Sex allocation in a simultaneously hermaphroditic marine shrimp

Two fundamental questions dealing with simultaneous hermaphrodites are how resources are optimally allocated to the male and female function and what conditions determine shifts in optimal sex allocation with age or size. In this study, I explored multiple factors that theoretically affect fitness gain curves (that depict the relationship between sex-specific investment and fitness gains) to predict and test the overall and size-dependent sex allocation in a simultaneously hermaphroditic brooding shrimp with an early male phase. In Lysmata wurdemanni, sperm competition is absent as hermaphrodites reproducing in the female role invariably mated only once with a single other shrimp. Shrimps acting as females preferred small over large shrimps as male mating partners, male mating ability was greater for small compared to large hermaphrodites, and adolescent males were predominant in the population during the breeding season. In addition, brooding constraints were not severe and varied linearly with body size whereas the ability to acquire resources increased markedly with body size. Using sex allocation theory as a framework, the findings above permitted to infer the shape of the male and female fitness gain curves for the hermaphrodites. The absence of sperm competition and the almost unconstrained brooding capacity imply that both curves saturate, however the male curve levels off much more quickly than the female curve with increasing level of investment. In turn, the predominance of adolescent males in the population implies that the absolute gain of the female curve is greater than that of the male curve. Last, the size-dependent female preference and male mating ability of hermaphrodites determines that the absolute gain of the male curve is greater for small than for large hermaphrodites. Taking into consideration the inferred shape of the fitness gain curves, two predictions with respect to the optimal sex allocation were formulated. First, overall sex allocation should be female biased; it permits hermaphrodites to profit from the female function that provides a greater fitness return than the male function. Second, sex allocation should be size-dependent with smaller hermaphrodites allocating more than proportionally resources to male reproduction than larger ones. This size-dependent sex allocation permits hermaphrodites to profit from male mating opportunities that are the greatest at small body sizes. Size-dependent sex allocation is also expected because the male fitness gain curve decelerates more quickly than the female gain curve and experiments indicated that resources are greater for large than small hermaphrodites. These two predictions were tested when determining the sex allocation of hermaphrodites by dissecting their gonad and quantifying ovaries versus testes mass. Supporting the predictions above, hermaphrodites allocated, on average, 118 times more to the female than to the male gonad and the proportion of resources devoted to male function was higher in small than in large hermaphrodites. A trade-off between male and female allocation is assumed by theory but no negative correlation between male and female reproductive investment was observed. In L. wurdemanni, the relationship between sex-specific investment and fitness changes during ontogeny in a way that is consistent with an adjustment of sex allocation to improve size-specific reproductive success.     

Different effects of mating group size as male and as female on sex allocation in a simultaneous hermaphrodite

Sex allocation theory predicts that the optimal sexual resource allocation of simultaneous hermaphrodites is affected by mating group size (MGS). Although the original concept assumes that the MGS does not differ between male and female functions, the MGS in the male function (MGSm; i.e., the number of sperm recipients the focal individual can deliver its sperm to plus one) and that in the female function (MGSf; the number of sperm donors plus one) do not always coincide and may differently affect the optimal sex allocation. Moreover, reproductive costs can be split into “variable” (e.g., sperm and eggs) and “fixed” (e.g., genitalia) costs, but these have been seldom distinguished in empirical studies. We examined the effects of MGSm and MGSf on the fixed and variable reproductive investments in the sessilian barnacle Balanus rostratus. The results showed that MGSm had a positive effect on sex allocation, whereas MGSf had a nearly significant negative effect. Moreover, the “fixed” cost varied with body size and both aspects of MGS. We argue that the two aspects of MGS should be distinguished for organisms with unilateral mating.     

