. (2020). Phylogenetic relationships of the Italian populations of Horseshoe Whip Snake Hemorrhois hippocrepis (Serpentes, Colubridae). Acta Herpetologica 15: 129-135.
Forsman, A. (2016). Is colour polymorphism advantageous to populations and species? Molecular Ecology 25: 2693-2698.
Fratianni, S. & Acquaotta, F. (2017). The climate of Italy, In M. Soldati & M. Marchetti (eds.) Landscapes and Landforms of Italy. Springer International Publishing, Cham, Switzerland, pp. 29-38.
Fritz, U. & Ihlow, F. (2022). Citizen science, taxonomy and grass snakes: iNaturalist helps to clarify variation of coloration and pattern in Natrix natrix subspecies. Vertebrate Zoology 72: 533-549.
Galán, P. (2000). Females That imitate males: dorsal coloration varies with reproductive stage in female Podarcis bocagei (Lacertidae). Copeia 2000: 819-825.
Geniez, P.; Cluchier, A. & De Haan, C.C. (2006). A multivariate analysis of the morphology of the colubrid snake Malpolon monspessulanus in Morocco and Western Sahara: biogeographic and systematic implications. Salamandra 42: 65-82.
Golay, P.; Monney, J.-C.; Conelli, A.; Durand, T.; Thiery, G.; Zuffi, M.A.L. & Ursenbacher, S. (2008). Systematics of the Swiss asp vipers: some implications for the European Vipera aspis (Linnaeus, 1758) complex (Serpentes: Viperidae) - A tribute to Eugen Kramer. Amphibia-Reptilia 29: 71-83.
Guiller, G.; Lourdais, O. & Ursenbacher, S. (2017). Hybridization between a Euro‐Siberian (Vipera berus) and a Para‐Mediterranean viper (V. aspis) at their contact zone in western France. Journal of Zoology 302: 138-147.
Haklay, M.; Dörler, D.; Heigl, F.; Manzoni, M.; Hecker, S. & Vohland, K. (2021). What is Citizen Science? The challenges of definition, In: K. Vohland, A. Land-Zandstra, L. Ceccaroni, R. Lemmens, J. Perelló, M. Ponti, R. Samson & K. Wagenknecht (eds.) The Science of Citizen Science. Springer International Publishing, Cham, Switzerland, pp. 13-33.
Hijmans, R.J. (2023a). Raster: Geographic Data Analysis and Modeling. R Foundation for Statistical Computing, Vienna, Austria. Available at https://cran.r-project.org/web/packages/raster/raster.pdf. Retrieved on 06 February 2024.
Hijmans, R.J. (2023b). Terra: Spatial Data Analysis. R Foundation for Statistical Computing, Vienna, Austria. Available at https://cran.r-project.org/web//packages/terra/terra.pdf. Retrieved on 06 February 2024.
Huyghe, K.; Van Oystaeyen, A.; Pasmans, F.; Tadić, Z.; Vanhooydonck, B. & Van Damme, R. (2010). Seasonal changes in parasite load and a cellular immune response in a colour polymorphic lizard. Oecologia 163: 867-874.
Kumar, B. (2009). Nove najdbe laškega gada (Vipera aspis) v Sloveniji. Natura Sloveniae 11: 59-63.
Lanza, B. & Vanni, S. (1989). Vipera Comune e Lucertole Muraiole. Atlante Tematico d’Italia. 29. Zoogeografia I. Touring Club Italiano e Consiglio Nazionale Delle Ricerche, Rome, Italy.
Lattanzio, M.S. & Buontempo, M.J. (2021). Ecogeographic divergence linked to dorsal coloration in eastern hog-nosed snakes (Heterodon platirhinos). Herpetologica 77: 134-145.
Lee, M.S.Y.; Sanders, K.L.; King, B. & Palci, A. (2016). Diversification rates and phenotypic evolution in venomous snakes (Elapidae). Royal Society Open Science 3: 150277.
Ligon, R.A. & McGraw, K.J. (2013). Chameleons communicate with complex colour changes during contests: different body regions convey different information. Biology Letters 9: 20130892.
Marshall, K.L.A.; Philpot, K.E. & Stevens, M. (2016). Microhabitat choice in island lizards enhances camouflage against avian predators. Scientific Reports 6: 19815.
Martínez-Freiría, F.; Santos, X.; Pleguezuelos, J.M.; Lizana, M. & Brito, J.C. (2009). Geographical patterns of morphological variation and environmental correlates in contact zones: a multi-scale approach using two Mediterranean vipers (Serpentes). Journal of Zoological Systematics and Evolutionary Research 47: 357-367.
Martínez-Freiría, F.; Toyama, K.S.; Freitas, I. & Kaliontzopoulou, A. (2020). Thermal melanism explains macroevolutionary variation of dorsal pigmentation in Eurasian vipers. Scientific Reports 10: 16122.
