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Selfing and Outcrossing in a Parasitic Hermaphrodite Helminth (Trematoda, Echinostomatidae)

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Selfing and Outcrossing in a Parasitic Hermaphrodite Helminth (Trematoda, Echinostomatidae) Heredity 77 (1996 1—8 Received 7 April 1995 Selfing and outcrossing in a parasitic hermaphrodite helminth (Trematoda, Echinostomatidae) SANDRINE TROUVE, FRANOIS RENAUDtI PATRICK DURAND & JOSEPH JOURDANE* Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Laboratoire de Biologie Animale, CNRS URA 698, Université de Perpignan, Avenue de Villeneuve, 66860 Perpignan Cedex and fLaboratoire de Parasitologie Comparée, CNRS URA 698, USTL Montpe/lier II, Place E. Batailon, 34095 Montpe/lier Cedex 05, France Echinostomesare simultaneous hermaphrodite trematodes, parasitizing the intestine of verte- brates. They are able to self- and cross-inseminate. Using electrophoretic markers specific for three geographical isolates (strains) of Echinostoma caproni, we studied the outcrossing rate from a 'progeny-array analysis' by comparing the mother genotype with those of its progeny. In a simultaneous infection of a single mouse with two individuals of two different strains, each individual exhibits an unrestricted mating pattern involving both self- and cross-fertilization. The association in mice of two adults of the same strain and one adult of another strain shows a marked mate preference between individuals of the same isolate. From mice coinfected with one parent of the three isolates, each parent was shown to be capable of giving and receiving sperm to and from at least two different partners. Mating system polymorphism in our parasitic model is thus discussed in the context of the theories usually advanced. Keywords:assortativemating, Echinostoma caproni, genetical markers, multiple fertilizations, selfing, sperm exchanges. much more so in plants (see Jam, 1976 for review) Introduction than animals. The breeding systems of most Theoccurrence in plants and animals of functionally hermaphrodite animals remain almost unknown, hermaphrodite organisms offers an ideal model to except for those of pulmonates (Jarne & Charles- examine the evolution and maintenance of two worth, 1993; Jarne et al., 1993 for review) and asci- different mating systems (selfing and outcrossing). Is dians (Ryland & Bishop, 1990; Bishop & Ryland, it more advantageous to invest completely in their 1993) which are well documented. own genome (selfing) or to look for a partner for The parasitic worms, especially the platyhel- exchange of genetic material (outcrossing) with the minths, which are almost all hermaphrodites, repre- risk of not finding one? Two main hypotheses are sent an ideal model to examine whether the usually proposed to explain the evolution of these polymorphous mating systems known in plants have two breeding systems. In organisms which have a animal counterparts. The biology of the parasites is low probability of meeting a partner, that is, species influenced by a double constraint: (i) the obligatory with low mobility or population density (Tomlinson, conquest of a living environment which often 1966; Ghiselin, 1969, 1974; Charnov et a!., 1976), produces parasite populations in low densities and selfing will be favoured. On the other hand, the patchy distributions (Renaud et al., 1992) and (ii) homozygosity resulting from selfing would generate the need within this host to find a mate for outcross- a genetic load by the accumulation of deleterious ing and avoiding inbreeding depression (Price, 1977, recessive mutations which would promote outcross- 1980). These two factors seem important to under- ing (Futuyma, 1986; Maynard Smith, 1989). Biolo- stand the evolution of breeding systems such as gists have studied this topic for a long time, but selfing and outcrossing. But few studies on the evolution of mating systems have been conducted in *Correspondence helminth parasites. Data obtained on the genetic 1996 The Genetical Society of Great Britain. 2 S. TROUVE ETAL. structure of populations of cestodes (Renaud et al., outcrossed offspring and then to calculate the rate 1983, 1986; Renaud & Gabrion, 1988) and trem- of selfing. Starch electrophoresis and histochemical atodes (Reversat et a!., 1989) have shown that tests on these isoenzymes were performed using the natural populations of such organisms seem panmic- technique of Pasteur et a!. (1987). tic. In other respects, experimental research using radioactive isotopes has shown sperm exchanges in Parasitedistribution in the mouse intestine digenetic trematodes (Nollen, 1983, 1990, 1993). Nevertheless, none of these studies estimates the Metacercariaewere obtained from experimentally rates of self-fertilization and cross-fertilization in infected snails by dissection and were fed to mice via this wide group of parasites. We present and discuss stomach tubes. At 20 days postinfection, the small in this paper the results of an experimental study on intestine of the mice was opened arid divided into the evolution of selfing vs. outcrossing presented by six equal sections, and the distribution of adult echi- these parasites in different situations of mixed nostomes along the intestine was noted. Parasites infections. were recovered individually and their genotypes systematically determined by electrophoresis. The different experiments carried out are presented in Materials and methods Table 1. This study was performed using mixed Model infections with the two strains E. c and E. 1. The parasite complex Echinostoma caproni used in this study consists of three geographical strains, the Geneticexchanges between strains first originating from Madagascar, the second from Metacercarialinfections and recovery of adults Egypt and the third from Cameroon. According to followed the previous procedure. The uterus of each Christensen et al.