Hermaphroditic Freshwater Snail Physa Acuta Research Articles

Environmental effects on the genetic architecture of fitness components in a simultaneous hermaphrodite.

Understanding how environmental change affects genetic variances and covariances of reproductive traits is key to formulate firm predictions on evolutionary responses. This is particularly true for sex-specific variance in reproductive success, which has been argued to affect how populations can adapt to environmental change. Our current knowledge on the impact of environmental stress on sex-specific genetic architecture of fitness components is still limited and restricted to separate-sexed organisms. However, hermaphroditism is widespread across animals and may entail interesting peculiarities with respect to genetic constraints imposed on the evolution of male and female reproduction. We explored how food restriction affects the genetic variance-covariance (G) matrix of body size and reproductive success of the simultaneously hermaphroditic freshwater snail Physa acuta. Our results provide strong evidence that the imposed environmental stress elevated the opportunity for selection in both sex functions. However, the G-matrix remained largely stable across the tested food treatments. Importantly, our results provide no support for cross-sex genetic correlations suggesting no strong evolutionary coupling of male and female reproductive traits. We discuss potential implications for the adaptation to changing environments and highlight the need for more quantitative genetic studies on male and female fitness components in simultaneous hermaphrodites.

Boldness to predator is not significantly correlated with mating behaviour in a simultaneously hermaphroditic snail

If one sex role is preferred over the other, the hermaphroditic mating system might not be maintained. Some simultaneous hermaphroditic species show unilateral mating. Behavioural syndromes that link two behaviours often maintain individual variations in the behaviours. We predict that a behavioural syndrome (boldness) also maintains variation in the sex role decision of the hermaphroditic freshwater snail Physa acuta. Boldness is assumed to reflect an individual’s personality to predation risk, and is measured as the latency to emerge from shells after an artificial stimulus. We examined whether the bolder snails exhibit more active mating behaviour such as male role, shorter latency to copulation and longer copulation duration. Significant repeatability indicated that boldness was a consistent trait within an individual. Furthermore, boldness was positively correlated with shell length and negatively with age, respectively. We found no significant relationships between boldness and mating behaviour (sex role, latency to copulate, and copulation duration). Therefore, the behavioural syndrome in the present context is not likely to maintain a sex role preference.

Consequences of mating and predation risk for longevity in a freshwater snail: abstinence makes the heart beat longer.

Senescence is not a static property of an individual or population, but rather it is a dynamic process that may be influenced by environmental conditions. This can occur in at least two ways: in the long-term across multiple generations, and in the short-term via phenotypic plasticity. The former has attracted a lot of attention, both theoretically and empirically; the latter has lagged behind. To determine whether two important environmental variables (predation risk and mate availability) affect the pattern of actuarial senescence (i.e. the increase in mortality with age), we reared 30 full-sib families of the simultaneously hermaphroditic freshwater snail Physa acuta under four different environmental conditions and tracked individuals until death. Individuals were reared in a 2×2 factorial experiment that manipulated the nonlethal presence of chemical cues from predatory crayfish (presence/absence) and the opportunity to mate with an unrelated partner (mated/not mated). Snails that receive a partner reproduce by outcrossing, whereas those that remain in isolation can reproduce by self-fertilization. We compared the cumulative survival curves to test for an effect of predation risk and mating. The hazard ratio (HR) for the predation risk comparison was 1.042 indicating no significant difference between the curves. However, the HR for the mating comparison was 4.021, reflecting a significant reduction in survival probability for mated snails relative to isolated snails. As such, mating resulted in a much shorter lifespan, an outcome that we interpret in terms of shifting resource allocation.

Environment-Dependent Sexual Selection: Bateman's Parameters under Varying Levels of Food Availability.

Sexual selection is a potent evolutionary force that has been shown to vary in strength and direction depending on demographic factors such as density and sex ratio. However, the effect of other environmental factors on the mode of sexual selection remains largely unexplored. Here, we tested experimentally how food restriction affects the potential for sexual selection in the male and the female sex function of the simultaneously hermaphroditic freshwater snail Physa acuta. We manipulated food availability and compared Bateman's metrics of sexual selection between groups of five well-fed and five food-restricted snails. Food-restricted individuals had a reduced female reproductive output, suggesting that we successfully manipulated the reproductive resources. Importantly, food restriction reduced the male opportunity for sexual selection (in terms of a lowered variance in male mating success) and led to diminishing returns of mating in both sexes (in terms of nonsignificant Bateman gradients). Furthermore, we observed significant changes in the relative contribution of different fitness components, suggesting stronger postcopulatory selection in the male sex role and stronger fecundity selection in the female sex role under restricted food conditions. This study highlights the need to incorporate ecological factors to better understand how sexual selection operates in the wild.

