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Testing local-scale panmixia provides insights into the cryptic ecology, evolution, and epidemiology of metazoan animal parasites

Published online by Cambridge University Press:  04 April 2012

MARY J. GORTON
Affiliation:
Department of Biology, Texas A&M University, 3258 TAMU, College Station, TX 77843, USA
EMILY L. KASL
Affiliation:
Department of Biology, Texas A&M University, 3258 TAMU, College Station, TX 77843, USA
JILLIAN T. DETWILER
Affiliation:
Department of Biology, Texas A&M University, 3258 TAMU, College Station, TX 77843, USA
CHARLES D. CRISCIONE*
Affiliation:
Department of Biology, Texas A&M University, 3258 TAMU, College Station, TX 77843, USA
*
*Corresponding author: Department of Biology, Texas A&M University, 3258 TAMU, College Station, TX 77843, USA. Tel: +979 845 0917. Fax: +979 845 2891. E-mail: [email protected]

Summary

When every individual has an equal chance of mating with other individuals, the population is classified as panmictic. Amongst metazoan parasites of animals, local-scale panmixia can be disrupted due to not only non-random mating, but also non-random transmission among individual hosts of a single host population or non-random transmission among sympatric host species. Population genetics theory and analyses can be used to test the null hypothesis of panmixia and thus, allow one to draw inferences about parasite population dynamics that are difficult to observe directly. We provide an outline that addresses 3 tiered questions when testing parasite panmixia on local scales: is there greater than 1 parasite population/species, is there genetic subdivision amongst infrapopulations within a host population, and is there asexual reproduction or a non-random mating system? In this review, we highlight the evolutionary significance of non-panmixia on local scales and the genetic patterns that have been used to identify the different factors that may cause or explain deviations from panmixia on a local scale. We also discuss how tests of local-scale panmixia can provide a means to infer parasite population dynamics and epidemiology of medically relevant parasites.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Agola, L. E., Steinauer, M. L., Mburu, D. N., Mungai, B. N., Mwangi, I. N., Magoma, G. N., Loker, E. S. and Mkoji, G. M. (2009). Genetic diversity and population structure of Schistosoma mansoni within human infrapopulations in Mwea, central Kenya assessed by microsatellite markers. Acta Tropica 111, 219225.CrossRefGoogle ScholarPubMed
Agrawal, A. F. and Lively, C. M. (2001). Parasites and the evolution of self-fertilization. Evolution 55, 869879.CrossRefGoogle ScholarPubMed
Arnaud-Haond, S., Duarte, C. M., Alberto, F. and Serrao, E. A. (2007). Standardizing methods to address clonality in population studies. Molecular Ecology 16, 51155139.CrossRefGoogle ScholarPubMed
Balloux, F. (2004). Heterozygote excess in small populations and the heterozygote-excess effective population size. Evolution 58, 18911900.Google ScholarPubMed
Balloux, F., Lehmann, L. and de Meeûs, T. (2003). The population genetics of clonal and partially clonal diploids. Genetics 164, 16351644.CrossRefGoogle ScholarPubMed
Barton, N. H. (2001). The role of hybridization in evolution. Molecular Ecology 10, 551568.CrossRefGoogle ScholarPubMed
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Caillaud, D., Prugnolle, F., Durand, P., Theron, A. and de Meeus, T. (2006). Host sex and parasite genetic diversity. Microbes and Infection 8, 24772483.CrossRefGoogle ScholarPubMed
