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The sympatric occurrence of two genetically divergent lineages of sucking louse, Polyplax arvicanthis (Phthiraptera: Anoplura), on the four-striped mouse genus, Rhabdomys (Rodentia: Muridae)

Published online by Cambridge University Press:  24 January 2013

NINA DU TOIT ,
SONJA MATTHEE  and
CONRAD A. MATTHEE
NINA DU TOIT
Affiliation:
Evolutionary Genomics Group, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
SONJA MATTHEE
Affiliation:
Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
CONRAD A. MATTHEE*
Affiliation:
Evolutionary Genomics Group, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
*
*Corresponding author: Evolutionary Genomics Group, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa. Tel: +27218083957. Fax: +27218082405. E-mail: [email protected]
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Summary

Within southern Africa, the widely distributed four-striped mouse genus (Rhabdomys) is parasitized by, amongst others, the specific ectoparasitic sucking louse, Polyplax arvicanthis. Given the presence of significant geographically structured genetic divergence in Rhabdomys, and the propensity of parasites to harbour cryptic diversity, the molecular systematics of P. arvicanthis was investigated. Representatives of P. arvicanthis were sampled from Rhabdomys at 16 localities throughout southern Africa. Parsimony and Bayesian gene trees were constructed for the mitochondrial COI, 12S rRNA, 16S rRNA and nuclear CAD genes. Our findings support the existence of 2 genetic groups within P. arvicanthis separated by at least 25% COI sequence divergence, which is comparable to that observed among recognized Polyplax species. We therefore propose that these 2 genetic lineages probably represent distinct species and that the apparent absence of clear morphological differences may point to cryptic speciation. The 2 taxa have sympatric distributions throughout most of the sampled host range and also occasionally occur sympatrically on the same host individual. The co-occurrence of these genetically distinct lineages probably resulted from parasite duplication via host-associated allopatric divergence and subsequent reciprocal range expansions of the 2 parasite taxa throughout southern Africa.

Keywords

PolyplaxRhabdomysAnopluraRodentiaparasite duplicationsympatryallopatric speciationmolecular phylogeny
Type
Research Article
Information
Parasitology , Volume 140 , Issue 5 , April 2013 , pp. 604 - 616
Copyright
Copyright © Cambridge University Press 2013

