Skip to main content

Advertisement

SpringerLink
Log in

Unidirectional Introgression and Evidence of Hybrid Superiority over Parental Populations in Eastern Iranian Plateau Population of Hares (Mammalia: Lepus Linnaeus, 1758)

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

Hares from Iran can be divided into three morphological groups, with Lepus europaeus inhabiting the western parts of Iran. Hares from lowland areas along the southeastern corner of the Caspian Sea are morphologically similar to both L. tolai and L. tibetanus, but diagnosis is complicated by a lack of taxonomic agreement. Mitochondrial DNA suggests L. tibetanus rather than L. tolai, although comparative material is not incontestable. The third group, in more xeric habitats of eastern Iran, shows a mixture of traits characteristic of both the west Iranian L. europaeus and the Golestan population, the southeast Caspian Sea. Mitochondrial and nuclear loci reveal conflicting patterns, where hares from eastern Iran cluster with L. europaeus based on mtDNA, but with the Golestan population based on nuclear transferrin, suggesting a mixed ancestry. Ecological niche modeling indicates that the preferred habitat of the Golestan population is more restricted than that of the other two groups. Pure L. europaeus occur in areas of high seasonality, low temperature, and high precipitation, whereas the population in eastern Iran inhabits areas characterized by high contrast in daily temperatures and the highest isothermality in eastern Iran. Parts of the range of this population are also indicated to correspond to the fundamental niche of L. europaeus, yet both parental forms appear to be absent from this area occupied by individuals of apparent mixed ancestry. This suggests that the population of mixed ancestry may have selective advantages over the parental forms, and that the absence of the latter from this area may be due to competitive exclusion. As the population of mixed ancestry thus appears to be self-sustaining, incipient speciation of a stabilized hybrid may be implied.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Allen JA (1877) The influence of physical conditions in the genesis of species. Radical Review 1:108-140

    Google Scholar 

  • Alves PC, Ferrand N, Suchentrunk F, Harris DJ (2003) Ancient introgression of Lepus timidus mtDNA into L. granatensis and L. europaeus in the Iberian Peninsula. Mol Phylogenet Evol 27:70-80

    CAS  PubMed  Google Scholar 

  • Anderson E (1948) Hybridization of the habitat. Evolution 2:1-9

    Google Scholar 

  • Angermann R (1983) The taxonomy of Old World Lepus. Acta Zool Fenn 174:17-21

    Google Scholar 

  • Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551-568

    CAS  PubMed  Google Scholar 

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Evol Syst 16:113-148

    Google Scholar 

  • Ben Slimen H, Suchentrunk F, Memmi A, Ben Ammar Elgaaied A (2005) Biochemical genetic relationships among Tunisian hares (Lepus sp.), South African cape hares (L. capensis), and European brown hares (L. europaeus). Biochem Genet 43:577-596

    CAS  PubMed  Google Scholar 

  • Ben Slimen H, Suchentrunk F, Stamatis C, Mamuris Z, Sert H, Alves PC, Kryger U, Shahin AB, Ben Ammar Elgaaied A (2008) Population genetics of cape and brown hares (Lepus capensis and L. europaeus): a test of Petter’s hypothesis of conspecificity. Biochem Syst Ecol 36:22-39

    CAS  Google Scholar 

  • Bergmann C (1847) Über die verhältnisse der warmeökonomie der thiere zu ihrer grosse. Göttinger Studien 1:595-708

    Google Scholar 

  • Blanford WT (1876) Eastern Persia, An Account of the Journeys of the Persian Boundary Commission 1870-72 (Vol II): Zoology and Geology. MacMillan, London

  • Bookstein FL, Chernoff B, Elder RL, Humpries JM, Smith GR, Strauss RE (1985) Morphometrics in Evolutionary Biology. Academy of Natural Sciences, Philadelphia, Special Publication 15

  • Burnaby TP (1966) Growth-invariant discriminant functions and generalized distances. Biometrics 22:96-110

    Google Scholar 

  • Corbet GB (1978) The Mammals of the Palaearctic Region: A Taxonomic Review. British Museum (Natural History), London

    Google Scholar 

  • Currat M, Ruedi M, Petit RJ, Excoffier L (2008) The hidden side of invasions: massive introgression by local genes. Evolution 62:1908-1920

    PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Drovetski SV, Semenov G, Red'kin YA, Sotnikov VN, Fadeev IV, Koblik EA (2015) Effects of asymmetric nuclear introgression, introgressive mitochondrial sweep, and purifying selection on phylogenetic reconstruction and divergence estimates in the Pacific clade of Locustella warblers. PLoS One 10: e0122590

    PubMed  PubMed Central  Google Scholar 

  • Ellerman JR, Morrison-Scott TCS (1951) Checklist of Palaearctic and Indian Mammals 1758 to 1946. Trustees of the British Museum (Natural History), London

  • Etemad E (1978) The Mammals of Iran (Volume 1). Rodents and Key to Their Classification. National Society for Protection of Natural Resources and Human Environment, Teheran (in Persian, with a summary in English)

  • Excoffier L, Foll M, Petit RJ (2008) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481-501

    Google Scholar 

  • Farber O, Kadmon R (2003) Assessment of alternative approaches for bioclimatic modeling with special emphasis on the Mahalanobis distance. Ecol Modell 160:115-130

    CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791

    PubMed  Google Scholar 

  • Fickel J, Hauffe HC, Pecchioli E, Soriguer R, Vapa L, Pitra C (2008) Cladogenesis of the European brown hare (Lepus europaeus Pallas, 1778). Eur J Wildlife Res 54:495

    Google Scholar 

  • Firouz E (2008) Fauna of Iran (Vertebrates). Iran University Press, Tehran (in Persian)

    Google Scholar 

  • Flux JEC, Angermann R (1990) The hares and jackrabbits. In: Chapman JA, Flux JEC (eds) Rabbits, Hares and Pikas: Status Survey and Conservation Action Plan. International Union for Conservation of Nature and Natural Resources, Gland, pp 61-94

    Google Scholar 

  • Fredsted T, Wincentz T, Villesen P (2006) Introgression of mountain hare (Lepus timidus) mitochondrial DNA into wild brown hares (Lepus europaeus) in Denmark. BMC Ecol 6:17

    PubMed  PubMed Central  Google Scholar 

  • Gemmell NJ, Metcalf VJ, Allendorf FW (2004) Mother’s curse: the effect of mtDNA on individual fitness and population viability. Trends Ecol Evol 19:238-244

    PubMed  Google Scholar 

  • Gromov IM, Baranova GI (1981) Catalogue of the Mammals of USSR. Nauka, Leningrad (in Russian)

    Google Scholar 

  • Gureev AA (1964) Zajceobranznye (Lagomorpha). Fauna SSSR 3, 1-176. Nauka, Moscow- Leningrad

  • Haldane JBS (1922) Sex ratio and unisexual sterility in hybrid animals. J Genet 12:101-109

    Google Scholar 

  • Hardisty AR, Bacall F, Beard N, Balcázar-Vargas MP, Balech B, Barcza Z, Bourlat SJ, De Giovanni R, de Jong Y, De Leo F, Dobor L, Donvito G, Fellows D, Guerra AF, Ferreira N, Fetyukova Y, Fosso B, Giddy J, Goble C, Güntsch A, Haines R, Ernst VH, Hettling H, Hidy D, Horváth F, Ittzés D, Ittzés P, Jones A, Kottmann R, Kulawik R, Leidenberger S, Lyytikäinen-Saarenmaa P, Mathew C, Morrison N, Nenadic A, de la Hidalga AN, Obst M, Oostermeijer G, Paymal E, Pesole G, Pinto S, Poigné A, Fernandez FQ, Santamaria M, Saarenmaa H, Sipos G, Sylla KH, Tähtinen M, Vicario S, Aldo Vos R, Williams AR, Yilmaz P (2016) BioVeL: a virtual laboratory for data analysis and modeling in biodiversity science and ecology. BMC Ecol 16:49

    PubMed  PubMed Central  Google Scholar 

  • Hoffmann RS, Smith AT (2005) Order Lagomorpha. In: Wilson DE, Reeder DM (eds) Mammals Species of the World: A Taxonomic and Geographic Reference, 3rd Edn, Volume 1. Johns Hopkins University Press, Baltimore, pp 185-211

  • Johnson MS (2000) Measuring and interpreting genetic structure to minimize the genetic risks of translocations. Aquac Res 31:133-143