Variation in reproductive success and gonadal allocation in the simultaneous hermaphrodite,Serranus fasciatus

Summary This paper examines the correlates of individual size, reproductive success, gonadal allocation, and growth in a hermaphroditic reef fish. Individuals in S. fasciatus mature as simultaneous hermaphrodites; large individuals subsequently lose female function and become functional males. Daily female reproductive success was highly correlated with both hermaphrodite size and amount of female gonadal tissue. Three separate comparisons gave a positive correlation between male reproductive success and male gonadal allocation: (1) Males had higher levels of male gonadal allocation and male reproductive success than hermaphrodites. (2) The percent of gonad allocated to male tissue in hermaphrodites was higher in the year they had higher male mating success. (3) Male gonadal tissue of hermaphrodites was positively correlated with male reproductive success in the year that male reproductive success by hermaphrodites was higher and more variable. There was no evidence for a trade-off between male function, female function, and growth among hermaphrodites. Many of these patterns have also been observed in plants, but the selective pressures leading to these patterns in S. fasciatus and plants are probably quite different.     

Sexual selection and reproductive success in hermaphroditic seabasses

Mating behavior in simultaneously hermaphroditic seabasses hasbeen often cited as an example of cooperation among unrelatedconspecifics. The predominant mating behavior in this groupinvolves egg trading, where individuals reciprocally fertilizeparcels of eggs from a partner. Egg trading has been suggestedas a good example of a tit-for-tat cooperative mating strategy.Although simultaneous hermaphroditic fishes are often held upas strong examples of cooperation in mating behavior, a closerexamination reveals significant sexual selection and sexualconflict between male and female roles among individuals. Inthe 7 species where data exist, there is a significant increasein male reproductive success with individual size, and in allbut 1 species success through male function increases fasterthan reproductive success through female function. Despite thismale-size advantage in simultaneous hermaphrodites, most speciesmaintain their hermaphroditism for their entire life, and theincreased male allocation while engaging in biased forms ofreciprocation appear to increase the evolutionary stabilityof hermaphroditism in these species. Thus, egg-trading behavioris probably more complicated than was initially recognized,with individuals releasing different numbers of eggs in spawns,spawning at different rates as males and females, and partitioningmale effort between pair and alternative mating tactics. Thedepartures from equal reciprocity can probably be best understoodby including aspects of traditional mating-system theory, withindividuals increasing male mating success through a varietyof behavioral tactics.     

Social status and availability of females determine patterns of sperm allocation in the fowl

Where sperm competition occurs, the number and quality of sperm males inseminate relative to rival males influences fertilization success. The number of sperm males produce, however, is limited, and theoretically males should allocate sperm according to the probability of gaining future reproductive opportunities and the reproductive benefits associated with copulations. However, the reproductive opportunities and value of copulations males obtain can change over their lifetime, but whether individuals respond to such changes by adjusting the way they allocate sperm is unclear. Here we show that, in the fowl, Gallus gallus, dominant males, which have preferential access to females, modulate the number of sperm they ejaculate according to the availability of females. When presented with two females, dominant males allocated more sperm to higher quality females, whereas when females were on their own, only copulation order had an affect on their sperm numbers. In contrast, subordinate males, whose mating activity is restricted by dominant males, allocated high numbers of sperm to initial copulations, irrespective of female availability. We further show, by manipulating male social status, that sperm allocation is both phenotypically plastic, with males adjusting their patterns of sperm allocation according to their dominance rank, and intrinsic, with males being consistently different in the way they allocate sperm, once the effects of social status are taken into account. This study suggests that males have evolved sophisticated patterns of sperm allocation to respond to frequent fluctuations in the value and frequency of reproductive opportunities.     

