Open Access Open Access  Restricted Access Subscription or Fee Access

Is Vipera orlovi a Distinct Hybrid Species?

Ulrich Joger, Oleksandr Zinenko

Abstract


The species status of Vipera orlovi is discussed in the context of the concept of hybrid speciation. The genome of this Caucasian viper is composed of the genomes of Vipera kaznakovi (major part) and of Vipera renardi (about 20%). V. orlovi is intermediate in ecology between its ‘parental species,’ however its habitat is not the typical habitat of neither V. kaznakovi nor V. renardi. As all three taxa are allopatric, there is no evidence of current geneflow between them. Pleistocene climatic changes may have mediated contact and hybridization between V. kaznakovi and V. renardi. The resulting hybrid flock may have had a wider ecological range than its parental species, enabling a descendant lineage to occupy a novel niche which was previously unoccupied. Similar scenarios of hybrid speciation have probably occurred in vipers throughout the Caucasus. Although the future fate of this hybrid speciation remains open unless full genetic isolation has occurred, we propose to grant species status to Vipera orlovi. This is in line with the genotypic cluster species concept and the unified species concept.

Keywords


hybrid speciation; Vipera; Caucasus; genetic variation; ecological niche

Full Text:

PDF

References


Comeault A. A. and Matute D. R. (2018), «Genetic divergence and the number of hybridizing species affect the path to homoploid speciation», PNAS, 115(39), 9761 – 9766.

De Queiroz K. (2007), «Species concepts and species delimitation», Syst. Biol., 56(5), 879 – 886.

Fitzpatrick B. M., Placyk J. R., Niemiller M. L., Casper G. S., and Burghardt G. M. (2008), «Distinctiveness in the face of gene flow: hybridization between specialist and generalist gartersnakes», Mol. Ecol., 17, 4107 – 4117.

Freitas I., Ursenbacher S., Mebert K., Zinenko O., Schweiger S., Wüster W., Brito J. C., Crnobrnja-Isailovic J., Halpern B., Fahd S., Santos X., Pleguezuelos J. M., Joger U., Orlov N., Mizsei E., Lourdais O., Zuffi M. A. L., Strugariu A., Zamfirescu S. R., Martinez-Solano I., Velo-Anton G., Kalionzopoulou A., and Martinez-Freiria A. (2020), «Evaluating taxonomic inflation: towards evidence-based species delimitation in Eurasian vipers (Serpentes: Viperinae)», Amphibia–Reptilia, 41, 285 – 311.

Guillemin I.. Bouchier C., Garrigues T., Wisner A., and Choumet V. (2003), «Sequences and structural organization of phospholipase A2 genes from Vipera aspis aspis, V. aspis zinnikeri and Vipera berus berus venom. Identification of the origin of a new viper population based on ammodytin I1 heterogeneity», Eur. J. Biochem., 270, 2697 – 2706.

Guiller G., Lourdais O., and Ursenbacher S. (2017), «Hybridization between a Euro-Siberian (Vipera berus) and a Para-Mediterranean viper (V. aspis) at their contact zone in western France», J. Zool., 302(2), 138 – 147.

Harvey M. B., Barker D. G., Ammerman L. K., and Chippindale P. T. (2000), «Systematics of pythons of the Morelia amethistina complex (Serpentes: Boidae) with the description of three new species», Herpetol. Monogr., 14, 39 – 185.

Joger U. (1993), «Adaptation», in: W. Kuttler (ed.), Handbuch zur Ökologie, Analytica, Essen, pp. 8 – 13.

Joger U. and Dely O. G. (2005), «Vipera (Pelias) renardi (Christoph, 1861) – Steppenotter», in U. Joger and N. Stümpel (eds.), Handbuch der Reptilien und Amphibien Europas, Aula, Wiebelsheim, pp. 343 – 354.

Joger U. and Stümpel N. (eds.) (2005), Handbuch der Reptilien und Amphibien Europas, Aula, Wiebelsheim.