    Google Scholar 

  • Karami M, Hutterer R, Benda P, Siahsarvie R, Kryštufek B (2008) Annotated check-list of the mammals of Iran. Lynx 39:63-102

    Google Scholar 

  • Kasapidis P, Suchentrunk F, Magoulas A, Kotoulas G (2005) The shaping of mitochondrial DNA phylogeographic patterns of the brown hare (Lepus europaeus) under the combined influence of late Pleistocene climatic fluctuations and anthropogenic translocations. Mol Phylogenet Evol 34:55-66

    CAS  PubMed  Google Scholar 

  • Khalili A (1973) Precipitation patterns of central Elburz. Archiv Meteorol Geophys Bioklimatol Serie B 21:215-232

    Google Scholar 

  • Lado S (2015) Population history and taxonomy of African hares (genus Lepus) inferred from genetic variation. MSc Thesis, CIBIO-InBio, Research Centre in Biodiversity and Genetic Resources, University of Porto, InBIO Associate Laboratory, Vairão

  • Land ED, Lacy RC (2000) Introgression level achieved through Florida panther genetic restoration. Endangered Species Update 17:100-105

    Google Scholar 

  • Lay DM (1967) A study of the mammals of Iran resulting from the Street expedition of 1962-63. Fieldiana Zool 54:1-282

    Google Scholar 

  • Leidenberger S, De Giovanni R, Kulawik R, Williams AR, Bourlat SJ (2015) Mapping present and future potential distribution patterns for a meso-grazer guild in the Baltic Sea. J Biogeogr 42:241-254

    PubMed  Google Scholar 

  • Levin DA (1979) Hybridization: An Evolutionary Perspective. Dowden, Hutchinson, and Ross, Stroudsberg

  • Liu J, Yu L, Arnold ML, Wu CH, Wu SF, Lu X, Zhang YP (2011) Reticulate evolution: frequent introgressive hybridization among Chinese hares (genus Lepus) revealed by analyses of multiple mitochondrial and nuclear DNA loci. BMC Evol Biol 11:223

    PubMed  PubMed Central  Google Scholar 

  • Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622-629

    PubMed  Google Scholar 

  • Mahalanobis PC (1936) On the Generalised distance in statistics. Proc Natl Acad Sci India 2:49-55

    Google Scholar 

  • Mathew C, Güntsch A, Obst M, Vicario S, Haines R, Williams A, de Jong Y, Goble C (2014) A semi-automated workflow for biodiversity data retrieval, cleaning, and quality control. Biodivers Data J 2:e4221

    Google Scholar 

  • Melo-Ferreira J, Boursot P, Randi E, Kryukov A, Suchentrunk F, Ferrand N, Alves PC (2007) The rise and fall of the mountain hare (Lepus timidus) during Pleistocene glaciations: expansion and retreat with hybridization in the Iberian Peninsula. Mol Ecol 16:605-618

  • Melo-Ferreira J, Boursot P, Suchentrunk F, Ferrand N, Alves PC (2005) Invasion from the cold past: extensive introgression of mountain hare (Lepus timidus) mitochondrial DNA into three other hare species in northern Iberia. Mol Ecol 14:2459-2464

  • Mohammadi Z, Darvish J, Aliabadian M, Yazdani Moghaddam F, Lissovsky AA, Olsson U (2018) Pleistocene diversification of Afghan pikas Ochotona rufescens (Gray, 1842) (Lagomorpha; Ochotonidae) in Western Asia. Mammal Biol 91:10-22

    Google Scholar 

  • Muñoz MES, De Giovanni R, de Siqueira MF, Sutton T, Brewer P, Pereira RS, Canhos DAL, Canhos VP (2011) openModeller: a generic approach to species’ potential distribution modelling. Geoinformatica 15:111-135

    Google Scholar 

  • Obolenskaya EV, Lee MY, Dokuchaev NE, Oshida T, Lee MS, Lee H, Lissovsky AA (2009) Diversity of Palaearctic chipmunks (Tamias, Sciuridae). Mammalia 73:281-298

