Simultaneous Hermaphrodite Snail Research Articles

Seasonal effects on egg production and level of paternity in a natural population of a simultaneous hermaphrodite snail.

In a seasonal environment, the suitable time window for females to reproduce is restricted by both environmental conditions and the availability of males. In simultaneous hermaphrodites, which are female and male at the same time, selection on a trait that is solely beneficial for one sexual function cannot occur independently. Therefore, it is assumed that the optimal time window for reproduction is a compromise between the two sexual functions in simultaneous hermaphrodites, mediated by environmental conditions. We examined seasonal patterns of reproduction and the resulting paternity in a natural population of the simultaneously hermaphroditic land snail Arianta arbustorum. Adult and premature individuals (snails in a short protandric phase) were collected on four occasions over the entire active season. The snails were allowed to deposit eggs after which we assessed the level of paternity in their hatched offspring. Individuals mated throughout the reproductive season, whereas egg production – the major task of the female function – was restricted to the first half of the season. Snails collected in autumn were allowed to hibernate under laboratory conditions. As a result, we found that premature individuals began to mate late in the reproductive season, but did not start to produce eggs before emerging from hibernation. Our results demonstrate a temporal shift of reproductive activities; the egg production and oviposition occur mainly in the first half of the season, while sperm production and mating occur over the entire season. In subadult and adult snails, sperm obtained from several partners in the second part of the reproductive season are stored during hibernation for the fertilization of eggs in the successive years. These results extend our understanding of the influence of both natural and sexual selection on reproductive strategies in hermaphrodites.

Sperm utilization in subadult and adult simultaneous hermaphrodite snails mating in the wild

In species with multiple mating and long-term sperm storage, males are expected to show a preference for mating with virgin and young females to reduce the risk of sperm competition. In various simultaneous hermaphrodite land snail species, sperm production precedes egg production by 2–4 weeks, resulting in a short period of protandric hermaphroditism before shell growth is completed. In a natural population, we collected copulating pairs of the simultaneous hermaphrodite land snail Arianta arbustorum (L., 1758) consisting either of two adults, of two subadults, or of one adult and one subadult snail, and determined the paternity of their hatchlings that emerged from subsequently deposited eggs. Adult snails used sperm received from subadult mating partners for egg fertilization in the same frequency as sperm from adults, indicating that subadult and adult snails do not differ in male function. Furthermore, an unfinished shell is not a reliable indicator for virginity, because 35% of the subadult individuals had already sperm stored from previous mating(s). Compared with adults, young individuals exhibited a lower risk of sperm competition, indicated by a higher last mate sperm precedence. However, subadult snails produced fewer eggs than adult snails, counteracting the evolutionary advantage of preferring a young partner with low sperm competition risk.

Evidence for age-dependent mating strategies in the simultaneous hermaphrodite snail,Lymnaea stagnalis(L.)

In many mating systems female reproductive capacity is a limiting resource over which males will compete. As a consequence, males and females have usually different fitness optimization strategies which may give rise to sexual conflict. Since simultaneous hermaphrodites have, in theory, the option to mate as male or as female at any time, conflict will occur if partners insist in taking the same role. Several lines of evidence exists that body size influences gender choice. However, growth in many invertebrates is indeterminate and therefore age is generally a covariant of size. We therefore investigated the effect of age on mating choices in the simultaneous hermaphrodite Lymnaea stagnalis. Using fully sexually mature animals sampled from three different age groups we show that copulation frequency declines with age. Specifically, in age-matched couples the frequency of primary and reciprocal copulations declines with age. Furthermore, the younger partner tends to mate as male with greater probability in couples of unequal age. Size was never a factor in the sex role preference of Lymnaea. Thus, young Lymnaea always attempt to copulate as male independent of the age of their partner, whereas senior snails act primarily as female. The sex role choices of middle-aged snails appear to depend on their partner's age. In addition, we demonstrate that the likelihood that an animal will copulate as male is not correlated with prostate gland size but correlates with the level of afferent electrical activity recorded in the nerve originating in the prostate gland. Together, our results indicate the existence of an age- and not size-dependent mating system in Lymnaea.