Mating Behaviour of the Sperm Trading Sea Slug Chelidonura hirundinina: Repeated Sex Role Alternation Balances Reciprocity

In animals with separate sexes, male fitness usually increases with the number of matings, whereas female fitness more directly depends on the amount of accessible reproductive resources. In simultaneous hermaphrodites, such differences in fitness pay‐offs between male and female sexual function can result in a preference to copulate in one particular sex role, generating conflicts over mating roles if mates share the same preference. Sperm trading, i.e. the conditional exchange of sperm between mates as found in some hermaphrodites, is often considered a possible solution for the conflict over mating roles. Conditional sperm exchange has recently been demonstrated in Chelidonura hirundinina (Opisthobranchia, Aglajidae), but its functional causes remain obscure. Based on a detailed characterization of mating in this species, we here assess two potential benefits of sperm trading, the balancing of sperm exchange between partners, and the acquisition of information about the partner’s fecundity. We found that the number of sperm droplets exchanged between partners varied more between than within pairs, supporting the first hypothesis. Moreover, larger individuals donated more sperm droplets and are known to produce more eggs. As body size is tightly linked to fecundity, a sperm recipient may use the number of received sperm droplets as an honest signal of the female quality of the sperm donor. Our findings thus help to elucidate how sperm trading may contribute to optimizing the investment of costly sperm in response to partner quality.     

The effect of cryptic female choice on sex allocation in simultaneous hermaphrodites

Sex allocation theory for simultaneous hermaphrodites has focused primarily on the effects of sperm competition, but the role of mate choice has so far been neglected. We present a model to study the coevolution of cryptic female choice and sex allocation in simultaneous hermaphrodites. We show that the mechanism of cryptic female choice has a strong effect on the evolutionary outcome: if individuals remove a fixed proportion of less-preferred sperm, the optimal sex allocation is more female biased (i.e. more biased towards egg production) than without cryptic female choice; conversely, if a fixed amount of sperm is removed, sex allocation is less female-biased than without cryptic female choice, and can easily become male biased (i.e. biased towards sperm production). Under male-biased sex allocation, hermaphroditism can become unstable and the population can split into pure males and hermaphrodites with a female-biased allocation. We discuss the idea that the evolution of sex allocation may depend on the outcome of sexual conflict over the fate of received sperm: the sperm donor may attempt to manipulate or by-pass cryptic female choice and the sperm recipient is expected to resist such manipulation. We conclude that cryptic female choice can have a strong influence on sex allocation in simultaneous hermaphrodites and strongly encourage empirical work on this question.     

Life history and sex allocation in the simultaneously hermaphroditic polychaete worm Ophryotrocha diadema: the role of sperm competition

Sex allocation theory predicts that, in hermaphroditic organisms,individuals allocate a fixed amount of resources divided amongmale and female functions to reproduction and that the proportiondevoted to each sex depends on the mating group size. As themating group size increases, hermaphrodites are predicted toallocate proportionally more resources to the male and lessresources to the female function (approaching equal allocationto both sexes) to face increased sperm competition. Up to nowlittle experimental evidence has been provided to support thetheory in hermaphroditic animals. Facultative shift betweenmale and female allocation in response to variation in localgroup size does occur in several taxa but not always in theexpected direction and not with similar patterns. In the protandricand then simultaneously hermaphroditic polychaete worm Ophryotrochadiadema reproductive resources are flexibly allocated in theprotandrous and the hermaphroditic phase. The cost of male reproductionduring adolescence is spread over the whole energy budget ofthe animal as shown by the shortening of lifespan and the loweringof growth rate in individuals with enhanced male expenditureduring the protandrous phase. Moreover, in this species, shortterm sex allocation adjustments differ from those describedin other taxa. Individuals regulate their reproductive outputso that where reproductive competitors are present, the numberof female gametes is strongly reduced but the number of malegametes (although it changes) is not significantly increased.Resources subtracted from the female function are not directlyallocated to sperm production, but to expensive male behaviorsthat are likely to enhance male reproductive success. Theseresults are discussed in the light of the relevance of sexualselection in large populations of hermaphrodites.     

