Bernard Delay

Microsatellite and morphological analysis of population structure in the parthenogenetic freshwater snail Melanoides tuberculata : insights into the creation of clonal variability

The distribution of variability was studied at various geographical scales in the tropical freshwater snail Melanoides tuberculata, in order to analyse the role of factors shaping this distribution, including the mating system and population dynamics. This parthenogenetic polyploid species reproduces mainly asexually, with males occurring at low frequency. About 800 individuals (38 sites) were sampled from Africa and the Middle East, where the species originated, and from recently colonized habitats in South and Central America, and especially the island of Martinique. We first described variation of general aspects and ornamentation of the shells. This analysis confirms the existence of discrete morphs. Second, individuals were studied at three microsatellite loci, showing that each morph is a genetic clone with some minor variation compatible with models of microsatellite evolution. The genetic analysis also showed much more variation within than between clones. However, two populations from Africa exhibited a large amount of variability, and a mixture of sexual and asexual reproduction might explain these genetic patterns. The worldwide distribution of variability is, therefore, compatible with the African origin of the species, and the introduction of a few clones in other parts of the world. These results also suggest that the distribution of variability in Martinique is influenced by flooding events, and that two morphs from Martinique can be interpreted as hybrids between two pre‐existing morphs, based on morphological, genetic and geographical arguments.

Genetic characterization of the hybridization betweenMytilus edulis andM. galloprovincialis on the Atlantic coast of France

A genetic study carried out on nine natural mussel populations on the French Atlantic coast from 1989–1990 revealed interdigitation between typicallyMytilus edulis and typicallyM. galloprovincialis populations and intermediate populations. The allele components of the populations followed aM. edulis/M. galloprovincialis gradient which does not correspond to a geographical gradient. Strong hybridization was evident in samples with intermediate allele frequencies. The respective importance of gene flow and selection is discussed in the light of the results and the evironmental features of the sampling zone.

SELF-FERTILIZATION VERSUS CROSS-FERTILIZATION IN THE HERMAPHRODITIC FRESHWATER SNAIL BULINUS GLOBOSUS

Self‐fertilization depression of fitness in the freshwater hermaphroditic snail Bulinus globosus, an intermediate host of the parasitic trematode Schistosoma, has been studied in a strain originating from Niger. B. globosus is an outcrosser that can self‐fertilize when isolated before any copulation has occurred. The self‐fertilization depression has been estimated during two successive generations. In the first generation, selfing was compared to outcrossing. Within each mating system group, selfing and outcrossing were compared again in the second generation. A striking difference was shown in favor of cross‐fertilization for the number of eggs laid, the survival at birth of young snails and the number of snails reaching sexual maturity. The overall self‐fertilization depression is 0.920 after two generations of selfing. We discuss the relative role of selfing and outcrossing in the evolution of freshwater snail populations.