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References

REFERENCES

Akaike, H. (1973). Information theory and an extention of the maximum likelihood principle. In Second International Symposium on Information Theory (ed. Petrov, P. N. and Csaki, F.), pp. 267–281. Adad Kiado, Budapest, Hungary.Google Scholar
Andrews, R. H., Monis, P. T., Ey, P. L. and Mayrhofer, G. (1998). Comparison of the levels of intraspecific genetic variation within Giardia muris and Giardia intestinalis . International Journal for Parasitology 28, 1179–1185. doi: 10.1016/S0020-7519(98)00097-6.Google Scholar
Bensch, S., Stjerman, M., Hasselquist, D., Ostman, O., Hansson, B., Westerdahl, H. and Pinheiro, R. T. (2000). Host specificity in avian blood parasites: a study of Plasmodium and Hemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London, B 267, 1583–1589. doi: 10.1098/rspb.2000.1181.Google Scholar
Burnham, K. P. and Anderson, D. A. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer-Verlag, New York, USA.Google Scholar
Burnham, K. P. and Anderson, D. A. (2004). Multi-model inference: understanding AIC and BIC in model selection. Sociological Methods and Research 33, 261–304. doi: 10.1177/0049124104268644.Google Scholar
Castiglia, R., Solano, E., Makundi, R. H., Hulselmans, J. and Verheyen, E. (2011). Rapid chromosomal evolution in the mesic four-striped grass rat Rhabdomys dilectus (Rodentia, Muridae) revealed by mtDNA phylogeographic analysis. Journal of Zoological Systematics and Evolutionary Research 50, 165–172. doi: 10.1111/j.1439-0469.2011.00627.x.Google Scholar
Danforth, B. N., Fang, J. and Spies, S. (2006). Analysis of family-level relationships in bees (Hymenoptera: Apiformes) using 28S and two previously unexplored nuclear genes: CAD and RNA polymerase II. Molecular Phylogenetics and Evolution 39, 358–372. doi: 10.1016/j.ympev.2005.09.022. Google Scholar
de León, G. P. P. and Nadler, S. A. (2010). What we don't recognize can hurt us: a plea for awareness about cryptic species. Journal of Parasitology 96, 453–464. doi: 10.1645/GE-2260.1.CrossRefGoogle Scholar
du Toit, N., Jansen van Vuuren, B., Matthee, S. and Matthee, C. A. (2012). Biome specificity of distinct genetic lineages within the four-striped mouse, Rhabdomys pumilio (Rodentia: Muridae) from southern Africa with implications for taxonomy. Molecular Phylogenetics and Evolution 65, 75–86. doi: 10.1016/j.ympev.2012.05.036.CrossRefGoogle ScholarPubMed
Durden, L. A. and Musser, G. G. (1994). The sucking lice (Insecta, Anoplura) of the world: a taxonomic checklist with records of Mammalian hosts and geographical distributions. Bulletin of the American Museum of Natural History 218, 1–90.Google Scholar
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.Google Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704. doi: 10.1080/10635150390235520.Google Scholar
Hafner, M. S., Sudman, P. D., Villablanca, F. X., Spradling, T. A., Demastes, J. W. and Nadler, S. A. (1994). Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265, 1087–1090.Google Scholar
Hall, T. (2005). BioEdit, Biological Sequence Alignment Editor for Win95/98/NT/2 K/XP. Available from http://www.mbio.ncsu.edu/BioEdit/bioedit.html.Google Scholar
Hopkins, G. H. E. (1949). The host association of the lice of mammals. Proceedings of the Zoological Society, London 119, 387–604.Google Scholar
Huyse, T., Poulin, R. and Theron, A. (2005). Speciation in parasites: a population genetics approach. Trends in Parasitology 21, 469–475. doi: 10.1016/j.pt.2005.08.009.Google Scholar
Johnson, P. T. (1960). The Anoplura of African rodents and insectivores. Technical Bulletin of the United States Department of Agriculture 1211, 1–116.Google Scholar
Johnson, K. P. and Clayton, D. H. (2004). Untangling coevolutionary history. Systematic Biology 53, 92–94. doi:10.1080/10635150490264824.Google Scholar
Kass, R. E. and Raftery, A. E. (1995). Bayes Factors. Journal of the American Statistical Assocciation 90, 773–795.Google Scholar
Kim, K. C. (2006). Blood-sucking lice (Anoplura) of small mammals: true parasites. In Micromammals and Macroparasites: From Evolutionary Ecology to Management (ed. Morand, S., Krasnov, B. R. and Poulin, R.), pp. 141–160. Springer-Verlag, Tokyo, Japan.Google Scholar