Kapfer J. M., Sloss B. L., Schuurman G. W., Paloski R. A., and Lorch J. M. (2013), «Evidence of hybridization between Common Gartersnakes (Thamnophis sirtalis) and Butler’s Gartersnakes (Thamnophis butleri) in Wisconsin, USA», J. Herpetol., 47(3), 400 – 405.

LeClere J. B., Hoaglund E. P., Scharosch J., Smith C. E., and Gamble T. (2012), «Naturally occuring intergeneric hybrid snakes (Pituophis catenifer sayi × Pantherophis vulpinus; Lampropeltini, Squamata) from the Midwestern United States», J. Herpetol., 46(2), 257 – 262.

Mallet J. (2007), «Hybrid speciation», Nature, 446, 279 – 283.

Masello J. F., Quillfeldt P., Sandoval-Castellanos E., Alferman R., Calderón L., Cherel Y., Cole T. L., Cuthbert R. J., Marin M., Massaro M., Navarro J., Phillips R. A., Tyan P. G., Shepherd L. D., Suazo C. G., Weimerskirch H., and Moodley Y. (2019), «Additive traits lead to feeding advantage and reproductive isolation, promoting hybrid speciation», Mol. Biol. Evol., 36(8), 1671 – 1685.

Mebert K. (2008), «Good species despite massive hybridization: genetic research on the contact zone between the watersnakes Nerodia sipedon and N. fasciata in the Carolinas, USA», Mol. Ecol., 17(8), 1918 – 1929.

Nolte A. W., Freyhof J., Stemshorn K. C., and Tautz D. (2005), «An invasive lineage of sculpins, Cottus sp. (Pisces, Teleostei) in the Rhine with new habitat adaptations has originated from hybridization between old phylogenetic groups», Proc. R. Soc. B, 272, 2379 – 2387.

Nolte A. W. and Tautz D. (2009), «Understanding the onset of hybrid speciation», Trends Gen., 26(2), 54 – 58.

Orlov N. and Tuniyev B. (1990), «Three species in the Vipera kaznakovi complex (Eurosiberian Group) in the Caucasus: Their present distribution, possible genesis, and phylogeny», Asiat. Herpetol. Res., 3, 1 – 36.

Orlov N. and Tuniyev B. (2005), «Vipera (Pelias) kaznakovi», in: U. Joger and N. Stümpel (eds.), Handbuch der Reptilien und Amphibien Europas, Aula, Wiebelsheim, pp. 325 – 341.

Ostrovskikh S. V. (2006), «Morphological variability of Eastern Meadow Viper — Vipera (Pelias) renardi in the North-Western Caucasus», Curr. Stud. Herpetol., 5/6, 61 – 70.

Ottenburghs J. (2018), «Exploring the hybrid speciation continuum in birds», Ecol. Evol., 8(24), 13027 – 13034.

Pavlov A. V., Zinenko O. I., Joger U., Stümpel N., Petrova I. V., Malenyov A. L., Zaitseva O. V., Shurshina I. V., and Bakiev A. G. (2011). «Natural hybridization of the Eastern Steppe Viper Vipera renardi and the Common Adder V. berus», Tr. Samar. NTs RAN [in Russian], 13(5), 172 – 178.

Placyk J. S., Jr., Fitzpatrick B. M., Casper G. S., Small R. L., Reynolds R. G., Noble D. W. A., Brooks R. J., and Burghardt G. M. (2012), «Hybridization between two gartersnake species (Thamnophis) of conservation concern: a threat or an important natural interaction?» Conserv. Genet., 13, 649 – 63.

Sackman A. M. and Rokyta D. R. (2013), «The adaptive potential of hybridization demonstrated with bacteriophages», J. Mol. Evol., 77, 221 – 230, DOI: 10.1007/ s00239-013-9586-8.

Saint Girons H. (1990a) «Morphologie comparée des hybrides de Vipera seoanei Lataste, 1879 × Vipera aspis (L.)», Amphibia–Reptilia, 11(2), 197 – 200.

