Self-fertilization Depression Research Articles

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

Inbreeding species of hermaphroditic animals practising copulation have been characterized by few copulations, no waiting time (the time that an isolated individual waits for a partner before initiating reproduction compared with paired individuals) and limited inbreeding (self-fertilization) depression. This syndrome, which has never been fully studied before in any species, is analysed here in the highly selfing freshwater snail Biomphalaria pfeifferi. We conducted an experiment under laboratory conditions over two generations (G1 and G2) using snails sampled from two populations (100 individuals per population). G1 individuals were either isolated or paired once a week (potentially allowing for crosses), and monitored during 29 weeks for growth, fecundity and survival. Very few copulations were observed in paired snails, and there was a positive correlation in copulatory activity (e.g. number of copulations) between the male and female sexual roles. The waiting time was either null or negative, meaning that isolated individuals initiated reproduction before paired ones. G2 offspring did not differ in hatching rate and survival (to 28 days) between treatments, but offspring from paired individuals grew faster than those from isolated individuals. On the whole, the self-fertilization depression was extremely low in both populations. Another important result is that paired G1 individuals began laying (selfed) eggs several weeks prior to initiating copulation: this is the first characterization of prior selfing (selfing initiated prior to any outcrossing) in a hermaphroditic animal. A significant population effect was observed on most traits studied. Our results are discussed with regard to the maintenance of low outcrossing rates in highly inbreeding species.

Predominance of outcrossing in Lymnaea stagnalis despite low apparent fitness costs of self‐fertilization

We have quantified the natural mating system in eight populations of the simultaneously hermaphroditic aquatic snail Lymnaea stagnalis, and studied the ecological and genetic forces that may be directing mating system evolution in this species. We investigated whether the natural mating system can be explained by the availability of mates, by the differential survival of self- and cross-fertilized snails in nature, and by the effects of mating system on parental fecundity and early survival. The natural mating system of L. stagnalis was found to be predominantly cross-fertilizing. Density of snails in the populations had no relationship with the mating system, suggesting that outcrossing rates are not limited by mate availability at the population densities observed. Contrary to expectations for outcrossing species, we detected no evidence for inbreeding depression in survival in nature with inferential population genetic methods. Further, experimental manipulations of mating system in the laboratory revealed that self-fertilization had no effect on parental fecundity, and only minor effects on offspring survival. Predominance of cross-fertilization despite low apparent fitness costs of self-fertilization is at odds with the paradigm that high self-fertilization depression is necessary for maintenance of cross-fertilization in self-compatible hermaphrodites.

Effects of Self-Fertilization, Environmental Stress and Exposure to Xenobiotics on Fitness-Related Traits of the Freshwater Snail Lymnaea stagnalis

Genetic and ecological factors may interact in their effects on fitness. Such interactions are thus to be expected between inbreeding and exposure of a population to a toxicant. The magnitude of inbreeding depression is thought to increase in stressful environments. To test this hypothesis, we investigated the combined effects of environmental conditions and inbreeding on fitness in the self-fertile snail Lymnaea stagnalis, using a stress gradient (0-2) applied to a 100 isolated and paired lineages: laboratory control (0), outdoor microcosm control (1) and pesticide exposure under outdoor microcosm conditions (2). Outdoor stress conditions were maintained for 28 days prior to measurements of fitness traits (fecundity, hatching success, and size at hatching) under laboratory conditions, so that delayed environmental effects could be estimated. Under laboratory control conditions, we found significant initial family level heterogeneity for most measured traits, including physiological performances as assessed through energetic biomarkers. Whatever the environmental conditions, inbreeding depression was very low for progeny performances. Negative values of self-fertilization depression (SFD) were obtained. Unexpectedly, SFD showed a negative relationship with the assumed stress intensity, reflecting a higher sensitivity under pairing than under selfing, mostly due to parental fecundity. This suggests that stressful conditions may favour selfing. Stress intensity increased the distribution limits of both depression indices, suggesting that changes in fitness are less predictable in a population under stress. Implications of such findings for environmental risk assessment of pesticides are discussed.