Cryptic male choice: sperm allocation strategies when female quality varies

We examined evolutionary stable sperm allocation and included stochastic variation in male mating frequency, not included in previous models examining sperm allocation strategies. We assumed sperm mixing and variation in female quality and used a genetic algorithm to analyse the evolution of male sperm allocation. Our results show that males should invest more sperm in initial copulations than in subsequent copulations as a male might fail to mate again. The inclusion of variation in female fecundity had no influence on the evolutionary stable sperm allocation strategy if males were unable to recognize female quality. If males were assumed to allocate sperm in response to female quality, the proportion of sperm allocated was positively correlated with female quality. Moreover, with increasing variance in female quality, males conserved more sperm for later copulations. Literature data on sperm allocation from diverse taxa show a good fit with the predictions given by our model.     

Reproductive costs of mating with a sibling male: sperm depletion and multiple mating in Cephalonomia hyalinipennis

Polygynous parasitoid males may be limited by the amount of sperm they can transmit to females, which in turn may become sperm limited. In this study, I tested the effect of male mating history on copula duration, female fecundity, and offspring sex ratio, and the likelihood that females will have multiple mates, in the gregarious parasitoid Cephalonomia hyalinipennis Ashmead (Hymenoptera: Bethylidae: Epyrinae), a likely candidate for sperm depletion due to its local mate competition system. Males were eager to mate with the seven females presented in rapid succession. Copula duration did not differ with male mating history, but latency before a first mating was significantly longer than before consecutive matings. Male mating history had no bearing on female fecundity (number of offspring), but significantly influenced offspring sex ratio. The last female to mate with a given male produced significantly more male offspring than the first one, and eventually became sperm depleted. In contrast, the offspring sex ratio of first‐mated females was female biased, denoting a high degree of sex allocation control. Once‐mated females, whether sperm‐depleted or not, accepted a second mating after a period of oviposition. Sperm‐depleted females resumed production of fertilized eggs after a second mating. Young, recently mated females also accepted a second mating, but extended in‐copula courtship was observed. Carrying out multiple matings in this species thus seems to reduce the cost of being constrained to produce only haploid males after accepting copulation with a sperm‐depleted male. I discuss the reproductive fitness costs that females experience when mating solely with their sibling males and the reproductive fitness gain of males that persist in mating, even when almost sperm‐depleted. Behavioural observations support the hypothesis that females monitor their sperm stock. It is concluded that C. hyalinipennis is a species with a partial local mating system.     

Mating strategy in Aleochara bilineata: sperm storage and allocation

Abstract By contrast to females that can maximize reproductive success with only one or a few copulations, males generally increase their fitness with frequency of mating. Sperm storage and allocation is therefore crucial for both male and female fitness. Sperm storage in Aleochara bilineata (Coleoptera; Staphylinidae) is investigated by measuring the number of spermatozoa stored in the female spermatheca after single, double or triple successive copulations with different males. The potential advantages of polyandry are studied in terms of the number of sperm stored by females mated twice with the same male (i.e. repeated copulation), compared with females mated twice with two different virgin males (i.e. polyandry). Level of polygyny is also estimated by measuring sperm allocation when ten successive mates are offered to a virgin male. Aleochara bilineata females store the sperm of the same or different males additively, suggesting no advantage for polyandry in terms of the number of sperm stored. A virgin male is able to inseminate ten different females but the number of sperm transferred decreases linearly. Finally, the latencies and durations of copulations are measured in all experiments to estimate changes according to the male or female status (i.e. virgin or mated). The latency before mating is higher when females are virgin than when females have already mated.     

