Advertisement

Friend-or-foe? Behavioural evidence suggests interspecific discrimination leading to low probability of hybridization in two coexisting rock lizard species (Lacertidae, Darevskia)

  • Eduard A. GaloyanEmail author
  • Elena Yu. Tsellarius
  • Marine S. Arakelyan
Original Article

Abstract

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.

Significance statement

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.

Keywords

Social behaviour Hybridization Darevskia Reproduction barrier Species recognition 

Notes

Acknowledgments

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.

Funding

This work was supported by research projects RFBR 17-00-0425, RFBR 17-00-0430 and RFBR 18-54-05020.

Compliance with ethical standards

Ethical approval

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.

Supplementary material

265_2019_2650_MOESM1_ESM.xlsx (58 kb)
Table S1 Copulations of the observed lizards during the study period in 2017 and 2018 (XLSX 57 kb)
265_2019_2650_MOESM2_ESM.xlsx (129 kb)
Table S2 Observed interactions of the adult lizards (XLSX 129 kb)
265_2019_2650_MOESM3_ESM.xlsx (47 kb)
Table S3 List of the lizards, marked D. raddei and D. portschinskii in 2017 and 2018 (XLSX 47 kb)
265_2019_2650_MOESM4_ESM.xlsx (50 kb)
Table S4 Body size (SVL) of the marked adult lizards D. raddei and D. portschinskii in 2017 and 2018 (XLSX 49 kb)
265_2019_2650_MOESM6_ESM.mp4 (159.5 mb)
Video S2 Male D. raddei N72 (black/red beads on the tail base) moves from towards male D. raddei (green bead on the tail base). They start ritualised fighting and fall down. Then the male D. portschinskii (N62) jumps to them and observes the fight in several cm without agonistic behaviour. Two males climb the wall and fall down again. Male N72 searches for the enemy and attacks heterospecific male N62, when he goes out from the grass on the wall. This attack is not vigorous and terminates soon (MP4 163,300 kb)
265_2019_2650_MOESM7_ESM.mp4 (224.9 mb)
Video S3 Male D. raddei N18 (two orange beads on the tail base) basking with female D. raddei N22 (black and red beads). Female overcreeps the male and lays nearby (MP4 230,309 kb)

