Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-28T02:46:15.879Z Has data issue: false hasContentIssue false

Co-phylogeography and morphological evolution of sika deer lice (Damalinia sika) with their hosts (Cervus nippon)

Published online by Cambridge University Press:  30 July 2012

ATSUSHI MIZUKOSHI
Affiliation:
Systematic Entomology, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
KEVIN P. JOHNSON
Affiliation:
Illinois Natural History Survey, University of Illinois, Champaign, IL 61820, USA
KAZUNORI YOSHIZAWA*
Affiliation:
Systematic Entomology, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
*
*Corresponding author: Systematic Entomology, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan. Tel: +81 11 706 2424. Fax: +81 11 706 4939. E-mail: [email protected]

Summary

Lice are obligate parasites of mammals and birds and have become an important model for studies of host-parasite co-evolution and co-phylogenetics. Population genetic and phylogeographic studies represent an important bridge between microevolution and co-phylogenetic patterns. We examine co-phylogeographic patterns in sika deer and their parasitic lice. Co-phylogeographic patterns in deer and lice were evaluated using homologous regions of mitochondrial COI sequences. The phylogeographic breaks recovered for deer populations matched those of previous studies. Comparisons of the phylogeographic tree topology for deer lice with that of their hosts revealed a significant level of congruence. However, comparisons of genetic distances between deer and lice suggested that one of the estimated co-divergence events is more likely a recent host switch. Taking into account genetic divergence, there is not strong evidence for complete phylogeographic co-divergence between deer and their parasitic lice. However, mitochondrial phylogenies only track genetic structure of female lineages, and the incongruence between deer and louse phylogeography may be explained by louse migration mediated by male deer. Morphological analysis of head shape variation based on an elliptic Fourier descriptor showed that overall morphological variation contained phylogenetic signal, suggesting that in general morphology of these lice evolves congruent to population history.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Banks, J. C., Palma, R. L. and Paterson, A. M. (2006). Cophylogenetic relationships between penguins and their chewing lice. Journal of Evolutionary Biology 19, 156166.CrossRefGoogle ScholarPubMed
Barbosa, A. M. and Carranza, J. (2010). Lack of geographic variation in Y-chromosomal introns of red deer (Cervus elaphus). Journal of Negative Results 7, 14.Google Scholar
Bengtsson, B. O. (2003). Genetic variation in organisms with sexual and asexual reproduction. Journal of Evolutionary Biology 16, 189199.CrossRefGoogle ScholarPubMed
Bush, S. E. and Clayton, D. H. (2006). The role of body size in host specificity: reciprocal transfer experiments with feather lice. Evolution 60, 21582167.Google ScholarPubMed
Cameron, S. L., Yoshizawa, K., Mizukoshi, A., Whiting, M. F. and Johnson, K. P. (2011). Mitochondrial genome deletions and minicircles are common in lice (Insecta: Phthiraptera). BMC Genomics 12, 394.CrossRefGoogle ScholarPubMed
Charleston, M. A. (1998). Jungles: a new solution to the host/parasite phylogeny reconciliation problem. Mathematical Biosciences 149, 191223.CrossRefGoogle Scholar
Clayton, D. H., Bush, S. E., Goates, B. M. and Johnson, K. P. (2003). Host defense reinforces host-parasite cospeciation. Proceedings of the National Academy of Sciences, USA 100, 1569415699.CrossRefGoogle ScholarPubMed
Clayton, D. H. and Johnson, K. P. (2003). Linking coevolutionary history to ecological processes: Doves and lice. Evolution 57, 23352341.Google ScholarPubMed
Demastes, J. W., Spradling, T. A., Hafner, M. S., Spies, G. R., Hafner, D. J. and Light, J. E. (2012). Cophylogeny on a fine scale: Geomydoecus chewing lice and their pocket gopher hosts, Pappogeomys bulleri. Journal of Parasitology http://dx.doi.org/10.1645/GE-2904.1.CrossRefGoogle ScholarPubMed
Farris, J. S., Kallersjo, M., Kluge, A. G. and Bult, C. (1994). Testing significance of congruence. Cladistics 10, 315320.CrossRefGoogle Scholar