Charlesworth, D. (2003). Effects of inbreeding on the genetic diversity of populations. Philosophical Transactions of the Royal Society (Series B) 358, 10511070.CrossRefGoogle ScholarPubMed
Chevillon, C., Koffi, B. B., Barre, N., Durand, P., Arnathau, C. and de Meeus, T. (2007). Direct and indirect inferences on parasite mating and gene transmission patterns: pangamy in the cattle tick Rhipicephalus (Boophilus) microplus. Infection Genetics and Evolution 7, 298304.CrossRefGoogle ScholarPubMed
Cornell, S. J., Isham, V. S., Smith, G. and Grenfell, B. T. (2003). Spatial parasite transmission, drug resistance, and the spread of rare genes. Proceedings of the National Academy of Sciences, USA 100, 74017405.CrossRefGoogle ScholarPubMed
Criscione, C. D., Anderson, J. D., Sudimack, D., Peng, W., Jha, B., Williams-Blangero, S. and Anderson, T. J. C. (2007). Disentangling hybridization and host colonization in parasitic roundworms of humans and pigs. Proceedings of the Royal Society of London, B 274, 26692677.Google ScholarPubMed
Criscione, C. D., Anderson, J. D., Sudimack, D., Subedi, J., Upadhayay, R. P., Jha, B., Williams, K. D., Williams-Blangero, S. and Anderson, T. J. C. (2010). Landscape genetics reveals focal transmission of a human macroparasite. Plos Neglected Tropical Diseases 4, e665.CrossRefGoogle ScholarPubMed
Criscione, C. D. and Blouin, M. S. (2004). Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58, 198202.Google ScholarPubMed
Criscione, C. D. and Blouin, M. S. (2005). Effective sizes of macroparasite populations: a conceptual model. Trends in Parasitology 21, 212217.CrossRefGoogle ScholarPubMed
Criscione, C. D. and Blouin, M. S. (2006). Minimal selfing, few clones, and no among-host genetic structure in a hermaphroditic parasite with asexual larval propagation. Evolution 60, 553562.Google Scholar
Criscione, C. D. and Blouin, M. S. (2007). Parasite phylogeographical congruence with salmon host evolutionarily significant units: implications for salmon conservation. Molecular Ecology 16, 9931005.CrossRefGoogle ScholarPubMed
Criscione, C. D., Poulin, R. and Blouin, M. S. (2005). Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 22472257.CrossRefGoogle ScholarPubMed
Criscione, C. D., Vilas, R., Paniagua, E. and Blouin, M. S. (2011). More than meets the eye: detecting cryptic microgeographic population structure in a parasite with a complex life cycle. Molecular Ecology 20, 25102524.CrossRefGoogle Scholar
Crow, J. F. and Denniston, C. (1988). Inbreeding and variance effective population numbers. Evolution 42, 482495.CrossRefGoogle ScholarPubMed
David, P., Pujol, B., Viard, F., Castella, V. and Goudet, J. (2007). Reliable selfing rate estimates from imperfect population genetic data. Molecular Ecology 16, 24742487.CrossRefGoogle ScholarPubMed
de Meeûs, T., Beati, L., Delaye, C., Aeschlimann, A. and Renaud, F. (2002). Sex-biased genetic structure in the vector of Lyme disease, Ixodes ricinus. Evolution 56, 18021807.Google ScholarPubMed
de Meeûs, T., Humair, P. F., Grunau, C., Delaye, C. and Renaud, F. (2004). Non-Mendelian transmission of alleles at microsatellite loci: an example in Ixodes ricinus, the vector of Lyme disease. International Journal for Parasitology 34, 943950.CrossRefGoogle ScholarPubMed
de Meeûs, T., Koffi, B. B., Barre, N., de Garine-Wichatitsky, M. and Chevillon, C. (2010). Swift sympatric adaptation of a species of cattle tick to a new deer host in New Caledonia. Infection Genetics and Evolution 10, 976983.CrossRefGoogle ScholarPubMed
