Sex allocation and investment into pre- and post-copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition

Sex allocation theory predicts the optimal allocation to male and female reproduction in sexual organisms. In animals, most work on sex allocation has focused on species with separate sexes and our understanding of simultaneous hermaphrodites is patchier. Recent theory predicts that sex allocation in simultaneous hermaphrodites should strongly be affected by post-copulatory sexual selection, while the role of pre-copulatory sexual selection is much less clear. Here, we review sex allocation and sexual selection theory for simultaneous hermaphrodites, and identify several strong and potentially unwarranted assumptions. We then present a model that treats allocation to sexually selected traits as components of sex allocation and explore patterns of allocation when some of these assumptions are relaxed. For example, when investment into a male sexually selected trait leads to skews in sperm competition, causing local sperm competition, this is expected to lead to a reduced allocation to sperm production. We conclude that understanding the evolution of sex allocation in simultaneous hermaphrodites requires detailed knowledge of the different sexual selection processes and their relative importance. However, little is currently known quantitatively about sexual selection in simultaneous hermaphrodites, about what the underlying traits are, and about what drives and constrains their evolution. Future work should therefore aim at quantifying sexual selection and identifying the underlying traits along the pre- to post-copulatory axis.     

Sperm as a paternal investment: a model of sex allocation in sperm-digesting hermaphrodites

Some simultaneously hermaphroditic animals are known to digest received sperm. To investigate the effect of sperm digestion on the sex allocation of simultaneous hermaphrodites, we constructed models about evolutionarily stable resource allocation between male and female functions. We assumed that resource obtained from sperm digestion is used for gametogenesis (sperm and/or egg production). As a result, we found that sperm digestion increases the evolutionarily stable allocation to male function under finite number of matings. This is because excess sperm function as nuptial gift or paternal investment when at least a fraction of digested sperm is translated into eggs. Therefore, some factors which affect the assurance of paternity for sperm donors, such as cryptic female choice and/or sperm displacement, may change the result. In addition, this result implies that sperm digestion does not necessarily make male role less preferred. Further studies on the usage of donated sperm are required to test the validity of our models.     

The effects of sex ratio and density on the expression of gender in the polychaeteCapitella capitata

Summary Large natural populations of the marine polychaeteCapitella capitata (species type I) contain males, females, and occasionally, hermaphrodites. Environmental conditions control the occurrence of hermaphrodites. At low density or in groups with female-biased sex ratios, males develop into hermaphrodites, and hermaphrodites are common. Crosses suggest that females are heterogametic, and males and hermaphrodites are homogametic. Heterogametic females do not become hermaphrodites.This study shows that in homogametic individuals, environmental conditions determine not only the development of hermaphroditism but also the expression of initial gender. Homogametic individuals can express either male or female gender initially, and homogametic individuals of either gender can develop subsequently into simultaneous hermaphrodites. The choice of initial gender depends on isolation. Most homogametic juveniles become females if reared alone but males if reared with other conspecifics. Homogametic males readily develop into hermaphrodites if females are rare. In contrast, homogametic females rarely become hermaphrodites.     

Mating frequency and resource allocation to male and female function in the simultaneous hermaphrodite land snail Arianta arbustorum

Sex allocation theory predicts that mating frequency and long‐term sperm storage affect the relative allocation to male and female function in simultaneous hermaphrodites. We examined the effect of mating frequency on male and female reproductive output (number of sperm delivered and eggs deposited) and on the resources allocated to the male and female function (dry mass, nitrogen and carbon contents of spermatophores and eggs) in individuals of the simultaneous hermaphrodite land snail Arianta arbustorum. Similar numbers of sperm were delivered in successive copulations. Consequently, the total number of sperm transferred increased with increasing number of copulations. In contrast, the total number of eggs produced was not influenced by the number of copulations. Energy allocation to gamete production expressed as dry mass, nitrogen or carbon content was highly female‐biased (>95% in all estimates). With increasing number of copulations the relative nitrogen allocation to the male function increased from 1.7% (one copulation) to 4.7% (three copulations), but the overall reproductive allocation remained highly female‐biased. At the individual level, we did not find any trade‐off between male and female reproductive function. In contrast, there was a significant positive correlation between the resources allocated to the male and female function. Snails that delivered many sperm also produced a large number of eggs. This finding contradicts current theory of sex allocation in simultaneous hermaphrodites.     