Diet alters delayed selfing, inbreeding depression, and reproductive senescence in a freshwater snail.

Reproductive success is a critical fitness attribute that is directly influenced by resource availability. Here, we investigate the effects of diet-based resource availability on three interrelated aspects of reproductive success: a change in mating system based on mate availability, consequent inbreeding depression, and the deterioration of reproductive efficiency with age (senescence). We employed a factorial experimental design using 22 full-sib families of the hermaphroditic freshwater snail Physa acuta to explore these interactions. Individual snails were reared in one of two mate-availability treatments (isolated [selfing] or occasionally paired [outcrossing]) and one of two diet treatments (boiled lettuce or Spirulina, an algae that is rich in protein, vitamins, and minerals). Spirulina-fed snails initiated reproduction at a 13% earlier age and 7% larger size than lettuce-fed snails. Spirulina also resulted in a 30% reduction in the time delay before selfing. Compared to lettuce, a diet of Spirulina increased inbreeding depression by 52% for egg hatching rate and 64% for posthatching juvenile survival. Furthermore, Spirulina led to a 15-fold increase in the rate of reproductive senescence compared with a diet of lettuce. These transgenerational, interactive effects of diet on inbreeding depression and reproductive senescence are discussed in the context of diet-induced phenotypic plasticity.

Inbreeding depression of mating behavior and its reproductive consequences in a freshwater snail

Theoretical work predicts that the magnitude of inbreeding depression is particularly high in traits that are closely related to fitness. Despite the extensive work on inbreeding depression of male and female reproductive performance, relatively little is known on how inbreeding impairs male and female mating behavior. We studied inbreeding depression of male and female mating behavior in the simultaneously hermaphroditic freshwater snail Physa acuta to test 1) whether there is inbreeding depression of mating behavior, 2) whether the potential of mate competition and mate choice has an effect on the strength of inbreeding depression, 3) whether the magnitude of inbreeding depression differs between both sex functions, and 4) how inbreeding depression of mating behavior translates into inbreeding depression of reproductive success. For this, we compared the mating behavior between selfed (inbred) and outcrossed (outbred) focal snails in a series of mating trials, in which we manipulated experimentally the potential of mate competition and mate choice. Our results provide evidence for moderate inbreeding depression of the number of copulatory encounters, the number of copulations, and the total time spent mating in both sex functions. The magnitude of inbreeding depression did not differ between the levels of competition and between both sex functions. Finally, our results suggest that inbreeding depression of mating behavior only explains a small fraction of the observed inbreeding depression of reproductive success. We discuss the implications of these findings with respect to precopulatory sexual selection and sex-specific inbreeding depression.

SEX-SPECIFIC INBREEDING DEPRESSION DEPENDS ON THE STRENGTH OF MALE-MALE COMPETITION

Inbreeding depression has become a central theme in evolutionary biology and is considered to be a driving force for the evolution of reproductive morphology, physiology, behavior, and mating systems. Despite the overwhelming body of empirical work on the reproductive consequences of inbreeding, relatively little is known on whether inbreeding depresses male and female fitness to the same extent. However, sex-specific inbreeding depression has been argued to affect the evolution of selfing rates in simultaneous hermaphrodites and provides a powerful approach to test whether selection is stronger in males than in females, which is predicted to be the consequence of sexual selection. We tested for sex-specific inbreeding depression in the simultaneously hermaphroditic freshwater snail Physa acuta by comparing the reproductive performance of both sex functions between selfed and outcrossed focal individuals under different levels of male-male competition. We found that inbreeding impaired both male and female reproductive success and that the magnitude of male inbreeding depression exceeded female inbreeding depression when the opportunity for sperm competition was highest. Our study provides the first evidence for sex-specific inbreeding depression in a hermaphroditic animal and highlights the importance of considering the level of male-male competition when assessing sex differences in inbreeding depression.

