Skip to main content

Advertisement

SpringerLink
Log in

Molecular evidence of conspecificity of South African hares conventionally considered Lepus capensis L., 1758

  • Original Investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

An Erratum to this article was published on 01 November 2009

This article has been updated

Abstract

Conventionally, Lepus capensis is considered to range across large parts of Africa, the Middle East, Central and Far East Asia. However, a recent morphological study restricts cape hares tentatively to a small range in the Western Cape Region of South Africa and groups all other L. capensis-type hares from South Africa into a new species: L. centralis. Here, we studied molecular relationships among L. capensis-type hares from South Africa. Phenotypically and morphologically the individuals matched either the newly described L. capensis or L. centralis. We examined 66 hares for allelic variation at 13 microsatellite loci and for sequence variation of the hypervariable domain 1 of the mitochondrial control region. All tree-generating analyses of the currently obtained sequences and all South African cape hare sequences downloaded from GenBank revealed monophyly when compared to sequences of various other Lepus species. A network analysis indicated close evolutionary relationships between hares of the “L. capensis-phenotype” and the “L. centralis-phenotype” (according to Palacios et al. 2008) from the southwest of the Western Cape, relative to their pronounced evolutionary divergence from all other more central, northern, and north-eastern L. capensis-type hares. F-statistics, a Bayesian admixture STRUCTURE model, as well as a principal coordinate analysis of microsatellite data indicated close genetic relationships among all South African L. capensis-type hares studied presently. A coalescence model-based migration analysis for microsatellite alleles indicated gene flow between most of the considered subspecies of cape hare, including L. capensis capensis and L. capensis centralis, theoretically sufficient to balance stochastic drift effects. Concordantly, AMOVA models revealed only little effects of partitioning microsatellite variation into the two suggested morpho-species “L. capensis” and “L. centralis”. Under an “Interbreeding Species Concept” (e.g. a strict or relaxed Biological Species Concept), the current molecular data demonstrate conspecificity of the two proposed morpho-species “L. capensis” and “L. centralis”. Based on the present molecular data the differentiation of subspecies of cape hares from southern Africa is discussed.

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

Similar content being viewed by others

Change history

  • 01 November 2009

    Please note that the captions for Fig. 4 and Fig. 5 were incorrect when first published. They have now been amended below. The Publisher apologises for any inconvenience caused.

References

  • Anderson, M.J. 2003. PCO: a Fortran computer program for principal coordinate analysis. Department of Statistics, University of Auckland, New Zealand https://doi.org/www.stat.auckland.ac.nz/∼mja.

    Google Scholar 

  • Angermann, R. 1965. Revision der palaearktischen und äthiopischen Arten der Gattung Lepus (Leporidae, Lagomorpha). Diss. Thesis, Humboldt University of Berlin.

  • Angermann, R. 1983. The taxonomy of Old World Lepus. Acta Zool. Fennica 174, 17–21.

    Google Scholar 

  • Angermann, R., Feiler, A. 1988. Zur Nomenklatur, Artabgrenzung und Variabilität der Hasen (Gattung Lepus)im westlichen Africa (Mammalia, Lagomorpha, Leporidae). Zool. Abh. Staatl. Mus. Tierk. Dresden 43, 149–167.

    Google Scholar 

  • Avise, J.C. 2000. Phylogeography. The History and Formation of Species. Harvard University Press, Cambridge, MA, USA.

    Google Scholar 

  • Baker, R.J., Bradley, R.D. 2006. Speciation in mammals and the genetic species concept. J. Mammal. 87, 43–662.

    Article  Google Scholar 

  • Bandelt, H.-J., Forster, P., Rohl, A. 1999. Median joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48.

    Article  CAS  PubMed  Google Scholar 

  • Beerli, P. 1997–2001. MIGRATE: documentation and program, part of LAMARC. Version 1.1. Revised April 30, 2001.

  • Beerli, P., Felsenstein, J. 2001. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations using a coalescent approach. Proc. Nat. Acad. Sci. USA 98, 4563–4568.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belkhir, K. 2004. GENETIX V. 4.0, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions CNRS UMR 5000, Université de Montpellier II, Montpellier (France).