    Google Scholar 

  • Ognev SI (1940) Zveri SSSR i prilezhashchykh stran: Gryzuny [Mammals of the USSR and Adjacent Countries, Vol. IV: Rodents Rodents]. Izd AN SSSR, Moscow-Leningrad [Academy of Sciences Press, Moscow and Leningrad] (in Russian)

  • Ognev SI, Heptner WG (1929) Mlekopitayushchie Srednego Kopetdaga i prilegayushchei ravniny [Mammals of Central Kopetdagh and Adjacent Plain]. Trudy Nauchno-issledovatel'skogo institute zoologii MGU [Trans Sci Res Inst Zoology of Moscow State Univ] 3:47-171 (in Russian)

  • Palacios F (1996) Systematic of the indigenous hares of Italy traditionally identified as Lepus europaeus Pallas, 1778 (Mammalia: Leporidae). Bonn Zool Beitr 46:59-91

    Google Scholar 

  • Peterson T, Papes M, Soberon J (2008) Rethinking receiver operating characteristic analysis applications in ecological niche modelling. Ecol Model 213:63-72

    Google Scholar 

  • Petter F (1961) Eléments d'une révision des Lievres européens et asiatiques du sous-genre Lepus. Z Säugetierk 26:30-40

  • Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modelling of species geographic distributions. Ecol Modell 190:231-259

    Google Scholar 

  • Pierpaoli M, Riga F, Trocchi V, Randi E (1999) Species extinction and evolutionary relationships of the Italian hare (Lepus corsicanus) as described by mitochondrial DNA sequencing. Mol Ecol 8:1805-1817

    CAS  PubMed  Google Scholar 

  • Pintur K, Dancevic N, Stedul I, Popovic N, Slijepcevic V (2014) Craniometric features of European hare (Lepus europaeus Pallas, 1778) from north-west Croatia and the island of Vir. Veterinarski arhiv 84:387-400

    Google Scholar 

  • Riga F, Trocchi V, Randi E, Toso S (2001) Morphometric differentiation between the Italian hare (Lepus corsicanus De Winton, 1898) and the European brown hare (Lepus europaeus Pallas, 1778). J Zool 253:241-252

    Google Scholar 

  • QGIS Development Team (2014) QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org/en/site/

  • Rissler LJ, Hijmans RJ, Graham CH, Moritz C, Wake DB (2006) Phylogeographic lineages and species comparisons in conservation analyses: a case study of California herpetofauna. Am Nat 167:655-666

    PubMed  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539-542

  • RStudio Team (2017) RStudio: Integrated Development Environment for R. RStudio, Inc., Boston, MA

  • Schölkopf B, Smola AJ (2001) Learning with Kernels: Support Vector Machines, Regularization, Optimization, and Beyond. MIT Press, Cambridge, London

    Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461-464

    Google Scholar 

  • Shurtliff QR (2013) Mammalian hybrid zones: a review. Mammal Rev 43:1-21

    Google Scholar 

  • Sludskii AA, Bernstein AD, Shubin IG, Fadeev VA, Orlov GI, Bekenov A, Kharitonov VI, Utinov SR (1980) Mlekopitayushchie Kazakhstana, tom 2, Zaitseobraznye [Mammals of Kazakhstan. vol. 2, Lagomorpha]. Nauka, Kazakhskoi SSR, Alma-Ata (in Russian)

  • Smith AT, Johnston CH, Alves PC, Hackländer K (2018) Lagomorphs: Pikas, Rabbits, and Hares of the World. Johns Hopkins University Press, Baltimore

  • Smith S, Turbill C, Suchentrunk F (2010) Introducing mother’s curse: low male fertility associated with an imported mtDNA haplotype in a captive colony of brown hares. Mol Ecol 19:36-43

  • Sokolov VE, Orlov VN (1980) Opredelitel’ mlekopitayushchikh Mongol’skoi Narodnoi Respubliki [Guide to the Mammals of the Mongolian People’s Republic]. Nauka, Moscow, (in Russian)

  • Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (* and other methods) version 4b10. Sinauer Associates, Sunderland

    Google Scholar 

  • Thulin CG, Tegelström H (2002) Biased geographical distribution of mitochondrial DNA that passed the species barrier from mountain hares to brown hares (genus Lepus): an effect of genetic incompatibility and mating behaviour? J Zool 258:299-306

