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Szidat's rule re-tested: relationships between flea and host phylogenetic clade ranks in four biogeographic realms

Published online by Cambridge University Press:  18 February 2016

BORIS R. KRASNOV ,
DANIEL KIEFER ,
ELIZABETH M. WARBURTON  and
IRINA S. KHOKHLOVA
BORIS R. KRASNOV*
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, 8499000 Midreshet Ben-Gurion, Israel
DANIEL KIEFER
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, 8499000 Midreshet Ben-Gurion, Israel
ELIZABETH M. WARBURTON
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, 8499000 Midreshet Ben-Gurion, Israel
IRINA S. KHOKHLOVA
Affiliation:
Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, 8499000 Midreshet Ben-Gurion, Israel
*
*Corresponding author. Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, 84990 Midreshet Ben-Gurion, Israel. Tel: +972 -8-6596841. Fax: +972-8-6596772. E-mail: [email protected]
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Summary

We tested Szidat's rule (the more primitive the host, the more primitive the parasites it harbours) by analysing the relationships between phylogenetic clade ranks of fleas and their small mammalian hosts in four biogeographic realms (Afrotropics, Neotropics, Nearctic and Palearctic). From the host perspective, we tested the association between host clade rank and the mean clade rank of all fleas collected from this host. From the flea perspective, we tested the relationships between flea clade rank and the mean clade rank of hosts on which this flea was recorded. First, we tested whether the analysis of the relationships between host and flea clade ranks should be controlled for phylogenetic dependence among either host or flea species. Then, we tested for the associations between host and flea clade ranks separately for each realm using either a phylogenetic general least-squares analysis or an ordinary least-squares analysis. In all realms, the mean clade rank of fleas parasitic on a given host increased with an increase of this host's clade rank, and the mean clade rank of hosts recorded on a given flea increased with an increase of this flea's clade rank, suggesting that Szidat's rule, at least to some extent, holds for fleas.

Keywords

Clade rankfleasmammalsphylogeny
Type
Research Article
Information
Parasitology , Volume 143 , Issue 6 , May 2016 , pp. 723 - 731
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Ashton, K. G. (2002). Patterns of within-species body size variation of birds: strong evidence for Bergmann's rule. Global Ecology and Biogeography 11, 505–523.CrossRefGoogle Scholar
Beaucournu, C. and Gallardo, M. H. (1991 a). Catalogue provisoire de Puces du Chili (Insecta; Siphonaptera). 1 partie. Bulletin de la Societe Francaise de Parasitologie 9, 237–270.Google Scholar
Beaucournu, C. and Gallardo, M. H. (1991 b). Catalogue provisoire de Puces du Chili (Insecta; Siphonaptera). 2 partie. Bulletin de la Societe Francaise de Parasitologie 10, 93–130.Google Scholar
Berrizbeitia, L., Fernanda, M., Diaz, M., Barquez, R. M. and Lareschi, M. (2013). Pulgas (Siphonaptera) parásitas de roedores (Rodentia: Cricetidae) de la provincia de Salta, Argentina: nuevos registros de distribución. Revista de la Sociedad Entomológica Argentina 72, 141–146.Google Scholar
Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L. and Purvis, A. (2007). The delayed rise of present-day mammals. Nature 446, 507–512.CrossRefGoogle ScholarPubMed
Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L. and Purvis, A. (2008). The delayed rise of present-day mammals. Corrigendum. Nature 458, 274.CrossRefGoogle Scholar
Blomberg, S. P., Garland, T. and Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745.Google ScholarPubMed