INBREEDING DEPRESSION, NEUTRAL POLYMORPHISM, AND COPULATORY BEHAVIOR IN FRESHWATER SNAILS: A SELF-FERTILIZATION SYNDROME

This paper examines the consequences of self‐fertilization on life‐history traits and neutral genetic polymorphism in natural populations of three species of hermaphrodite freshwater snails: Biomphalaria straminea, Bulinus globosus, and the aphallic species Bulinus truncatus. Life‐history traits (fecundity, growth, hatching rate, and survival of offspring) are compared under laboratory conditions between isolated (obligatory selfing) and paired (outcrossing possible) snails in one population of B. straminea and B. globosus and two populations of B. truncatus. The genetic polymorphism of the same four populations is analyzed using electrophoretic markers in B. straminea and B. globosus and microsatellite markers in B. truncatus. In B. truncatus and B. straminea, isolated snails have a higher fecundity than paired snails, whereas the contrary is observed in B. globosus. For all populations, no difference in hatching rate and offspring survival is detected between the two treatments. Genetic analyses using microsatellite markers conducted in B. truncatus on progeny of paired snails reveal a high selfing rate in spite of high copulation rates, highlighting the difficulties of obtaining outcrossing in highly selfing snails. The high survival of selfed offspring in B. truncatus and B. straminea indicates that inbreeding depression is limited. The extent of inbreeding depression in B. globosus is less clear. Overall, fitness decrease in this species is limited to fecundity. The extent of allozyme polymorphism is very limited whereas a much higher variability is observed with microsatellites. Biomphalaria straminea and B. truncatus populations are also characterized by very low observed heterozygosities and large heterozygote deficiencies, whereas the B. globosus population does not exhibit such a deficiency. Overall these results allow the definition of a self‐fertilization syndrome in hermaphrodite freshwater snails: selfing populations (such as those of B. straminea and B. truncatus studied here) are characterized by high selfing rates in spite of copulations, limited deleterious effects of selfing, limited neutral genetic polymorphism, and large heterozygote deficiencies.

Cost of resistance, expressed as a delayed maturity, detected in the host–parasite system Biomphalaria glabrata/Echinostoma caproni

Theoretical models have shown that when susceptibility to a parasite is genetically determined, polymorphism with regard to susceptibility can only be maintained by costs associated with resistance. However, an apparent resistance, or nonsusceptibility, may result from a lack of adaptation of the parasite, which does not imply any costs for the host. In this study, we analysed whether susceptibility was genetically determined in the Biomphalaria glabrata/Echinostoma caproni system, and we investigated the existence of costs associated with nonsusceptibility. Results showed that nonsusceptibility of B. glabrata to E. caproni was genetically determined and could be strongly selected for through generations. Furthermore, analysis of age at maturity among offspring segregating for susceptibility revealed that nonsusceptible individuals reached maturity later than susceptible ones. The delay in maturity is statistically significant and reflects a cost associated with resistance.

Differential susceptibility to a trematode parasite among genotypes of the Mytilus edulis/galloprovincialis complex

We show that parasitism by the trematode Prosorhynchus squamatus in parental and introgressed Mytilus edulis/galloprovincialis (Bivalvia) mussels occurs in individuals with a predominantly M. edulis genome. This result suggests that the restricted specificity of P. squamatus is dependent on genetic factor(s) present in M. edulis. Because of its strong pathogenic effects (i.e. total castration and possible death), this parasite may be a source of intense selection against M. edulis genomes when they are present in a site. As a consequence, it may favour the geographic extension of the M. galloprovincialis genome. Previous studies have indicated that, in hybrid zones, recombinant genotypes are more susceptible to parasitic infections than either parental genotype. We demonstrate that this is not the case for the M. edulis/M. galloprovincialis system, and that the parental genotype alone determines susceptibility.

Inbreeding depression and self-fertilization in Lymnaea peregra (Gastropoda: Pulmonata)

The effects of self-fertilization and cross-fertilization on several fitness traits were examined in the freshwater hermaphrodite snail Lymnaea peregra. Laboratory strains were established from Lake Geneva populations. Comparisons of F2 snails and their offspring showed that there are no differences in hatching time, nor in the size of young snails monitored over one month. But there was a significant difference, when the distribution of the capsule weight against the number of eggs was compared, although the effects of this on fitness are probably small. There was also a significant difference for egg production and juvenile viability over one month; the selfing snails are 94 per cent less fit for these two traits than the outcrossing.