Masseti, M. & Zuffi, M.A.L. (2011). On the origin of the asp viper Vipera aspis hugyi Schinz, 1833, on the island of Montecristo, Northern Tyrrhenian Sea (Tuscan archipelago, Italy). Herpetological Bulletin 117: 1-9.
Mebert, K.; Zwahlen, V.; Golay, P.; Durand, T. & Ursenbacher, S. (2011). Ungewöhnlich hoher Farb-Polymorphismus in alpinen Aspisvipern in Frankreich? Zufall oder natürliche Selektion? Elaphe 19: 13-19.
Meier, N.; Lucek, K.; Zuffi, M.A.L.; Storniolo, F.; Mezzasalma, M.; Geniez, P.; Dubey, S.; Sacchi, R.; Scali, S. & Ursenbacher, S. (2023). Extensive gene flow suggests lack of reproductive barriers between the two subspecies of the green whip snake, Hierophis viridiflavus (Squamata: Colubridae). Biological Journal of the Linnean Society 141: 133-147.
Niskanen, M. & Mappes, J. (2005). Significance of the dorsal zigzag pattern of Vipera latastei gaditana against avian predators. Journal of Animal Ecology 74: 1091-1101.
Pfennig, D.W.; Wund, M.A.; Snell-Rood, E.C.; Cruickshank, T.; Schlichting, C.D. & Moczek, A.P. (2010). Phenotypic plasticity’s impacts on diversification and speciation. Trends in Ecology and Evolution 25: 459-467.
Pinna, S. (2017). Lineamenti di Climatologia. Aracne Editrice, Ariccia, Italy.
Pizzatto, L. & Dubey, S. (2012). Colour-polymorphic snake species are older. Biological Journal of the Linnean Society 107: 210-218.
Pizzigalli, C.; Banfi, F.; Ficetola, G.F.; Falaschi, M.; Mangiacotti, M.; Sacchi, R.; Zuffi, M.A.L. & Scali, S. (2020). Eco-geographical determinants of the evolution of ornamentation in vipers. Biological Journal of the Linnean Society 130: 345-358.
R Core Team (2022): R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Regnet, R.A.; Quintela, F.M.; Roedder, D. & Loebmann, D. (2022). Attributes of the population structure and ventral polychromatism of Helicops infrataeniatus Jan, 1865 (Serpentes, Colubridae, Dipsadinae) in subtropical Brazil. North-Western Journal of Zoology 18:161-167.
Reynolds, R.G.; Gerber, G.P.; Burgess, J.P.; Waters, G.H. & Manco, B.N. (2020). Characterization of Color Pattern Dimorphism in Turks and Caicos Boas, Chilabothrus chrysogaster chrysogaster, on Big Ambergris Cay, Turks and Caicos Islands. Journal of Herpetology 54: 337-346.
Salvi, D.; Lucente, D.; Mendes, J.; Liuzzi, C.; Harris, D.J. & Bologna, M.A. (2017). Diversity and distribution of the Italian Aesculapian snake Zamenis lineatus : A phylogeographic assessment with implications for conservation. Journal of Zoological Systematics and Evolutionary Research 55: 222-237.
Santos, X.; Vidal-García, M.; Brito, J.C.; Fahd, S.; Llorente, G.A.; Martínez-Freiría, F.; Parellada, X.; Pleguezuelos, J.M. & Sillero, N. (2014). Phylogeographic and environmental correlates support the cryptic function of the zigzag pattern in a European viper. Evolutionary Ecology 28: 611-626.
Schultze, N.; Laufer, H.; Kindler, C. & Fritz, U. (2019). Distribution and hybridisation of barred and common grass snakes (Natrix helvetica, N. natrix) in Baden-Württemberg, south-western Germany. Herpetozoa 32: 229-236.
Schultze, N.; Spitzweg, C.; Corti, C.; Delaugerre, M.; Di Nicola, M.R.; Geniez, P.; Lapini, L.; Liuzzi, C.; Lunghi, E.; Novarini, N.; Picariello, O.; Razzetti, E.; Sperone, E.; Stellati, L.; Vignoli, L.; Asztalos, M.; Kindler, C. & Fritz, U. (2020). Mitochondrial ghost lineages blur phylogeography and taxonomy of Natrix helvetica and N. natrix in Italy and Corsica. Zoologica Scripta 49: 395-411.
Sindaco, R. & Razzetti, E. (2021). An updated check-list of Italian amphibians and reptiles. Natural History Sciences 8: 35-46.
Storniolo, F.; Mangiacotti, M.; Zuffi, M.A.L.; Scali, S. & Sacchi, R. (2023). Large scale phenotypic characterisation of Hierophis viridiflavus (Squamata: Serpentes): climatic and environmental drivers suggest the role of evolutionary processes in a polymorphic species. Evolutionary Ecology 37: 419-434.