Saint Girons H. (1990b) «Croissance, maturité sexuelle et variations ontogéniques des periodes d’alimentation et des mues chez deux vipères hybrides (Vipera aspis × Vipera seoanei) dans des conditions semi-naturelles», Bull. Soc. Herpetol. Fr., 54, 62 – 68.

Sanders K. L., Rasmussen A. R., and Guinea M. L. (2014), «High rates of hybridisation reveal fragile reproductive barriers between endangered Australian sea snakes», Biol. Conserv., 171, 200 – 208.

Shiryaev K. A. (2005), «New data on reproductive biology of Caucasian species of the genus Vipera», in: N. Ananjeva and O. Tsinenko (eds.), Herpetologia Petropolitana, St. Petersburg, pp. 213 – 215.

Tarroso P., Pereira R. J., Martínez-Freiría F., Godinho R., and Brito J. C. (2014). «Hybridization at an ecotone: ecological and genetic barriers between three Iberian vipers», Mol. Ecol. 23(5), 1108 – 1123.

Tuniyev B. S., Orlov N. L., Ananjeva N. B., and Agasjan A. L. (2009), The Snakes of the Caucasus [in Russian], KMK, St. Petersburg – Moscow.

Tuniyev B. S. and Ostrovskikh S. V. (2001), «Two new species of vipers of kaznakovi complex (Ophidia, Viperidae) from western Caucasus», Russ. J. Herpetol., 8(2), 117 – 126.

Tuniyev S. B., Kidov, A. A., and Tuniyev B. S. (2016), Additions to the description and rapid assessment of the current status of a population of the relic viper (Pelias magnifica (Tuniyev et Ostrovskikh, 2001)), (Ophidia, Viperinae) at a Type Locality», Curr. Stud. Herpetol., 16(1/2), 43 – 50.

Uecker H., Setter D., and Hermisson J. (2015). «Adaptive gene Introgression after secondary contact», J. Math. Biol., 70(7), 1523 – 1580.

Vandewege M. W., Rodriguez D., Weaver J. P., Hibbitts T. D., Forstner M. R. J., and Densmore L. D., III (2012), «Evidence of hybridization between Elaphe bairdi and Elaphe obsoleta lindheimeri including comparative population genetics inferred from microsatellites and mitochondrial DNA source», J. Herpetol., 46(1), 56 – 63.

Venczel M. and Ghira I. (1994), «A preliminary study on the osteology of nose-horned viper (Vipera ammodytes ammodytes L. 1758) from Boiu de Sus, Romania», Sargetia. Ser. Sci. Nat., 16, 145 – 150.

Zinenko O. I. (2004), «New data about hybridization between Vipera nikolskii Vedmederya, Grubant et Rudaeva, 1986 and Vipera berus berus (Linnaeus, 1758) and their contact zones in Ukraine», Mertensiella, 15, 17 – 28.

Zinenko O., Stümpel N., Mazanaeva L., Shiryaev K., Nilson G., Orlov N. L., Tuniyev S., Ananjeva N. B., Murphy R. W., and Joger U. (2013), «The puzzling phylogeny of the Vipera kaznakovi complex», in: Abstrs. of the 17th Eur. Congr. Herpetol., Veszprem, Hungary, p. 197.

Zinenko O., Stümpel N., Mazanaeva L., Bakiev A., Shiryaev K., Pavlov A., Kotenko T., Kukushkin O., Chikin Y., Duisebajeva T., Nilson G., Orlov N. L., Tuniyev B., Ananjeva N. B., Murphy R. W., and Joger U. (2015), «Mitochondrial phylogeny shows multiply independent ecological transitions and northern dispersion despite of Pleistocene glaciations in meadow and steppe vipers (Vipera ursinii and Vipera renardi)», Mol. Phylogen. Evol., 84, 85 – 100.

Zinenko O., Sovic M., Joger U., and Lisle Gibbs H. (2016), «Hybrid origin of European vipers (Vipera orlovi and Vipera magnifica) from the Caucasus determined using genomic scale DNA markers», BMC Evol. Biol., 16, 76.




DOI: https://doi.org/10.30906/1026-2296-2021-28-1-60-66

Refbacks

  • There are currently no refbacks.