Farris, J. S., Kallesjo, M., Kluge, A. G. and Bult, C. (1995). Constructing a significance test for incongruence. Systematic Biology 44, 570572.CrossRefGoogle Scholar
Goodman, S. J., Tamate, H. B., Wilson, R., Nagata, J., Tatsuzawa, S., Swanson, G. M., Pemberton, J. M. and McCullough, D. R. (2001). Bottlenecks, drift and differentiation: the population structure and demographic history of sika deer (Cervus nippon) in Japanese archipelago. Molecular Ecology 20, 13571370.CrossRefGoogle Scholar
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3·0. Systematic Biology 59, 307321.CrossRefGoogle ScholarPubMed
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, 10871090.CrossRefGoogle ScholarPubMed
Harbison, C. W. and Clayton, D. H. (2011). Community interaction govern host-switching with implication for host-parasite coevolutionary history. Proceedings of the National Academy of Sciences, USA 108, 95259529.CrossRefGoogle ScholarPubMed
Harbison, C. W., Jacobsen, M. V. and Clayton, D. H. (2009). Hitchhiker's guide to parasite transmission: phoretic behavior of feather lice. International Journal for Parasitology 39, 569575.CrossRefGoogle ScholarPubMed
Henry, L., Schwander, T. and Crespi, B. J. (2012). Deleterious mutation accumulation in asexual Timema stick insects. Molecular Biology and Evolution 29, 401408.CrossRefGoogle ScholarPubMed
Hopkins, G. H. E. (1942). The Mallophaga as an aid to the classification of birds. Ibis 84, 94106.CrossRefGoogle Scholar
Huelsenbeck, J. P., Rannala, B. and Yang, Z. (1997). Statistical tests of host-parasite cospeciation. Evolution 51, 410419.CrossRefGoogle ScholarPubMed
Huson, D. H. and Bryant, D. (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23, 254267.CrossRefGoogle ScholarPubMed
Iwata, H. and Ukai, Y. (2002). SHAPE: a computer program package for quantitative evolution of biological shapes based on elliptic Fourier descriptors. Journal of Heredity 93, 384385.CrossRefGoogle Scholar
Johnson, K. P., Adams, R. J. and Clayton, D. H. (2002 a). The phylogeny of the louse genus Brueelia does not reflect host phylogeny. Biological Journal of the Linnean Society 77, 233247.CrossRefGoogle Scholar
Johnson, K. P., Adams, R. J., Page, R. D. M. and Clayton, D. H. (2003 a). When do parasites fail to speciate in response to host speciation? Systematic Biology 52, 3747.CrossRefGoogle ScholarPubMed
Johnson, K. P., Bush, S. E. and Clayton, D. H. (2005). Correlated evolution of host and parasite body size: Tests of Harrison's Rule using birds and lice. Evolution 59, 17441753.Google ScholarPubMed
Johnson, K. P., Cruickshank, R. H., Adams, R. J., Smith, V. S., Page, R. D. M. and Clayton, D. H. (2003 b). Dramatically elevated rate of mitochondrial substitution in lice (Insecta: Phthiraptera). Molecular Phylogenetics and Evolution 26, 231242.CrossRefGoogle ScholarPubMed
Johnson, K. P., Drown, D. M. and Clayton, D. H. (2001). A data based parsimony method of cophylogenetic analysis. Zoologica Scripta 30, 7987.CrossRefGoogle Scholar
Johnson, K. P., Kennedy, M. and McCracken, K. G. (2006). Reinterpreting the origins of flamingo lice: cospeciation or host-switching? Biology Letters 2, 275278.CrossRefGoogle ScholarPubMed
Johnson, K. P., Shreve, S. M. and Smith, V. S. (2012). Repeated adaptive divergence of microhabitat specialization in avian feather lice. BMC Biology.CrossRefGoogle ScholarPubMed
Johnson, K. P., Williams, B. L., Drown, D. M., Adams, R. J. and Clayton, D. H. (2002 b). The population genetics of host specificity: genetic differentiation in dove lice (Insecta: Phthiraptera). Molecular Ecology 11, 2538.CrossRefGoogle ScholarPubMed
Johnson, K. P., Yoshizawa, K. and Smith, V. S. (2004). Multiple origins of parasitism in lice. Proceedings of the Royal Society of London, B 271, 17711776.CrossRefGoogle ScholarPubMed
Klingenberg, C. P. and Gidaszewski, N. A. (2010). Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Systematic Biology 59, 245261.CrossRefGoogle ScholarPubMed
Kuhl, F. P. and Giardina, C. R. (1982). Elliptic Fourier features of a closed contour. Computer Graphics and Image Processing 18, 236258.CrossRefGoogle Scholar
