Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T11:57:57.480Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative host–parasite population genetic structures: obligate fly ectoparasites on Galapagos seabirds

Published online by Cambridge University Press:  10 May 2013

IRIS I. LEVIN  and
PATRICIA G. PARKER
IRIS I. LEVIN*
Affiliation:
Department of Biology, University of Missouri – St. Louis, One University Blvd, St. Louis, MO 63121, USA Whitney R. Harris World Ecology Center, University of Missouri – St. Louis, One University Blvd, St. Louis, MO 63121, USA
PATRICIA G. PARKER
Affiliation:
Department of Biology, University of Missouri – St. Louis, One University Blvd, St. Louis, MO 63121, USA Whitney R. Harris World Ecology Center, University of Missouri – St. Louis, One University Blvd, St. Louis, MO 63121, USA WildCare Center, Saint Louis Zoo One Government Dr., St. Louis, MO 63110, USA
*
*Corresponding author: Department of Biology, University of Missouri – St. Louis, R223 Research Building, One University BlvdSt. Louis, MO 63121, USA. E-mail: Iris.Levin@umsl.edu
Get access Rights & Permissions [Opens in a new window]

Summary

Parasites often have shorter generation times and, in some cases, faster mutation rates than their hosts, which can lead to greater population differentiation in the parasite relative to the host. Here we present a population genetic study of two ectoparasitic flies, Olfersia spinifera and Olfersia aenescens compared with their respective bird hosts, great frigatebirds (Fregata minor) and Nazca boobies (Sula granti). Olfersia spinifera is the vector of a haemosporidian parasite, Haemoproteus iwa, which infects frigatebirds throughout their range. Interestingly, there is no genetic differentiation in the haemosporidian parasite across this range despite strong genetic differentiation between Galapagos frigatebirds and their non-Galapagos conspecifics. It is possible that the broad distribution of this one H. iwa lineage could be facilitated by movement of infected O. spinifera. Therefore, we predicted more gene flow in both fly species compared with the bird hosts. Mitochondrial DNA sequence data from three genes per species indicated that despite marked differences in the genetic structure of the bird hosts, gene flow was very high in both fly species. A likely explanation involves non-breeding movements of hosts, including movement of juveniles, and movement by adult birds whose breeding attempt has failed, although we cannot rule out the possibility that closely related host species may be involved.

Keywords

population genetic structurehippoboscidseabirdGalapagos
Type
Research Article
Information
Parasitology , Volume 140 , Issue 9 , August 2013 , pp. 1061 - 1069
Copyright
Copyright © Cambridge University Press 2013 