Stuart-Fox, D. & Moussalli, A. (2009). Camouflage, communication and thermoregulation: lessons from colour changing organisms. Philosophical Transactions of the Royal Society B 364: 463-470.
Sweet, S.S. (1985). Geographic variation, convergent crypsis and mimicry in gopher snakes (Pituophis melanoleucus) and Western rattlesnakes (Crotalus viridis). Journal of Herpetology 19: 55-67.
Tessa, G. (2016). Preliminary data on distribution of a rare dorsal pattern in Vipera aspis aspis (Ophidia: Viperidae) in the Gran Paradiso National Park. In Atti XI Congresso Nazionale Della Societas Herpetologica Italica. Societas Herpetologica Italica, Trento, Italy, pp. 22-25.
Troscianko, J.; Wilson-Aggarwal, J.; Stevens, M. & Spottiswoode, C.N. (2016). Camouflage predicts survival in ground-nesting birds. Scientific Reports 6: 19966.
Ursenbacher, S.; Conelli, A.; Golay, P.; Monney, J.-C.; Zuffi, M.A.L.; Thiery, G.; Durand, T. & Fumagalli, L. (2006). Phylogeography of the asp viper (Vipera aspis) inferred from mitochondrial DNA sequence data: Evidence for multiple Mediterranean refugial areas. Molecular Phylogenetics and Evolution 38: 546-552.
Vences, M.; Galán, P.; Vieites, D.R.; Puente, M.; Oetter, K. & Wanke, S. (2002). Field body temperatures and heating rates in a montane frog population: the importance of black dorsal pattern for thermoregulation. Annales Zoologici Fennici 39: 209-220.
Wolf, M. & Werner, Y.L. (1994). The striped colour pattern and striped/non‐striped polymorphism in snakes (Reptilia: Ophidia). Biological Reviews 69: 599-610.
Yang, W.; Feiner, N.; Laakkonen, H.; Sacchi, R.; Zuffi, M.A.L.; Scali, S.; While, G.M. & Uller, T. (2020). Spatial variation in gene flow across a hybrid zone reveals causes of reproductive isolation and asymmetric introgression in wall lizards. Evolution 74: 1289-1300.
Zamora-Camacho, F.J.; Rubiño-Hispán, M.V.; Reguera, S. & Moreno-Rueda, G. (2015). Thermal dependence of sprint performance in the lizard Psammodromus algirus along a 2200-meter elevational gradient: Cold-habitat lizards do not perform better at low temperatures. Journal of Thermal Biology 52: 90-96.
Zamudio, K.R.; Bell, R.C. & Mason, N.A. (2016). Phenotypes in phylogeography: Species’ traits, environmental variation, and vertebrate diversification. Proceedings of the National Academy of Sciences 113: 8041-8048.
Zuffi, M.A.L. (2002). A critique of the systematic position of the asp viper subspecies Vipera aspis aspis (Linnaeus, 1758), Vipera aspis atra Meisner, 1820, Vipera aspis francisciredi Laurenti, 1768, Vipera aspis hugyi Schinz, 1833 and Vipera aspis zinnikeri Kramer, 1958. Amphibia-Reptilia 23: 191-213.
Zuffi, M.A.L. (2008). Colour pattern variation in populations of the European Whip snake, Hierophis viridiflavus: does geography explain everything? Amphibia-Reptilia 29: 229-233.
Zuffi, M.A.L. (2014). Teeth number variation and cranial morphology within Vipera aspis group. Basic and Applied Herpetology 28: 87-97.
Zuffi, M.A.L. & Bonnet, X. (1999). Italian subspecies of the asp viper, Vipera aspis: Patterns of variability and distribution. Italian Journal of Zoology 66: 87-95.
Zuffi, M.A.L.; Gentilli, A.; Razzetti, E. & Scali, S. (2002). Transition hybridization areas in parapatric Vipera aspis subspecies from northern Italy. Biota 3: l9l-196.
Zuffi, M.A.L.; Gentilli, A. & Luiselli, L. (2011). Vipera aspis (Linnaeus, 1758), In C. Corti, M. Capula, L. Luiselli, E. Razzetti & R. Sindaco (eds.). Fauna d’Italia - Vol. XLV - Reptilia. Calderini, Bologna, Italy, pp. 608-617.
Zwahlen, V.; Lourdais, O.; Ursenbacher, S. & Guiller, G. (2022). Rare genetic admixture and unidirectional gene flow between Vipera aspis and Vipera berus at their contact zone in western France. Amphibia-Reptilia 43: 181-194.
Downloads
Published
Issue
Section
License
Copyright (c) 2024 See B&AH copyright notice
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
