The influence of host dispersal on the gene flow and genetic diversity of generalist and specialist ectoparasites

References

• Araya-Anchetta A, Busch JD, Scoles GA, Wagner DM. 2015. Thirty years of tick population genetics: a comprehensive review. Infection, Genetics and Evolution 29: 164–179. https://doi.org/10.1016/j.meegid.2014.11.008. doi: 10.1016/j.meegid.2014.11.008
   PubMed Web of Science ®Google Scholar
• Appelgren ASC, Saladin V, Richner H, Doligez B, McCoy KD. 2018. Gene flow and adaptive potential in a generalist ectoparasite. BMC Evolutionary Biology 18: 99. https://doi.org/10.1186/s12862-018-1205-2.
   PubMed Web of Science ®Google Scholar
• Barrett LG, Thrall PH, Burdon JJ, Linde CC. 2008. Life history determines genetic structure and evolutionary potential of host–parasite interactions. Trends in Ecology & Evolution 23: 678–685. https://doi.org/10.1016/j.tree.2008.06.017.
   PubMed Web of Science ®Google Scholar
• Blasco-Costa I, Waters JM, Poulin R. 2012. Swimming against the current: genetic structure, host mobility and the drift paradox in trematode parasites. Molecular Ecology 21: 207–217. https://doi.org/10.1111/j.1365-294X.2011.05374.x.
   PubMed Web of Science ®Google Scholar
• Bohonak AT. 1999. Dispersal, Gene Flow, and Population Structure. The Quarterly Review of Biology 74: 21–45. https://doi.org/10.1086/392950.
   PubMed Web of Science ®Google Scholar
• Bothma JC, Matthee S, Matthee CA. (in review). Comparative phylogeography between parasitic sucking lice and their host the Namaqua rock mouse, Micaelamys namaquensis (Rodentia: Muridae). Zoological Journal of the Linnean Society.
   Google Scholar
• Bournez L, Cangi N, Lancelot R, Pradel DR, Stachurski F, Bouyer J, Martinez D, Lefrancois T, Neves L, Pradal J. 2015. Parapatric distribution and sexual competition between two tick species, Amblyomma variegatum and A. hebraeum (Acari, Ixodidae), in Mozambique. Parasites & Vectors 8: 504. https://doi.org/10.1186/s13071-015-1116-7.
   PubMed Web of Science ®Google Scholar
• Cangi N, Horak IG, Apanaskevich DA, Matthee S, das Neves LCB, Estrada-Peña A, Matthee CA. 2013. The influence of interspecific competition and host preference on the phylogeography of two African ixodid tick species. PloS one 8(10): e76930. https://doi.org/10.1371/journal.pone.0076930.
   PubMed Web of Science ®Google Scholar
• Cayuela H, Rougemont Q, Prunier JG, Moore JS, Clobert J, Besnard A, Bernatchez L. 2018. Demographic and genetic approaches to study dispersal in wild animal populations: A methodological review. Molecular Ecology 27: 3976–4010. https://doi.org/10.1111/mec.14848.
   PubMed Web of Science ®Google Scholar
• Charlesworth D. 2003. Effects of inbreeding on the genetic diversity of populations. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 358: 1051–1070. https://doi.org/10.1098/rstb.2003.1296.
   PubMed Web of Science ®Google Scholar
• Clegg SM, Phillimore AB. 2010. The influence of gene flow and drift on genetic and phenotypic divergence in two species of Zosterops in Vanuatu. Philosophical Transactions of the Royal Society B 365: 1077–1092. https://doi.org/10.1098/rstb.2009.0281.
   PubMed Web of Science ®Google Scholar
• DiBlasi E, Johnson KP, Stringham SA, Hansen AH, Beach AB, Clayton DH, Bush SE. 2018. Phoretic dispersal influences parasite population genetic structure. Molecular Ecology 27: 2770–2779. https://doi.org/10.1111/mec.14719.
   PubMed Web of Science ®Google Scholar
• Dick CW, Patterson BD. 2007. Against all odds: Explaining high host specificity in dispersal-prone parasites. International Journal for Parasitology 37: 871–876. https://doi.org/10.1016/j.ijpara.2007.02.004.
