Biol Invasions (2010) 12:191–209 DOI 10.1007/s10530-009-9442-3 ORIGINAL PAPER Reduction in post-invasion genetic diversity in Crangonyx pseudogracilis (Amphipoda: Crustacea): a genetic bottleneck or the work of hitchhiking vertically transmitted microparasites? Johanna G. M. Slothouber Galbreath Æ Judith E. Smith Æ James J. Becnel Æ Roger K. Butlin Æ Alison M. Dunn Received: 14 July 2008 / Accepted: 22 January 2009 / Published online: 7 February 2009 Ó Springer Science+Business Media B.V. 2009 Abstract Parasites can strongly influence the suc- parasites may evade the stochastic processes and cess of biological invasions. However, as invading selective pressures leading to enemy release. As hosts and parasites may be derived from a small microsporidia may be vertically or horizontally subset of genotypes in the native range, it is important transmitted, we compared the diversity of these to examine the distribution and invasion of parasites microparasites in the native and invasive ranges of in the context of host population genetics. We the host. In contrast to the reduction in host genetic demonstrate that invasive European populations of diversity, we find no evidence for enemy release from the North American Crangonyx pseudogracilis have microsporidian parasites in the invasive populations. experienced a reduction in post-invasion genetic Indeed, a single, vertically transmitted, microsporid- diversity. We predict that vertically transmitted ian sex ratio distorter dominates the microsporidian parasite assemblage in the invasive range and appears to have invaded with the host. We propose that Electronic supplementary material The online version of overproduction of female offspring as a result of this article (doi:10.1007/s10530-009-9442-3) contains supplementary material, which is available to authorized users. parasitic sex ratio distortion may facilitate host invasion success. We also propose that a selective J. G. M. Slothouber Galbreath Á J. E. Smith Á sweep resulting from the increase in infected individ- & A. M. Dunn ( ) uals during the establishment may have contributed to Faculty of Biological Sciences, Institute of Integrative and Comparative Biology, University of Leeds, the reduction in genetic diversity in invasive Crang- Leeds LS2 9JT, UK onyx pseudogracilis populations. e-mail: [email protected] Keywords Biological invasions Á J. G. M. Slothouber Galbreath Institute of Biological and Environmental Sciences, Enemy release Á Emergent disease Á University of Aberdeen, Zoology Building, Microsporidia Á Sex ratio distortion Á Aberdeen AB24 2TZ, UK Vertical transmission J. J. Becnel USDA/ARS, Center for Medical, Agricultural and Veterinary Entomology, P.O. Box 14565, Introduction Gainesville, FL 32604, USA Two important factors affecting the success of an R. K. Butlin Department of Animal and Plant Sciences, University invasion and its impact on the native biota are the of Sheffield, Western Bank, Sheffield S10 2TN, UK changes in genetic diversity as a result of the invasion 123 192 J. G. M. Slothouber Galbreath et al. (Miura 2007) and the impact of parasitism (Hatcher ranges (Mitchell and Power 2003; Torchin et al. et al. 2006). Invasion success is dependent on the size 2003) as well as individual empirical studies demon- and origin of introduced populations and on the strating a reduction in parasitism in invasive range frequency of introductions (Kolar and Lodge 2001; compared with the native range. This reduced impact Suarez et al. 2005) and invasion filters are predicted on host fitness may be realized as a reduction in to cause a reduction in post-invasion genetic diversity parasite diversity (Marr et al. 2007) or a reduction in with genetic bottlenecks historically considered a parasite prevalence and intensity in the invasive host general characteristic of invasion events (Cristescu (Torchin et al. 2001). However, invading hosts and et al. 2004; Muller et al. 2002). For example, the parasites are often derived from a small subset of a Ponto-Caspian freshwater amphipod Echinogamma- generally much larger pool of candidate genotypes in rus ischnus has experienced a severe reduction in the native range (Colautti et al. 2004). Hence, tests post-invasion genetic diversity throughout its Euro- for enemy release that do not restrict comparison pean and North American invaded range (Cristescu between the invasive population and the source et al. 2004). However, several recent studies find no population from which it was founded may lead to reduction in genetic diversity (e.g. Astenei et al. exaggerated estimates of enemy release (Colautti 2005; Wattier et al. 2007) or even an increase in et al. 2004). diversity. A study of invasive populations of the North American amphipod Gammarus tigrinus Study system