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Understanding the dispersal and genetic structure of invasive insects across islands is …

Biology Articles » Biomathematics » Genetic variation in the invasive avian parasite, Philornis downsi (Diptera, Muscidae) on the Galápagos archipelago » Background

- Genetic variation in the invasive avian parasite, Philornis downsi (Diptera, Muscidae) on the Galápagos archipelago

Biological invasions threaten biodiversity and ecosystem function, with pronounced negative effects on islands in particular [1-3]. Genetic studies of invasive species can identify the adaptive potential of invaders to deal with new environmental conditions [4] or help to predict evolutionary responses to management practices (e.g. pesticides, biological control agents) [5]. Population bottlenecks affect many invasive species because they frequently experience founding effects that reduce genetic variability, but paradoxically, invasive species still manage to successfully establish and adapt to new environments [6]. However, the effects of bottlenecks may be countered by the occurrence of multiple introductions, high reproductive rates, and subsequent migration between locally bottlenecked populations that are genetically differentiated [7].

For invasive arthropod parasites, these factors are inextricably linked with the distribution, genetics, and behaviour of host species [8-10]. The recent integration of molecular ecology with parasitology has provided a path for answering a number of questions concerning the genetic structure of parasite populations, which can uncover a wealth of information regarding ecological and evolutionary processes for invasive parasites [10]. Highly variable multilocus genotypes are particularly suited to analyses of non-equilibrium or bottlenecked populations because they provide adequate variation for assessing recent gene flow and identifying migrants [11].

The introduced fly, Philornis downsi, is an avian ectoparasite that is considered to be a serious threat to the persistence of endemic finch populations on the Galápagos Islands [12-14]. Recently, P. downsi was given the highest risk ranking affecting endemic fauna in the Galápagos archipelago [3]. Other pathogens affecting Galápagos birds such as avian pox virus [15] and intestinal protozoans [16] are of less concern, but may also cause high fitness impacts under certain conditions. The fly was first formally identified from Darwin finch nests in 1997 and has since been found on 11 of 13 major islands in nests of 14 endemic species [12,13]. However, P. downsi colonised the islands at least 40 years ago, as the fly was identified recently from collections made in 1964 [13]. The blood-feeding larvae of P. downsi are associated with 62–100% nestling mortality in Darwin's finches [12,14,17], as well as physiological costs [18] and reduced growth rates in nestlings [14]. Little is known about the ecology and biology of Philornis flies and the dispersal behaviour and population genetics of the genus Philornis or of any other myiasis-causing parasite of birds [reviewed in [13]].

One potential control method to eradicate P. downsi is the sterile insect technique (SIT), which is renowned for its effectiveness at eradicating or suppressing fruit fly and screw-worm fly populations across the globe [19,20]. SIT involves the large-scale release of laboratory-reared sterile male (and/or female) flies that eventually suppress fly populations by reducing population fecundity [reviewed in [20]]. SIT requires a thorough understanding of the reproductive ecology and population dynamics of the target species. The effectiveness of SIT is affected by the occurrence of genetically divergent 'strains' of the target species across the geographic area under control because this is detrimental to the mating success of sterile flies [19,21,22]. Specifically, high genetic divergence may reflect differences in behaviour and/or morphological characteristics that result in mating incompatibility among populations of the target species [21,23]. Thus, target populations that show low genetic divergence are not likely to show reproductive isolation and influence the success of a particular sterile strain.

The Galápagos archipelago offers a unique system to examine the population genetics of an introduced avian parasite that causes severe fitness costs and that is still within a relatively early phase of invasion. We collected parasites in 2004, 2005 and 2006 from three islands of the Galápagos. Using mitochondrial data, we firstly determine whether the three island populations from which we sampled are of the one fly species. We then use microsatellite data to examine gene flow within and among islands to: (1) determine whether dispersal and genetic divergence are occurring among islands and between habitats within islands (wet highlands, arid lowlands), (2) determine the presence of population bottlenecks resulting from the invasion process, and (3) determine whether inter-island genetic differentiation may be of concern to the potential success of an archipelago-wide SIT program for controlling P. downsi.

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