   PubMed Web of Science ®Google Scholar
• Duranton M, Bonhomme F, Gagnaire P. 2019. The spatial scale of dispersal revealed by admixture tracts. Evolutionary Applications 12: 1743–1756. https://doi.org/10.1111/eva.12829.
   PubMed Web of Science ®Google Scholar
• Edwards S, Claude J, van Vuuren BJ, Matthee CA. 2011 Evolutionary history of the Karoo bush rat, Myotomys unisulcatus (Rodentia: Muridae): Disconcordance between morphology and genetics Biological Journal of the Linnean Society. Linnean Society of London 102: 510–526. https://doi.org/10.1111/j.1095-8312.2010.01583.x.
   Web of Science ®Google Scholar
• du Toit N, Jansen van Vuuren B, Matthee S, Matthee CA. 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. https://doi.org/10.1016/j.ympev.2012.05.036.
   PubMed Web of Science ®Google Scholar
• du Toit N, Jansen van Vuuren B, Matthee S, Matthee CA. 2013. Biogeography and host-related factors trump parasite life-history: limited congruence among the genetic structures of specific ectoparasitic lice and their rodent hosts. Molecular Ecology 22: 5185–5204. https://doi.org/10.1111/mec.12459.
   PubMed Web of Science ®Google Scholar
• Engelbrecht A, Taylor PJ, Daniels SR, Rambau RV. 2011. Cryptic speciation in the southern African vlei rat Otomys irroratus complex: evidence derived from mitochondrial cyt b and niche modelling. Biological Journal of the Linnean Society. Linnean Society of London 104: 192–206. https://doi.org/10.1111/j.1095-8312.2011.01696.x.
   Web of Science ®Google Scholar
• Engelbrecht, A, Matthee S, du Toit, N, Matthee CA. 2016. Limited dispersal in an ectoparasitic mite, Laelaps giganteus, contributes to significant phylogeographic congruence with the rodent host, Rhabdomys. Molecular Ecology 25: 1006–1021. https://doi.org/10.1111/mec.13523.
   PubMed Web of Science ®Google Scholar
• Excoffier L, Lischer HEL. 2010. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x.
   PubMed Web of Science ®Google Scholar
• Excoffier L, Smouse PE, Quattro JM. 1992. Analysis of Molecular Variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131: 479–491.
   PubMed Web of Science ®Google Scholar
• Harimalala M, Telfer S, Delatte H, Watts PC, Miarinjara A, Ramihangihajason TR, Rahelinirina S, Rajerison M, Boyer S. 2017. Genetic structure and gene flow of the flea Xenopsylla cheopis in Madagascar and Mayotte. Parasites & Vectors 10: 347. https://doi.org/10.1186/s13071-017-2290-6.
   PubMed Web of Science ®Google Scholar
• Huber K, Jacquet S, Rivallan R, Adakal H, Vachiery N, Risterucci AM, Chevillon C. 2019. Low effective population sizes in Amblyomma variegatum, the tropical bont tick. Ticks and Tick-Borne Diseases 10: 93–99. https://doi.org/10.1016/j.ttbdis.2018.08.019.
   PubMed Web of Science ®Google Scholar
• Huyse T, Poulin R, Théron A. 2005. Speciation in parasites: a population genetics approach. Trends in Parasitology 21: 469–475. https://doi.org/10.1016/j.pt.2005.08.009.
   PubMed Web of Science ®Google Scholar
• Li S, Jovelin R, Yoshiga T, Tanaka R, Cutter AD. 2014. Specialist versus generalist life histories and nucleotide diversity in Caenorhabditis nematodes. Proceedings. Biological Sciences 281: 2858.
   Web of Science ®Google Scholar
• Librado P, Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics (Oxford, England) 25: 1451–1452. https://doi.org/10.1093/bioinformatics/btp187.
   Google Scholar
• Lorenzen ED, Heller R, Siegismund HR. 2012. Comparative phylogeography of African savanna ungulates. Molecular Ecology 21: 3656–3670. https://doi.org/10.1111/j.1365-294X.2012.05650.x.
   PubMed Web of Science ®Google Scholar
• Martinů J, Hypša V, Štefka J. 2018. Host specificity driving genetic structure and diversity in ectoparasite populations: Coevolutionary patterns in Apodemus mice and their lice. Ecology and Evolution 8: 10008–10022. https://doi.org/10.1002/ece3.4424.