Brooks, D. R. (1979). Testing the context and extent of host–parasite coevolution. Systematic Zoology 28, 299–307.CrossRefGoogle Scholar
Brooks, D. R. (1985). Historical ecology: a new approach to studying the evolution of associations. Annals of the Missouri Botanical Gardens 72, 660–680.CrossRefGoogle Scholar
Brooks, D. R. (1988). Macroevolutionary comparisons of host and parasite phylogenies. Annual Review of Ecology and Systematics 19, 235–259.CrossRefGoogle Scholar
Brooks, D. R. and McLennan, D. A. (1991). Phylogeny, Ecology, and Behaviour: A Research Program in Comparative Biology. University of Chicago, Chicago.Google Scholar
Brooks, D. R., León-Règagnon, V., McLennan, D. A. and Zelmer, D. (2006). Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87, S76–S85.CrossRefGoogle ScholarPubMed
Caira, J. N. and Jensen, K. (2001). An investigation of the co-evolutionary relationships between onchobothriid tapeworms and their elasmobranch hosts. International Journal for Parasitology 31, 960–75.CrossRefGoogle ScholarPubMed
Craw, R. C., Grehan, J. R. and Heads, M. J. (1999). Panbiogeography: Tracking the History of Life. Oxford University Press, NY.Google Scholar
Desdevises, Y., Jovelin, R., Jousson, O. and Morand, S. (2000). Comparison of ribosomal DNA sequences of Lamellodiscus spp. (Monogenea, Diplectanidae) parasitising Pagellus (Sparidae, Teleostei) in the north Mediterranean Sea: species divergence and coevolutionary interactions. International Journal for Parasitology 30, 741–746.CrossRefGoogle ScholarPubMed
Desdevises, Y., Morand, S., Jousson, O. and Legendre, P. (2002). Coevolution between Lamellodiscus (Monogenea: Diplectanidae) and Sparidae (Teleostei): the study of a complex host-parasite system. Evolution 56, 2459–2471.Google Scholar
Diniz-Filho, J. A. F. (2001). Phylogenetic autocorrelation under distinct evolutionary processes. Evolution 55, 1104–1109.CrossRefGoogle ScholarPubMed
Ezenwa, V. O., Price, S. A., Altizer, S., Vitone, N. D. and Cook, K. C. (2006). Host traits and parasite species richness in even and odd-toed hoofed mammals, Artiodactyla and Perissodactyla. Oikos 115, 526–536.CrossRefGoogle Scholar
Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist 125, 1–15.CrossRefGoogle Scholar
Freckleton, R. P., Harvey, P. H. and Pagel, M. (2002). Phylogenetic analysis and comparative data: a test and review of the evidence. American Naturalist 160, 712–726.CrossRefGoogle Scholar
Grafen, A. (1989). The phylogenetic regression. Philosophical Transactions of the Royal Society of London B 326, 119–157.Google ScholarPubMed
Hafner, M. S. and Nadler, S. A. (1988). Phylogenetic trees support the coevolution of parasites and their hosts. Nature 332, 258–259.CrossRefGoogle ScholarPubMed
Hafner, M. S. and Nadler, S. A. (1990). Cospeciation in host-parasite assemblages: comparative analysis of rates of evolution and timing of cospeciation events. Systematic Zoology 39, 192–204.CrossRefGoogle Scholar
Hafner, M. S. and Page, R. D. M. (1995). Molecular phylogenies and host–parasite cospeciation: gophers and lice as a model system. Philosophical Transactions of the Royal Society of London B 349, 77–83.Google ScholarPubMed
Hansen, T. F. (1997). Stabilizing selection and the comparative analysis of adaptation. Evolution 51, 1341–1351.CrossRefGoogle ScholarPubMed
Harvey, P. H. and Pagel, M. (1991). The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.CrossRefGoogle Scholar
Hoberg, E. P., Brooks, D. R. and Siegel-Causey, D. (1997). Host-parasite co-speciation: history, principles, and prospects. In Host–Parasite Evolution: General Principles and Avian Models (ed. Clayton, D. H. and Moore, J.), pp. 212–235. Oxford University Press, Oxford.CrossRefGoogle Scholar
Janzen, D. H. (1985). On ecological fitting. Oikos 45, 308–310.CrossRefGoogle Scholar