    Google Scholar 

  • Ben Slimen, H., Suchentrunk, F., Shahin, A.A.B., Ben Ammar Elgaaied, A. 2007. Phylogenetic analysis of mtCR-1 sequences of Tunisian and Egyptian hares (Lepus sp. or spp., Lagomorpha) with different coat colours. Mamm. Biol. 72, 224–239.

    Article  Google Scholar 

  • Ben Slimen, H., Suchentrunk, F., Ben Ammar Elgaaied, A. 2008a. On shortcomings of using mtDNA sequence divergence for the systematics of hares (genus Lepus): an example from cape hares. Mamm. Biol. 73, 25–39.

    Article  Google Scholar 

  • Ben Slimen, H., Suchentrunk, F., Stamatis, C., Mamuris, Z., Sert, H., Alves, P.C., Kryger, U., Shahin, A.A.B., Ben Ammar Elgaaied, A. 2008b. 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.

    Article  CAS  Google Scholar 

  • Cavalli-Sforza, L.L., Edwards, A.W. 1967. Phylogenetic analysis: models and estimation procedures. Am. J. Hum. Genet. 19, 233–257.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chantry-Darmon, C., Urien, C., Hayes, H., Bertaud, M., Chadi-Taourit, S., Chardon, P., Vaiman, D., Rogel-Gaillard, C. 2005. Construction of a cytogenetically anchored microsatellite map in rabbit. Mammal. Gen. 16, 442–459.

    Article  CAS  Google Scholar 

  • Collins, K. 2005. Order Lagomorpha. In: Skinner, J.D., Chimimba, C.T. (Eds.), The Mammals of the Southern African Sub-Region. Cambridge University Press, Cambridge, UK, pp. 63–78.

    Chapter  Google Scholar 

  • Cornuet, J.M., Luikart, G. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cornuet, J.M., Piry, S., Luikart, G., Estoup, A., Solignac, M. 1999. New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153, 1989–2000.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coyne, J.A., Orr, H. 2004. Speciation. Sinaur Assoc., Inc. Publ., Sunderland, MA, USA.

    Google Scholar 

  • Degen, B. 2000. SGS: Spatial Genetic Software. Computer Program and User’s Manual. https://doi.org/kourou.cirad.fr/genetique/software.html.

  • Dieringer, D., Schlötterer, C. 2002. Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol. Ecol. Notes 3, 167–169.

    Article  Google Scholar 

  • Di Rienzo, A., Peterson, A.C., Garza, J.C., Valdes, A.M., Slatkin, M., Freimer, N.B. 1994. Mutational processes of simple-sequence repeat loci in human populations. Proc. Natl. Acad. Sci. 91, 3166–3170.

    Article  PubMed  PubMed Central  Google Scholar 

  • Epperson, B.K. 2003. Geographical Genetics. Monographs in Population Biology 38. Princton University Press, Princton and Oxford.

    Google Scholar 

  • Evanno, G., Regnaut, S., Goudet, J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620.

    Article  CAS  PubMed  Google Scholar 

  • Falush, D., Stephens, M., Pritchard, J.K. 2003. Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics 164, 1567–1587.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.

    PubMed  Google Scholar 

  • Flux, J.E.C. 1983. Introduction to taxonomic problems in hares. Acta Zool. Fennica 174, 7–10.

    Google Scholar 

  • Flux, J.E.C., Angermann, R. 1990. Hares and jackrabbits. In: Chapman, J.A., Flux, J.E.C. (Eds.), Rabbits, Hares and Pikas. Status Survey and Conservation Action Plan. IUCN/ SSC Lagomorph Specialist Group, Gland, pp. 61–94.

    Google Scholar 

  • Frost, D.R., Hillis, D.M. 1990. Species in concept and practice: herpetological considerations. Herpetologica 46, 87–104.

    Google Scholar 

  • Gissi, C., Gullber, A., Arnason, U. 1998. The complete mitochondrial DNA sequence of the rabbit, Oryctolagus cuniculus. Genomics 50, 161–169.