de Meeûs, T., Lehmann, L. and Balloux, F. (2006). Molecular epidemiology of clonal diploids: A quick overview and a short DIY (do it yourself) notice. Infection Genetics and Evolution 6, 163170.CrossRefGoogle Scholar
de Meeûs, T., McCoy, K. D., Prugnolle, F., Chevillon, C., Durand, P., Hurtrez-Bousses, S. and Renaud, F. (2007 a). Population genetics and molecular epidemiology or how to “debusquer la bete”. Infection Genetics and Evolution 7, 308332.CrossRefGoogle Scholar
de Meeûs, T., Prugnolle, F. and Agnew, P. (2007 b). Asexual reproduction: Genetics and evolutionary aspects. Cellular and Molecular Life Sciences 64, 13551372.CrossRefGoogle ScholarPubMed
Detwiler, J. T. and Criscione, C. D. (2010). An infectious topic in reticulate evolution: Introgression and hybridization in animal parasites. Genes 1, 102123.CrossRefGoogle ScholarPubMed
Detwiler, J. T. and Criscione, C. D. (2011). Testing Mendelian inheritance from field-collected parasites: Revealing duplicated loci enables correct inference of reproductive mode and mating system. International Journal for Parasitology 41, 11851195.CrossRefGoogle ScholarPubMed
Dharmarajan, G., Beasley, J. C. and Rhodes, O. E. (2010). Spatial and temporal factors affecting parasite genotypes encountered by hosts: Empirical data from American dog ticks (Dermacentor variabilis) parasitising raccoons (Procyon lotor). International Journal for Parasitology 40, 787795.CrossRefGoogle ScholarPubMed
Dharmarajan, G., Beasley, J. C. and Rhodes, O. E. (2011). Heterozygote deficiencies in parasite populations: an evaluation of interrelated hypotheses in the raccoon tick, Ixodes texanus. Heredity 106, 253260.CrossRefGoogle ScholarPubMed
Fisher, M. C. and Viney, M. E. (1998). The population genetic stucture of the facultatively sexual parasitic nematode Strongyloides ratti in wild rats. Proceedings of the Royal Society of London, B 265, 703709.CrossRefGoogle Scholar
Gomez-Diaz, E., Doherty, P. F., Duneau, D. and McCoy, K. D. (2010). Cryptic vector divergence masks vector-specific patterns of infection: an example from the marine cycle of Lyme borreliosis. Evolutionary Applications 3, 391401.CrossRefGoogle ScholarPubMed
Goodwillie, C., Kalisz, S. and Eckert, C. G. (2005). The evolutionary enigma of mixed mating systems in plants: Occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology Evolution and Systematics 36, 4779.CrossRefGoogle Scholar
Gregorius, H. R. (2005). Testing for clonal propagation. Heredity 94, 173179.CrossRefGoogle ScholarPubMed
Grillo, V., Craig, B. H., Wimmer, B. and Gilleard, J. S. (2008). Microsatellite genotyping supports the hypothesis that Teladorsagia davtiani and Teladorsagia trifurcata are morphotypes of Teladorsagia circumcincta. Molecular and Biochemical Parasitology 159, 5963.CrossRefGoogle ScholarPubMed
Grillo, V., Jackson, F., Cabaret, J. and Gilleard, J. S. (2007). Population genetic analysis of the ovine parasitic nematode Teladorsagia circumcincta and evidence for a cryptic species. International Journal for Parasitology 37, 435447.CrossRefGoogle ScholarPubMed
Gurarie, D. and Seto, E. Y. W. (2009). Connectivity sustains disease transmission in environments with low potential for endemicity: modeling schistosomiasis with hydrologic and social connectivities. Journal of the Royal Society Interface 6, 495508.CrossRefGoogle ScholarPubMed
Guzinski, J., Bull, C. M., Donnellan, S. C. and Gardner, M. G. (2009). Molecular genetic data provide support for a model of transmission dynamics in an Australian reptile tick, Bothriocroton hydrosauri. Molecular Ecology 18, 227234.CrossRefGoogle Scholar