Kim, K. C., Emerson, K. C. and Traub, R. (1990). Diversity of parasitic insects: Anoplura, Mallophaga, and Siphonaptera. In Systematics of the North American Insects and Arachnids: Status and Needs, Vol. 90–1 (ed. Kosztarab, M. and Schaefer, C. W.), pp. 91–103. Virginia Agricultural Experiment Station Information Series, Blacksburg, Virginia, USA.Google Scholar
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. and Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948. doi:10.1093/bioinformatics/btm404.CrossRefGoogle ScholarPubMed
Ledger, J. A. (1980). The Arthropod Parasites of Vertebrates in Africa South of the Sahara, Volume IV: Phthiraptera (Insecta). Publications of the South African Institute for Medical Research No. 56, Johannesburg, South Africa.Google Scholar
Light, J. E. and Reed, D. L. (2009). Multigene analysis of phylogenetic relationships and divergence times of primate sucking lice (Phthiraptera: Anoplura). Molecular Phylogenetics and Evolution 50, 376–390. doi: 10.1016/j.ympev.2008.10.023.CrossRefGoogle ScholarPubMed
Light, J. E., Smith, S. S., Allen, J. M., Durden, L. A. and Reed, D. L. (2010). Evolutionary history of mammalian sucking lice (Phthiraptera: Anoplura). BMC Evolutionary Biology 10, 292. doi: 10.1186/1471-2148-10-292.Google Scholar
Locke, S., McLaughlin, J. D. and Marcogliese, D. J. (2010). DNA barcodes show cryptic diversity and potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Molecular Ecology 19, 2813–2827. doi: 10.1111/j.1365-294X.2010.04713.x.Google Scholar
Marshall, A. G. (1981). The Ecology of Ectoparasitic Insects. Aberdeen University Academic Press, London, UK.Google Scholar
Matthee, C. A., Burzlaff, J. D., Taylor, J. F. and Davis, S. K. (2001). Mining the mammalian genome for artiodactyl systematics. Systematic Biology 50, 367–390. doi: 10.1080/10635150119683.Google Scholar
Matthee, S., Horak, I. G., Beaucournu, J.-C., Durden, L. A., Ueckermann, E. A. and McGeoch, M. A. (2007). Epifaunistic arthropod parasites of the four-striped mouse, Rhabdomys pumilio, in the Western Cape Province, South Africa. Journal of Parasitology 93, 47–59. doi: 10.1645/GE-819R2.1.Google Scholar
Matthee, S., McGeoch, M. A. and Krasnov, B. (2010). Parasite-specific variation and the extent of male-biased parasitism; an example with a South African rodent and ectoparasitic arthropods. Parasitology 137, 651–660. doi: 10.1017/S0031182009991338.Google Scholar
McCoy, K. D. (2003). Sympatric speciation in parasites – what is sympatry? Trends in Parasitology 19, 400–404. doi: 10.1016/S1471-4922(03)00194-6.Google Scholar
McManus, D. P. and Bowles, J. (1996). Molecular genetic approaches to parasite identification: their value in diagnostic parasitology and systematics. International Journal for Parasitology 26, 687–794. doi: 10.1016/0020-7519(96)82612-9.Google Scholar
Meester, J. A. J., Rautenbach, I. L., Dippenaar, N. J. and Baker, C. M. (1986). Classification of southern African Mammals. Transvaal Museum Monograph 5, 275–277.Google Scholar
Musser, G. G. and Carleton, M. D. (2005). Order Rodentia. In Mammal Species of the World. A Taxonomic and Geographic Reference Vol. 2. (ed. Wilson, D. E. and Reeder, D. M.), pp. 1494–1496. The John Hopkins University Press, Baltimore, MD, USA.Google Scholar
Nadler, S. A. (2002). Species delimitation and Nematode biodiversity: Phylogenies rules. Nematology 4, 615–625. doi: 10.1163/15685410260438908.Google Scholar
Nadler, S. A. and de León, G. P. P. (2011). Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138, 1688–1709. doi: 10.1017/S003118201000168X.Google Scholar
Newton, M. A. and Raftery, A. E. (1994). Approximate Bayesian inference with the weighted likelihood bootstrap. Journal of the Royal Statistical Society: Series B 56, 3–48.Google Scholar
Nieberding, C., Morand, S., Libois, R. and Michaux, J. R. (2004). A parasite reveals cryptic phylogeographic history of its host. Procceedings of the Royal Society of London, B 271, 2559–2568. doi: 10.1098/rspb.2004.2930.Google Scholar
Page, R. D. M. (2003). Tangled Trees: Phylogeny, Cospeciation, and Coevolution. University of Chicago Press, Chicago, IL, USA.Google Scholar
