The influence of genetic factors and population dynamics on the mating system of the hermaphroditic freshwater snail Biomphalaria pfeifferi

Abstract

P. 2005. The influence of genetic factors and population dynamics on the mating system of the hermaphroditic freshwater snail Biomphalaria pfeifferi . Á/ Oikos 108: 283 Á/296.Although self-fertilization and its evolutionary consequences have been widely studied, the relative influence of genetic and environmental factors on the determination of mixed-mating systems remains poorly known. In 1999 and 2000, we surveyed the mating system, the population dynamics and some life-history traits of four populations of the freshwater snail Biomphalaria pfeifferi , the major intermediate host of Schistosoma mansoni in Africa, in two areas of Madagascar (Itasy and Antananarivo). We confirmed that B. pfeifferi is a predominant selfer, with selfing rates ranging between 80 and 100%. Temporal and geographical variation of the selfing rate was observed at both local and large spatial scale. Historical processes of colonization and invasion of B. pfeifferi in Madagascar could explain the geographical variation of the mating system observed at regional scale. Pure selfing has probably evolved in the two populations of Antananarivo area as a reproductive assurance strategy in a metapopulation where extinction is frequent and migration rare. The reproductive assurance hypothesis does not explain the spatio-temporal mating system variations observed in Itasy area. However genetic factors including inbreeding depression-the expression of which can be environmentally mediated-and metapopulation dynamics could influence the mating system in both populations sampled in Itasy and lead to different levels of evolutionary stable intermediate selfing rate in this region. Our results therefore highlight the influence of environmental heterogeneity and stochasticity on mating system.

Prior selfing and the selfing syndrome in animals: an experimental approach in the freshwater snailBiomphalaria pfeifferi

“…Moreover, experimental conditions enforcing the presence of partners tend to decrease the selfing rate in selfing snail species, as shown in another highly selfing snail species, Bulinus truncatus, using molecular markers (P. David and P. Jarne, unpublished data). Low inbreeding depression is consistent with an average selfing rate of about 90 % in B. pfeifferi (Charbonnel et al, 2005). Genetic models of the evolution of the selfing rate indeed predict limited inbreeding depression (<0 .…”

“…However, the observed mean selfing rate per population is about 90 % (Charbonnel et al, 2005), as observed in other species of freshwater snails (Viard et al, 1997 ;Trouve´et al, 2004). An open question is what maintains this residual outcrossing rate.…”

“…However, copulation does occur, and the copulatory sequence has already been detailed (Rupp & Woolhouse, 1999). Indirect evidence suggested that inbreeding depression is limited in this species (Charbonnel et al, 2005). However, we do not know of any formal investigation of the waiting time, and more generally of the selfing syndrome.…”

“…In these animals, the selfing syndrome has been defined as 'high selfing rate, low inbreeding depression and a limited propensity to copulate ' (Doums et al, 1996). More recent work indicates that a limited waiting time (the time that an isolated individual waits for a partner before initiating reproduction compared with paired snails) is also expected in highly selfing species in which outcrossing requires copulation (Tsitrone et al, 2003 a, b;Charbonnel et al, 2005). However, even in snails, the suite of traits ' inbreeding depression, mating activity and waiting time' has not been studied experimentally in any species.…”

Contrasting the distribution of phenotypic and molecular variation in the freshwater snail Biomphalaria pfeifferi, the intermediate host of Schistosoma mansoni

“…Populations may experience density variation associated with flooding and drought, leading to bottlenecks and recolonization events (Jarne and Delay, 1991;Charbonnel et al, 2002a,b). Analysis of the genetic structure of natural populations (Charbonnel et al, 2002a,b,c), progeny-arrays analyses (Charbonnel et al, 2005) and laboratory experiments (Tian-Bi et al, 2008) showed that B. pfeifferi is a highly selfing species. A consequence of both population demography and the mating system is limited neutral variability within populations and fairly large genetic differentiation among populations (Charbonnel et al, 2002a).…”