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Parasite Assemblages Distinguish Populations of a Migratory Passerine on Its Breeding Grounds K Journal of Zoology. Print ISSN 0952-8369 Parasite assemblages distinguish populations of a migratory passerine on its breeding grounds K. L. Durrant1, P. P. Marra2, S. M. Fallon1, G. J. Colbeck3, H. L. Gibbs4, K. A. Hobson5, D. R. Norris6, B. Bernik1, V. L. Lloyd1 & R. C. Fleischer1 1 Genetics Program, Smithsonian Institution, NW, Washington, DC, USA 2 Smithsonian Migratory Bird Center, National Zoological Park, NW, Washington, DC, USA 3 School of Biological Sciences, Washington State University, Pullman, WA, USA 4 Department of Evolution, Ecology and Organismal Biology, The Ohio State University, Aronoff Laboratory, Columbus, OH, USA 5 Environment Canada, Saskatoon, SK, Canada 6 Department of Integrative Biology, University of Guelph, Guelph, ON, Canada Keywords Abstract Setophaga ruticilla; migration; Plasmodium; Haemoproteus; avian malaria; blood parasite. We attempted to establish migratory connectivity patterns for American redstarts Setophaga ruticilla between their breeding and wintering grounds by characteriz- Correspondence ing the composition of their haematozoan parasite assemblages in different parts Kate L. Durrant. Current address: of their range. We detected significant but limited geographic structuring of Department of Animal and Plant Sciences, haematozoan parasite lineages across the breeding range of the redstart. We found The University of Sheffield, Sheffield S10 that redstarts from the south-eastern (SE) region of the breeding range had a 2TN, UK. significantly different haematozoan parasite assemblage compared with popula- Email: k.l.durrant@sheffield.ac.uk tions sampled throughout the rest of the breeding range. Evidence using stable isotopes from feathers previously demonstrated that redstarts from the SE of the Received 19 July 2007; accepted breeding range also have a unique and separate wintering range. Thus, although 26 September 2007 two methods of estimating migratory connectivity have now both shown the SE US breeding sub-population of redstarts to be distinct from other populations on doi:10.1111/j.1469-7998.2007.00387.x both the breeding and wintering grounds, conclusive migratory connectivity for this species as a whole could not be established. Introduction 1997; Marra et al., 1998; Hobson, 2005; Norris et al., 2006a). However, both Hobson (2005) and Norris, Wunder Despite intense interest, we still lack understanding of how & Boulet (2006b) noted several potential sources of error populations of many migratory species are geographically with isotopic data, for example, variability in stable hydro- structured throughout the year (Webster et al., 2002; Norris gen isotope compositions, and recommended confirmation et al., 2006b). Conditions on the wintering grounds are of results by incorporating data from other tracking meth- known to influence individuals and populations in subse- ods such as satellite telemetry, or genetic data (e.g. Dockx quent breeding seasons, and birds may face differing selec- et al., 2004; Dunn et al., 2006). tive pressures in their breeding and non-breeding ranges Endo-parasites offer another potential tool for measuring (Marra, Hobson & Holmes, 1998; Studds & Marra, 2005; migratory connectivity, either through phylogeographic Webster & Marra, 2005). Therefore, for a complete under- variation of individual parasite species or through geo- standing of migratory animal ecology, evolution and con- graphic variation in the assemblage of parasite species in a servation, it is essential that all phases of the migrant’s life, particular host. Because the generation times of many including breeding, migratory and wintering periods, are parasites are short relative to those of their hosts, variation linked. in genetic markers of parasites could become localized with- Determining wintering locations and migratory con- in host populations (Ricklefs & Fallon, 2002). Parasite nectivity has proven to be a challenge when dealing with lineages might also become localized with respect to the small-bodied passerines. Traditional techniques such as distribution of their vectors, and so have the potential to mark–recapture have a low success rate, and some newer reveal fine-scale geographical information about hosts technologies like satellite transmitters are not suited to (Webster et al., 2002; but see Ricklefs et al., 2005a). When small-bodied animals (reviewed in Webster et al., 2002; parasites are localized within the breeding range and are also Hobson, 2003). One useful technique for determining mi- present in the wintering population, or vice versa, it is gratory connectivity is examining patterns of stable isotopic possible to connect breeding and wintering populations and signatures in tissues or feathers (Hobson & Wassenaar, therefore establish migratory connectivity using parasite 318 Journal of Zoology 274 (2008) 318–326 c 2008 The Authors. Journal compilation c 2008 The Zoological Society of London K. L. Durrant et al. Haematozoan assemblages distinguish host populations data alone. This information can also be combined with and the Caribbean (Sherry & Holmes, 1997; Norris et al., other methods of tracking the migratory movements of 2006a). small passerines to improve our understanding of migratory connectivity for these species throughout the year. Parasite sampling and screening DNA sequencing has shown that avian haematozoan parasites are highly diversified and exhibit varying levels of Redstarts were captured using mistnets and playback and host specialization. Although these parasites are distributed sampled for blood. Sampling locations and sample sizes are throughout the world, except for Antarctica (Valkiunas, summarized in Fig. 1. DNA samples were also obtained 2005), some genetically distinguishable lineages tend to be from other researchers to supplement our geographic localized geographically (Ricklefs et al., 2005a; Beadell sampling (combined total n=437 birds). Of 437 redstart et al., 2006; Kimura, Dhondt & Lovette, 2006). Geographi- samples collected between 2001 and 2006, 68 were obtained cally localized populations of hosts could carry disparate on the wintering grounds and the remainder from breeding parasite assemblages. If these parasites could be recognized populations in North America (for locations see Fig. 1a). in individuals throughout the year, one could connect We extracted host and parasite DNA from the lysis-buffer- populations on the tropical wintering grounds and tempe- preserved samples using the manufacturer’s protocols sup- rate breeding grounds (Ricklefs et al., 2005a). plied with Qiagen DNeasy kits. We verified successful DNA Localizing host populations through their parasites has extractions for samples by amplifying avian cytochrome b been attempted in few avian species. Haematozoan parasites (cyt b) DNA using primers cyt b-2RC and cyt b-wow of two Nearctic–Neotropical migratory warblers, the Black- (268 bp, Dumbacher, Pratt & Fleischer, 2003). throated blue warbler Dendroica caerulescens (Fallon, We screened each sample four times using different primer Fleischer & Graves, 2006) and the Common yellowthroat sets designed to amplify the blood parasites Plasmodium Geothlypis trichas (Pagenkopp et al., in press) do not exhibit and Haemoproteus. The use of different primer sets allows geographical structure. Plasmodium lineages have been for detection of multiple genera of haematozoa given se- found to differ between western and eastern US populations quence variation at the priming sites, and also maximizes the of House finches Carpodacus mexicanus (Kimura et al., chances of amplifying all infections. Although our primer 2006); however, these birds are short-distance migrants. sets were sensitive to small quantities of parasite DNA In this study, we investigated the geographical structuring (Beadell & Fleischer, 2005), success can be reduced by large of haematozoan parasites of American redstarts Setophaga quantities of host DNA or DNA degradation. Screening ruticilla (hereafter ‘redstart’) across their breeding range and samples more than once considerably reduced the occurrence in several wintering locations. Redstarts are long-distance of false negatives and ensured that a realistic picture of migrants between their breeding range in eastern North infection prevalence was obtained (Beadell et al., 2004; America and their wintering range in Central America and Beadell & Fleischer, 2005). Short fragments were initially the West Indies. Although banding data have not revealed amplified using each of four primer sets: F2/R2 (132 bp, connections between breeding and wintering populations, mtDNA cyt b); 850F/1024R (167 bp, mtDNA COIII, Bea- geographical structuring has been suggested by stable iso- dell et al., 2004); 213F/372R (160 bp mtDNA cyt b, Beadell tope analysis (Norris et al., 2006a). Given the availability of & Fleischer, 2005) and 343F/496F (154 bp mtDNA rRNA, independent data on migratory connectivity, the redstart is Fallon et al., 2003). PCR typically followed conditions an excellent species in which to test the feasibility of using developed for ‘ancient’ DNA, to increase the probability of geographic structure in parasite populations or assemblages successful amplification of degraded samples or samples with to assess the relationship between breeding and wintering few parasitemia (Fleischer et al., 2000). Multiple positive and areas. Accordingly, we have surveyed the haematozoan negative controls were included in every PCR. Samples that parasite assemblages of redstarts sampled across the breed- produced UV-visible bands after
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