Differential sperm expenditure reveals a possible role for post‐copulatory sexual selection in a lekking moth

Male reproductive success in the lesser wax moth Achroia grisella is strongly determined by pre‐copulatory mate choice, during which females choose among males aggregated in small leks based on the attractiveness of ultrasonic songs. Nothing is known about the potential of post‐copulatory mechanisms to affect male reproductive success. However, there is evidence that females at least occasionally remate with a second male and that males are unable to produce ejaculates quickly after a previous copulation. Here we investigated the effects of mating history on ejaculate size and demonstrate that the number of transferred sperm significantly decreased from first (i.e., virgin) to second (i.e., nonvirgin) copulation within individual males. For males of identical age, the number of sperm transferred was higher in virgin than in nonvirgin copulations, too, demonstrating that mating history, is responsible for the decrease in sperm numbers transferred and not the concomitant age difference. Furthermore, the number of transferred sperm was significantly repeatable within males. The demonstrated variation in ejaculate size both between subsequent copulations as well as among individuals suggests that there is allocation of a possibly limited amount of sperm. Because female fecundity is not limited by sperm availability in this system, post‐copulatory mechanisms, in particular sperm competition, may play a previously underappreciated role in the lesser wax moth mating system.     

Multiple paternity and mate competition in non-selfing,monogamous, egg-trading hermaphrodites

In animals in which the two sexes invest relatively similar amounts of resources in their young, the number of mates is expected to affect male and female reproductive success similarly and gender conflicts on the number of mates may not arise. Correspondingly, in non-selfing, simultaneous hermaphrodites with long-term monogamy, the two partners are expected to alternate repeatedly their sexual roles and invest similarly in their offspring. Therefore, the gender conflict on the number of mating partners should not arise. However, when >2 conspecifics are present, hermaphrodites are known to plastically adjust their behavior and sex allocation and compete for mating repeatedly in the male role. We tested whether this leads to multiple paternities of single egg clutches in experimental replicates of small and large groups of non-selfing, egg-trading, behaviorally monogamous polychaete worms (Ophryotrocha diadema) by using neutral genetic markers to estimate paternity. Multiply fertilized egg cocoons were common in these worms; two or more individuals succeeded in fertilizing the same egg cocoon and mate competition increased with group size. Multiply fertilized egg cocoons had a higher proportion of eggs developing into mature worms than singly fertilized egg cocoons. Possibly singly fertilized cocoons had a lower fertilization rate owing to low sperm counts and aflagellate sperm.     

Influence of male mating history on female reproductive success among monandrous Naryciinae (Lepidoptera: Psychidae)

1. Multiple male copulations can have detrimental effects on female fitness due to sperm limitation. 2. Monandrous Naryciinae females are immobile while the males are short‐lived and do not feed. Multiple male mating is therefore expected to lead to sperm limitation in females. Sperm limitation and male limitation are hypothesised as causes of the repeated evolution of parthenogenetic reproduction in the Psychidae. 3. In this study, the effects of multiple male mating on female reproduction are investigated in several species of Naryciinae by allowing males multiple copulations. The results for two species, Siederia listerella and Dahlica lichenella, are compared. The sex ratios of 53 natural populations are examined for indications of male limitation. 4. Previous copulations by the male increased the female's risk of remaining unfertilised. However, contrary to expectations, those unfertilised females were capable of successful re‐mating. 5. In S. listerella, the number of previous copulations of males negatively influenced female fitness. Females produced 30% fewer offspring if they mated with a previously mated male. In D. lichenella, the older the male and the lower its number of total lifetime copulations, the higher the female's reproductive success. 6. Only a fraction of the investigated populations had a female‐skewed sex ratio, but differences in development time between males and females could lead to reproductive asynchrony. 7. In conclusion, male mating history did not lead to strong sperm limitation in Naryciinae as had been suggested by their life history.     

Determinants of mating and sperm‐transfer success in a simultaneous hermaphrodite

