Reproductive behavior,egg trading,and correlates of male mating success in the simultaneous hermaphrodite,Serranus tabacarius

Synopsis Serranus tabacarius (Serranidae), the tobaccofish, is a simultaneous hermaphrodite which belongs to a group of seabasses that exhibit a wide variety of social and mating systems. The reproductive behavior of tobaccofish is similar to other hermaphroditic seabasses, with individuals assuming sex-specific spawning behaviors that allow for the assignment of male and female roles in a mating sequence. Virtually all matings involved pairs of individuals, although streaking, an alternative male mating tactic, was observed once. Pairs engage in egg trading, where individuals divide their daily clutch into a series of sequentially released parcels and take turns releasing eggs for their partner to fertilize. Individuals mate over a late afternoon spawning period with a number of partners sequentially. Larger individuals have both more total matings and more spawning partners. Egg trading is not symmetrical, the number of male and female matings for an individual in a spawning sequence is often unequal. Overall, the ratio of male to female matings increases with individual size. Large individuals are socially dominant, chase conspecifics during the reproductive period, and are more likely to end a spawning bout with a partner immediately after mating in the male role. In addition, larger individuals are less likely to reciprocate female matings by a partner, either by only mating once (as a male) in a spawning bout or by mating consecutively as a male within a series of matings. Although larger individuals show this relative specialization in the male role, they maintain their simultaneous hermaphroditism and obtain a substantial percentage of their mating success through female function. Egg trading appears to reduce the opportunity for large individuals to specialize as pure males, and thus interacts with the environmental potential for polygamy in shaping the mating system and sex allocation pattern in this species.     

Ovulation does not constrain egg parcel size in the simultaneous hermaphrodite Serranus subligarius

Among egg trading hermaphrodites, any factor which limits the number of eggs released by a female role hermaphrodite can potentially limit the mating success of the male role hermaphrodite fertilizing those eggs. This work examines the hypothesis that the timing of ovulation constrains the size of egg parcels and thereby limits male mating success in the egg parceling hermaphroditic fish Serranus subligarius. Two alternatives were evaluated: (1) Ovulation is a discrete event preceding spawning. It does not constrain the size of egg parcels and therefore does not limit mating success of male role partners. (2) Ovulation is an incremental process occurring throughout the spawning period. It limits the number of eggs available for release in each parcel and thereby limits mating success of the male role partner. Assessment of ovulation was conducted in a field stock of S. subligarius. Fish from size matched pairs were manually stripped at the onset of the spawning period or quarantined and sampled at the end of the spawning period. Fish sampled at either time point had the same number of eggs, suggesting that ovulation was a discrete event occurring at the onset of the spawning period. The diurnal cycle of ovulation was observed in naturally spawning hermaphrodites captured at intervals throughout the day. Ovulation began 2–4 h before spawning began. Some fish appeared to ovulate the entire day's clutch of eggs before spawning, while other fish released egg parcels before completing ovulation. I conclude that the pattern of ovulation is not uniform throughout the spawning stock. Because of the variability in timing of ovulation relative to parcel release, ovulation does not consistently limit the size of egg parcels and therefore is unlikely to be a physiological limit to male role mating success in S. subligarius hermaphrodites.     

The association between rank,mating effort,and reproductive success in male Barbary macaques (Macaca sylvanus)

The association between social rank, mating effort, and reproductive success of male Barbary macaques (Macaca sylvanus) has been evaluated by longterm behavioral observations and subsequent paternity determination via oligonucleotide DNA fingerprinting in a large semifreeranging group. All offspring born between 1985 and 1988 that survived to at least 1 year of age (n=75) were available for paternity testing. The exclusion of all but one of the potential fathers from paternity was possible in 70 cases (93%). Mating activities were recorded using ad lib. and focal female sampling techniques. The analysis of male mating effort was restricted to the most likely days of conception. Male rank correlated significantly with male mating success in all four breeding seasons and with male reproductive success in three of the four seasons. Mating success and reproductive success also showed a significant correlation, with the exception of one breeding season, in which the proportion of males per fertilizable female was especially high. Poor mating success was almost always associated with poor reproductive success, while good mating success was less predictive for a male's actual reproductive success. This was apparently a consequence of sperm competition, resulting from the promiscuous mating system. Male mating success is not necessarily an unreliable indicator for reproductive success, provided that sufficient sample sizes are available and that conception periods can be determined. Sperm competition and other factors may weaken the association, however.     

圈养猞猁多雄交配雄性的成功繁殖

研究了笼养猞猁多雄交配的结果以及雄性的成功繁殖。雄兽与发情雌兽随机配对,其繁殖成功(所产生的后代数量)不取决于与雌兽的交配顺序、交配次数与持续时间、遗传关系或雄兽的行为特征,但似乎取决于精子质量,特别是取决于形态正常精子的百分率。繁殖成功的雄兽比其竞争对手具有更多的形态正常的精子,似乎更能成功地诱发交配雌兽的排卵。证实了4窝(占总窝数的20%)幼兽的双重父亲身份。在所有情形下, 2雄1雌的交配间隔为24h 。     

蒙古沙冬青花序内性分配的变化、传粉者运动与繁殖成功

性分配理论主要研究繁殖资源在雌雄功能间的最优分配,从雌雄功能的角度考虑其个体适合度.对花序内不同部位花的雌性与雄性资源分配变化的研究,对于我们理解植物采取哪种繁殖对策保障繁殖成功具有重要意义.本文对生长在中国科学院吐鲁番沙漠植物园内的蒙古沙冬青(Ammopiptanthus mongolicus)连续开花花序内不同部位...     