Hedrick, P. W. (2005). Genetics of Populations , 3rd Edn. Jones and Bartlett Publishers, Sudbury, MA, USA.Google Scholar
Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P. (Eds.) (2002). The Ecology of Wildlife Diseases. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Jarne, P. and Auld, J. R. (2006). Animals mix it up too: The distribution of self-fertilization among hermaphroditic animals. Evolution 60, 18161824.Google ScholarPubMed
Jarne, P. and David, P. (2008). Quantifying inbreeding in natural populations of hermaphroditic organisms. Heredity 100, 431439.CrossRefGoogle ScholarPubMed
Jones, P. H. and Britten, H. B. (2010). The absence of concordant population genetic structure in the black-tailed prairie dog and the flea, Oropsylla hirsuta, with implications for the spread of Yersinia pestis. Molecular Ecology 19, 20382049.CrossRefGoogle ScholarPubMed
Keeney, D. B., Waters, J. M. and Poulin, R. (2007 a). Clonal diversity of the marine trematode Maritrema novaezealandensis within intermediate hosts: the molecular ecology of parasite life cycles. Molecular Ecology 16, 431439.CrossRefGoogle ScholarPubMed
Keeney, D. B., Waters, J. M. and Poulin, R. (2007 b). Diversity of trematode genetic clones within amphipods and the timing of same-clone infections. International Journal for Parasitology 37, 351357.CrossRefGoogle ScholarPubMed
Kempf, F., Boulinier, T., de Meeûs, T., Arnathau, C. and McCoy, K. D. (2009). Recent evolution of host-associated divergence in the seabird tick Ixodes uriae. Molecular Ecology 18, 44504462.CrossRefGoogle ScholarPubMed
Kempf, F., de Meeûs, T., Arnathau, C., Degeilh, B. and McCoy, K. D. (2009). Assortative pairing in Ixodes ricinus (Acari: Ixodidae), the European vector of lyme borreliosis. Journal of Medical Entomology 46, 471474.CrossRefGoogle ScholarPubMed
Kempf, F., McCoy, K. D. and de Meeûs, T. (2010). Wahlund effects and sex-biased dispersal in Ixodes ricinus, the European vector of Lyme borreliosis: New tools for old data. Infection Genetics and Evolution 10, 989997.CrossRefGoogle ScholarPubMed
Knapp, J., Guislain, M. H., Bart, J. M., Raoul, F., Gottstein, B., Giraudoux, P. and Piarroux, R. (2008). Genetic diversity of Echinococcus multilocularis on a local scale. Infection Genetics and Evolution 8, 367373.CrossRefGoogle ScholarPubMed
Koffi, B. B., de Meeûs, T., Barre, N., Durand, P., Arnathau, C. and Chevillon, C. (2006). Founder effects, inbreeding and effective sizes in the Southern cattle tick: the effect of transmission dynamics and implications for pest management. Molecular Ecology 15, 46034611.CrossRefGoogle ScholarPubMed
Lagrue, C., Poulin, R. and Keeney, D. B. (2009). Effects of clonality in mutliple infections on the life-history strategy of the trematode Coitocaecum parvum in its amphipod intermediate host. Evolution 63, 14171426.CrossRefGoogle Scholar
Leignel, V., Cabaret, J. and Humbert, J. F. (2002). New molecular evidence that Teladorsagia circumcincta (Nematoda: Trichostrongylidea) is a species complex. Journal of Parasitology 88, 135140.CrossRefGoogle ScholarPubMed
Leung, T. L. F., Poulin, R. and Keeney, D. B. (2009). Accumulation of diverse parasite genotypes within the bivalve second intermediate host of the digenean Gymnophallus sp. International Journal for Parasitology 39, 327331.CrossRefGoogle ScholarPubMed
Louhi, K. R., Karvonen, A., Rellstab, C. and Jokela, J. (2010). Is the population genetic structure of complex life cycle parasites determined by the geographic range of the most motile host? Infection Genetics and Evolution 10, 12711277.CrossRefGoogle ScholarPubMed