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

Anton, C., Zeisset, I., Musche, M., Durka, W., Boomsma, J. J. and Settele, J. (2007). Population structure of a large blue butterfly and its specialist parasitoid in a fragmented landscape. Molecular Ecology 16, 3828–3838.CrossRefGoogle Scholar
Baker, J. R. (1967). A review of the role played by the Hippoboscidae (Diptera) as vectors of endoparasites. Journal of Parasitology 53, 412–418.CrossRefGoogle ScholarPubMed
Bishopp, F. C. (1929). The pigeon fly – an important pest of pigeons in the United States. Journal of Economic Entomology 22, 947–987.CrossRefGoogle Scholar
Bohonak, A. J. (2002). IBD (Isolation by Distance): a program for analyses of isolation by distance. Journal of Heredity 93, 153–154.CrossRefGoogle ScholarPubMed
Bruyndonckx, N., Henry, I., Christe, P. and Kerth, G. (2009). Spatio-temporal population genetic structure of the parasitic mite Spinturnix bechsteini is shaped by its own demography and social system of its bat host. Molecular Ecology 18, 3581–3591.CrossRefGoogle ScholarPubMed
Coatney, G. (1931). On the biology of the pigeon fly, Pseudolynchia maura Bigot (Diptera, Hippoboscidae). Parasitology 12, 525–532.CrossRefGoogle Scholar
Davies, C. M., Webster, J. P., Krüger, O., Munatsi, A., Ndamba, J. and Woolhouse, M. E. J. (1999). Host–parasite population genetics: a cross-sectional comparison of Bulinus globosus and Schistosoma haematobium. Parasitology 119, 295–302.CrossRefGoogle ScholarPubMed
Dearborn, D. C., Anders, A. D., Schreiber, E. A., Adams, R. M. M. and Mueller, U. G. (2003). Inter-island movements and population differentiation in a pelagic seabird. Molecular Ecology 12, 2835–2843.CrossRefGoogle Scholar
Delmotte, F., Bucheli, E. and Shykoff, J. A. (1999). Host and parasite population structure in a natural plant–pathogen system. Heredity 82, 300–308.CrossRefGoogle Scholar
Dybdahl, M. F. and Lively, C. M. (1996). The geography of coevolution: comparative population structures for a snail and its trematode parasite. Evolution 50, 2264–2275.CrossRefGoogle ScholarPubMed
Excoffier, L., Smouse, P. E. and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. and Schneider, S. (2005). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1, 47–50.CrossRefGoogle Scholar
Felso, B. and Rozsa, L. (2006). Reduced taxonomic richness of lice (Insecta: Phthiraptera) in diving birds. Journal of Parasitology 92, 867–869.CrossRefGoogle ScholarPubMed
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Friesen, V., Burg, T. and McCoy, K. D. (2007). Mechanisms of population differentiation in seabirds. Molecular Ecology 16, 1765–1785.CrossRefGoogle ScholarPubMed
Gandon, S. and Michalakis, Y. (2002). Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology 15, 452–462.CrossRefGoogle Scholar
Gandon, S., Capoweiz, Y., Dubois, Y., Michalakis, Y. and Olivieri, I. (1996). Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society of London, B 263, 1003–1009.Google Scholar
Gómez-Díaz, E., González-Solís, M., Peinado, M. A. and Page, R. D. M. (2007). Lack of host-dependent genetic structure in ectoparasites of Calonectris shearwaters. Molecular Ecology 16, 5204–5215.CrossRefGoogle ScholarPubMed
Gómez-Díaz, E., Morris-Pocock, J. A., Gonzales-Solis, J. and McCoy, K. D. (2012). Trans-oceanic host dispersal explains high seabird tick diversity on Cape Verde islands. Biology Letters 8, 616–619.CrossRefGoogle ScholarPubMed
Hailer, F., Schreiber, E. A., Miller, J. M., Levin, I. I., Parker, P. G., Chesser, R. T. and Fleischer, R. C. (2011). Long-term isolation of a highly mobile seabird on the Galapagos. Proceedings of the Royal Society of London, B 287, 817–825.Google Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Harbison, C. W. and Clayton, D. G. (2011). Community interactions govern host-switching with implications for host–parasite coevolutionary history. Proceedings of the National Academy of Sciences, USA 108, 9525–9529.CrossRefGoogle ScholarPubMed
Harbison, C. W., Jacobsen, M. V. and Clayton, D. H. (2009). A hitchhiker's guide to parasite transmission: the phoretic behavior of feather lice. International Journal for Parasitology 39, 569–575.CrossRefGoogle ScholarPubMed
Hughes, J. and Page, R. D. M. (2007). Comparative tests of ectoparasite species richness in seabirds. BMC Evolutionary Biology 7, 227.CrossRefGoogle ScholarPubMed
Huyvaert, K. P. and Anderson, D. J. (2004). Limited dispersal by Nazca boobies. Journal of Avian Biology 35, 46–53.CrossRefGoogle Scholar
Johnson, K. P., Williams, B. L., Drown, D. M., Adams, R. J. and Clayton, D. H. (2002). The population genetics of host specificity: genetic differentiation in dove lice (Insecta: Phthiraptera). Molecular Ecology 11, 25–38.CrossRefGoogle ScholarPubMed
Jones, C. (1985). Heavy hippoboscid infestations on buzzards. British Birds 78, 592.Google Scholar