Aphally Versus Euphally in Self-Fertile Hermaphrodite Snails from the Species Bulinus truncatus (Pulmonata: Planorbidae)

Different reproductive systems have evolved in hermaphrodite plants that allow species to reproduce simultaneously by both self-fertilization a d cross-fertilization (see Charlesworth and Charlesworth 1978; Lloyd 1979)-for example, cleistogamy (Schoen and Lloyd 1984) and gynodioecy (Gouyon and Couvet 1987). Aphally may be such a feature in hermaphrodite animals, particularly Pulmonate snails. Whereas the reproductive structure of snails usually consists of one hermaphrodite gonad and of male and female ducts with accessory glands, aphallic individuals lack the male copulatory organ (Geraerts and Joosse 1984; Tompa 1984). Aphally has been reported in land snails (Tompa 1984; Pokrysko 1987) and in freshwater snails of the genus Bulinus, the intermediate African host of the trematode Schistosoma that infects humans (Brown 1980). In Bulinus, aphallic individuals lack not only the copulatory organ but the prostate and vas deferens as well (Larambergue 1939). Bulinus species are self-fertile hermaphrodites whose usual mating system is cross-fertilization by unilateral copulation, in which one individual acts as male while the other acts as female (Larambergue 1939; Rudolph 1979; Rollinson et al. 1989). The foreign sperm is used for cross-fertilization almost immediately after copulation. If an individual is isolated after copulation, sperm storing allows outcrossing during the subsequent few months. However, the selfing rate increases in time as the sperm stored is exhausted or dies. Virgin isolated individuals also reproduce by selfing (Rudolph and Bailey 1985). A euphallic Bulinus is able to receive sperm, to self-fertilize, and to transfer its sperm to another individual by copulation, whereas an aphallic individual can only receive sperm and self-fertilize. Larambergue (1939) showed that, in Bulinus truncatus (contortus), pure euphallic, pure aphallic, and mixed populations can be found over the range of the species. He also showed that aphally has a genetic basis that appears polygenic. His results suggest that B. truncatus may be a partial selfer as a consequence of being aphallic (Larambergue 1939, p. 194). Our results support this hypothesis. A prediction of the theory of sex allocation (Charnov 1982), as applied to the case of B. truncatus, is that aphallic selfing snails can invest more in reproduction than euphallic ones because there is no cost related to the building and maintenance of male organs, if one assumes that both types of snails invest the same amount in growth and in survival. We addressed this question by studying the relative fitness of self-fertilizing aphallic and euphallic individuals. As expected, we show that aphallic snails lay more eggs than euphallics.

Population genetics of freshwater snails

Freshwater snails have attracted the attention of biologists for a long time, because they are intermediate hosts of schistosomes, agents of bilharziases. However, population-genetic studies of freshwater snails have been undertaken only during the past decade, covering topics such as the relative roles of genetic drift and gene flow in subdivided populations and the roles of extinction and recolonization events in determining population structure. Other studies in freshwater snails have investigated the maintenance of sex and the evolution of selling, widening a debate restricted mainly to plant populations. The possible role of parasites in freshwater-snail population genetics has also been investigated.

Genetic differentiation, dispersal and mating system in the schistosome-transmitting freshwater snail Biomphalaria glabrata

Biomphalaria glabrata is the main intermediate host of Schistosoma mansoni in America and one of the most intensely studied species of freshwater snail, yet very little is known about its population biology. Here, we used seven highly polymorphic microsatellite loci to analyse genetic diversity in populations from three regions (Lesser Antilles, Venezuela and southern Brazil). Considerable genetic variation was detected, with an average (s.d.) H0 = 0.32 (0.24). More diversity per population was found in the Valencia lake basin in Central Venezuela, which suggests an influence of dispersal (via inter-population connectivity) on the restoring of genetic diversity after the demographic bottlenecks recurrently experienced by populations. A marked population structure was detected and there seems to be a relationship between mean differentiation and genetic diversity within regions. There is also a significant isolation-by-distance pattern. The Lesser Antilles populations appear clearly differentiated from the rest, which suggests a single colonisation event followed by local radiation within these islands or multiple colonisation events from the same source area. Our results indicate that B. glabrata essentially cross-fertilises, with little variation in selfing rates among populations. However, significant deficits in heterozygotes and linkage disequilibria were detected in two Venezuelan populations suggesting a mixture of at least two different genetic entities, probably with differences in their respective mating systems.