Lymbery, A. J., Constantine, C. C. and Thompson, R. C. A. (1997). Self-fertilization without genomic or population structuring in a parasitic tapeworm. Evolution 51, 289294.CrossRefGoogle ScholarPubMed
Lymbery, A. J. L., Thompson, R. C. A. and Hobbs, R. P. (1990). Genetic diversity and genetic differentiation in Echinococcus granulosus (Batsch, 1786) from domestic and sylvatic hosts on the mainland Australia. Parasitology 101, 283289.CrossRefGoogle Scholar
McCoy, K. D. (2003). Sympatric speciation in parasites – what is sympatry? Trends in Parasitology 19, 400404.CrossRefGoogle ScholarPubMed
McCoy, K. D., Boulinier, T., Schjorring, S. and Michalakis, Y. (2002). Local adaptation of the ectoparasite Ixodes uriae to its seabird host. Evolutionary Ecology Research 4, 441456.Google Scholar
McCoy, K. D., Boulinier, T., Tirard, C. and Michalakis, Y. (2001). Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae. Journal of Evolutionary Biology 14, 395405.CrossRefGoogle Scholar
McCoy, K. D., Chapuis, E., Tirard, C., Boulinier, T., Michalakis, Y., Le Bohec, C., Le Maho, Y. and Gauthier-Clerc, M. (2005). Recurrent evolution of host-specialized races in a globally distributed parasite. Proceedings of the Royal Society of London, B 272, 23892395.Google Scholar
McCoy, K. D., Tirard, C. and Michalakis, Y. (2003). Spatial genetic structure of the ectoparasite Ixodes uriae within breeding cliffs of its colonial seabird host. Heredity 91, 422429.CrossRefGoogle ScholarPubMed
Meirmans, P. G. and Hedrick, P. W. (2011). Assessing population structure: F-ST and related measures. Molecular Ecology Resources 11, 518.CrossRefGoogle ScholarPubMed
Mulvey, M., Aho, J. M., Lydeard, C., Leberg, P. L. and Smith, M. H. (1991). Comparative population genetic structure of a parasite (Fascioloides magna) and its definitive host. Evolution 45, 16281640.Google ScholarPubMed
Nadler, S. A. (1995). Microevolution and the genetic structure of parasite populations. Journal of Parasitology 81, 395403.CrossRefGoogle ScholarPubMed
Nadler, S. A., Hafner, M. S., Hafner, J. C. and Hafner, D. J. (1990). Genetic differentiation among chewing louse populations (Mallophaga: Trichodectidae) in a pocket gopher contact zone (Rodentia: Geomydiae). Evolution 44, 942951.CrossRefGoogle Scholar
Nadler, S. A. and Pérez-Ponce de León, G. (2011). Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138, 16881709.CrossRefGoogle ScholarPubMed
Nieberding, C., Morand, S., Libois, R. and Michaux, J. R. (2006). Parasites and the island syndrome: the colonization of the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845). Journal of Biogeography 33, 12121222.CrossRefGoogle Scholar
Paterson, S., Fisher, M. C. and Viney, M. E. (2000). Inferring infection processes of a parasitic nematode using population genetics. Parasitology 120, 185194.CrossRefGoogle ScholarPubMed
Pérez-Ponce de León, G. and Nadler, S. A. (2010). What we don't recognize can hurt us: a plea for awareness about cryptic species. Journal of Parasitology 96, 453464.CrossRefGoogle Scholar
Perkins, S. L., Martinsen, E. S. and Falk, B. G. (2011). Do molecules matter more than morphology? Promises and pitfalls in parasites. Parasitology 138, 16641674.CrossRefGoogle ScholarPubMed
Poulin, R. (2011). Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biology Letters 7, 241244.CrossRefGoogle ScholarPubMed
Prugnolle, F., Choisy, M., Theron, A., Durand, P. and de Meeûs, T. (2004 a). Sex-specific correlation between heterozygosity and clone size in the trematode Schistosoma mansoni. Molecular Ecology 13, 28592864.CrossRefGoogle ScholarPubMed
