Friend-or-foe? Behavioural evidence suggests interspecific discrimination leading to low probability of hybridization in two coexisting rock lizard species (Lacertidae, Darevskia)
The parthenogenetic rock lizard Darevskia rostombekowi is considered to be the product of hybridization between female Darevskia raddei and male Darevskia portschinskii. These two species coexist within several secondary contact areas; however, no trace of their hybridization has been previously reported. We conducted focal observations of individually marked lizards in 2017 and 2018 to establish if there is behavioural isolation between these species. We demonstrate that individuals distinguish between lizards of the same and different species. Individuals of both studied species interacted regularly, but we found no evidence of males of either species using interspecific interference competition for resources or for females. Neutral reactions prevailed in the reactions of males to the individuals of the different species; aggressive or submissive behaviour was more common towards males of the same species. The differences in reactions of males to females of the same and different species were less clear and interspecific social interactions were almost as common as intraspecific interactions. Interspecific male mating behaviour was rare and unsuccessful; only a single female with heterospecific copulation marks on the body was found. The mating period in both species overlapped broadly in late May and early June; body size (SVL) in females of both species was equal. Hence, we suggest that the selection of the sexual partner and preference of the conspecific partner for the social and sexual contacts is the most plausible explanation of the revealed behavioural asymmetry in intra- and interspecific relationship.
Here, we present the first description of the social and sexual behaviour of two bisexual species of rock lizard belonging to the Darevskia genus. Most works devoted to the study of reticulate evolution in lizards have used genetic and morphological approaches rather than behavioural observations. The study of the proximal mechanisms of evolution is important in understanding how evolution occurs. The results indicate that even in ecologically similar species, social and sexual selection tend towards separation of the species rather than mixing, although they are able to coexist peacefully.
KeywordsSocial behaviour Hybridization Darevskia Reproduction barrier Species recognition
Many thanks to Alexey Tsellarius, Natella Mirzoyan and two reviewers for their help in the improvement of the present manuscript and valuable critics of the text. We are grateful to Martin Whiting for his valuable suggestions and editing of the present manuscript.
This work was supported by research projects RFBR 17-00-0425, RFBR 17-00-0430 and RFBR 18-54-05020.
Compliance with ethical standards
The research was approved by the Armenian Ministry of Nature Protection (N5/22.1/51043). All applicable international, national and institutional (Yerevan State and Moscow State Universities) guidelines for the care and use of animals were followed.
Conflict of interest
The authors declare that they have no conflicts of interest.
- Arakelyan MS (2001) Skeletochronological study of rock lizards from Armenia and some questions of their ecology. PhD thesis, Zoological Institute, St. Petersburg, RussiaGoogle Scholar
- Arakelyan MS (2012) The speciation of bisexual species in sympatric populations of rock lizards of genus Darevskia. Biol J Armenia 64:10–15Google Scholar
- Arakelyan M, Danielyan F (2014) New evidence on hybrid zones of bisexual species of rock lizards of genus Darevskia. In: Proceedings of the International conference “Biological diversity and conservation problems of the fauna of the Caucasus-2”, volume 2. YerevanGoogle Scholar
- Arakelyan MS, Danielyan FD, Corti C, Sindaco R, Leviton AE (2011) Herpetofauna of Armenia and Nagorno-Karabakh. Society for the Study of Amphibians and Reptiles, IthacaGoogle Scholar
- Arribas OJ (1999) Phylogeny and relationships of the mountain lizards of Europe and Near East (Archaeolacerta Mertrns, 1921, sensu lato) and their relationships among the Eurasian lacertid radiation. Rus J Herpetol 1:1–22Google Scholar
- Bolnick DI, Near TJ, Wainwright PC (2006) Body size divergence promotes postzygotic reproductive isolation in centrarchids. Evol Ecol Res 8:903–913Google Scholar
- Borkin LJ, Darevsky IS (1980) Reticular (hybridogeneous) speciation in vertebrate. Zh Obshch Biol 16:485–507 [In Russian]Google Scholar
- Cole CJ, Dessauer HC, Barrowclough GF (1988) Hybrid origin of a unisexual species of whiptail lizard, Cnemidophorus neomexicanus, in western North America: new evidence and a review. Am Mus Novit 2905:1–38Google Scholar
- Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal, Complex Systems 1695. http://igraph.org. Accessed 15 Oct 2018
- Danielyan FD (1965) Mechanisms of reproductive isolation in some Armenian forms of rock lizards (Lacerta saxicola Eversmann). Izvestia Akad Nauk Arm SSR (Biol) 18:75–80 [In Russian]Google Scholar
- Darevsky IS (1958) Natural parthenogenesis in certain subspecies of rock lizards. Dokladi Akad Nauk SSSR 122:730–732 [In Russian]Google Scholar
- Darevsky IS (1967) Rock lizards of the Caucasus (systematics, ecology, and phylogeny of the polymorphic lizards of the Caucasus of the subgenus Archaeolacerta). Nauka, Saint Petersburg Leningrad, published for the Smithsonian Institution and the National Science Foundation, Washington DC by the Indian National Scientific Documentation Centre, New DehliGoogle Scholar
- Darevsky IS (1995) Epistandart evolution and hybridogenous speciation in reptiles. J Obshei Biol 56:310–315Google Scholar
- Darevsky IS, Kupriyanova LA, Uzzel T (1985) Parthenogenesis in reptiles. In: Gans C, Billet F (eds) Biology of the reptilian, vol 15. John Wiley and Sons Inc., New York, pp 412–526Google Scholar
- Fisher JW, Muth A (1989) A technique for permanently marking lizards. Herpetol Rev 20:45–46Google Scholar
- Galoyan E, Moskalenko V, Gabelaia M, Tarkhnishvili D, Spangenberg V, Kolomiets O, Arakelyan M (2019) Why a new parthenogenetic rock lizard doesn’t appear now: morphological, genetic and cytogenetic features of the two coexisting rock lizards Darevskia raddei and D. portschinskii. Amphibia-Reptilia (published online). https://doi.org/10.13140/RG.2.2.11844.48006
- Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California Press, BerkeleyGoogle Scholar
- Panov EN, Zykova LY (2016) Rock lizards of Eurasia. KMK, MoscowGoogle Scholar
- Pianka ER, Vitt LJ (2003) Lizards. Windows to the evolution of diversity. University of California Press, BerkeleyGoogle Scholar
- Tsellarius AY, Men’shikov YG (1994) Indirect communications and its role in the formation of social structure in Varanus griseus. Russ J Herpetol 2:121–132Google Scholar
- Tsellarius AY, Tsellarius EY (2001) Dynamics of population spatial structure in Lacerta saxicola in deciduous forests of Navagir mountain ridge. Russ J Zool 80:1–8 [In Russian]Google Scholar
- Tsellarius AY, Tsellarius EY, Galoyan EA (2008) Interrelations of adults and juveniles of rock lizards—Darevskia brauneri (Reptilia, Zauria) in Navagir Mountain Ridge. Sovr Gerp 8:170–186 [In Russian]Google Scholar
- Uzzel T, Darevsky I (1973) The relationships of Lacerta portschinskii and Lacerta raddei (Sauria, Lacertidae). Herpetologica 29:1–6Google Scholar
- Verbeek B (1972) Ethologische Untersuchungen an einigen europäischen Eidechsen. Bonn Zool Beitr 23:122–151Google Scholar
- Vrijenhoek RC (1989) Genetic and ecological constraints on the origins and establishment of unisexual vertebrates. In: Dawley R, Bogart J (eds) Evolution and ecology of unisexual vertebrates. NY State Museum, Albany, pp 24–31Google Scholar