References

  1. Anderson E (1948) Hybridization of the habitat. Evolution 2:1–9CrossRefGoogle Scholar
  2. Arakelyan MS (2001) Skeletochronological study of rock lizards from Armenia and some questions of their ecology. PhD thesis, Zoological Institute, St. Petersburg, RussiaGoogle Scholar
  3. Arakelyan MS (2012) The speciation of bisexual species in sympatric populations of rock lizards of genus Darevskia. Biol J Armenia 64:10–15Google Scholar
  4. 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
  5. 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
  6. 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
  7. Axtell RW (1972) Hybridization between western collared lizards with a proposed taxonomic rearrangement. Copeia 4:707–727CrossRefGoogle Scholar
  8. Bolnick DI, Near TJ, Wainwright PC (2006) Body size divergence promotes postzygotic reproductive isolation in centrarchids. Evol Ecol Res 8:903–913Google Scholar
  9. Borkin LJ, Darevsky IS (1980) Reticular (hybridogeneous) speciation in vertebrate. Zh Obshch Biol 16:485–507 [In Russian]Google Scholar
  10. Bull CM (2000) Monogamy in lizards. Behav Process 51:7–20CrossRefGoogle Scholar
  11. Capula M (1993) Natural hybridization in Podarcis sicula and P. wagleriana (Reptilia, Lacertidae). Biochem Syst Ecol 21:373–380CrossRefGoogle Scholar
  12. Chapple DG, Keogh JS (2005) Complex mating system and dispersal patterns in a social lizard, Egernia whitii. Mol Ecol 14:1215–1227CrossRefGoogle Scholar
  13. Cole CJ, Townsend CR (1990) Parthenogenetic lizards as vertebrate systems. J Exp Zool 256:174–176CrossRefGoogle Scholar
  14. 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
  15. Cole CJ, Taylor HL, Baumann DP, Baumann P (2014) Neaves’ whiptail lizard: the first known tetraploid parthenogenetic tetrapod (Reptilia: Squamata: Teiidae). Breviora 539:1–19CrossRefGoogle Scholar
  16. Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal, Complex Systems 1695. http://igraph.org. Accessed 15 Oct 2018
  17. Cuellar O (1974) On the origin of parthenogenesis in vertebrates. Am Nat 963:625–648CrossRefGoogle Scholar
  18. 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
  19. Danielyan F, Arakelyan M, Stepanyan I (2008) Hybrids of Darevskia valentini, D. armeniaca and D. unisexualis from a sympatric population in Armenia. Amphibia-Reptilia 29:487–504CrossRefGoogle Scholar
  20. Darevsky IS (1958) Natural parthenogenesis in certain subspecies of rock lizards. Dokladi Akad Nauk SSSR 122:730–732 [In Russian]Google Scholar
  21. 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
  22. Darevsky IS (1995) Epistandart evolution and hybridogenous speciation in reptiles. J Obshei Biol 56:310–315Google Scholar
  23. 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
  24. Dehghani A, Hosseinian S, Rastegar-Pouyani N, Mohammadpour A (2014) Sexual size dimorphism in Darevskia raddei (Sauria: Lacertidae) from Northwest Iran. Zool Middle East 60:120–124CrossRefGoogle Scholar
  25. Dessauer HC, Cole CJ, Townsend CR (2000) Hybridization among western whiptail lizards (Cnemidophorus tigris) in southwestern New Mexico: population genetics, morphology, and ecology in three contact zones. Bull Am Mus Nat Hist 246:1–148CrossRefGoogle Scholar
  26. Dreiss AN, Cote J, Richard M, Federici P, Clobert J (2010) Age- and sex-specific response to population density and sex ratio. Behav Ecol 21:356–364CrossRefGoogle Scholar
  27. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 4300:215–223CrossRefGoogle Scholar
  28. Fisher JW, Muth A (1989) A technique for permanently marking lizards. Herpetol Rev 20:45–46Google Scholar
  29. Freitas S, Rocha S, Campos J et al (2016) Parthenogenesis through the ice ages: a biogeographic analysis of Caucasian rock lizards (genus Darevskia). Mol Phylogenet Evol 102:117–127CrossRefGoogle Scholar
  30. Fu J, MacCulloch R, Murphy R, Darevsky I (2000a) Clonal variation in the Caucasian rock lizard Lacerta armeniaca and its origin. Amphibia-Reptilia 21:83–89CrossRefGoogle Scholar
  31. Fu J, MacCulloch R, Murphy R, Darevsky I (2000b) Divergence of the cytochrome b gene in the Lacerta raddei complex and its parthenogenetic daughter species: evidence for recent multiple origins. Copeia 2:432–440CrossRefGoogle Scholar
  32. Gabirot M, Castilla AM, López P, Martín J (2010) Chemosensory species recognition may reduce the frequency of hybridization between native and introduced lizards. Can J Zool 88:73–80CrossRefGoogle Scholar
  33. Galoyan EA (2013) Joint space use in a parthenogenetic Armenian rock lizard (Darevskia armeniaca) suggests weak competition among monoclonal females. J Herpetol 47:97–104CrossRefGoogle Scholar
  34. Galoyan EA (2017) Unstable social structure indicates low diversity of relationships in the forest spotted skink Sphenomorphus maculatus. Amphibia-Reptilia 38:381–393CrossRefGoogle Scholar
  35. 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
  36. Grismer JL, Grismer LL (2010) Who’s your mommy? Identifying maternal ancestors of asexual species of Leiolepis Cuvier, 1829 and the description of a new endemic species of asexual Leiolepis Cuvier, 1829 from southern Vietnam. Zootaxa 2433:47–61CrossRefGoogle Scholar
  37. Grismer JL, Bauer AM, Grismer LL, Jackmann T (2014) Multiple origins of parthenogenesis, and a revised species phylogeny for the Southeast Asian butterfly lizards, Leiolepis. Biol J Linn Soc 113:1080–1093CrossRefGoogle Scholar