Peptidergic modulation of male sexual behavior in Lymnaea stagnalis: structural and functional characterization of -FVamide neuropeptides.

In the simultaneous hermaphrodite snail Lymnaea stagnalis, copulation as a male is controlled by neurons that send axons to the male copulatory organs via a single penis nerve. Using direct mass spectrometry of a penis nerve sample, we show that one of the molecular ions has a mass corresponding to GAPRFVamide, previously identified from the buccal ganglia, and named Lymnaea inhibitory peptide (LIP). The identity of this peptide is confirmed by partial peptide purification from the penis nerve, followed by post source decay mass spectrometry. We cloned the LIP-encoding cDNA, which predicts a prohormone that gives rise to five copies of LIP (now re-named LIP A), two other -FVamide peptides (LIPs B and C), and five structurally unrelated peptides. The LIP gene is expressed in neurons of the right cerebral ventral lobe that send their axons into the penis nerve. We show that the LIP A peptide is present in these neurons and in the penis nerve, and confirmed the presence of LIP B and C in the penis nerve by post source decay mass spectrometry. Finally, we demonstrate that LIP A, B and C inhibit the contractions of the penis retractor muscle, thereby implicating their role in male copulation behavior.

Gender contests in a simultaneous hermaphrodite snail: a size-advantage model for behaviour

Adaptive gender expression in simultaneous hermaphrodites will reflect the relative costs and benefits of each sexual function. The net gain through either or both functions may vary with body size. Shell length measurements of Physa gyrinaand P. heterostropha in the laboratory and P. heterostropha in the field revealed that successful mating generally involved smaller sperm donors and larger recipients. In contrast, attempts by larger snails to donate sperm were contested by smaller snails. These data suggest substantial plasticity in gender expression in accordance with a game-theoretic extension of Ghiselin’s (1969, Q. Rev. Biol., 44,189–208, 1974; The Economy of Nature and the Evolution of Sex) size-advantage model. Specifically, the larger of two interacting snails is more fecund, so the smaller snail has more to gain by donating sperm. This asymmetry creates a contest in which the smaller snail can afford to escalate the contest more and still profit, so long as escalation costs are not greater for the smaller snail. In the present study, the usual form of contest escalation was a visually obvious shell-swinging display, which attracts predators. Thus, the smaller of two contestants can use the risk of predation as a weapon in contest escalations (i.e. a game of chicken), rather than using a purely physical contest that might favour the larger contestant.

Co-localized neuropeptides conopressin and ALA-PRO-GLY-TRP-NH2 have antagonistic effects on the vas deferens of Lymnaea.

We examined functional aspects of co-localization of neuropeptides involved in the regulation of male copulation behaviour in the simultaneous hermaphrodite snail Lymnaea stagnalis. The copulation behaviour is controlled by several types of peptidergic neurons that include a cluster of neurons in the anterior lobe of the right cerebral ganglion. All anterior lobe neurons express the gene encoding Ala-Pro-Gly-Trp-NH2 (APGWamide), and a subset of neurons also express the vasopressin-related conopressin gene. Immunocytochemical and peptide chemical experiments show that both APGWamide and conopressin are transported to the penis complex and the vas deferens via the penis nerve. Co-localization of the two peptides was also observed in some, but not all, axon bundles that run along the vas deferens. APGWamide and conopressin were structurally identified from the penis complex with vas deferens. Conopressin excites the vas deferens in vitro, whereas APGWamide inhibits the excitatory effects of conopressin, both in a dose-dependent fashion. We propose that the antagonistic effects of these peptides on the vas deferens underlie its peristalsis. Thus, these peptides play an important role in the control of ejaculation of semen during copulation.

