Genetic structure and gene flow of the flea Xenopsylla cheopis in Madagascar and Mayotte

Mireille Harimalala, Sandra Telfer, Hélène Delatte, Phillip C. Watts, Adélaïde Miarinjara, Tojo Rindra Ramihangihajason, Soanandrasana Rahelinirina, Minoarisoa Rajerison, Sébastien Boyer

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Abstract

Background: The flea Xenopsylla cheopis (Siphonaptera: Pulicidae) is a vector of plague. Despite this insect’s medical importance, especially in Madagascar where plague is endemic, little is known about the organization of its natural populations. We undertook population genetic analyses (i) to determine the spatial genetic structure of X. cheopis in Madagascar and (ii) to determine the potential risk of plague introduction in the neighboring island of Mayotte.
Results: We genotyped 205 fleas from 12 sites using nine microsatellite markers. Madagascan populations of X. cheopis differed, with the mean number of alleles per locus per population ranging from 1.78 to 4.44 and with moderate to high levels of genetic differentiation between populations. Three distinct genetic clusters were identified, with different geographical distributions but with some apparent gene flow between both islands and within Malagasy regions. The approximate Bayesian computation (ABC) used to test the predominant direction of flea dispersal implied a recent population introduction from Mayotte to Madagascar, which was estimated to have occurred between 1993 and 2012. The impact of this flea introduction in terms of plague transmission in Madagascar is unclear, but the low level of flea exchange between the two islands seems to keep Mayotte free of plague for now.
Conclusion: This study highlights the occurrence of genetic structure among populations of the flea vector of plague, X. cheopis, in Madagascar and suggests that a flea population from Mayotte has been introduced to Madagascar recently. As plague has not been reported in Mayotte, this introduction is unlikely to present a major concern for plague transmission. Nonetheless, evidence of connectivity among flea populations in the two islands indicates a possibility for dispersal by fleas in the opposite direction and thus a risk of plague introduction to Mayotte.
Original languageEnglish
Article number347
Pages (from-to)1-13
Number of pages13
JournalParasites & Vectors
Volume10
DOIs
Publication statusPublished - 20 Jul 2017

Bibliographical note

Acknowledgements
Thanks to the GIS team of the Institut Pasteur of Madagascar (IPM) for supplying base maps. Also, thanks to the IBIZA platform of the Mixed Research Unit (UMR PVBMT) of CIRAD in La Réunion for hosting genotyping lab works. Many thanks for Christophe Simiand for his help during genotyping lab-works.

Funding
Epidemiological surveys and laboratory works were funded by the Agence Régional de la Santé - Océan Indien (ARS-OI) (n°2/DSP/Etudes et Statistiques/2013) and the Institut Pasteur of Madagascar. Microsatellite primer development was supported by the Wellcome Trust (a part of Research Career Development Fellowship to S. Telfer #081705 and Senior Fellowship to S. Telfer #095171).

Keywords

  • Madagascar
  • Mayotte
  • Xenopsylla cheopis
  • Microsatellites
  • Genetic structure
  • Gene flow
  • Plague

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