Joris M. Koene

Shooting darts: co-evolution and counter-adaptation in hermaphroditic snails

BackgroundEvolutionary conflicts of interest between the sexes often lead to co-evolutionary arms races consisting of repeated arisal of traits advantageous for one sex but harmful to the other sex, and counter-adaptations by the latter. In hermaphrodites, these antagonistic interactions are at least an equally important driving force. Here, we investigate the evolution of one of the most striking examples of sexual conflict in hermaphrodites, the so-called shooting of love-darts in land snails. Stabbing this calcareous dart through the partners skin ultimately increases paternity. This trait is obviously beneficial for the shooter, but it manipulates sperm storage in the receiver. Hence, an arms race between the love-dart and the spermatophore receiving organs may be expected.ResultsWe performed a detailed phylogenetic analysis of 28S ribosomal RNA gene sequences from dart-possessing land snail species. Both the Shimodaira-Hasegawa test and Bayesian posterior probabilities rejected a monophyletic origin of most reproductive structures, including the love-dart, indicating that most traits arose repeatedly. Based on the inferred phylogenetic trees, we calculated phylogenetically independent contrasts for the different reproductive traits. Subsequent principal component and correlation analyses demonstrated that these contrasts covary, meaning that correlated evolution of these traits occurred.ConclusionOur study represents the first comprehensive comparative analysis of reproductive organ characteristics in simultaneous hermaphrodites. Moreover, it strongly suggests that co-evolutionary arms races can result from sexual conflict in these organisms and play a key role in the evolution of hermaphroditic mating systems.

PATTERNS OF MATING-SYSTEM EVOLUTION IN HERMAPHRODITIC ANIMALS: CORRELATIONS AMONG SELFING RATE, INBREEDING DEPRESSION, AND THE TIMING OF REPRODUCTION

In hermaphrodites, traits that influence the selfing rate can coevolve with inbreeding depression, leading to the emergence of evolutionary syndromes. Theory predicts a negative correlation between inbreeding depression and selfing rate across species. This prediction has only been examined and validated in vascular plants. Furthermore, selfing rates are often influenced by environmental conditions (e.g., lack of mates or pollinators), and species are predicted to evolve mechanisms to buffer this variation. We extend previous studies of mating‐system syndromes in two ways. First, we assembled a new dataset on Basommatophoran snails (17 species, including new data on 12 species). Second, we measured how species responded to variation in mate availability. Specifically, we quantified the waiting time before selfing (i.e., how long the onset of reproduction is delayed in the absence of mates). Selfing rates were negatively correlated with both inbreeding depression and the waiting time. Species with stronger inbreeding depression exhibited longer waiting times. These patterns obtained on Basommatophorans still hold when including eight other hermaphroditic animals. Our results support the hypothesis that selection drives the evolution of mating‐system syndromes in animals. The reaction norm of selfing rates to mate availability is a key target of natural selection in this context.

Bateman Gradients in Hermaphrodites: An Extended Approach to Quantify Sexual Selection

Sexual selection is often quantified using Bateman gradients, which represent sex‐specific regression slopes of reproductive success on mating success and thus describe the expected fitness returns from mating more often. Although the analytical framework for Bateman gradients aimed at covering all sexual systems, empirical studies are biased toward separate‐sex organisms, probably because important characteristics of other systems remain incompletely treated. Our synthesis complements the existing Bateman gradient approach with three essential reproductive features of simultaneous hermaphrodites. First, mating in one sex may affect fitness via the opposite sex, for example, through energetic trade‐offs. We integrate cross‐sex selection effects and show how they help characterizing sexually mutualistic versus antagonistic selection. Second, male and female mating successes may be correlated, complicating the interpretation of Bateman gradients. We show how to quantify the impact of this correlation on sexual selection and propose a principal component analysis on male and female mating success to facilitate interpretation. Third, self‐fertilization is accounted for by adding selfed progeny as a separate category of reproductive success to analyses of Bateman gradients. Finally, using a worked example from the snail Biomphalaria glabrata, we illustrate how the extended analytical framework can enhance our understanding of sexual selection in hermaphroditic animals and plants.

