Advertisement

Parasitology Research

, Volume 118, Issue 2, pp 667–672 | Cite as

Comparative mtDNA phylogeographic patterns reveal marked differences in population genetic structure between generalist and specialist ectoparasites of the African penguin (Spheniscus demersus)

  • C. Wessels
  • S. Matthee
  • M. P. A. Espinaze
  • C. A. MattheeEmail author
Genetics, Evolution, and Phylogeny - Short Communication

Abstract

To address factors affecting genetic diversity and dispersal of ectoparasites, we compared mitochondrial DNA (mtDNA) population genetic structures of the generalist soft tick Ornithodoros capensis to the more host-specific nest flea Parapsyllus humboldti. A total of 103 ticks and 92 fleas were sampled at five distinct South African island/mainland African penguin (Spheniscus demersus) colonies. With its wide host range, O. capensis showed no evidence of significant cytochrome c oxidase subunit I (COI) mtDNA population differentiation among the five sampling sites (φst = 0.00 ± 0.004; p = 0.80), as well as a higher level of genetic diversity (π = 0.8% ± 0.06%) when compared to P. humboldti. In contrast, the flea showed significant population structure among most of the same sampling sites (φst = 0.22 ± 0.11; p ≤ 0.05) and a lower level of genetic diversity (π = 0.2% ± 0.01%). Our findings suggest that despite both parasites being mostly nest bound, O. capensis have few barriers to dispersal among island and mainland colonies. However, P. humboldti are more dependent on the African penguin for dispersal and thus have more impediments to gene flow among the same colonies. These findings broadly support the SGVH (specialist generalist variation hypothesis) and provide the first evidence for this hypothesis in parasites restricted to seabird colonies.

Keywords

Ornithodoros capensis Parapsyllus humboldti South Africa Specialist generalist variation hypothesis Population structure Ectoparasite 

Notes

Acknowledgements

We thank the managers and fieldworkers at CapeNature, South African National Parks and the Southern African Foundation for the Conservation of Coastal Birds (SANCCOB) for assisting with the specimen collection. MPAE was awarded a scholarship from the Chilean National Scholarship Program for Graduate Studies (Becas-Chile) of the National Commission for Scientific and Technological Research (CONICYT).

Funding information

This work was supported by the International Penguin and Marine Mammal Foundation, the National Research Foundation and Stellenbosch University.

Compliance with ethical standards

Ethical approval was obtained from Stellenbosch University Animal Ethics Committee (SU-ACUD15-00114) who followed the South African National Standard (SANS) for the Care and Use of Animals for Scientific Purposes (SANS 10386:2008).

Conflict of interest

The authors declare that there is no conflict of interest.