    Google Scholar 

  • Thulin CG, Fang M, Averianov AO (2006) Introgression from Lepus europaeus to L. timidus in Russia revealed by mitochondrial single nucleotide polymorphisms and nuclear microsatellites. Hereditas 143:68-76

  • Thulin CG, Jaarola M, Tegelström H (1997) The occurrence of mountain hare mitochondrial DNA in wild brown hares. Mol Ecol 6:463-467

  • Werle E, Schneider C, Renner M, Volker M, Fiehn W (1994) Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Res 22:4354-4355

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu YH, Xia L, Zhang Q, Yang QS, Meng XX (2011) Bidirectional introgressive hybridization between Lepus capensis and Lepus yarkandensis. Mol Phylogenet Evol 59:545-555

    CAS  PubMed  Google Scholar 

  • Zachos FE, Ben Slimen H, Hackländer K, Giacometti M, Suchentrunk F (2010) Regional genetic in situ differentiation despite phylogenetic heterogeneity in Alpine mountain hares. J Zool 282:47-53

    Google Scholar 

  • Ziaie H (2008) A Field Guide to the Mammals of Iran. Department of Environment, Tehran (in Persian)

Download references

Acknowledgements

This research was financially supported by Faculty of Science, Ferdowsi University of Mashhad (FUM), (grant numbers 3/32482, and 39184). Permission to collect was authorized by the Iranian Department of Environment (Permission Number: 93/53381; 2015; 25th January). This research is dedicated to the memory of my supervisor, Prof. Jamshid Darvish, who passed away during this project. The first author also appreciates Dr. Asghar Khajeh, Seyed Mohammad Nosrati, and Bahare Shahriyari for their kind cooperation in sampling. ZM and FG are in debt to members and staffs of the University of Gothenburg, Department of Biology and Environmental Sciences for their kind cooperations. Also, we are grateful to Dr. Haji Gholi Kami Golestan University, for providing access to the archive of mammals deposited in Zoological Museum of Golestan University and for his kind help. We gratefully thank Renate Angermann (Dresden and Berlin) for many insightful comments and suggestions.

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

    Zeinolabedin Mohammadi, Mansour Aliabadian, Fatemeh Ghorbani & Faezeh Yazdani Moghaddam

  2. Zoological Innovations Research Department, Institute of Applied Zoology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

    Mansour Aliabadian & Faezeh Yazdani Moghaddam

  3. Zoological Museum, Moscow State University, B. Nikitskaya, 6, Moscow, 125009, Russia

    Andrey A. Lissovsky

  4. Department of Marine Sciences, University of Gothenburg, Box 461, SE-405 30, Göteborg, Sweden

    Matthias Obst

  5. Department of Biology and Environmental Sciences, Systematics and Biodiversity, University of Gothenburg, Box 463, SE-405 30, Göteborg, Sweden

    Urban Olsson

  6. Gothenburg Global Biodiversity Centre, Box 461, SE-405 30, Gothenburg, Sweden

    Urban Olsson

Authors
  1. Zeinolabedin Mohammadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mansour Aliabadian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fatemeh Ghorbani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Faezeh Yazdani Moghaddam
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrey A. Lissovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Matthias Obst
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Urban Olsson
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ZA and MA designed the study. ZA, UO and FG performed the data collection, statistical analysis, the lab work, analyzed the data, prepared the figures and wrote the initial version of the manuscript. MA and UO were supervisors of the project and provided the funds and the labs for morphological and molecular studies, respectively. FYM was advisor of the project. AL provided museum samples from Russia and contributed to interpretation of results. MO helped running the ecological analysis and added comments. MA reviewed the preliminary version of the manuscript. All authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Mansour Aliabadian.

Electronic supplementary material

Fig. S1

(PDF 360 kb)

Fig. S2

(PDF 133 kb)

Fig. S3

(PDF 78 kb)

ESM 1

(DOCX 94.2 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mohammadi, Z., Aliabadian, M., Ghorbani, F. et al. Unidirectional Introgression and Evidence of Hybrid Superiority over Parental Populations in Eastern Iranian Plateau Population of Hares (Mammalia: Lepus Linnaeus, 1758). J Mammal Evol 27, 723–743 (2020). https://doi.org/10.1007/s10914-019-09478-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-019-09478-5

Keywords

Search

Navigation