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

BackgroundThe 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.ResultsThe 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.ConclusionOur 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.

Sexual selection favors harmful mating in hermaphrodites more than in gonochorists

Hermaphroditic animals often exhibit mating mechanisms that seem more damaging than those in species with separate sexes. Our analyses indicate that this difference is real. While females only remate when the benefit is positive, hermaphrodites remate even when this implies losing female fitness. This occurs because hermaphrodites can outweigh losses in the female function by gaining paternity. In an extended model we ask whether this favors the evolution of more male harm in hermaphrodites. When male harm only suppresses remating in the receiver it neither evolves in hermaphrodites nor in gonochorists. However, when male harm is coupled to a fertilization advantage, it evolves in both forms of gender expression with the highest levels in hermaphrodites. Hence, hermaphrodites are more prone to be caught in costly escalations than gonochorists. We discuss the implications for the evolution of gender expression in animals and plants.

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 recipients 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.

How does breeding system variation modulate sexual antagonism

The study of sexually antagonistic (SA) traits remains largely limited to dioecious (separate sex), mobile animals. However, the occurrence of sexual conflict is restricted neither by breeding system (the mode of sexual reproduction, e.g. dioecy or hermaphroditism) nor by sessility. Here, we synthesize how variation in breeding system can affect the evolution and expression of intra- and inter-locus sexual conflicts in plants and animals. We predict that, in hermaphrodites, SA traits will (i) display lower levels of polymorphism; (ii) respond more quickly to selection; and (iii) involve unique forms of interlocus conflict over sex allocation, mating roles and selfing rates. Explicit modelling and empirical tests in a broader range of breeding systems are necessary to obtain a general understanding of the evolution of SA traits.

Piercing the partner's skin influences sperm uptake in the earthworm Lumbricus terrestris

Sexual conflict between mating partners can give rise to strategies that are advantageous for one sex but harmful to the opposite sex. Usually, sperm donors develop (offensive) traits to enhance their chances in sperm competition, while sperm recipients evolve (defensive) traits that allow them to stay in control of who fathers their offspring. Here, we demonstrate that these processes are also at work in simultaneous hermaphrodites. The hermaphroditic earthworm Lumbricus terrestris uses 40 to 44 copulatory setae to pierce into its partners skin, causing damage and injecting a substance from its setal glands. Experimental injection of the gland substance indicates that a refractory period may be induced. More importantly, removal of the copulatory setae shows that they influence the partners sperm uptake. When the setae are present, more sperm are taken up and sperm are distributed more equally over the four spermathecae. We interpret this as a strategy that stacks the odds for the donors sperm in fertilizing cocoons.

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.

Tales of two snails: sexual selection and sexual conflict in Lymnaea stagnalis and Helix aspersa.

Sexual selection and sexual conflict have been shown to play key roles in the evolution of species with separate sexes. Experimental evidence is accumulating that this is also true for simultaneous hermaphrodites. For example, many species of land snails forcefully stab their mating partners with love darts. In the brown garden snail (Helix aspersa, now called Cantareus asperses), this dart increases sperm storage and paternity, probably via the transfer of an allohormone that inhibits sperm digestion. A recent interspecies comparison of dart-possessing land snails revealed coevolution between darts and spermatophore-receiving organs that is consistent with counteradaptation against an allohormonal manipulation. The great pond snail (Lymnaea stagnalis) seems to use a seminal product to manipulate its partner and mates in the male role when enough seminal fluid is available in the prostate gland. Receipt of semen not only initiates egg laying in virgin animals, but also feminizes the mating partner later in life. These increases in the female function have been shown to go at the expense of growth and seminal fluid production of the sperm recipient. Although in Helix, and probably also Lymnaea, the sperm donor benefits from the induced changes through increased fertilization success, the sperm recipient may experience injury, imposed reallocation of resources, and altered sperm storage. These findings support the existence of sexual conflict in simultaneously hermaphroditic snails, and its importance for the evolution of mating behaviors and reproductive morphologies is discussed.