   PubMed Web of Science ®Google Scholar
• Matthee CA, Engelbrecht A, Matthee S. 2018. Comparative phylogeography of parasitic Laelaps mites contribute new insights into the specialist-generalist variation hypothesis (SGVH). BMC Evolutionary Biology 18: 131. https://doi.org/10.1186/s12862-018-1245-7.
   PubMed Web of Science ®Google Scholar
• Medina I. Cooke GM, Ord TJ. 2018. Walk, swim or fly? Locomotor mode predicts genetic differentiation in vertebrates. Ecology Letters: 638. https://doi.org/10.1111/ele.12930.
   Google Scholar
• Nadler SA. 1995. Microevolution and the genetic structure of parasite populations. The Journal of Parasitology 81: 395–403. https://doi.org/10.2307/3283821.
   PubMed Web of Science ®Google Scholar
• Nei M, Maruyama T, Chakraborty R. 1975. The bottleneck effect and genetic variability in populations. Evolution; International Journal of Organic Evolution 29: 1–10. https://doi.org/10.1111/j.1558-5646.1975.tb00807.x.
   PubMed Web of Science ®Google Scholar
• Nieberding CM, Durette-Desset MC, Vanderpoorten A, Casanova JC, Ribas A, Deffontaine RV, Feliu C, Morand S, Libois R, Michaux JR. 2008. Geography and host biogeography matter for understanding the phylogeography of a parasite. Molecular Phylogenetics and Evolution 47: 538–554. https://doi.org/10.1016/j.ympev.2008.01.028.
   PubMed Web of Science ®Google Scholar
• Russo IRM, Chimimba CT, Bloomer P. 2010. Bioregion heterogeneity correlates with extensive mitochondrial DNA diversity in the Namaqua rock mouse, Micaelamys namaquensis (Rodentia: Muridae) from southern Africa-evidence for a species complex. BMC Evolutionary Biology 10: 307. https://doi.org/10.1186/1471-2148-10-307.
   PubMed Web of Science ®Google Scholar
• Sands AF, Apanaskevich DA, Matthee S, Horak IG, Matthee CA. 2017. The effect of host vicariance and parasite life history on the dispersal of the multi-host ectoparasite, Hyalomma truncatum. Journal of Biogeography 44: 1124–1136. https://doi.org/10.1111/jbi.12948.
   Web of Science ®Google Scholar
• Sands AF, Matthee S, Mfune JKE, Matthee CA. 2015. The influence of life history and climate driven diversification on the mtDNA phylogeographic structures of two southern African Mastomys species (Rodentia: Muridae: Murinae). Biological Journal of the Linnean Society. Linnean Society of London 114: 58–68. https://doi.org/10.1111/bij.12397.
   Web of Science ®Google Scholar
• Slatkin, M. 1985. Gene flow in natural populations. Annual Review of Ecology and Systematics 16: 393–430. https://doi.org/10.1146/annurev.es.16.110185.002141.
   Google Scholar
• Smit HA, Robinson TJ, van Vuuren BJ. 2007. Coalescence methods reveal the impact of vicariance on the spatial genetic structure of Elephantulus edwardii (Afrotheria, Macroscelidea). Molecular Ecology 16: 2680–2692. https://doi.org/10.1111/j.1365-294X.2007.03334.x.
   PubMed Web of Science ®Google Scholar
• Song G, Yu LJ, Gao B, Zhang RY, Qu YH, Lambert DM, Li SH, Zhou TL, Lei FM. 2013. Gene flow maintains genetic diversity and colonization potential in recently range-expanded populations of an Oriental bird, the Light-vented bulbul (Pycnonotus sinensis, Aves: Pycnonotidae). Diversity & Distributions 19: 1248–1262. https://doi.org/10.1111/ddi.12067.
   Web of Science ®Google Scholar
• Steele CD, Court DS, Balding DJ. 2014. Worldwide Fst estimates relative to five continental-scale populations. Annals of Human Genetics 78: 468–477. https://doi.org/10.1111/ahg.12081.