The number of mating partners an individual has within a population is a crucial parameter in sex allocation theory for simultaneous hermaphrodites because it is predicted to be one of the main parameters influencing sex allocation. However, little is known about the factors that determine the number of mates in simultaneous hermaphrodites. Furthermore, in order to understand the benefits obtained by resource allocation into the male function it is important to identify the factors that predict sperm‐transfer success, i.e. the number of sperm a donor manages to store in a mate. In this study we experimentally tested how social group size (i.e. the number of all potential mates within a population) and density affect the number of mates and sperm‐transfer success in the outcrossing hermaphroditic flatworm Macrostomum lignano. In addition, we assessed whether these parameters covary with morphological traits, such as body size, testis size and genital morphology. For this we used a method, which allows tracking sperm of a labelled donor in an unlabelled mate. We found considerable variation in the number of mates and sperm‐transfer success between individuals. The number of mates increased with social group size, and was higher in worms with larger testes, but there was no effect of density. Similarly, sperm‐transfer success was affected by social group size and testis size, but in addition this parameter was influenced by genital morphology. Our study demonstrates for the first time that the social context and the morphology of sperm donors are important predictors of the number of mates and sperm‐transfer success in a simultaneous hermaphrodite. Based on these findings, we hypothesize that sex allocation influences the mating behaviour and outcome of sperm competition.     

Strategic Ejaculation in the Black Scavenger Fly Sepsis cynipsea Revisited: Copula Duration as a Function of Sperm Depletion and Body Size

The massive numbers of sperm males transfer during a single mating are physiologically costly and the amount of sperm that can be stored is limited. Therefore, males can perform only a finite number of successive copulations without loss of fertility, and males should allocate sperm prudently. We investigated sperm availability and depletion in male black scavenger flies, Sepsis cynipsea (Diptera: Sepsidae), asking whether males adjust copula duration according to nutrition, their sperm stores, their own and their partner’s body size, as predicted by theory. We created a gradient of sperm limitation by restricting dung (their protein resource as adults) and subjecting males to a varying number of copulations. While male fertility did not depend on access to fresh dung (contrary to females), it did decline after three copulations, and more so when males were small. Larger females tended to lay more unfertilized eggs after copulating with previously mated males. However, copula duration was not influenced by a male’s number of previous copulations, and therefore apparently not by his current sperm stores. Nevertheless, copula duration varied with male size, with small males copulating longer, and with female size, as copulations lasted longer with larger females, suggesting that males are investing more sperm in larger, more fecund females. While male copula adjustments to their own nutrition and body size may be simple (proximate) physiological responses, responses to female size indicate more strategic and sophisticated sperm‐allocation strategies than previously thought.     

Modern Portfolio Theory and the prudent hermaphrodite

Summary

Employment of Markowitz's Modern Portfolio Theory, economic models designed to predict the effect of variance and covariance on optimal investment allocation, may explain a wide variety of anomalies in reproductive biology. Natural selection appears to favor genetic diversity among offspring to a greater extent than is predicted by current theory. Consideration of the possible increase in fitness by reducing the covariance among offspring may help explain a variety of phenomena from multiple mating to the evolution of recombination (i.e., overcoming “the cost of meiosis”). Modern Portfolio Theory also make novel predictions as to when hermaphrodites should prefer the male vs. female role, i.e., engage in egg- vs. sperm-trading. It predicts that the sexual role with the lower variance in reproductive success will be preferred in hermaphrodites. This contradicts Bateman's principle that the male role is usually preferred due to energetic considerations but is consistent with Gillespie's principle. The available data suggest that mating hermaphrodites are risk-averse; gamete-trading whether of eggs or sperm is a strategy to reduce risk. In addition to overall variance, the skew of the distribution can be used to predict the mating systems of hermaphrodites and thus clarify the factors that are responsible for observed patterns of sex allocation and sexual conflict. The reduction of covariance among offspring may also help resolve “Williams' paradox”; that the observed distribution of dieoecy vs. simultaneous hermaphroditism in the Animal Kingdom cannot be explained by the prevailing models of the evolution of hermaphroditism.     