    Article  CAS  PubMed  Google Scholar 

  • Goodman, S.J. 1997. RST CALC: a collection of computer programs for calculating unbiased estimates of genetic differentiation and determining their significance for microsatellite data. Mol. Ecol. 6, 881–885.

    Article  CAS  Google Scholar 

  • Gregorius, H.R. 1978. The concept of genetic diversity and its formal relationship to heterozygosity and genetic distance. Math. Biosci. 41, 253–271.

    Article  Google Scholar 

  • Hamill, R.M., Doyle, D., Duke, E.J. 2006. Spatial patterns of genetic diversity across European subspecies of the mountain hare, Lepus timidus L. Heredity 97, 355–365.

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann, R.S. 1993. Lagomorpha. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World — A Taxonomic and Geographic Reference, second ed. Smithsonian Inst. Press, Washington, London.

    Google Scholar 

  • Hoffmann, R.S., Smith, A.T. 2005. Lagomorpha. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World — A Taxonomic and Geographic Reference, third ed. Johns Hopkins University Press, Baltimore.

    Google Scholar 

  • Kraus, O. 2000. Int. Komm. F. Zool. Nomenkatur. International Rules for the Zoological Nomenclature. Official German Text, fourth ed. Abh. Naturwiss. Ver. in Hamburg (NF) 34. Goecke and Evers, Keltern-Weiler.

    Google Scholar 

  • Kryger, U. 2002. Genetic variation among South African hares (Lepus spec.) as inferred from mitochondrial DNA and microsatellites. Ph.D. Thesis, University of Pretoria, R.S.A.

  • Kryger, U., Robinson, J.T., Bloomer, P. 2002. Isolation and characterization of six polymorphic microsatellite loci in South African hares (Lepus saxatilis F. Cuvier, 1823 and Lepus capensis Linnaeus, 1758). Mol. Ecol. Notes 2, 422–424.

    Article  CAS  Google Scholar 

  • Kryger, U., Robinson, T.J., Bloomer, P. 2004. Population structure and history of southern African scrub hares, Lepus saxatilis. J. Zool. 263, 121–133.

    Article  Google Scholar 

  • Lee, M.S.Y. 2003. Species concepts and species reality: salvaging a Linnaean rank. J. Evol. Biol. 16, 179–188.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y.-C., Korl, A.B., Fahima, T., Beiles, A., Nevo, E. 2002. Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol. Ecol. 11, 2452–2465.

    Article  Google Scholar 

  • Matthee, C., Robinson, T.J. 1996. Mitochondrial DNA differentiation among geographical populations of Pronolagus rupestris, Smith’s red rock rabbit (Mammalia, Lagomoropha). Heredity 76, 514–523.

    Article  CAS  PubMed  Google Scholar 

  • Mayr, E. 1963. Animal Species and Evolution. Belknap Press, Cambridge, MA.

    Book  Google Scholar 

  • Mayr, E. 1995. Species, classification, and evolution. In: Arai, R., Kato, M., Doi, Y. (Eds.), Biodiversity and Evolution. National Science Foundation, Tokyo, pp. 3–12.

    Google Scholar 

  • Mithen, S. 2003. After the Ice: A Global Human History, 20,000-5000 BC. Harvard University Press, Chambridge, MA.

    Google Scholar 

  • Mougel, F., Mounolou, J.C., Monnerot, M. 1997. Nine polymorphic microsatellite loci in the rabbit, Oryctolagus cuniculus. Anim. Genet. 28, 58–59.

    Article  CAS  PubMed  Google Scholar 

  • Mucina, L., Rutherford, M.C. 2006. The vegetation of South Africa, Lesotho and Swaziland. South African National Biodiversity Inst, Strelitzia 19, Pretoria.

    Google Scholar 

  • Narum, S.R. 2006. Beyond Bonferroni: less conservative analyses for conservation genetics. Cons. Genet. 7, 783–787.

    Article  CAS  Google Scholar 

  • Nei, M. 1972. Genetic distance between populations. Am. Nat. 106, 283–292.