   PubMed Web of Science ®Google Scholar
• Spies I, Hauser L, Jorde PE, Knutsen H, Punt AE, Rogers LA, Stenseth NC. 2018. Inferring genetic connectivity in real populations, exemplified by coastal and oceanic Atlantic cod. Proceedings of the National Academy of Sciences of the United States of America 115: 4945–4950. https://doi.org/10.1073/pnas.1800096115. doi: 10.1073/pnas.1800096115
   PubMed Web of Science ®Google Scholar
• Schneider CJ. 2000. Natural selection and speciation. Proceedings of the National Academy of Sciences of the United States of America 97: 12398–12399. https://doi.org/10.1073/pnas.240463297.
   PubMed Web of Science ®Google Scholar
• Sovic MG, Fries A, Martin SA, Lisle Gibbs H. 2018. Genetic signatures of small effective population sizes and demographic declines in an endangered rattlesnake, Sistrurus catenatus. Evolutionary Applications 12: 664–678. https://doi.org/10.1111/eva.12731.
   Web of Science ®Google Scholar
• Stefan LM, Gómez-Díaz E, Mironov SV, González-Solís J, McCoy KD. 2018. More than meets the eye: Cryptic diversity and contrasting patterns of host-specificity in feather mites inhabiting seabirds. Frontiers in Ecology and Evolution 6: 97. https://doi.org/10.3389/fevo.2018.00097.
   Web of Science ®Google Scholar
• Talbot B, Vonhof MJ, Broders HG, Fenton B, Keyghobadi N. 2017. Comparative analysis of landscape effects on spatial genetic structure of the big brown bat and one of its cimicid ectoparasites. Ecology and Evolution 7: 8210–8219. https://doi.org/10.1002/ece3.3329.
   PubMed Web of Science ®Google Scholar
• van der Mescht L, Matthee S, Matthee CA. 2015. Comparative phylogeography between two generalist flea species reveal a complex interaction between parasite life history and host vicariance: Parasite-host association matters. BMC Evolutionary Biology 15: 105. https://doi.org/10.1186/s12862-015-0389-y.
   PubMed Web of Science ®Google Scholar
• van Schaik J, Kerth G, Bruyndonckx N, Christe P. 2014. The effect of host social system on parasite population genetic structure: comparative population genetics of two ectoparasitic mites and their bat hosts. BMC Evolutionary Biology 14: 18. https://doi.org/10.1186/1471-2148-14-18.
   PubMed Web of Science ®Google Scholar
• Waples RS. 1998. Separating the wheat from the chaff: Patterns of genetic differentiation in high gene flow species. The Journal of Heredity 89: 438–450. https://doi.org/10.1093/jhered/89.5.438.
   Web of Science ®Google Scholar
• Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.
   PubMed Web of Science ®Google Scholar
• Wessels C, Matthee S, Espinaze MPA, Matthee CA. 2019. Comparative mtDNA phylogeographic patterns reveal marked differences in population genetic structure between generalist and specialist ectoparasites of the African penguin. Parasitology Research 118: 667–672. https://doi.org/10.1007/s00436-018-6150-x.
   PubMed Web of Science ®Google Scholar
• Whitlock MC, McCauley DE. 1999. Indirect measures of gene flow and migration: Fst ≠ 1/(4Nm+1). Heredity 82: 117–25. https://doi.org/10.1038/sj.hdy.6884960.
   PubMed Web of Science ®Google Scholar
• Willing EM, Dreyer C, van Oosterhout C. 2012. Estimates of genetic differentiation measured by F(ST) do not necessarily require large sample sizes when using many SNP markers. PLoS ONE 7: e42649. https://doi.org/10.1371/journal.pone.0042649.
   PubMed Web of Science ®Google Scholar
• Willows-Munro S, Matthee CA. 2011. Linking lineage diversification to climate and habitat heterogeneity: Phylogeography of the southern African shrew Myosorex varius. Journal of Biogeography 38: 1976–1991. https://doi.org/10.1111/j.1365-2699.2011.02543.x.
   Web of Science ®Google Scholar
• Wright S. 1949. The genetical structure of populations. Annals of Human Genetics 15: 323–354.
   Google Scholar
• Zhou X, Xie Y, Zhang Z, Wang C, Sun Y, Gu X, Wang S, Peng X, Yang G. 2013. Analysis of the genetic diversity of the nematode parasite Baylisascaris schroederi from wild giant pandas in different mountain ranges in China. Parasites & Vectors 6: 233. https://doi.org/10.1186/1756-3305-6-233.
   PubMed Web of Science ®Google Scholar