Prugnolle, F. and de Meeûs, T. (2002). Inferring sex biased dispersal from population genetic tools: a review. Heredity 88, 161165.CrossRefGoogle ScholarPubMed
Prugnolle, F., de Meeûs, T., Durand, P., Sire, C. and Theron, A. (2002). Sex-specific genetic structure in Schistosoma mansoni evolutionary and epidemiology implications. Molecular Ecology 11, 12311238.CrossRefGoogle Scholar
Prugnolle, F., Durand, P., Theron, A., Chevillon, C. and de Meeûs, T. (2003). Sex-specific genetic structure: new trends for dioecious parasites. Trends in Parasitology 19, 171174.CrossRefGoogle ScholarPubMed
Prugnolle, F., Liu, H., de Meeûs, T. and Balloux, F. (2005 a). Population genetics of complex life-cycle parasites: an illustration with trematodes. International Journal of Parasitology 35, 255263.CrossRefGoogle ScholarPubMed
Prugnolle, F., Roze, D., Theron, A. and de Meeûs, T. (2005 b). F-statistics under alternation of sexual and asexual reproduction: a model and data from schistosomes (platyhelminth parasites). Molecular Ecology 14, 13551365.CrossRefGoogle Scholar
Prugnolle, F., Theron, A., Durand, P. and de Meeûs, T. (2004 b). Test of pangamy by genetic analysis of Schistosoma mansoni pairs within its natural murine host in Guadeloupe. Journal of Parasitology 90, 507509.CrossRefGoogle ScholarPubMed
Rauch, G., Kalbe, M. and Reusch, T. B. H. (2005). How a complex life cycle can improve a parasite's sex life. Journal of Evolutionary Biology 18, 10691075.CrossRefGoogle ScholarPubMed
Renaud, F. and Gabrion, C. (1988). Speciation of cestoda: evidence for two sibling species in the complex Bothrimonus nylandicus (Schneider 1902) (Cestoda: Cyathocephalidae). Parasitology 97, 139147.CrossRefGoogle Scholar
Reversat, J., Renaud, F. and Maillard, C. (1989). Biology of parasite populations: The differential specificity of the genus Helicometra Odhner, 1902 (Trematoda, Opecoelidae) the Mediterranean Sea demonstrated by enzyme electrophoresis. International Journal for Parasitology 19, 885890.CrossRefGoogle Scholar
Rudge, J. W., Carabin, H., Balolong, E., Tallo, V., Shrivastava, J., Lu, D. B., Basanez, M. G., Olveda, R., McGarvey, S. T. and Webster, J. P. (2008). Population genetics of Schistosoma japonicum within the Philippines suggest high levels of transmission between humans and dogs. Plos Neglected Tropical Diseases 2, e340.CrossRefGoogle ScholarPubMed
Rudge, J. W., Lu, D. B., Fang, G. R., Wang, T. P., Basanez, M. G. and Webster, J. P. (2009). Parasite genetic differentiation by habitat type and host species: molecular epidemiology of Schistosoma japonicum in hilly and marshland areas of Anhui Province, China. Molecular Ecology 18, 21342147.CrossRefGoogle ScholarPubMed
Schwab, A. E., Churcher, T. S., Schwab, A. J., Basanez, M. G. and Prichard, R. K. (2006). Population genetics of concurrent selection with albendazole and ivermectin or diethylcarbamazine on the possible spread of albendazole resistance in Wuchereria bancrofti. Parasitology 133, 589601.CrossRefGoogle ScholarPubMed
Smyth, J. D. and McManus, D. P. (1989). The Physiology and Biochemistry of Cestodes, Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Šnábel, V., Hanzelová, V., Mattiucci, S., D'Amelio, S. and Paggi, L. (1996). Genetic polymorphism in Proteocephalus exiguus shown by enzyme electrophoresis. Journal of Helminthology 70, 345349.CrossRefGoogle Scholar
Štefka, J., Hypša, V. and Scholz, T. (2009). Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Molecular Ecology 18, 11871206.CrossRefGoogle ScholarPubMed