Light, J. E. and Hafner, M. S. (2007). Cophylogeny and disparate rates of evolution in sympatric lineages of chewing lice on pocket gophers. Molecular Phylogenetics and Evolution 45, 9971013.CrossRefGoogle ScholarPubMed
Light, J. E. and Hafner, M. S. (2008). Codivergence in heteromyid rodents (Rodentia: Heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: Anoplura). Systematic Biology 57, 449465.CrossRefGoogle ScholarPubMed
Lyal, C. H. C. (1985). A cladistic analysis and classification of trichodectid mammal lice (Phthiraptera: Ischnocera). Bulletin of the British Museum of Natural History (Entomology) 51, 187346.Google Scholar
Mertins, J. W., Mortenson, J. A., Bernatowicz, J. A. and Briggs Hall, P. (2011). Bovicola tibialis (Phthiraptera: Trichodectidae): occurrence of an exotic chewing louse on cervids in North America. Journal of Medical Entomology 48, 112.CrossRefGoogle ScholarPubMed
Miura, S. (1984). Social behavior and territoriality in male sika deer (Cervus nippon Temminck 1838) during the rut. Zeitschrift fur Tierpsychologie 64, 3373.CrossRefGoogle Scholar
Mogi, M. (1975). A new species of Lipoptena (Diptera, Hippoboscidae) from the Japanese deer. Kontyû 43, 387392.Google Scholar
Mogi, M., Mano, T. and Sawada, I. (2002). Records of Hippoboscidae, Nycteribiidae and Streblidae (Diptera) from Japan. Medical Entomology and Zoology 53, 141165.CrossRefGoogle Scholar
Nagata, J., Masuda, R., Tamate, H. B., Hamasaki, S., Ochiai, K., Asada, M., Tatsuzawa, S., Suda, K., Tado, H. and Yoshida, M. C. (1999). Two genetically distinct lineages of the sika deer, Cervus nippon, in Japanese islands: Comparison of mitochondrial D-loop region sequences. Molecular Phylogenetics and Evolution 13, 511519.CrossRefGoogle ScholarPubMed
Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.Google Scholar
Ohdachi, S. D., Ishibashi, Y., Iwasa, M. A. and Saito, T. (2009). The Wild Mammals of Japan. Shoukadoh, Kyoto, Japan.Google Scholar
Ohtaishi, N. (1986). Preliminary memorandum of classification, distribution and geographic variation on Sika deer. Mammal Science 53, 1317.Google Scholar
Okada, A. (2008). Genetics and ecology: Sika deer. In Middle- and Large-sized Mammals including Primates (Mammalogy in Japan 2) (ed. Takatsuki, N. and Yamagiwa, J.), pp. 273296. University of Tokyo Press, Tokyo, Japan.Google Scholar
Page, R. D. M. (1996). Temporal congruence revisited: comparison of mitochondrial DNA sequence divergence in cospeciating pocket gophers and their chewing lice. Systematic Biology 45, 151167.CrossRefGoogle Scholar
Page, R. D. M. (2002). Tangled Trees: Phylogeny, Cospeciation and Coevolution. University of Chicago Press, Chicago, IL, USA.Google Scholar
Page, R. D. M. and Charleston, M. A. (1998). Trees within trees: phylogeny and historical associations. Trends Ecology and Evolution 13, 356359.CrossRefGoogle ScholarPubMed
Page, R. D. M., Lee, P. L. M., Becher, S. A., Griffiths, R. and Clayton, D. H. (1998). A different tempo of mitochondrial DNA evolution in birds and their parasitic lice. Molecular Phylogenetics and Evolution 9, 276293.CrossRefGoogle ScholarPubMed
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle ScholarPubMed
Poulin, R., Krasnov, B. R., Mouillot, D. and Thieltges, D. W. (2011). The comparative ecology and biogeography of parasites. Philosophical Transactions of the Royal Society, B 366, 23792390.CrossRefGoogle ScholarPubMed
Reed, D. L., Hafner, M. S. and Allen, S. K. (2000). Mammalian hair diameter as a possible mechanism for host specialization in chewing lice. Journal of Mammalogy 81, 9991007.2.0.CO;2>CrossRefGoogle Scholar
Reed, D. L., Smith, V. S., Rogers, A. R., Hammond, S. L. and Clayton, D. H. (2004). Molecular genetic analysis of human lice supports direct contact between modern and archaic humans. PLoS Biology 2, e340.CrossRefGoogle ScholarPubMed
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinfomatics 19, 15721574.CrossRefGoogle ScholarPubMed
SAS Institute Inc. (2011). JMP, Version 9. SAS Institute Inc., North Carolina, USA.Google Scholar
Shimodaira, H. (2002). An approximately unbiased test of phylogenetic tree selection. Systematic Biology 51, 492508.CrossRefGoogle ScholarPubMed
Shimodaira, H. and Hasegawa, M. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17, 12461247.CrossRefGoogle ScholarPubMed