Jombart, T. and Dray, S. (2010). Adephylo: exploratory analyses for the phylogenetic comparative method. Bioinformatics 26, 1907–1909.CrossRefGoogle Scholar
Klassen, G. J. (1992). Coevolution: a history of the macroevolutionary approach to studying host-parasite associations. Journal of Parasitology 78, 573–587.CrossRefGoogle ScholarPubMed
Klein, J. M. and Uilenberg, G. (1966). Données faunistiques et écologiques sur les puces de Madagascar (Siphonaptera). Cahiers O.R.S.T.O.M., série Entomologie Médicale 4, 31–60.Google Scholar
Knouft, J. H. and Page, L. M. (2003). The evolution of body size in extant groups of North American freshwater fishes: speciation, size distributions, and Cope's rule. American Naturalist 161, 413–421.CrossRefGoogle ScholarPubMed
Krasnov, B. R. (2008). Functional and Evolutionary Ecology of Fleas. A Model for Ecological Parasitology. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Krasnov, B. R. and Khokhlova, I. S. (2001). The effect of behavioural interactions on the transfer of fleas (Siphonaptera) between two rodent species. Journal of Vector Ecology 26, 191–190.Google ScholarPubMed
Krasnov, B. R. and Shenbrot, G. I. (2002). Coevolutionary events in history of association of jerboas (Rodentia: Dipodidae) and their flea parasites. Israel Journal of Zoology 48, 331–350.CrossRefGoogle Scholar
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S. and Poulin, R. (2004). Relationships between parasite abundance and the taxonomic distance among a parasite's host species: an example with fleas parasitic on small mammals. International Journal for Parasitology 34, 1289–1297.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Poulin, R. and Mouillot, D. (2011). Scale-dependence of phylogenetic signal in ecological traits of ectoparasites. Ecography 34, 114–122.CrossRefGoogle Scholar
Lehane, M. (2005). The Biology of Blood-Sucking in Insects, 2nd Edn. Cambridge University Press, Cambridge.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, 997–1013.CrossRefGoogle ScholarPubMed
Light, J. E., Smith, V. 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.CrossRefGoogle ScholarPubMed
Lu, L. and Wu, H. (2005). Morphological phylogeny of Geusibia Jordan, 1932 (Siphonaptera: Leptopsyllidae) and the host-parasite relationships with pikas. Systematic Parasitology 61, 65–78.Google Scholar
Maddison, W. P. and Maddison, D. R. (2011). Mesquite: a Modular System for Evolutionary Analysis, Version 2.75. http://mesquiteproject.org Google Scholar
Martins, E. P. and Hansen, T. F. (1997). Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. American Naturalist 149, 646–667.CrossRefGoogle Scholar
Medvedev, S. (2005). An Attempted System Analysis of the Evolution of the Order of Fleas (Siphonaptera). Lectures in Memoriam N. A. Kholodkovsky, No. 57. Russian Entomological Society and Zoological Institute of Russian Academy of Sciences (in Russian), Saint Petersburg, Russia.Google Scholar
Medvedev, S. G. (1997 a). Host-parasite relations in fleas (Siphonaptera). I. Entomological Review 77, 318–337.Google Scholar
Medvedev, S. G. (1997 b). Host-parasite relations in fleas (Siphonaptera). II. Entomological Review 77, 511–521.Google Scholar
Morrone, J. J. and Gutiérrez, A. (2005). Do fleas (Insecta: Siphonaptera) parallel their mammal host diversification in the Mexican transition zone? Journal of Biogeography 32, 1315–1325.CrossRefGoogle Scholar
Morrone, J. J., Acosta, R. and Gutiérrez, A. (2000). Cladistics, biogeography, and host relationships of the flea subgenus Ctenophthalmus (Alloctenus), with the description of a new Mexican species (Siphonaptera: Ctenophthalmidae). Journal of the New York Entomological Society 108, 1–12.CrossRefGoogle Scholar
