Neuro-Endocrine Control of Reproduction in Hermaphroditic Freshwater Snails: Mechanisms and Evolution

Invertebrates are used extensively as model species to investigate neuro-endocrine processes regulating behaviors, and many of these processes may be extrapolated to vertebrates. However, when it comes to reproductive processes, many of these model species differ notably in their mode of reproduction. A point in case are simultaneously hermaphroditic molluscs. In this review I aim to achieve two things. On the one hand, I provide a comprehensive overview of the neuro-endocrine control of male and female reproductive processes in freshwater snails. Even though the focus will necessarily be on Lymnaea stagnalis, since this is the best-studied species in this respect, extensions to other species are made wherever possible. On the other hand, I will place these findings in the actual context of the whole animal, after all these are simultaneous hermaphrodites. By considering the hermaphroditic situation, I uncover a numbers of possible links between the regulation of the two reproductive systems that are present within this animal, and suggest a few possible mechanisms via which this animal can effectively switch between the two sexual roles in the flexible way that it does. Evidently, this opens up a number of new research questions and areas that explicitly integrate knowledge about behavioral decisions (e.g., mating, insemination, egg laying) and sexual selection processes (e.g., mate choice, sperm allocation) with the actual underlying neuronal and endocrine mechanisms required for these processes to act and function effectively

Disentangling female postmating responses induced by semen transfer components in a simultaneous hermaphrodite

Optimizing reproductive success is an essential part of evolution for both sexes. Females can optimize mating by avoiding superfluous mating advances and insemination, since both take time away from other activities and may incur costs related to sperm receipt. While many separate-sexed organisms are known to exhibit mate avoidance, much less is known about this for simultaneous hermaphrodites. We addressed this here, using a simultaneously hermaphroditic species that can choose to mate in either of the two sex roles during each mating interaction. Recently, avoidance behaviours in response to natural matings were observed in the hermaphroditic pond snail Lymnaea stagnalis, potentially deterring insemination. To disentangle whether such behaviours are mediated by the mechanical act of mating or the receipt of accessory gland proteins and/or sperm, we intravaginally injected individuals with control or test fluids. Our results show that the avoidance behaviours, crawl-out and biting, were more frequently expressed when individuals were inseminated with accessory gland proteins and/or sperm. These behavioural components of the recipient increased time in courtship prior to insemination, which is concordant with the hypothesis that the partner tries to discourage the potential sperm donor from inseminating. Understanding the mechanism underlying the effects that molluscan accessory gland proteins induce contributes to our understanding of the molecular basis of the recipient's (behavioural) responses as well as how such biochemical postcopulatory strategies evolve

Coolidge effect in pond snails: male motivation in a simultaneous hermaphrodite

Background. The simultaneously hermaphroditic pond snail, Lymnaea stagnalis, can mate in the male and female role, but within one copulation only one sexual role is performed at a time. Previous work has shown that male motivation is determined by the availability of seminal fluid in the prostate gland, which is detected via a nervous connection by the brain area controlling male behaviour. Based on this knowledge, patterns of sexual role alternations within mating pairs can be explained. Results. The data presented here reveal that these snails can donate and receive sperm several times within 24 hours, and that they have increased mating rates in larger groups (i.e. more mating opportunities). For mating pairs we show, by introducing novel mating partners after copulation, that animals do inseminate new partners, while they are no longer motivated to inseminate their original partners. Conclusion. Our findings provide the first direct evidence for higher motivation in a hermaphrodite to copulate when a new partner is encountered. This Coolidge effect seems to be attenuated when mucus trails are excluded, which suggests that a chemical or textural cue may be responsible for mediating this response to sperm competition. © 2007 Koene and Ter Maat; licensee BioMed Central Ltd

Allohormones and sensory traps: a fundamental difference between hermaphrodites and gonochorists

Summary Multiple mating, sperm storage and sperm digestion cause uncertainty about the fate of donated sperm. In invertebrates these are common processes and increase the selective pressure for tactics that enhance fertilization success. Hence, to assure that donated sperm will be used for their rightful purpose, many different strategies can evolve. For example, biochemical substances -such as pheromones and allohormones -can be employed to improve the chances of fertilizing the partner's eggs. Several recent examples of such substances in gonochoric and hermaphroditic invertebrates are reviewed here. Moreover, I argue that a simple but fundamental difference may exist in the evolution of allohormones between the two modes of gender expression, primarily based on the differences in gene expression between species with separate sexes and hermaphrodites. This idea suggests that a biochemical sensory trap could occur more readily in hermaphrodites, and, depending on the mode of transfer of these allohormones, this should be reflected in a different speed of allohormone evolution