Temperature-Determined Outcrossing Ability in Wild Populations of a Simultaneous Hermaphrodite Snail

Phally, a genital polymorphism found in some species of self-compatible simultaneous hermaphrodites, presents an opportunity to examine environmental and genetic influences on mating system traits. Both aphallics and euphallics can self-fertilize, but aphallics cannot donate sperm because they do not develop a functional penis and prostate. Previous studies of the freshwater gastropod Bulinus truncatus (Mollusca: Pul- monata) suggest that in at least some laboratory populations, phally is determined by temperature during egg and hatchling stages, with colder temperatures favoring the de- velopment of euphally. Here we provide evidence for temperature-influenced phally de- termination in natural populations of B. truncatus in northern Nigeria. The prevalence of euphally across 49 populations ranged from 0 to 81%. Levels of euphally increased sig- nificantly both within and across sites as temperatures decreased during the dry-cool season. Across sites, time of year (date) was the strongest single predictor of proportion of euphallics. When the effects of time of year were controlled for, there was a significant negative correlation between temperature during phally development and proportion of euphallics. In addition, maximum water temperature during the 1st wk of the study predicted pro- portions of euphallics in the next snail generation. A laboratory study of snails from three of these populations demonstrated that temperature sensitivities differed between popu- lations: one population that remained 100% aphallic over the course of field observations showed only low levels of temperature sensitivity in the laboratory, while a population that tripled in proportion of euphallics in the field showed strong levels of temperature sensitivity. Furthermore, individuals within populations varied in their temperature sen- sitivities. These results are discussed in light of the adaptive significance of labile phally determination.

Ecological Correlates of Male Outcrossing Ability in a Simultaneous Hermaphrodite Snail

Phally, a genital dimorphism found in some species of self-compatible simultaneous hermaphrodites, presents an opportunity to examine factors maintaining outcrossing within an animal species that can self-fertilize. Both aphallics and euphallics can self-fertilize, but aphailics cannot donate sperm because they do not develop a functional prostate and penis. In this field study of Nigerian populations of the freshwater gastropod, Bulinus truncatus (Mollusca: Pulmonata), we evaluate ecological correlates of euphally to test hypotheses predicting a selectire advantage of outcrossing due to the production of genetically variable offspring. The prevalence of euphally across 49 populations ranged from 0% to 81%. We found no association between prevalence of euphally and any of the following: population density, snail density, mollusk species abundance, water pH, oxidation-reduction potential, dissolved oxygen content, habitat instability (as estimated by habitat type), human activity, vegetation density, desiccation rate, and water chemistry variation. There was a significant but weak correlation between conductivity and proportion of euphallics (r2 = 10%), with lower ion concentrations favoring higher levels of euphally. The prevalence of the most abundant trematode taxon (Xiphidiocercariae) correlated positively with proportion of euphallics, explaining 10% of the variation in proportion of euphallics after we controlled for mean snail age and time of year. Trematode richness (number of taxa per population) was not associated with proportion of euphallics across sites when we controlled for time of year. However, indexes of trematode diversity that incorporated both prevalence and richness did correlate significantly with proportion of euphallics. These results are consistent with hypotheses predicting an advantage of outcrossing due to temporal fluctuations in the biotic environment.

Heritability of male outcrossing ability in the simultaneous hermaphrodite, Bulinus truncatus (Gastropoda: Planorbidae)

The heritability of phally, a dichotomous trait defined by the functional state of the male reproductive tract, was measured in a laboratory population of the simultaneous hermaphrodite snail Bulinus truncatus by means of a breeding experiment and a selection experiment. Euphallic individuals develop a fully functional male and female tract and are capable of receiving and donating sperm. In aphallic individuals the male tract does not develop fully, preventing sperm donation. There was no evidence of a heritable component to phally in the breeding experiment, but the selection experiment demonstrated a slight heritable effect. In both experiments there was more variation in the observed proportion of euphallics than expected by chance alone and no evidence of line or family effects, implicating environmental determination of male outcrossing ability even under controlled laboratory conditions. Previous studies of populations of B. truncatus reported that the proportion of euphallics was under strong genetic control. We suggest that there may be population differences in the extent of environmental control over phally, analogous to that reported for sex determination.

The Cost of Mating

The Cost of Mating