Steinauer, M. L., Blouin, M. S. and Criscione, C. D. (2010). Applying evolutionary genetics to schistosome epidemiology. Infection Genetics and Evolution 10, 433443.CrossRefGoogle ScholarPubMed
Steinauer, M. L., Hanelt, B., Agola, L. E., Mkoji, G. M. and Loker, E. S. (2009). Genetic structure of Schstosoma mansoni in western Kenya: The effects of geography and host sharing. International Journal for Parasitology 39, 13531362.CrossRefGoogle ScholarPubMed
Steinauer, M. L., Hanelt, B., Mwangi, I. N., Maina, G. M., Agola, L. E., Kinuthia, J. M., Mutuku, M. W., Mungai, B. N., Wilson, W. D., Mkoji, G. M. and Loker, E. S. (2008). Introgressive hybridization of human and rodent schistosome parasites in western Kenya. Molecular Ecology 17, 50625074.CrossRefGoogle ScholarPubMed
Thiele, E. A., Sorensen, R. E., Gazzinelli, A. and Minchella, D. J. (2008). Genetic diversity and population structuring of Schistosoma mansoni in a Brazilian village. International Journal for Parasitology 38, 389399.CrossRefGoogle Scholar
Vilas, R. and Paniagua, E. (2004). Estimation of the prevalence of outcrossing in the hermaphrodite trematode Lecithochirium rufoviride by allozyme analysis. Acta Parasitologica 49, 1215.Google Scholar
Vilas, R., Paniagua, E. and Sanmartin, M. L. (2003). Genetic variation within and among infrapopulations of the marine digenetic trematode Lecithochirium fusiforme. Parasitology 126, 465472.CrossRefGoogle ScholarPubMed
Vilas, R., Vázquez-Prieto, S. and Paniagua, E. (2012). Contrasting patterns of population genetic structure of Fasciola hepatica from cattle and sheep: Implications for the evolution of anthelmintic resistance. Infection Genetics and Evolution 12, 4552.CrossRefGoogle ScholarPubMed
Whiteman, N. K., Kimball, R. T. and Parker, P. G. (2007). Co-phylogeography and comparative population genetics of the threatened Galapagos hawk and three ectoparasite species: ecology shapes population histories within parasite communities. Molecular Ecology 16, 47594773.CrossRefGoogle ScholarPubMed
Whitfield, P. J. and Evans, N. A. (1983). Parthenogenesis and asexual multiplication among parasitic platyhelminths. Parasitology 86, 121160.CrossRefGoogle ScholarPubMed
Whitlock, M. C. and McCauley, D. E. (1999). Indirect measures of gene flow and migration: F ST ≠ 1/(4Nm+1). Heredity 82, 117125.CrossRefGoogle Scholar
Wielgoss, S., Hollandt, F., Wirth, T. and Meyer, A. (2010). Genetic signatures in an invasive parasite of Anguilla anguilla correlate with differential stock management. Journal of Fish Biology 77, 191210.CrossRefGoogle Scholar
Wielgoss, S., Taraschewski, H., Meyer, A. and Wirth, T. (2008). Population structure of the parasitic nematode Anguillicola crassus, an invader of declining North Atlantic eel stocks. Molecular Ecology 17, 34783495.CrossRefGoogle ScholarPubMed
Woolhouse, M. E. J., Dye, C., Etard, J. F., Smith, T., Charlwood, J. D., Garnett, G. P., Hagan, P., Hii, J. L. K., Ndhlovu, P. D., Quinnell, R. J., Watts, C. H., Chandiwana, S. K. and Anderson, R. M. (1997). Heterogeneities in the transmission of infectious agents: Implications for the design of control programs. Proceedings of the National Academy of Sciences, USA 94, 338342.CrossRefGoogle ScholarPubMed
Woolhouse, M. E. J., Etard, J. F., Dietz, K., Ndhlovu, P. D. and Chandiwana, S. K. (1998). Heterogeneities in schistosome transmission dynamics and control. Parasitology 117, 475482.CrossRefGoogle ScholarPubMed
Wright, S. (1969). Evolution and the Genetics of Populations. II. The Theory of Gene Frequencies. University of Chicago Press, Chicago, USA.Google Scholar