Costs of receipt and donation of ejaculates in a simultaneous hermaphrodite

<p>Abstract</p> <p>Background</p> <p>Sexual conflicts between mating partners can strongly impact the evolutionary trajectories of species. This impact is determined by the balance between the costs and benefits of mating. However, due to sex-specific costs it is unclear how costs compare between males and females. Simultaneous hermaphrodites offer a unique opportunity to determine such costs, since both genders are expressed concurrently. By limiting copulation of focal individuals in pairs of pond snails (<it>Lymnaea stagnalis</it>) to either the male role or the female role, we were able to compare the fecundity of single sex individuals with paired hermaphrodites and non-copulants. Additionally, we examined the investment in sperm and seminal fluid of donors towards feminized snails and hermaphrodites.</p> <p>Results</p> <p>Compared to non-mating focal snails, reciprocating individuals as well as male and female copulants experienced a significant fecundity reduction (~40%) after, on average, 3.07 ± 0.12 copulations in their allowed roles (for donors 2.98 ± 0.16 copulations and for recipients 3.14 ± 0.12 copulations). In a single copulation, significantly more sperm was donated to partners that were restricted to mating in the female role than to hermaphrodites, while seminal fluid transfer was unaffected by recipient type.</p> <p>Conclusions</p> <p>Our data indicate that the costs of mating in both sex functions are high in <it>L. stagnalis</it>. This conclusion is based on fecundity data collected separately for male and female copulants. Male mating costs result from investment in expensive ejaculates, composed of sperm and seminal fluid. For female copulants, fecundity reduction correlated with transferred sperm numbers in the first copulation, while differences in transferred quantities of seminal fluid were not detected. These findings may point toward a "sperm effect" as a novel feature of pond snail reproductive ecology. In conclusion, sex allocation and sexual conflict both contribute to decreased female fecundity in pond snails.</p

Male Accessory Gland Protein Reduces Egg Laying in a Simultaneous Hermaphrodite

Seminal fluid is an important part of the ejaculate of internally fertilizing animals. This fluid contains substances that nourish and activate sperm for successful fertilization. Additionally, it contains components that influence female physiology to further enhance fertilization success of the sperm donor, possibly beyond the recipient's optimum. Although evidence for such substances abounds, few studies have unraveled their identities, and focus has been exclusively on separate-sex species. We present the first detailed study into the seminal fluid composition of a hermaphrodite (Lymnaea stagnalis). Eight novel peptides and proteins were identified from the seminal-fluid-producing prostate gland and tested for effects on oviposition, hatching and consumption. The gene for the protein found to suppress egg mass production, Ovipostatin, was sequenced, thereby providing the first fully-characterized seminal fluid substance in a simultaneous hermaphrodite. Thus, seminal fluid peptides and proteins have evolved and can play a crucial role in sexual selection even when the sexes are combined

The fate of received sperm in the reproductive tract of a hermaphroditic snail and its implications for fertilisation.

Multiple mating, sperm storage and internal fertilisation enhance sperm competition. The great pond snail can use stored sperm for over three months, and frequently mates with different partners. This hermaphrodite, Lymnaea stagnalis, can also self-fertilise and often produces egg masses containing both selfed and outcrossed eggs. Hence, a sperm recipient may exert considerable control over paternity. Using microsatellite markers, we show that when allosperm are present, all genotyped eggs are cross-fertilised. We also find that sperm have the opportunity to compete, because double matings lead on average to equal paternity for each sperm donor. This indicates that received sperm are randomly mixed in storage. To gain further insight into the mechanisms underlying the process of sperm storage, digestion and utilisation, we investigated the fate of donated sperm at different times after copulation. We find that within 3 h after transfer most sperm have been transported into the sperm-digesting organ. Fluorescent labelling of sperm in histological sections further reveals that allosperm are not stored in the fertilisation pouch, but upstream in either the hermaphroditic duct, seminal vesicles, or ovotestis. Besides contributing to the understanding of the mechanisms underlying sperm competition and/or cryptic sperm choice, this study shows that mixed mating cannot be treated as a separate issue in hermaphroditic animals. © Springer Science+Business Media B.V. 2008