Palumbi, S., Martin, A., Romano, S., McMillian, W. O., Stice, L. and Grabowski, G. (1991). The Simple Fool's Guide to PCR. University of Hawaii, Honolulu, USA.Google Scholar
Paterson, A. M. and Banks, J. (2001). Analytical approaches to measuring cospeciation of host and parasites: through a looking glass, darkly. International Journal for Parasitology 31, 1012–1022. doi: 10.1016/S0020-7519(01)00199-0.Google Scholar
Perkins, L., Martinsen, E. S. and Falk, B. G. (2011). Do molecules matter more than morphology? Promises and pitfalls in parasites. Parasitology 138, 1664–1674. doi: 10.1017/S0031182011000679.Google Scholar
Posada, D. (2004). Collapse 1.2: Describing Haplotypes from Sequence Alignments. Available from http://darwin.uvigo.es/software/collapse.html.Google Scholar
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256. doi: 10.1093/molbev/msn083.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (2004). Parasite Biodiversity. Smithsonian Institution, Washington DC, USA.Google Scholar
Rambau, R. V., Robinson, T. J. and Stanyon, R. (2003). Molecular genetics of Rhabdomys pumilio subspecies boundaries: mtDNA phylogeography and karyotypic analysis by fluorescence in situ hybridization. Molecular Phylogenetics and Evolution 28, 564–575. doi: 10.1016/S1055-7903(03)00058-7.Google Scholar
Rambaut, A. and Drummond, A. J. (2007). Tracer v1·5. Available from http://beast.bio.ed.ac.uk/Tracer.Google Scholar
Reed, D. L., Smith, V. S., Hammond, S. L., Rogers, A. R. and Clayton, D. H. (2004). Genetic analysis of lice supports direct contact between modern and archaic humans. PLOS Biology 2, e340. doi: 10.1371/journal.pbio.0020340.Google Scholar
Rivas, L. R. (1964). A reinterpretation of the concepts “sympatric” and “allopatric” with proposal of the additional terms “syntopic” and “allotopic”. Systematic Zoology 13, 42–43.Google Scholar
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A. and Huelsenbeck, J. P. (2012). MrBayes 3·2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542. doi: 10.1093/sysbio/sys029.Google Scholar
Schlick-Steiner, B. C., Seifert, B., Stauffer, C., Christian, E., Crozier, R. H. and Steiner, F. M. (2007). Without morphology, cryptic species stay in taxonomic crypsis following discovery. Trends in Ecology and Evolution 22, 391–392. doi: 10.1016/j.tree.2007.05.004.Google Scholar
Shao, R., Kirkness, E. F. and Barker, S. C. (2009). The single mitochondrial chromosome typical of animals has evolved into 18 minichromosomes in the human body louse, Pediculus humanus . Genome Research 19, 904–912. doi: 10.1101/gr.083188.108. CrossRefGoogle ScholarPubMed
Skinner, J. D. and Chimimba, C. T. (2005). The Mammals of the South African Subregion, 3rd Edn. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Smith, V. S., Ford, T., Johnson, K. P., Johnson, P. C. D., Yoshizawa, K. and Light, J. E. (2011). Multiple lineages of lice pass through the K-Pg boundary. Biology Letters 7, 782–785. doi: 10.1098/rsbl.2011.0105.Google Scholar
Štefka, J. and Hypša, V. (2008). Host specificity and genealogy of the louse Polyplax serrata on field mice, Apodemus species: a case of parasite duplication or colonization? International Journal for Parasitology 38, 731–741. doi: 10.1016/j.ijpara.2007.09.011.Google Scholar
Suchard, M. A., Weiss, R. A. and Sinsheimer, J. S. (2001). Bayesian selection of continuous-time Markov chain evolutionary models. Molecular Biology and Evolution 18, 1001–1013.Google Scholar
Swofford, D. L. (2000). PAUP: Phylogenetic Analysis Using Parsimony (and Other Methods). Sinauer Associates, Sunderland, MA, USA.Google Scholar
Whiteman, N. K. and Parker, P. G. (2005). Using parasites to infer host population history: a new rationale for parasite conservation. Animal Conservation 8, 175–181. doi: 10.1017/S1367943005001915.Google Scholar
Yoshizawa, K. and Johnson, K. P. (2006). Morphology of male genitalia in lice and their relatives and phylogenetic implications. Systematic Entomology 31, 350–361. doi: 10.1111/j.1365-3113.2005.00323.x.Google Scholar
Zachos, J. (2001). Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693. doi: 10.1126/science.1059412.Google Scholar