(1990), these three strains parasite was then torn to release the eggs. The eggs (geographical isolates in fact) belong to the same of each offspring developed in about 15 days in species, E. caproni. They freely interbreed under spring water at 27°C in a Petri dish and, stimulated experimental conditions. In the text, the Madagas- by artificial light, the miracidia (infecting larvae of can strain will be called E. c, the Egyptian strain E. the first intermediate host) hatched. Thirty miracidia 1 and the Cameroonian strain E. k. of each laying were separately brought into contact The life cycle of E. caproni includes three succes- with each mollusc. Because the parasite—mollusc sive hosts (Huffman & Fried, 1990): the first inter- compatibility was not absolute, some molluscs did mediate host (mollusc) where rediae and cercariae not become infected. Consequently, the number of develop, the second intermediate host (mollusc or offspring analysed for each adult corresponds to the amphibian) where cercariae transform into infec- number of infected molluscs. Because clonal multi- tious metacercariae, and the definitivehost plication takes place in the snail, we could obtain a (mammal or bird) where metacercariae develop into sufficient quantity of parasitic tissues (rediae) 25 sexually mature adults. In the laboratory, E. caproni days after the infection to carry out electrophoresis. is routinely cycled through two hosts: the snail The genetic exchanges were assessed by comparison Biomphalaria pfeifferi which acts as first and second between parent and offspring genotypes. The intermediate host and the mouse (Swiss OF1 stock) different infections conducted to estimate the rates which acts as definitive host. of selfing and outcrossing are shown in Table 1. Genetic analysis Dataanalysis Thethree strains are three different genetic entities TheFisher exact test (Sokal & Rolf, 1981), which can be identified by three diagnostic loci. developed by Raymond & Rousset (1995), was used These are the phosphoglucomutase (Pgm, EC to compare the rate of outcrossing amongst the 5.4.2.2), the glucose-6-phosphate isomerase (Gpi, different experiments. This statistical analysis was EC 5.3.1.9) and the mannose-6-phosphate isomerase performed using the program GENEPOP (Raymond & (Mpi, EC 5.3.1.8). The first two loci (i.e. Pgm and Rousset, 1995). Because of the complexity of our Gpi) were described by Voltz et a!. (1986, 1987, data (several infection types and samples) the 1988), the third was discovered by us. The codomi- sequential Bonferroni method was used to adjust the nance and Mendelian segregation of these alleles significance level (Rice, 1989). For the global statis- allow us to distinguish between selfed and tics we also calculated the P-values according to The Genetical Society of Great Britain, Heredity, 77, 1—8. MATING SYSTEMS IN TREMATODES 3 Table 1 Design of the experiments No. individuals of No. experiments each strain infecting performed = eachmouse no. mice infected Distribution of parasites in small intestine 5E.c+5E.l 11 40 1OE.c+1OE.l 10 Genetic exchanges between different strains 1E.c+1E.l 7j- 1E.c+1E.k 7t 1E.c+1E.c+1E.l 3t 1E.c+1E.l+1E.k 4t E. c, Madagascan strain of Echinostoma caproni; E. 1, I II III IV V VI INTESTINAL SEGPEN1B Egyptian strain of E. caproni; E. k, Cameroonian strain of Duenum Jojunum Ileufli E.caproni. tFor each infection type, 30 offspring (rediae) of each Fig.1 Distribution of the two strains of Echinostoma adult were genetically determined at three loci. caproni in the small intestine of mice. The data from the E. c. and E. L infections, performed with 10 and 20 meta- cercariae, respectively, have been pooled. E. c: Mada- gascar strain of E. caproni, E. 1: Egyptian strain of E. Fisher's method for combining independent test caproni. results (Manly, 1987). Results be attributed to the result of one experiment (i.e. experiment 1, Table 2). Parasite distribution in the mouse intestine The distribution of 198 individual parasites (98 E. c Simultaneous infection with one E. c and one E. k. and 100 E. 1) was examined for the two infection A high variability was shown in the outcrossing types (Table 1). Nearly all the Echinostoma (i.e. >90 proportions with values from 48 to 86 per cent for per cent) colonized the lower third of the small E. c and from 0 to 100 per cent for E. k, except for intestine (the ileum) (Fig. 1). Moreover, there was experiments 8 and 9 where pure selfing was no significant difference in the distribution of the observed for both individuals (Table 3). These two two strains.
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