The influence of self-fertilization and grouping on fitness attributes in the freshwater snail Physa acuta: population and individual inbreeding depression

Abstract The genetic structure, selfing rate and inbreeding depression of the hermaphroditic freshwater snail Physa acuta were jointly analysed in a population near Montpellier, France. Allozymic markers revealed moderate gene diversity (0.138), and no heterozygote deficiency. The mean outcrossing rate, estimated by using progeny arrays, was 0.9, with substantial variation among families. This also suggests that the number of fathers among outcrossed offspring of a given mother is low. Inbreeding depression was estimated over more than one generation using 83 first-laboratory-generation (G1) families. The main parameters measured were parental (G1) fecundity, offspring (G2) survival and fecundity. Size and growth were also monitored. Parental fecundity was analysed under several conditions (isolation, pair and quadruplet outcrossing). The self-fertilization depression, including parental fecundity, offspring survival and fecundity, was about 0.9 at the population level. The genetic data obtained in the same population indicate a value of about 0.3 using Ritland’s (1990) technique, suggesting that the depression over the whole life-cyle might be even higher than 0.9. Grouping affected neither fecundity nor self-fertilization depression. Substantial variation in depression for survival was detected among individuals, from no survival in some selfed families to better survival than that of outbred families in others. The overall result (outbred population structure, high outcrossing rate and high self-fertilization depression) is consistent with what is expected in large outcrossing populations in which inbreeding depression is maintained by mutation-selection balance.

Social facilitation affects longevity and lifetime reproductive success in a self-fertilizing land snail

Factors that reduce the reproductive output of self-fertilizing hermaphrodites are receiving increasing attention. The combined effects of reduced fecundity of selfing parents and inbreeding depression of the progeny have been referred to as self-fertilization depression. In isolated freshwater snails the reproductive output of selfing individuals also decreases due to the lack of social facilitation (absence of a conspecific). We examined the effect of social facilitation on lifetime reproductive success (number of young produced and longevity) over two generations in the simultaneously hermaphroditic land snail Balea perversa. In a parallel study we showed that B. perversa kept singly and in pairs reproduced exclusively by self-fertilization. In the parent generation, snails kept singly produced less offspring than snails kept in pairs. The difference in lifetime number of young was mainly due to differences in adult life span. Snails of the two groups did not differ in reproductive rate (number of young produced per 100 d of reproductive life) and hatchling size. In the offspring generation, snails kept singly did not differ from individuals kept in pairs in the lifetime number of young and hatchling survival. As in the parent generation, snails kept singly reproduced during a shorter period than snails kept in pairs. However, the shorter reproductive life span of snails kept singly was compensated for by a slightly (but not significantly) higher reproductive rate which resulted in a similar number of offspring produced for both groups. In both generations, snails of the two groups did not differ in size at first reproduction, adult growth rate and size at death. These findings suggest that social facilitation may affect longevity in selfing B. perversa.

INBREEDING AND FITNESS IN THE FRESHWATER SNAIL LYMNAEA PEREGRA: AN EVALUATION OVER TWO GENERATIONS OF SELF-FERTILIZATION.

Inbreeding depression was estimated from an outbreeding population of the freshwater snail Lymnaea peregra, on the basis of two successive generations of enforced selling and outcrossing, and 70 maternal lineages. Outcrossing was analyzed under two treatments, groups of two and five individuals. The fitness parameters measured included fecundity, growth, and survival. In the first generation, we contrasted three treatments (selfers vs. paired outcrossers and group outcrossers). Very similar results were obtained between the two outcrossing treatments. A strong self-fertilization depression (which includes parental fecundity and progeny fitness) was detected in the selling treatment (about 90%). In the second generation, there was again marked evidence for self-fertilization depression, with the highest contributions coming from parental fecundity and progeny hatching rate. Our results suggest that the decreased parental fecundity is a consequence of the mating system in the previous generation, although the role of partial self-incompatibility and the copulation behavior could not be ruled out. Hatching rate and early survival data are suggestive of purging of lethal mutations. Significant variation in fitness among selfing lineages was found for most fitness traits. Our experimental design also allowed to test for interactions among fitness loci. Only one trait of the nine studied behaved as expected under synergistic interactions. However we cannot rule out some purging during the experiment, which could have biased results towards linearity. Inbreeding depression was also inferred from the change of inbreeding level across generations in the same population. We obtained a value similar to the experimental estimate.

