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Prevalence, Transmission and Intensity of Infection by a Microsporidian Sex Ratio Distorter in Natural Gammarus Duebeni Populations

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Prevalence, Transmission and Intensity of Infection by a Microsporidian Sex Ratio Distorter in Natural Gammarus Duebeni Populations This is a repository copy of Prevalence, transmission and intensity of infection by a microsporidian sex ratio distorter in natural Gammarus duebeni populations. White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/1007/ Article: Dunn, A.M. and Hatcher, M.J. (1997) Prevalence, transmission and intensity of infection by a microsporidian sex ratio distorter in natural Gammarus duebeni populations. Parasitology, 114 (3). pp. 231-236. ISSN 1469-8161 https://doi.org/10.1017/S0031182096008475 Reuse See Attached Takedown If you consider content in White Rose Research Online to be in breach of UK law, please notify us by emailing [email protected] including the URL of the record and the reason for the withdrawal request. [email protected] https://eprints.whiterose.ac.uk/ 231 Prevalence, transmission and intensity of infection by a microsporidian sex ratio distorter in natural Gammarus duebeni populations A. M. DUNN* and M.J.HATCHER Department of Biology, University of Leeds, Leeds LS2 9JT, UK (Received 13 May 1996; revised 16 August 1996; accepted 16 August 1996) This is a report of the prevalence, transmission and intensity of infection of a microsporidian sex ratio distorter in natural populations of its crustacean host Gammarus duebeni. Prevalence in the adult host population reflects differences in the intensity of infection in transovarially infected embryos and in adult gonadal tissue. The efficiency of transovarial parasite transmission to young also differs between populations, but this alone is insufficient to explain observed patterns of prevalence. Infection intensity may be important in determining future infection of target tissue in the adult and subsequent transmission to future host generations. We consider patterns of parasite infection in terms of selection on transmission and virulence. Key words: transovarial transmission, parasite burden, microsporidian, sex ratio distorter. distorter described as Octosporea effeminans (Bulnheim & Vavra, 1968). The microsporidian is Parasitic sex ratio distorters have important impli- transovarially transmitted in the cytoplasm of the cations for the ecology and evolution of their host ova and is not passed on through males. There is no populations. They have the potential to drive the evidence of horizontal transmission (Bulnheim, evolution of the host population sex ratio (Werren, 1978; Dunn et al. 1993). The parasite feminizes its 1987; Taylor, 1990; Hatcher & Dunn, 1995), impose host by converting putative males into functional selective pressures on host sex determination (Bull, females capable of transmitting the parasite to future 1983; Rigaud, Mocquard & Juchault, 1992; generations (Smith & Dunn, 1991; Dunn et al. Juchault, Rigaud & Mocquard, 1992; Hatcher & 1993). Hence, parasite-induced feminization boosts Dunn, 1995; Dunn et al. 1995) and may affect host the effective transmission base of the parasite, population size, stability and extinction (Werren, enabling parasite invasion and maintenance at higher 1987; Werren & Beukeboom, 1993). In this paper we prevalences in host populations (Hatcher & Dunn, examine prevalence, transmission and intensity of 1995). infection by a microsporidian sex ratio distorter Theoretical analyses (Werren, 1987; Taylor, 1990; infecting the crustacean Gammarus duebeni. Hatcher & Dunn, 1995) have shown that invasion Vertically transmitted parasites are transmitted and equilibrium prevalence of parasitic sex ratio from parent to offspring via the host’s gametes. If distorters in host populations depend upon the these parasites are uniparentally inherited, selection efficiency of parasite transmission, the efficiency of favours parasites which bias the host sex ratio parasite-induced feminization of the host, the rela- towards the transmitting sex (Lewis, 1941; Howard, tive fitness of infected hosts and the underlying host 1942; Hamilton, 1967). Vertically transmitted micro- population sex ratio. Although parasite prevalence sporidia have been found to distort host sex ratio has been shown to be sensitive to parasite trans- through killing male hosts which releases spores for mission efficiency (Werren, 1987; Hatcher & Dunn, horizontal transmission (Kellen & Wills, 1962; 1995), parasite burden and its relationship with Kellen et al. 1965; Hazard & Weiser, 1968) and transmission and prevalence has not been explicitly through feminization in which genetic males are considered. Here we examine parasite prevalence, converted into phenotypic females, so directly in- parasite transmission efficiency and parasite burden creasing the relative frequency of the transmitting in 3 