Pagel, M. (1997). Inferring evolutionary processes from phylogenies. Zoologica Scripta 26, 331–348.CrossRefGoogle Scholar
Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature 410, 877–884.CrossRefGoogle Scholar
Pagel, M. (2002). Modelling the evolution of continuously varying characters on phylogenetic trees. In Morphology, Shape and Phylogeny (ed. MacLeod, N., Foley, P. L.), pp. 269–286. Taylor & Francis, London.CrossRefGoogle Scholar
Paradis, E., Claude, J. and Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290.CrossRefGoogle ScholarPubMed
Paterson, A. M. and Gray, R. D. (1997). Host-parasite co-speciation, host switching, and missing the boat. In Host-Parasite Evolution: General Principles and Avian Models (ed. Clayton, D. H. and Moore, J.), pp. 236–250. Oxford University Press, Oxford.CrossRefGoogle Scholar
Paterson, A. M. and Banks, J. (2001). Analytical approaches to measuring cospeciation of host and parasites: through a glass, darkly. International Journal forParasitology 31, 1012–1022.Google ScholarPubMed
Paterson, A. M., Wallis, G. P., Wallis, L. J. and Gray, R. D. (2000). Seabird and louse coevolution: complex histories revealed by 12S rRNA sequences and reconciliation analyses. Systematic Biology 38, 144–153.Google Scholar
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. and R Core Team (2015). nlme: linear and nonlinear mixed effects models. R package version 3.1–122, http://CRAN.R-project.org/package=nlme Google Scholar
Poulin, R. (2005). Evolutionary trends in body size of parasitic flatworms. Biological Journal of the Linnean Society 85, 181–189.CrossRefGoogle Scholar
Poulin, R., Krasnov, B. R., Shenbrot, G. I., Mouillot, D. and Khokhlova, I. S. (2006). Evolution of host specificity in fleas: is it directional and irreversible? International Journal for Parasitology 36, 185–191.CrossRefGoogle ScholarPubMed
R Core Team (2015). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ Google Scholar
Revell, L. J. (2010). Phylogenetic signal and linear regression on species data. Methods in Ecology and Evolution 1, 319–329.CrossRefGoogle Scholar
Revell, L. J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3, 217–223.CrossRefGoogle Scholar
Ronquist, F. and Liljeblad, J. (2001). Evolution of the gall wasp-host plant association. Evolution 55, 2503–2522.Google ScholarPubMed
Roy, B. A. (2001). Patterns of association between crucifers and their flower-mimic pathogens: host jumps are more common than coevolution or cospeciation. Evolution 55, 41–53.Google ScholarPubMed
Shenbrot, G. I., Krasnov, B. R. and Lu, L. (2007). Geographic range size and host specificity in ectoparasites: a case study with Amphipsylla fleas and rodent hosts. Journal of Biogeography 34, 1679–690.CrossRefGoogle Scholar
Traub, R. (1980). The zoogeography and evolution of some fleas, lice and mammals. In Fleas. Proceedings of the International Conference on Fleas, Ashton Wold, Peterborough, UK, 21–25 June 1977 (ed. Traub, R. and Starke, H.), pp. 93–172. A.A. Balkema, Rotterdam.Google Scholar
Traub, R. (1985). Coevolution of fleas and mammals. In Coevolution of Parasitic Arthropods and Mammals (ed. Kim, K. C.), pp. 295–437. John Wiley & Sons, NY.Google Scholar
Von Ihering, H. (1891). On the ancient relations between New Zealand and South America. Transactions and Proceedings of the New Zealand Institute 24, 431–445.Google Scholar
Whiting, M. F., Whiting, S., Hastriter, M. W. and Dittmar, K. (2008). A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. Cladistics 24, 677–707.CrossRefGoogle Scholar
Zhu, Q., Hastriter, M. W., Whiting, M. F. and Dittmar, K. (2015). Fleas (Siphonaptera) are cretaceous, and evolved with Theria. Molecular Phylogenetics and Evolution 90, 129–139.CrossRefGoogle ScholarPubMed
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