References

  1. Araya-Anchetta A, Busch JD, Scoles GA, Wagner DM (2015) Thirty years of tick population genetics: a comprehensive review. Infect Genet Evol 29:164–179CrossRefGoogle Scholar
  2. Berkman LK, Nielsen CK, Charlotte LR, Heist EJ (2015) Comparative genetic structure of sympatric Leporids in southern Illinois. J Mammal 96:552–563CrossRefGoogle Scholar
  3. Bitam I, Dittmar K, Parola P, Whiting MF, Raoult D (2010) Fleas and flea-borne diseases. Int J Infect Dis 14:667–676CrossRefGoogle Scholar
  4. Boyd EM (1951) The external parasites of birds: a review. Wilson Bull 63:363–369Google Scholar
  5. Clement M, Posada DCKA, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefGoogle Scholar
  6. Crawford RJM, Williams AJ, Hofmeyer JH, Klages NTW, Randall RM, Cooper J, Dyer BMCY (1995) Trends of African penguin Spheniscus demersus populations in the 20th century. S Afr J Mar Sci 16:101–118CrossRefGoogle Scholar
  7. Duffy DC (1983) The ecology of tick parasitism on densely nesting Peruvian seabirds. Ecology 64:110–119CrossRefGoogle Scholar
  8. Duffy DC (1988) Ticks among the seabirds. Living Bird Q 7:8–13Google Scholar
  9. Dupraz M, Toty C, Noël V, Estrada-Peňa A, González-Solís J, Boulinier T, Dujardin J, McCoy K (2016) Linking morphometric and genetic divergence with host use in the tick complex, Ornithodoros capensis sensu lato. Infect Genet Evol 46:12–22CrossRefGoogle Scholar
  10. Engelbrecht A, Matthee S, Matthee CA (2016) Limited dispersal in an ectoparasitic mite, Laelaps giganteus, contributes to significant phylogeographic congruence with the rodent host, Rhabdomys. Mol Ecol 25:1006–1021CrossRefGoogle Scholar
  11. Excoffier L, Lischer HEL (2010) Arlequin Suite Ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefGoogle Scholar
  12. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
  13. Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788CrossRefGoogle Scholar
  14. Gómez-Díaz E, Morris-Pocock JA, González-Solís J, McCoy KD (2012) Trans-oceanic host dispersal explains high seabird tick diversity on Cape Verde islands. Biol Lett 8:616–619CrossRefGoogle Scholar
  15. Hoogstraal H, Wassef HY, Hays C, Keirans JE (1985) Ornithodoros (Alectorobius) spheniscus n. sp. [Acarina: Ixodoidea: Argasidae: Ornithodoros (Alectorobius) capensis group], a tick parasite of the Humboldt penguin in Peru. J Parasitol 71:635–644CrossRefGoogle Scholar
  16. Janecka JE, Tewes ME, Davis IA, Haines AM, Caso A, Blankenship TL, Honeycutt RL (2016) Genetic differences in the response to landscape fragmentation by a habitat generalist, the bobcat, and a habitat specialist, the ocelot. Conserv Genet 17:1093–1108CrossRefGoogle Scholar
  17. Jordan K (1942) On Parapsyllus and some closely related genera of Siphonaptera. Eos 18:7–29Google Scholar
  18. Jurik M (1974) Bionomics of fleas in bird’s nests in the territory of Czechoslovakia. Acta Sc Nat Brno 8:1–54Google Scholar
  19. Leigh JW, Bryant D (2015) PopART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116CrossRefGoogle Scholar
  20. Li S, Jovelin R, Yoshiga T, Tanaka R, Cutter AD (2014) Specialist versus generalist life histories and nucleotide diversity in Caenorhabditis nematodes. Proc R Soc Lond B 281:2013–2858Google Scholar
  21. MacLeod CJ, Paterson AM, Tompkins D, Duncan RP (2010) Parasites lost – do invaders miss the boat or drown on arrival? Ecol Lett 13:516–527CrossRefGoogle Scholar
  22. Marshall AG (1981) The ecology of ectoparasitic insects. Academic, London; New YorkGoogle Scholar
  23. Martinossi-Allibert I, Clavel J, Ducatez S, Le Viol I, Teplitsky C (2017) Does habitat specialization shape the evolutionary potential of wild bird populations? J Avian Biol 48:1158–1165CrossRefGoogle Scholar
  24. Matthee CA, Engelbrecht A, Matthee S (2018) Comparative phylogeography of parasitic Laelaps mites contribute new insights into the specialist-generalist variation hypothesis (SGVH). BMC Evol Biol 18:131CrossRefGoogle Scholar
  25. McCoy KD, Boulinier T, Tirard C (2005) Comparative host-parasite population structures: disentangling prospecting and dispersal in the black-legged kittiwake Rissa tridactyla. Mol Ecol 14:2825–2838CrossRefGoogle Scholar
  26. Moon KL, Banks SC, Fraser CI (2015) Phylogeographic structure in penguin ticks across an ocean basin indicates allopatric divergence and rare trans-oceanic dispersal. PLoS One 10:e0128514CrossRefGoogle Scholar
  27. Muñoz-Leal S, Dias RA, Abrahão CR, Labruna MB (2017) The Ornithodoros capensis group (Acari: Argasidae): a morphological diagnosis and molecular characterization of O. capensis sensu stricto from Queimada Grande Island, Brazil. Syst Appl Acarol 22:28–41CrossRefGoogle Scholar
  28. Murray MD, Vestjens WJM (1967) Studies on the ectoparasites of seals and penguins III. The distribution of the tick Ixodes uriae White and the flea Parapsyllus magellanicus heardi de Meillon on Macquarie Island. Aust J Zool 15:715–725CrossRefGoogle Scholar
  29. Segerman J (1995) Siphonaptera of southern Africa. Handbook for the identification of fleas. Publications of the South African Institute for Medical Research, No. 57, JohannesburgGoogle Scholar
  30. Smith KM, Karesh WB, Majluf P, Paredes R, Zavalaga C, Hoogesteijn Reul A, Stetter M, Braselton WE, Puche H, Cook RA (2008) Health evaluation of free-ranging Humboldt penguins (Spheniscus humboldti) in Peru. Avian Dis 52:130–135CrossRefGoogle Scholar
  31. Sonenshine DE (1991) Life cycles of ticks. In: Sonenshine DE (ed) Biology of ticks. Oxford University Press, New York, pp 51–66Google Scholar
  32. Sonenshine DE (1993) Ecology of nidicolous ticks. In: Sonenshine DE (ed) Biology of ticks. Oxford University Press, New York, pp 66–91Google Scholar
  33. Sutherst RW (1971) An experimental investigation into the effects of flooding on the ixodid tick Boophilus microplus (Canestrini). Oecologia 6:208–222CrossRefGoogle Scholar
  34. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  35. 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 Evol Biol 15:105CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Evolutionary Genomics Group, Department of Botany and Zoology, Faculty of ScienceStellenbosch UniversityStellenboschSouth Africa
  2. 2.Department of Conservation Ecology and Entomology, Faculty of AgriScienceStellenbosch UniversityStellenboschSouth Africa

Personalised recommendations