Size‐dependent sex allocation in a simultaneous hermaphrodite parasite

Most models of sex allocation distinguish between sequential and simultaneous hermaphrodites, although an intermediate sexual pattern, size‐dependent sex allocation, is widespread in plants. Here we investigated sex allocation in a simultaneous hermaphrodite animal, the tapeworm Schistocephalus solidus, in which adult size is highly variable. Sex allocation was determined using stereological techniques, which allow measuring somatic and reproductive tissues in a common currency, namely volume. We investigated the relationships between individual volume and allocation to different reproductive tissues using an allometric model. One measure of female allocation, yolk gland volume, increased more than proportionally with individual volume. This is in contrast to the measure of male allocation, testis volume, which showed a strong tendency to increase less than proportionally with individual volume. Together these patterns led to sex allocation being strongly related to individual volume, with large individuals being more biased towards female allocation. We discuss these findings in the light of current ideas about size‐dependent sex allocation in, primarily, plants and try to extend them to simultaneous hermaphrodite animals.     

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.     

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.     

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.     

TESTS OF SEX ALLOCATION THEORY IN SIMULTANEOUSLY HERMAPHRODITIC ANIMALS

Sex allocation is a crucial life-history parameter in all sexual organisms. Over the last decades a body of evolutionary theory, sex allocation theory, was developed, which has yielded capital insight into the evolution of optimal sex allocation patterns and adaptive evolution in general. Most empirical work, however, has focused on species with separate sexes. Here I review sex allocation theory for simultaneous hermaphrodites and summarize over 50 empirical studies, which have aimed at evaluating this theory in a diversity of simultaneous hermaphrodites spanning nine animal phyla. These studies have yielded considerable qualitative support for several predictions of sex allocation theory, such as a female-biased sex allocation when the number of mates is limited, and a shift toward a more male-biased sex allocation with increasing numbers of mates. In contrast, many fundamental assumptions, such as the trade-off between male and female allocation, and numerous predictions, such as brooding limiting the returns from female allocation, are still poorly supported. Measuring sex allocation in simultaneously hermaphroditic animals remains experimentally demanding, which renders evaluation of more quantitative predictions a challenging task. I identify the main questions that need to be addressed and point to promising avenues for future research.     

Skewed paternity and sex allocation in hermaphroditic plants and animals

Models predict a reduced allocation to sperm when females preferentially use one of two males' sperm and the males do not know who is favoured. An analogous discounting occurs in plants when their paternity success is skewed by random, non-heritable factors such as location in the population and pollinator behaviour. We present a model that shows that skewed paternity can affect the sex allocation of hermaphrodites, that is it leads to a female-biased investment. The model highlights the close links between local mate competition and sperm competition. We use paternity data from Ficus in order to illustrate that skews in paternity success can lead to a high degree of sibling gamete competition in an apparently open breeding system. Since skews in paternity are ubiquitous in hermaphroditic plants and animals these findings should apply broadly.     

Size-dependent sex allocation and sexual selection in Aplysia kurodai, a hermaphrodite with nonreciprocal mating

Abstract. For simultaneous hermaphrodites, a male-to-female shift in sex allocation with growth, and weak sexual selection on the male function, is predicted by many theories, although empirical data for both predictions are insufficient for internally fertilizing hermaphrodites with nonreciprocal mating. To address these issues, I studied mating and egg-laying behavior of the sea hare, Aplysia kurodai (Gastropoda: Opisthobranchia) in the laboratory. Both frequency and duration of egg laying increased with body weight, indicating that fecundity increased with weight. On the other hand, frequency and duration of mating as males did not increase with body weight, suggesting that sperm usage was independent of weight. Therefore, sex allocation shifted from male to female functions with growth. The lack of a relationship between body weight and mating activities as males also suggests that there was no "female" choice for large partners. However, the frequency of mating as females increased with body weight, suggesting "male" choice for large partners. This "male" choice is further supported by the presence of size-assortative mating and a longer duration of mating when the female partner was large. In addition, the variance in mating frequency as females was larger than that as males. As a whole, the mating behavior in A. kurodai can be summarized as choosy as males and unchoosy as females, the opposite of the patterns known in most gonochoric and hermaphroditic animals.     

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.     

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.     

Phenotypically flexible sex allocation in a simultaneous hermaphrodite

Previous studies on sex allocation in simultaneous hermaphrodites have typically focused either on evolutionary or one-time, ontogenetic optimization of sex allocation, ignoring variation within an individual's lifetime. Here, we study whether hermaphrodites also possess facultative sex allocation, that is, a phenotypic flexibility, allowing them to distribute resources to either sex in an opportunistic way during their adult lifetime. We used the simultaneously hermaphroditic free-living flatworm Macrostomum lignano and raised individuals in pairs and groups of eight worms (further called octets) until sexual maturity was reached and sex allocation for the current conditions was expected to be set. Treatment groups were subsequently transferred to the alternative group size, that is, from pairs to octets or from octets to pairs, and compared to two control groups, which were transferred without changing group size. The results show that worms in treatment groups responded as expected by the local mate competition theory for simultaneous hermaphrodites: increasing group size resulted in a shift toward a more male-biased sex allocation and vice versa. These findings reveal that sex allocation in these animals is not fixed during ontogeny, but remains flexible after maturation. We argue that phenotypically flexible sex allocation in hermaphroditic animals may help us to understand the evolution and ecology of hermaphroditism.     

Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

SEX ALLOCATION AND MALE FITNESS GAIN IN A COLONIAL,HERMAPHRODITIC MARINE INVERTEBRATE

While simultaneous hermaphroditism occurs in most animal phyla, theories for its adaptive significance remain untested. Sex allocation theory predicts that combined sexes are favored in sedentary and sessile organisms because localized gamete dispersal and local mate competition (LMC) among gametes promote decelerating fitness “gain curves” that relate male investment to reproductive success. Under this LMC model, males fertilize all locally available eggs at low sperm output, additional output leads to proportionally fewer fertilizations, and combined sexes with female-biased sex allocation are favored. Decelerating male gain curves have been found in hermaphroditic flowering plants, but the present paper reports the first analysis in an animal. The colonial hermaphroditic bryozoan Celleporella hyalina forms unisexual male and female zooids that can be counted to estimate absolute and relative gender allocations. I placed “sperm donor” colonies—each with different numbers of male zooids, and each homozygous for diagnostic allozyme alleles—among target maternal colonies on field mating arrays, and estimated donor fertilization success by scoring allozyme markers in target-colony progeny. Fertilization success increased with numbers of donor male zooids, but linear and not decelerating curves fit the data best. Mean sex allocation was not female biased, consistent with nondecelerating male gain. Sperm donors, moreover, did not monopolize matings as expected under high LMC, but rather shared paternity with rival colonies. Hence localized water-borne gamete dispersal alone may not yield decelerating male gain and favor the maintenance of hermaphroditism; relaxed sperm competition in low density populations might also be required. In free-spawning marine organisms, males cannot control access to fertilizations, intense sperm competition may be commonplace, and high male sex allocation may be selected to enhance siring success under competition.     

Hermaphroditism: What's not to like?

Hermaphroditism is rare and phylogenically in decline among animal species. The evolutionary basis for this development is not well understood. This paper focusses on self-incompatible simultaneous hermaphroditism in animals. It proposes that such hermaphroditism is not stable in sufficiently heterogeneous populations, suggesting a possible reason for why hermaphroditism is rare among evolved animal species. The argument turns on the Bateman principle, namely that male reproductive success (RS) is limited by partner availability, while female RS is not. We show that: low-quality individuals do better if female; secondary sexual differentiation may be important for understanding the existence of males; and that hermaphroditic mating is reciprocal. Reciprocity may be key to understanding promiscuity and attendant phenomena such as cryptic female choice, sperm competition and love darts-common features of hermaphroditic mating. We also argue that hermaphrodites are especially vulnerable to male violence, suggesting a reason for the rarity of trioecy. Finally, we propose that external fertilization, and the scope for streaking, may be one reason fish are the only simultaneously hermaphroditic vertebrates.     

Female resistance behaviour and progeny sex ratio in two Bradysia species (Diptera: Sciaridae) with paternal genome elimination

The relationship between female mating preferences and sex allocation has received considerable theoretical and empirical support. Typically, choosier females adjust their progeny sex ratio towards sons, who inherit the attractive traits of their father. However, in species with paternal genome elimination, where male sperm do not contain the paternal genome, predictions for the direction of progeny sex ratio biases and their relationship with female choosiness are atypical. Paternal genome elimination also creates a potential for male–female conflict over sex allocation, and any influence of female mate choice on sex ratio outcomes have interesting implications for sexually antagonistic coevolution. Within the Sciaridae (Diptera) are species that produce single‐sex progeny (monogenic species) and others in which progeny comprise both sexes (digenic species). Paternal genome elimination occurs in both species. We explore female mate resistance behaviour in a monogenic and digenic species of mushroom gnat from the genus Bradysia. Our experiments confirmed our theoretical predictions, revealing that in the monogenic and digenic species, females producing female‐biased progeny were more likely to have resisted at least one mating attempt.     

Facultative sex ratio shifts by a herbivorous insect in response to variation in host plant quality

Summary We tested predictions of sex allocation theory with a series of field experiments on sex allocation in an herbivorous, haplodiploid, sawfly, Euura lasiolepis. Our experiments demonstrated the following points. 1) Adult females allocated progeny sex in response to plant growth. 2) Population sex ratios varied in response to plant quality, being male-biased where plant growth was slow and female-biased where plant growth was rapid. 3) Family sex ratios varied in response to plant quality, being male-biased on slow-growing plants and female-biased on rapidly-growing plants. 4) Female fitness increased more rapidly as the result of developing on more rapidly-growing plants than male mass. We conclude from these results that there are unequal returns on investment in male and female progeny. This results in facultatively biased sawfly sex ratios as an adaptive response to variation in plant quality.