Shreve, S., Mockford, E. L. and Johnson, K. P. (2011). Elevated genetic diversity of mitochondrial genes in asexual population of bark lice (“Psocoptera”: Echmepteryx hageni). Molecular Ecology 20, 44334451.CrossRefGoogle ScholarPubMed
Smith, V. S. (2000). Avian louse phylogeny (Phthiraptera: Ischnocera): A cladistic study based on morphology. Ph.D. thesis, University of Glasgow, Glasgow, UK.Google Scholar
Smith, V. S. (2001). Avian louse phylogeny (Phthiraptera: Ischnocera): A cladistic study based on morphology. Zoological Journal of the Linnean Society 132, 81144.CrossRefGoogle Scholar
Smith, V. S., Light, J. E. and Durden, L. A. (2008). Rodent louse diversity, phylogeny, and cospeciation in the Manu Biosphere Reserve, Peru. Biological Journal of the Linnean Society 95, 598610.CrossRefGoogle Scholar
Smith, V. S., Page, R. D. M. and Johnson, K. P. (2004). Data incongruence and the problem of avian louse phylogeny. Zoologica Scripta 33, 239259.CrossRefGoogle Scholar
Štefka, J., Hoeck, P. E. A., Keller, L. F. and Smith, V. S. (2011). A hitchhikers guide to the Galápagos: co-phylogeography of Galápagos mockingvirds and their parasites. BMC Evolutionary Biology 11, 284.CrossRefGoogle Scholar
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis using Parsimony (*and Other Methods). Version 4. Sinauer Association, Sunderland, MA, USA.Google Scholar
Takatsuki, S. (2006). Ecological History of Sika Deer. University of Tokyo Press, Tokyo, Japan.Google Scholar
Tamate, H. B., Tatsuzawa, S., Suda, K., Izawa, M., Doi, T., Sunagawa, K., Miyahara, M. and Tado, H. (1998). Mitochondrial DNA variation in local populations of the Japanese sika deer Cervus nippon. Journal of Mammalogy 79, 13961403.CrossRefGoogle Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.CrossRefGoogle ScholarPubMed
Torii, H. and Tatsuzawa, S. (2009). Sika deer in Nara park: Unique huan-wildlife relations. In Sika Deer: Biology and Management of Native and Introduced Populations (ed. MacCullough, D. R., Kaji, K. and Takatsuki, S.), pp. 347363. Springer, Tokyo, Japan.CrossRefGoogle Scholar
Weckstein, J. D. (2004). Biogeography explains cophylogenetic patterns in toucan chewing lice. Systematic Biology 53, 154614.CrossRefGoogle ScholarPubMed
Whiteman, N. K., Kimball, R. T. and Parker, P. G. (2007). Co-phylogeography and comparative population genetics of the threatened Galápagos hawk and three ectoparasitic species: ecology shapes population histories within parasite communities. Molecular Ecology 16, 47594773.CrossRefGoogle ScholarPubMed
Yamauchi, T. and Nakayama, H. (2006). Two species of deer keds (Diptera: Hippoboscidae) in Miyajima, Hiroshima Prefecture, Japan. Medical Entomology and Zoology 57, 5558.CrossRefGoogle Scholar
Yoshizawa, K. and Johnson, K. P. (2003). Phylogenetic position of Phthiraptera (Insecta: Paraneoptera) and elevated rate of evolution in mitochondrial 12S and 16S rDNA. Molecular Phylogenetics and Evolution 29, 102114.CrossRefGoogle Scholar
Yoshizawa, K. and Johnson, K. P. (2006). Morphology of male genitalia in lice and their relatives and phylogenetic implications. Systematic Entomology 31, 350361.CrossRefGoogle Scholar
Yoshizawa, K. and Johnson, K. P. (2010). How stable is the “Polyphyly of Lice” hypothesis (Insecta: Psocodea)?: A comparison of phylogenetic signal in multiple genes. Molecular Phylogenetics and Evolution 55, 939951.CrossRefGoogle ScholarPubMed
Zohdy, S., Kemp, A. D., Durden, L. A., Wright, P. C. and Jernvall, J. (2012). Mapping the social network: Tracking lice in a wild primate (Microcebus rufus) population to infer social contacts and vector potential. BMC Ecology 12, 4.CrossRefGoogle Scholar
Supplementary material: File

Mizukoshi Supplementary Material

Supplementary Material_1-5.zip

Download Mizukoshi Supplementary Material(File)
File 11.6 KB
Supplementary material: File

Mizukoshi Supplementary Material

Supplementary Data.xls

Download Mizukoshi Supplementary Material(File)
File 22.7 KB
Supplementary material: PDF

Mizukoshi Supplementary Material

Figure1.pdf

Download Mizukoshi Supplementary Material(PDF)
PDF 85.1 KB
Supplementary material: PDF

Mizukoshi Supplementary Material

Figure2.pdf

Download Mizukoshi Supplementary Material(PDF)
PDF 76.9 KB