INTRASPECIFIC VARIATION IN SEX ALLOCATION IN A SIMULTANEOUS HERMAPHRODITE: THE EFFECT OF INDIVIDUAL SIZE

Within a population of simultaneous hermaphrodites, individuals may vary in both their current reproductive investment (biomass invested in gonads) and in how they allocate that investment between male and female function. In the chalk bass, Serranus tortugarum, estimates of both reproductive allocation and reproductive success as a male and a female can be made for individuals of different sizes. As individuals increase in size, their investment in gamete production increases, and there is a shift in allocation to a stronger female bias. Spawning frequency as a female in pair spawnings and as a male in both pair spawning and streaking (an alternative mating tactic) does not vary with individual size. As a result, larger individuals should release more sperm or eggs per spawn. Size-assortative pair spawning in this species leads to larger individuals having higher potential returns in total male reproductive success than smaller individuals, which should lead to increases in absolute levels of sperm production in larger individuals when individuals compete for fertilizations through sperm competition. However, smaller individuals contribute a smaller proportion of the sperm released in spawns with multiple spawners and thus are under more intense sperm competition than larger individuals, which should select for increases in male allocation in smaller individuals, all else equal. A local-mate-competition (LMC) model predicts that these factors select for increasing absolute male and female investment with individual size but a relative shift to more female-biased allocation as individual size increases. These predictions are supported by gonadal data. The predictions of average male allocation from the quantitative LMC model were 21.6% and 25.7%, whereas the collections averaged 21.3%. This close agreement of both the mean male allocation and its relative shift with individual size between model and data support the hypothesis that size-specific shifts in sex allocation in this species represent an adaptive response to patterns of mating success and sperm competition.     

Female sperm use and storage between fertilization events drive sperm competition and male ejaculate allocation

Sperm competition theory has traditionally focused on how male allocation responds to female promiscuity, when males compete to fertilize a single clutch of eggs. Here, we develop a model to ask how female sperm use and storage across consecutive reproductive events affect male ejaculate allocation and patterns of mating and paternity. In our model, sperm use (a single parameter under female control) is the main determinant of sperm competition, which alters the effect of female promiscuity on male success and, ultimately, male reproductive allocation. Our theory reproduces the general pattern predicted by existing theory that increased sperm competition favors increased allocation to ejaculates. However, our model predicts a negative correlation between male ejaculate allocation and female promiscuity, challenging the generality of a prevailing expectation of sperm competition theory. Early models assumed that the energetic costs of precopulatory competition and the level of sperm competition are both determined by female promiscuity, which leads to an assumed covariation between these two processes. By modeling precopulatory costs and sperm competition independently, our theoretical framework allows us to examine how male allocation should respond independently to variation in sperm competition and energetic trade‐offs in mating systems that have been overlooked in the past.     

No Plastic Responses to Experimental Manipulation of Sperm Competition per se in a Free‐Living Flatworm

In the absence of sperm competition evolutionary theory predicts low mating rates and low ejaculate expenditure per mating, and sex allocation theory for simultaneous hermaphrodites predicts a strongly female‐biased sex allocation. In the presence of sperm competition a shift towards a more male‐biased sex allocation and a higher ejaculate expenditure are predicted. The free‐living flatworm Macrostomum lignano has been shown to respond plastically in mating rate, testis size, and sperm transfer to manipulation of the social group size, a proxy of the strength of sperm competition. However, manipulation of social group size may manipulate not only sperm competition, but also other factors, such as food supply and metabolite concentration. In this study we therefore manipulated sperm competition per se by repeatedly exposing individuals to partners that have either mated with rivals or not, while keeping the social group size constant. Our results suggest that M. lignano does not have the ability to detect sperm competition per se, as worms experimentally exposed to the presence or absence of sperm competition did not differ in sex allocation, sperm transfer or mating behavior. A response to our manipulation would have required individual recognition, the ability to detect self‐referencing tags, or tags or traces left by rivals on or in the mating partners. We first discuss the possibility that highly efficient sperm displacement may have decreased the difference between the treatment groups and then propose three alternative cues that may allow M. lignano to respond plastically to the social group size manipulation used in earlier studies: assessment of the mating rate, chemical cues, or tactile cues.