Selfing, Outcrossing, and Mixed Mating in the Freshwater Snail Physa heterostropha: Lifetime Fitness and Inbreeding Depression

Selfing, Outcrossing, and Mixed Mating in the Freshwater Snail Physa heterostropha: Lifetime Fitness and Inbreeding Depression

A PROBLEM WITH THE ESTIMATE OF SELF-FERTILIZATION DEPRESSION IN THE HERMAPHRODITE FRESHWATER SNAIL BULINUS TRUNCATUS: THE EFFECT OF GROUPING.

The evolution of self-fertilization has been the subject of both numerous theoretical and empirical studies (reviewed by Jain 1976; Charlesworth and Charlesworth 1987; Uyenoyama et al. 1993; Jarne and Charlesworth 1993). These studies have shown that inbreeding depression, that is, the lowered fitness of inbred as compared with outbred individuals, is an important factor determining this evolution. Although most research has focused on plants, some studies have been performed on hermaphrodite animals (see Jarne and Charlesworth 1993) and particularly freshwater snails (see Jarne et al. 1993). Differences in survival rates between progeny of selfing and outcrossing individuals have been shown and interpreted as resulting from inbreeding depression. Selfing snails also have a lower fecundity than outcrossing snails. The whole effect (fecundity of parents and inbreeding depression of their progeny) has been referred to as self-fertilization depression (Jarne et al. 1991). However, specific problems may arise when estimating self-fertilization depression in animals. In experiments on hermaphroditic freshwater snails, selfed progenies have been produced usually by isolated virgin adults, and outcrossed progenies have been produced by grouped adults (review in Jarne et al. 1993). The effect of the mating system (outcrossing) and the effect of grouping are therefore associated when analyzing the results of outcrossing. It has been shown for various species of freshwater snails that both population density and size influence growth, survival, and fecundity (Chernin and Michelson 1956a,b; Thomas et al. 1974; Thomas and Benjamin 1974; Ahmed et al. 1986; Chaudhry and Morgan 1987). Increased density and population size is generally associated with a reduced fecundity and could lead to an underestimate of self-fertilization depression. In this paper, we investigate whether previous estimates of self-fertilization depression may have been biased by a grouping effect. By using aphallic individuals of the hermaphrodite freshwater snail Bulinus truncatus (see below), we can estimate the effect of grouping selffertilized for isolated and grouped snails. This is done by comparing the fitness of isolated snails with that of individuals at various group size and densities. Bulinus truncatus is a self-fertile hermaphrodite with two sexual morphs, euphallic and aphallic individuals, occurring in natural populations. Euphallic snails can self-fertilize as well as outcross as males or as females. Aphallic snails are characterized by the absence of the male copulatory organ (Larambergue 1939). They can selffertilize and receive sperm from an euphallic partner. However, they cannot transfer their own sperm to a partner (Larambergue 1939). No mutual exchange of sperm occurs during copulation in hermaphrodite freshwater snails: one individual acts as the female when its partner acts as the male. The determinism of aphally is still unclear; some results indicate a genetic determinism (Larambergue 1939), whereas others point strongly to the role of temperature (Schrag and Read 1992). A consequence of aphally is that purely aphallic populations can only self-fertilize. By using aphallic snails, the consequences of grouping can therefore be estimated without interference of the mating system. The aim of the present work is to test (1) whether a grouping effect occurs in the conditions previously used to analyze the self-fertilization depression (about 150 mL of water per snail with group size of 5 to 10 snails) (Jarne and Delay 1990; Jarne et al.

A Problem with the Estimate of Self-Fertilization Depression in the Hermaphrodite Freshwater Snail Bulinus truncatus: The Effect of Grouping

A Problem with the Estimate of Self-Fertilization Depression in the Hermaphrodite Freshwater Snail Bulinus truncatus: The Effect of Grouping

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.