    Article  Google Scholar 

  • O’Brien, S.J., Mayr, E. 1991. Bureaucratic mischief: recognizing endangered species and subspecies. Science 251, 1187–1188.

    Article  PubMed  Google Scholar 

  • Ohta, T., Kimura, M. 1973. The model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a genetic population. Genet. Res. 22, 201–204.

    Article  CAS  PubMed  Google Scholar 

  • Paetkau, D., Slade, R., Burden, M., Estoup, A. 2004. Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol. Ecol. 13, 55–65.

    Article  CAS  PubMed  Google Scholar 

  • Palacios, F., Angelone, C., Germán, A., Reig, S. 2008. Morphological evidence of species differentiation within Lepus capensis Linnaeus, 1758 (Leporidae, Lagomorpha) in Cape Province, South Africa. Mamm. Biol. 73, 358–370.

    Article  Google Scholar 

  • Petter, F. 1959. Eléments d’une révision des lièvres africains du sous-genre Lepus. Mammalia 23, 41–67.

    Google Scholar 

  • Piry, S., Alapetite, A., Cornuet, J.-M., Paetkau, D., Baudouin, L., Estoup, A. 2004. GeneClass2: a software for genetic assignment and first-generation migrant detection. J. Hered. 95, 536–539.

    Article  CAS  PubMed  Google Scholar 

  • Posada, D., Crandall, K.A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.

    Article  CAS  PubMed  Google Scholar 

  • Pritchard, J.K., Wen, W. 2003. Documentation for STRUCTURE software: version 2. Available from <https://doi.org/pritch.bsd.uchicago.edu>.

  • Pritchard, J.K., Stephens, M., Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rannala, B., Mountain, J.L. 1997. Detecting immigration by using multilocus genotypes. Proc. Natl. Acad. Sci. USA 94, 9197–9201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond, M., Rousset, F. 1995. Genepop (version 1.2): population genetics software for exact tests and ecumenism. J. Hered. 86, 248–249.

    Article  Google Scholar 

  • Rice, W.R. 1989. Analysing tables of statistical tests. Evolution 43, 223–225.

    Article  PubMed  Google Scholar 

  • Rico, C., Rico, I., Webb, N., Smith, S., Bell, D., Hewitt, G. 1994. Four polymorphic loci for the European wild rabbit, Oryctolagus cuniculus. Anim. Genet. 25, 397.

    Google Scholar 

  • Roberts, A. 1951. The Mammals of South Africa. Central News Agency, Trusties of “The Mammals of South Africa” Book Fund, South Africa.

    Google Scholar 

  • Robinson, T.J. 1986. Incisor morphology as an aid in the systematics of the South African Leporidae (Mammalia: Lagomorpha). S. Afr. J. Zool. 21, 297–302.

    Google Scholar 

  • Robinson, T.J., Matthee, C.A. 2005. Phylogeny and evolutionary origins of the Leporidae: a review of cytogenetics, molecular analyses and a supermatrix analysis. Mammal Rev. 35, 231–247.

    Article  Google Scholar 

  • Rozas, J., Sänchez-Del Barrio, J.C., Messeguer, X., Rozas, R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.

    Article  CAS  PubMed  Google Scholar 

  • Scandura, M., Iacolina, L., Ben Slimen, H., Suchentrunk, F., Apollonio, M. 2007. Mitochondrial CR-1 variation in Sardinian hares and its relationships with other old world hares (Genus Lepus). Biochem. Genet. 45, 305–323.

    Article  CAS  PubMed  Google Scholar 

  • Schneider, S., Roessli, D., Excoffier, L. 2000. Arlequin: A Software for Population Genetics Data Analysis, Ver 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of Geneva, Geneva.

    Google Scholar 

  • Sert, H., Ben Slimen, H., Erdoğan, A., Suchentrunk, F. Mitochondrial HVI sequence variation in Anatolian hares (Lepus europaeus Pallas 1778). Mamm. Biol. 74, 286–297.