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, 2038–2049.CrossRefGoogle ScholarPubMed
Levin, I. I. and Parker, P. G. (2012). Philopatry drives genetic differentiation in an island archipelago: comparative population genetics of Galapagos Nazca boobies (Sula granti) and great frigatebirds (Fregata minor). Ecology and Evolution 2, 2775–2787.CrossRefGoogle Scholar
Levin, I. I., Valkiunas, G., Santiago-Alarcon, D., Cruz, L. L., Iezhova, T. A., O'Brien, S. L., Dearborn, D., Schreiber, E. A., Fleischer, R. C., Ricklefs, R. E. and Parker, P. G. (2011). Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos Pelecaniform birds: evidence from molecular and morphological studies, with a description of Haemoproteus iwa. International Journal for Parasitology 41, 1019–1027.CrossRefGoogle ScholarPubMed
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.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 Evolution 10, 1271–1277.CrossRefGoogle ScholarPubMed
McCoy, K. D., Boulinier, T., Schjørring, S. and Michalakis, Y. (2002). Local adaptation of the ectoparasite Ixodes uriae to its seabird host. Evolutionary Ecology Research 4, 441–456.Google Scholar
McCoy, K. D., Boulinier, T., Tirard, C. and Michalakis, Y. (2003). Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57, 288–296.Google ScholarPubMed
McCoy, K. D., Boulinier, T. and Tirard, C. (2005). Comparative host–parasite population structures: disentangling prospecting and dispersal in the Black legged kittwake Rissa tridactyla. Molecular Ecology 14, 2825–2838.CrossRefGoogle Scholar
McCoy, K. D., Beis, P., Barbosa, A., Cuervo, J. J., Fraser, W. R., González-Solís, J., Jourdain, E., Poisbleau, M., Quillfeldt, P., Léger, E. and Dietrich, M. (2012). Population genetic structure and colonization of the western Antarctic Peninsula by the seabird tick Ixodes uriae. Marine Ecology Progress Series 459, 109–120.CrossRefGoogle Scholar
Metz, V. G. and Schreiber, E. A. (2002). Great frigatebird (Fregata minor). In The Birds of North America, No. 681 (ed. Poole, A. and Gill, F.). The Academy of Natural Sciences, Philadelphia, PA, USA and The American Ornithologists’ Union, Washington, DC, USA.Google Scholar
Mutikainen, P. and Koskela, T. (2002). Population structure of a parasitic plant and perennial host. Heredity 89, 318–324.CrossRefGoogle ScholarPubMed
Nelson, W. A., Keirans, J. E., Bell, J. F. and Clifford, C. M. (1975). Host–ectoparasite relationships. Journal of Medical Entomology 12, 143–166.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, 276–293.CrossRefGoogle ScholarPubMed
Simon, C., Frati, F., Beckenback, A., Crespl, B., Liu, H. and Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–704.CrossRefGoogle Scholar
Stefka, J., Hoeck, P. E. A., Keller, L. F. and Smith, V. S. (2011). A hitchhikers guide to the Galapagos: co-phylogeography of Galapagos mockingbirds and their parasites. BMC Evolutionary Biology 11, 284.CrossRefGoogle Scholar
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Taylor, S. A., Maclagan, L., Anderson, D. J. and Friesen, V. L. (2011). Could specialization to cold-water upwelling systems influence gene flow and population differentiation in marine organisms? A case study using the blue-footed booby, Sula nebouxii. Journal of Biogeography 38, 883–893.CrossRefGoogle Scholar
Teacher, A. G. F. and Griffiths, D. J. (2011). HapStar: automated haplotype network layout and visualization. Molecular Ecology Resources 11, 151–153.CrossRefGoogle ScholarPubMed
Valle, C. A., Cruz, F., Cruz, J. B., Merlen, G. and Coulter, M. C. (1987). The impact of the 1982–1983 El Niño-Southern Oscillation on seabirds in the Galapagos Islands, Ecuador. Journal of Geophysical Research 92, 437–444.CrossRefGoogle Scholar
Valle, C. A., de Vries, T. and Hernandez, C. (2006). Plumage and sexual maturation in the Great Frigatebird Fregata minor in the Galapagos Islands. Marine Ornithology 34, 51–59.Google Scholar
Weckstein, J. D. (2004). Biogeography explains cophylogenetic patterns in toucan chewing lice. Systematic Biology 53, 154–164.CrossRefGoogle ScholarPubMed
Weimerskirch, H., le Corre, M., Marsac, F., Barbraud, C., Tostain, O. and Chastel, O. (2006). Postbreeding movements of frigatebirds tracked with satellite telemetry. Condor 108, 220–225.CrossRefGoogle Scholar
Whiteman, N. K., Sanchez, P., Merkel, J., Klompen, H. and Parker, P. G. (2006). Cryptic host specificity of an avian skin mite (Epidermoptidae) vectored by louseflies (Hippoboscidae) associated with two endemic Galapagos bird species. Journal of Parasitology 92, 1218–1228.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 22, 4759–4773.CrossRefGoogle Scholar
Wright, S. (1951). The genetical structure of populations. Annals of Eugenics 15, 3233–3354.Google ScholarPubMed