G. duebeni field populations. sex (Smith & Dunn, 1991; Dunn, Adams & Smith, 1993). G. duebeni is host to a microsporidian sex ratio During the breeding season of 1995 we collected * Corresponding author. Tel: j0113 2332856. Fax: random samples of adult animals from 3 Gammarus j0113 2441175. E-mail: a.dunn!leeds.ac.uk. duebeni field populations: Budle Bay, Northumber- Parasitology (1997), 114, 231–236 Copyright # 1997 Cambridge University Press A. M. Dunn and M. J. Hatcher 232 land, UK, Totton Marsh, Hampshire UK, and assessed by looking at the reduction in deviance Douarnenez, Finestere, France. Parasite prevalence caused by deletion of a term from the maximal and the intensity of infection in adult females were model. Data for parasite load and for clutch size estimated by light microscopy. Individuals were are count data, therefore we specified a Poisson fixed in 10% formalin, dehydrated and embedded in error distribution. We corrected for overdispersion # paraffin wax. Previous studies indicated that the with a heterogeneity factor (Hf l Pearson’s χ \..; microsporidian is restricted to the gonadal tissue of Crawley, 1993). Changes in deviance caused by infected females where spore (Dunn et al. 1993) and removing a factor from the model were compared vegetative stages (Dunn, unpublished observations) with χ# tables. Data for parasite transmission have been observed. Therefore, serial transverse efficiency were proportion data (number of infected sections through the thorax (the site of the gonad) eggs\total number of eggs) and were analysed were stained with Giemsa’s stain and examined for specifying a binomial error structure, taking the total the microsporidian and measurements taken of the number of eggs as the binomial denominator. A number of parasites infecting the mature oocytes of heterogeneity factor was used to correct for over- infected females. dispersion and changes in deviance caused by The efficiency of transovarial parasite transmission removing a factor from the model were assessed to young was estimated by examining early stage using an F-test. embryos produced by infected mothers for the presence or absence of infection. Parasite burden was measured by counting total parasite load in these embryos. To determine the infection status of Parasite prevalence females from the field it is necessary to kill them. Parasite prevalence differed significantly between Therefore, we collected embryos from a random the field sites (χ#,2..l28n74, P ! 0n001). The sample of infected and uninfected females from each highest level of infection was at Budle Bay site and screened the mother and her embryos for where 30% of females were infected (N l 70), at infection after breeding. G. duebeni form precopula Douarnenez 15n6% (Nl64) were infected and the pairs a few days before they mate. Pairs of animals lowest level of infection, 6n3% (Nl127), was found were set up in individual containers in brackish at Totton Marsh (Table 1). water (specific gravity 1005m, corresponding to field salinity) at 12 mC and examined daily. Females mate and lay their eggs when they moult, approximately Parasite burden in adults every 3 weeks. Eggs are laid into a marsupium Parasite burden in the oocytes of adult females also formed from a series of overlapping plates differed between the 3 field sites and the pattern of (oostegites) on the ventral surface of the thorax and parasite load was in accord with differences in are brooded for 3–4 weeks. Within 24 h of prevalence: mean parasite load per oocyte was fertilization, early-stage embryos (1–128 cells) were highest at Budle Bay, and lowest at Totton Marsh flushed from the marsupium using a syringe filled (Table 1). From Fig. 1, in infected Totton Marsh with brackish water. Clutch size and blotted wet females most (80%) oocytes had a very low parasite weight of the female were recorded. Embryos were burden (0–4 parasites) and the maximum burden freeze fractured, fixed and stained with DAPI (4,6- recorded was 52 parasites. In contrast, 64% of diamidino-2-phenyl-indole), a fluorescent dye for oocytes in infected Budle Bay females had a burden DNA, and examined using a Zeiss Axiovert 10 of more than 10 parasites with 12% having a burden fluorescent microscope. This enabled us to see host in excess of 90. nuclei and the nuclei of parasites lying in the Parasite load differed significantly between the cytoplasm of the embryo cells (Dunn et al. 1995). sites (χ#,2..l45n2, P ! 0n001). In addition, Under fluorescence microscopy, a parasite nucleus within a population, parasite burden differed can sometime be resolved into 2 nuclei, although it is between families. Taking the brood of an individual not possible to determine whether this is a diplo- mother to represent a family we found that incor- karyon or a dividing nucleus. However, the increase poration into the model of a (site.mother) inter- in parasite number during progressive stages of host action
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