revealed decreased genetic diversity in some invasive European populations, whilst others had increased Amphipod Crustacea are successful invaders globally genetic diversity reflecting multiple sources of intro- (Cristescu et al. 2004; Dick and Platvoet 2000; duction (Kelly et al. 2006). Hence it is important to Jazdzewski et al. 2004; Devin and Beisel 2008) and consider the effect of the source and the history of an many species are successful intercontinental invaders invasion on genetic diversity. (Colautti et al. 2005; Holeck et al. 2004; Bij de Vaate Parasites have been shown to be important in et al. 2002). Amphipod invasions have led to determining the success and impact of biological dramatic changes in community structure (Krisp invasions. Parasites may directly influence the suc- and Maier 2005; Van Riel et al. 2006) including cess of the invading host (Prenter et al. 2004) as well extinction of native species, reduced species diversity as mediate the outcome of interactions between and richness (Dick and Platvoet 2000), and changes native and invasive species during invasion events in fish productivity (Kelly and Dick 2005). Some (MacNeil et al. 2003a, b; Prenter et al. 2004). invasive amphipods, including Echinogammarus is- Invasive species may introduce novel pathogens to chnus (Cristescu et al. 2004), have experienced a naı¨ve hosts (Daszak et al. 2000; Lips et al. 2006; sharp decline in post-invasion genetic diversity. For Tompkins et al. 2003), they may themselves acquire others, the invasion process appears to have had little new parasites from the invasive range (Krakau et al. discernable effect on post-invasion genetic diversity. 2006), or they may benefit from the loss of parasites One example is the freshwater amphipod Dikero- (Enemy release) during an invasion event (Mitchell gammarus villosus which has successfully invaded and Power 2003; Torchin et al. 2003). Release from the major river systems of Western Europe from a natural enemies has been proposed as a major factor Ponto-Caspian origin without any discernable loss of in the success of biological invasions. Subsampling, genetic diversity or loss of microparasites (Wattier stochastic factors, and selective pressures (Drake et al. 2007). There have also been several instances of 2003; Mitchell and Power 2003; Prenter et al. 2004) cryptic invasions by amphipod crustaceans which during the invasion event may all contribute to the were only detected through the use of molecular loss of hosts with parasite-impaired fitness and markers (Muller 2001; Muller et al. 2002). consequently of parasites and susceptible host geno- Amphipods are host to a diverse range of parasites types (Mitchell and Power 2003; Torchin et al. 2003). (Dunn and Dick 1998) several of which play a role in Support for the enemy release hypothesis has native invader interactions (MacNeil et al. 2003a, b; come from both meta-analysis of the natural enemies Rigaud and Moret 2003; Bauer et al. 2005). For of non-indigenous species in their native and invasive example, the microsporidian Pleistophora mulleri 123 Reduction in post-invasion genetic diversity in Crangonyx pseudogracilis (Amphipoda: Crustacea) 193 reduces the predatory impact of the native G. duebeni Furthermore, there has been relatively little charac- on two invasive amphipods, thereby facilitating the terisation of the invasion history of C. pseudogracilis invasion process (MacNeil et al. 2003a, b; MacNeil compared to other gammarid amphipods invasive in et al. 2004). Acanthocephalan infections do not Europe. This amphipod is found mainly in ponds, manipulate the behaviour of the invasive amphipod lakes and slow moving streams (Holland 1976; Zhang Gammarus roeseli (Bauer et al. 2005; Tain et al. and Holsinger 2003; Josens et al. 2005) and is 1 of 42 2006), but do alter the phototactic response of the species of Crangonyx described from North America native amphipod G. pulex in France, making it (Zhang and Holsinger 2003). It is a primarily fresh- vulnerable to predation by the definitive fish host water species that will tolerate some salinity (Chlo- (Cezilly et al. 2000), and so may facilitate invasion. ride: 250–350 mg/l) but does not become established Furthermore, when the invasive D. villosus is present in organically polluted sites or sites experiencing in the system, the resulting manipulation of host fluvatile conditions (Holland 1976). Crangonyx has behaviour by the acanthocephalan Polymorhpus often been found in seemingly isolated sites and this minutus is stronger to ensure predation by the appro- has been attributed to introduction by anglers (acci- priate ultimate host rather than this predatory amphi- dental or deliberate; Holland 1976) and movement pod (Medoc et al. 2006). between sites by means of damp