SEXUAL SELECTION WITHOUT SEXUAL DIMORPHISM: BATEMAN GRADIENTS IN A SIMULTANEOUS HERMAPHRODITE

One of the most general patterns in sexual selection is stronger selection on mating activity in males than in females. This asymmetry is thought to result from the higher energetic cost of producing one female compared to one male gamete (anisogamy). However, most studies focused on gonochoric species with strong sexual dimorphism, in which males and females are necessarily under different selection regimes. The question remains whether anisogamy alone would suffice to produce such differences. In simultaneous hermaphrodites one can compare sexual selection on the male and female functions in the absence of sexual dimorphism. Here we quantify sexual selection in the hermaphroditic freshwater snail Physa acuta under laboratory conditions. We combine exhaustive behavioral records of mating activity in mating groups and molecular paternity assignment to measure the mating success and reproductive success of 120 individuals. Our results validate the prediction of stronger selection to gain mating partners in the male than in the female function. Moreover, we did not detect cross-sex effects on fitness, or correlations between male and female production of offspring over the course of our experiment. We conclude that with respect to sexual selection P. acuta is comparable to gonochorists, confirming that anisogamy is a sufficient explanation for the differences in sexual selection regimes between sexes.

Gender-role alternation in the simultaneously hermaphroditic freshwater snail Physa acuta: not with the same partner

In simultaneous hermaphrodites, gender conflicts that arise from two potential mates sharing the same gender preference may be solved through conditional reciprocity (or gamete trading). Conditional reciprocity had initially been considered widespread, but recent studies suggest that its real occurrence may have been overestimated, possibly because most mating observations have been performed on isolated pairs of individuals. Some resulting patterns (e.g., non-random alternation of sexual roles) were indeed compatible with conditional reciprocity but could also have stemmed from the two partners independently executing their own mating strategy and being experimentally enforced to do so with the same partner. Non-random alternation of gender roles was recently documented in the simultaneously hermaphroditic freshwater snail Physa acuta. To distinguish between conditional and unconditional gender alternations, we observed copulations of individually marked snails reared at three contrasted densities. We showed that density affected the overall frequency of copulations during the first 2 days of the experiment with high-density boxes showing more copulations than low density boxes, but it did not affect gender alternation patterns. A change in gender role was observed more often than expected by chance over two successive copulations by the same individual, confirming previous studies. However, gender switches did not preferentially occur with the same partner. We conclude that gender alternation is not due to conditional reciprocity in P. acuta. It may rather stem from each individual having a preference for gender alternation. We finally discuss the mechanisms and the potential extent of this unconditional reciprocity.

Experimental evidence of inbreeding avoidance in the hermaphroditic snail Physa acuta

Inbreeding depression should select for inbreeding avoidance behaviours. Here we test this hypothesis in two populations of the simultaneous hermaphroditic freshwater snail Physa acuta. We recorded the copulatory behaviour of 288 pairs of sib-mates, non-kin mates from the same population, or non-kin mates from two different populations. We find that kin discriminatory behaviours exist in this species, exclusively expressed by individuals playing the female role. We discuss the relevance of our finding in the context of the evolution of recognition systems and the consequences of such a behaviour in natural populations.

Is delayed selfing adjusted to chemical cues of density in the freshwater snail Physa acuta?

Delayed selfing allows self‐fertile organisms to reproduce even in the absence of mate, and is thought to have evolved as a reproductive assurance strategy. In animal species with strong inbreeding depression, the time during which selfing should be postponed in the absence of mates (referred to as the waiting time) is predicted to have evolved as a function of inbreeding depression, resource reallocation and survival. Under the same theoretical perspective, variation in population density should trigger the evolution of a plastic adjustment of the waiting time. A condition is that individuals should be able to perceive environmental cues (e.g. chemicals) of the density of potential mates. These predictions were tested here using the hermaphroditic freshwater snail Physa acuta, based on two experiments in which rearing water was conditioned such as to manipulate the probability of mate encounter through chemical signals emitted by snails. First, a choice trial experiment showed that the exploration behaviour of individuals is sensible to chemical signals. The second experiment aimed at documenting fitness components (age at first reproduction, growth before and after reproduction, and fecundity over a three‐week period) under five treatments (20 individuals per treatment) with different water‐conditioning and access to mate. As predicted theoretically, this experiment detected the occurrence of a waiting time (11 days) and resource reallocation to growth when comparing individuals from pure water (no chemicals) and outcrossing individuals. However, the waiting time and resource reallocation to future fecundity did not increase with increasing chemical cues of conspecifics density. There is therefore no evidence that delayed selfing is plastic and adjusted according to mate encounter probability.

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.