Reduction in post-invasion genetic diversity in Crangonyx pseudogracilis (Amphipoda: Crustacea): a genetic bottleneck or the work of hitchhiking vertically transmitted microparasites?
- 315 Downloads
Parasites can strongly influence the success of biological invasions. However, as invading hosts and parasites may be derived from a small subset of genotypes in the native range, it is important to examine the distribution and invasion of parasites in the context of host population genetics. We demonstrate that invasive European populations of the North American Crangonyx pseudogracilis have experienced a reduction in post-invasion genetic diversity. We predict that vertically transmitted parasites may evade the stochastic processes and selective pressures leading to enemy release. As microsporidia may be vertically or horizontally transmitted, we compared the diversity of these microparasites in the native and invasive ranges of the host. In contrast to the reduction in host genetic diversity, we find no evidence for enemy release from microsporidian parasites in the invasive populations. Indeed, a single, vertically transmitted, microsporidian sex ratio distorter dominates the microsporidian parasite assemblage in the invasive range and appears to have invaded with the host. We propose that overproduction of female offspring as a result of parasitic sex ratio distortion may facilitate host invasion success. We also propose that a selective sweep resulting from the increase in infected individuals during the establishment may have contributed to the reduction in genetic diversity in invasive Crangonyx pseudogracilis populations.
KeywordsBiological invasions Enemy release Emergent disease Microsporidia Sex ratio distortion Vertical transmission
This research was carried out at The University of Leeds. JSG was supported by an ORS award and a University of Leeds John Henry Garner scholarship. Samples were collected with the assistance of an Ann Bishop Travel Award from the British Society for Parasitology. JS and AD acknowledge support from the Natural Environment Research Council and the Biotechnology and Biological Sciences Research Council (NE/DO12937/1). We thank Beth McClymont, Genie White, Lucas Terracina, Joan Jass, William Brooks and Alex Douglas for technical support and two anonymous referees for helpful suggestions.
- Bauer A, Haine ER, Perrot-Minnot MJ, Rigaud T (2005) The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipod hosts: the native Gammarus pulex and the invasive Gammarus roeseli. J Zool 267:39–43. doi: 10.1017/S0952836905007223 CrossRefGoogle Scholar
- Englisch U, Coleman CO, Wagele JW (2003) First observations on the phylogeny of the families Gammaridae, Crangonyctidae, Melitidae, Niphargidae, Megaluropidae and Oedicerotidae (Amphipoda, Crustacea), using small subunit rDNA gene sequences. J Nat Hist 37:2461–2486. doi: 10.1080/00222930210144352 CrossRefGoogle Scholar
- Haine ER, Brondani E, Hume KD, Perrot-Minnot M-J, Gaillard M, Rigaud T (2004) Coexistence of three microsporidia parasites in populations of the freshwater amphipod Gammarus roeseli: evidence for vertical transmission and positive effects on reproduction. Int J Parasitol 34:1137–1146. doi: 10.1016/j.ijpara.2004.06.006 CrossRefPubMedGoogle Scholar
- Hall TA (2001) Bioedit: biological sequence alignment editor for Windows 95/98/NT edition 5.0.9Google Scholar
- Harris PM, Roosa BR, Norment L (2002) Underground dispersal by amphipods (Crangonyx pseudogracilis) between temporary ponds. J Freshwat Ecol 17:589–594Google Scholar
- Holmes JMC (1975) Crangonyx pseudogracilis Bousfield a freshwater amphipod new to Ireland. Ir Nat J 18:25Google Scholar
- Hynes HBN (1955) The reproductive cycle of some British freshwater Gammaridae. J Ecol 21:352–387Google Scholar
- Jass J, Klausmeier B (2003) Utilization of lotic, lentic and temporary habitats by the amphipod Crangonyx gracilis. J Freshwat Ecol 18:635–638Google Scholar
- Krisp H, Maier G (2005) Consumption of macroinvertberates by invasive and native gammarids: a comparison. J Limnol 64:55–59Google Scholar
- Maitland P, Adams C (2001) Introduced freshwater invertebrates in Scotland: enhanced biodiversity or a threat to native species? In Conference: alien species: friends or foes? Glasgow. Glasg Nat Hist SocGoogle Scholar
- NDC Publications and US Waterway Data CD, vol 10 (2004) Alexandria, US Army Corps of EngineersGoogle Scholar
- Pinkster S, Dieleman J, Platvoet D (1980) The present position of Gammarus tigrinus Sexton, 1930, in the Netherlands, with the description of a newly discovered amphipod species, Crangonyx pseudogracilis Bousfield, 1958 (Crustacea, Amphipoda). Bull Zool Mus Univ Amst 7:33–45Google Scholar
- Slothouber Galbreath JGM, Smith JE, Terry RS, Becnel JJ, Dunn AM (2004) Invasion success of Fibrillanosema crangonycis, n. sp., n.g., a novel vertically transmitted microsporidian parasite from the invasive amphipod host Crangonyx pseudogracilis. Int J Parasitol 34:235–244. doi: 10.1016/j.ijpara.2003.10.009 CrossRefPubMedGoogle Scholar
- Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), v 4.0b10. Sinauer, SunderlandGoogle Scholar
- Terry RS, MacNeil C, Dick JTA, Smith JE, Dunn AM (2003) Resolution of a Taxonomic conundrum: an Ultrastructural and Molecular Description of the Life Cycle of Pleistophora mulleri (Pfeiffer 1895; Georgevitch 1929). J Eukaryot Microbiol 50:266–273. doi: 10.1111/j.1550-7408.2003.tb00133.x CrossRefPubMedGoogle Scholar
- Vossbrinck CR, Baker MD, Didier ES, Debrunner-Vossbrinck BA, Shadduck JA (1993) Ribosomal DNA sequences of Encephalitozoon hellem and Encephalitozoon cuniculi: species identification and phylogenetic construction. J Eukaryot Microbiol 40:354–362. doi: 10.1111/j.1550-7408.1993.tb04928.x CrossRefPubMedGoogle Scholar
- Weiss LM, Zhu X, Cali A, Tanowitz HB, Wittner M (1994) Utility of microsporidian rRNA in diagnosis and phylogeny: a review. Folia Parasitol (Praha) 41:81–90Google Scholar
- Wittner M (1999) Historic perspective on the microsporidia: expanding horizons. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. Washington, ASM Press, pp 1–6Google Scholar
- Zhang J, Holsinger JR (2003) Systematics of the freshwater amphipod genus Crangonyx (Crangonyctidae) in North America. Memoir number 6. Virginia Museum of Natural History, MartinsvilleGoogle Scholar