  38. Husak JF, Fox SF (2003) Adult male collared lizards, Crotaphytus collaris, increase aggression towards displaced neighbours. Anim Behav 65:391–396CrossRefGoogle Scholar
  39. Jančúchová-Lásková J, Landová E, Frynta D (2015) Are genetically distinct lizard species able to hybridize? A review. Curr Zool 61:155–180CrossRefGoogle Scholar
  40. Jenssen TA (1977) Morphological, behavioural and electrophoretic evidence of hybridization between the lizards, Anolis grahami and Anolis lineatopus neckeri, on Jamaica. Copeia 1977:270–276CrossRefGoogle Scholar
  41. Kearney M (2005) Hybridization, glaciation and geographical parthenogenesis. Trends Ecol Evol 20:495–502CrossRefGoogle Scholar
  42. Lena JP, de Fraipont M (1998) Kin recognition in the common lizard. Behav Ecol Sociobiol 42:341–347CrossRefGoogle Scholar
  43. Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California Press, BerkeleyGoogle Scholar
  44. Moritz C, Uzzell T, Spolsky C, Hotz H, Darevsky I, Kupriyanova L, Danielyan F (1992) The material ancestry and approximate age of parthenogenetic species of Caucasian rock lizards (Lacerta: Lacertidae). Genetica 87:53–62CrossRefGoogle Scholar
  45. Murphy RW, Fu J, MacCulloch RD, Darevsky IS, Kupriyanova LA (2000) A fine line between sex and unisexuality: the phylogenetic constraints on parthenogenesis in lacertid lizards. Zool J Linnean Soc 130:527–549CrossRefGoogle Scholar
  46. Ng J, Geneva AJ, Noll S, Glor RE (2017) Signals and speciation: Anolis dewlap color as a reproductive barrier. J Herpetol 51:437–447CrossRefGoogle Scholar
  47. Nicholson KE, Richards PM (2011) Home-range size and overlap within an introduced population of the Cuban Knight Anole, Anolis equestris (Squamata: Iguanidae). Phyllomedusa 10:65–73CrossRefGoogle Scholar
  48. Panov EN, Zykova LY (2016) Rock lizards of Eurasia. KMK, MoscowGoogle Scholar
  49. Pianka ER, Vitt LJ (2003) Lizards. Windows to the evolution of diversity. University of California Press, BerkeleyGoogle Scholar
  50. Pinho C, Kaliontzopoulou A, Carretero MA, Harris DJ, Ferrand N (2009) Genetic admixture between the Iberian endemic lizards Podarcis bocagei and Podarcis carbonelli: evidence for limited natural hybridization and a bimodal hybrid zone. J Zool Syst Evol Res 47:368–377CrossRefGoogle Scholar
  51. Rosenthal GG (2013) Individual mating decisions and hybridization. J Evol Biol 26:252–255CrossRefGoogle Scholar
  52. Ruby DE (1978) Seasonal changes in territorial behaviour of the iguanid lizard Sceloporus jarrovi. Copeia 3:430–438CrossRefGoogle Scholar
  53. Ryskov AP, Osipov FA, Omelchenko AV, Semyenova SK, Girnyk AE, Kochagin VI, Vergun AA, Murphy RW (2017) The origin of multiple clones in the parthenogenetic lizard species Darevskia rostombekowi. PLoS One 12:e0185161CrossRefGoogle Scholar
  54. Schultz RJ (1973) Unisexual fish: laboratory synthesis of a “species”. Science 179:180–181CrossRefGoogle Scholar
  55. Spangenberg V, Arakelyan M, Galoyan E, Matveevsky S, Petrosyan R, Bogdanov Y, Danielyan F, Kolomiets O (2017) Reticulate evolution of the rock lizards: meiotic chromosome dynamics and spermatogenesis in diploid and triploid males of the genus Darevskia. Genes 8:149CrossRefGoogle Scholar
  56. Tarroso P, Pereira RJ, Martínez-Freiría F, Godinho R, Brito JC (2014) Hybridization at an ecotone: ecological and genetic barriers between three Iberian vipers. Mol Ecol 23:1108–1123CrossRefGoogle Scholar
  57. Taylor HL, Cole CJ, Hardy LM, Dessauer HC, Townsend CR, Walker JM, Cordes JE (2001) Natural hybridization between the teiid lizards Cnemidophorus tesselatus (parthenogenetic) and C. tigris marmoratus (bisexual): assessment of evolutionary alternatives. Am Mus Novit 3345:1–64CrossRefGoogle Scholar
  58. 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
  59. 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
  60. 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
  61. Tsellarius AY, Tsellarius EY, Galoyan EA (2016) Social relationships between males and females in the rock lizard (Darevskia brauneri, Lacertidae): 1. Friendly monogyny in males and polyandry in females. Biol Bull 43:1077–1086CrossRefGoogle Scholar
  62. Uzzel T, Darevsky I (1973) The relationships of Lacerta portschinskii and Lacerta raddei (Sauria, Lacertidae). Herpetologica 29:1–6Google Scholar
  63. Verbeek B (1972) Ethologische Untersuchungen an einigen europäischen Eidechsen. Bonn Zool Beitr 23:122–151Google Scholar
  64. 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
  65. Willis PM, Ryan MJ, Rosenthal GG (2011) Encounter rates with conspecific males influence female mate choice in a naturally hybridizing fish. Behav Ecol 22:1234–1240CrossRefGoogle Scholar
  66. Willis PM, Rosenthal GG, Ryan MJ (2012) An indirect cue of predation risk counteracts female preference for conspecifics in a naturally hybridizing fish Xiphophorus birchmanni. PLoS One 7:e34802CrossRefGoogle Scholar
  67. Wirtz P (1999) Mother species–father species: unidirectional hybridization in animals with female choice. Anim Behav 58:1–12CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Zoological MuseumLomonosov Moscow State UniversityMoscowRussia
  2. 2.A. N. Severtsov Institute of Ecology and EvolutionMoscowRussia
  3. 3.Department of ZoologyYerevan State UniversityYerevanArmenia

Personalised recommendations