    Article  Google Scholar 

  • Shriver, M.D., Jin, L., Chakraborty, R., Boerwinkle, E. 1993. VNTR allele frequency distributions under stepwise mutation mode: a computer simulation approach. Genetics 134, 983–993.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Slatkin, M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457–462.

    CAS  PubMed  PubMed Central  Google Scholar 

  • S-Plus 2000. Professional Release 2©. Lucent Technologies, Inc.

  • Sokal, R.R. 1998. Local spatial autocorrelation in biological variables. Biol. J. Linn. Soc. 65, 41–62.

    Article  Google Scholar 

  • Sokal, R.R., Oden, N.L. 1978. Spatial autocorrelation in biology. 1. Methodology. Biol. J. Linn. Soc. 10, 199–228.

    Article  Google Scholar 

  • Suchentrunk, F., Flux, J.E.C., Flux, M.M., Ben Slimen, H. 2007. Multivariate discrimination between East African cape hares (Lepus capensis) and savanna hares (L. victoriae) based on occipital bone shape. Mamm. Biol. 72, 373–383.

    Article  Google Scholar 

  • Surridge, A.K., Bell, D.J., Rico, C., Hewitt, G.M. 1997. Polymorphic microsatellite loci in the European rabbit (Oryctolagus cuniculus) are also amplified in other lagomorph species. Anim. Genet. 28, 302–305.

    Article  CAS  PubMed  Google Scholar 

  • Swofford, D.L. 2003. PAUP*: Phylogenetic Analysis using Parsimony (*and other Methods). Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G. 1997. The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24, 4876–4882.

    Article  Google Scholar 

  • Valdes, A.M., Slatkin, M., Freimer, B. 1993. Allele freuencies at microsatellite loci: the stepwise mutation model revisited. Genetics 133, 737–749.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Valdiosera, C.E., García, N., Anderung, C., Dalén, L., Crégut-Bonnoure, E., Kahlke, R.-D., Stiller, M., Brandström, M., Thomas, M.G., Arsuaga, J.L., Götherström, A., Barnes, I. 2007. Staying out in the cold: glacial refugia and mitochondrial DNA phylogeography in ancient European brown bears. Mol. Ecol. 16, 5140–5148.

    Article  CAS  PubMed  Google Scholar 

  • van Oosterhout, C., Hutchinson, B., Wills, D., Shipley, P. 2005. Microchecker vers. 2.2.3. <https://doi.org/www.microchecker.hull.ac.uk/&gt.

  • Weir, B.S., Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.

    CAS  PubMed  Google Scholar 

  • Wiley, E.O. 1981. Phylogenetics: the Theory and Practice of Phylogenetic Systematics. John Wiley and Sons, New York.

    Google Scholar 

  • Winston, J.E. 1999. Describing Species. Practical Taxonomic Procedure for Biologists. Columbia University Press, New York.

    Google Scholar 

  • Zachos, F.E., Otto, M., Unici, R., Lorenzini, R., Hartl, G.B. 2008. Evidence of a phylogeographic break in the Romanian brown bear (Ursus arctos) population from the Carpathians. Mamm. Biol. 73, 93–101.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Research Institute of Wildlife Ecology, University of Veterinary Medicine Vienna, Savoyenstr. 1, 1160, Vienna, Austria

    Franz Suchentrunk

  2. Laboratoire de Génétique Moléculaire, Immunologie et Biotechnologie, Université de Tunis, Campus Universitaire El Manar, 2029, Tunis, Tunisia

    Hichem Ben Slimen

  3. Department of Zoology and Entomology, University of Pretoria, Pretoria, 0002, South Africa

    Ute Kryger

Authors
  1. Franz Suchentrunk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hichem Ben Slimen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ute Kryger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Franz Suchentrunk.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suchentrunk, F., Ben Slimen, H. & Kryger, U. Molecular evidence of conspecificity of South African hares conventionally considered Lepus capensis L., 1758. Mamm Biol 74, 325–343 (2009). https://doi.org/10.1016/j.mambio.2009.05.005

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2009.05.005

Keywords

Search

Navigation