The timing of spawning and egg production as constraints on male mating success in a simultaneously hermaphroditic fish

Synopsis The evolutionary stability of simultaneous hermaphroditism depends in part on the existence of constraints on the potential for male mating success. In the seabasses (Serranidae), several species of simultaneous hermaphrodites divide each day's clutch of eggs into parcels that are spawned sequentially and alternately with a partner. This behavior is thought to be one source of constraint on male mating success. A possible related source is the pattern of egg production. A study was therefore performed on the chalk bass,Serranus tortugarum, to examine this pattern. The results indicate that eggs are readied for spawning gradually over the course of the daily spawning period. The pattern of egg production acts jointly with spawning behavior in constraining male mating success. This pattern may be a pre-existing state to which the mating system has been adjusted, or it may have co-evolved with the mating system.     

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.     

Social situation,sperm competition and sex allocation in a simultaneous hermaphrodite parasite,the cestode Schistocephalus solidus

Evolutionary theory predicts an influence of mating group size on sex allocation in simultaneous hermaphrodites. We experimentally manipulated the social situation during reproduction in a simultaneous hermaphrodite parasite, the tapeworm Schistocephalus solidus, by placing worms as singles, pairs or triplets into an in vitro system that replaces the final host. We then determined the reproductive allocation patterns after 24 h (i.e. before the start of egg release) and after 72 h (i.e. around the peak of egg release rate) using stereology. After 24 h, sex allocation strongly depended on worm volume (which is determined in the second intermediate host), but was not significantly affected by the social situation experienced during reproduction. After 72 h, worms in groups had less vesicular sperm (i.e. sperm to be used in future inseminations) than singles. They also stored significantly more received sperm in their seminal receptacles than singles, suggesting that more sperm had been transferred in groups. Moreover, worms in triplets stored significantly more received sperm than worms in pairs, suggesting that they either mated more often and/or transferred more sperm per mating. This suggests a behavioural response to the increased risk of sperm competition in triplets. We further discuss the relative importance of sex allocation decisions at different life‐history stages.     

Sex allocation in simultaneous hermaphrodites: Trade-offs between sex-specific costs and lifespan

Fitness in self-incompatible simultaneous hermaphrodites incorporates gains and costs from both male and female reproductive function, and evolutionarily stable allocation of gonadal tissue to male or female function depends on these gains and costs. Paradoxically, despite the often equal expected gains but different costs associated with each sex, contributions to expected reproductive success through male and female function must be identical. Whenever allocation costs are unequal and limiting resources are energetically expensive or risky to acquire, these costs must ultimately be paid through reduced survival, resolving the paradox by equally diminishing expected reproductive success as male and as female. Maximizing fitness as lifetime reproductive success – not just reproductive rate alone, as in previous studies – maximizes the product of expected survival time and reproductive rate. The analysis shows how male-biased allocation can thereby arise and generate novel predictions on the relation between intensity of sperm competition and allocation to male function.     

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.     

Reproductive behavior of females and its relation to the mating success of two male forms inMnais pruinosa (Zygoptera: Calopterygidae)

The behavior of females of the damselflyMnais pruinosa was observed in the breeding season. Males consisted of both territorial (esakii) and non-territorial (strigata) types in the study area. Females sometimes arrived at a stream for mating and oviposition. The staying time of females in the stream was 1–3 hours, while that of males was 5–8 hours. The proportion of the males that copulated with the females did not differ between the two male forms present in the stream. In the Calopterygidae, of which the females usually perform multiple copulation, oviposition without subsequent recopulation is considered to be advantageous for a mated male in order to avoid the risk of sperm displacement. From such a viewpoint, the time spent for oviposition was measured for females that arrived at the stream after copulation with different male forms. The ratio was 69.1: 11.5–30.9 betweenesakii andstrigata males. Assuming that the oviposition time is proportional to the number of fertilized eggs laid, this ratio would represent the relative reproductive success of the two male forms. In fact, the relative abundance of the two male forms was also biased in favor ofesakii males (61.7:38.3) in this population. The mechanism of coexistence of the two male forms is discussed in relation to their reproductive success.     

Condition dependence of male and female reproductive success: insights from a simultaneous hermaphrodite

Sexually selected traits are predicted to show condition dependence by capturing the genetic quality of its bearer. In separate‐sexed organisms, this will ultimately translate into condition dependence of reproductive success of the sex that experiences sexual selection, which is typically the male. Such condition dependence of reproductive success is predicted to be higher in males than females under conditions promoting intense sexual selection. For simultaneous hermaphrodites, however, sex allocation theory predicts that individuals in poor condition channel relatively more resources into the male sex function at the expense of the female function. Thus, male reproductive success is expected to be less condition dependent than female reproductive success. We subjected individuals of the simultaneously hermaphroditic snail Physa acuta to two feeding treatments to test for condition dependence of male and female reproductive success under varying levels of male–male competition. Condition dependence was found for female, but not for male, reproductive success, meaning that selection on condition is relatively stronger through the female sex function. This effect was consistent over both male–male competition treatments. Decomposition of male and female reproductive performance revealed that individuals in poor condition copulated more in their male role, indicating an increased male allocation to mate acquisition. These findings suggest that sex‐specific condition dependence of reproductive success is at least partially driven by condition‐dependent sex allocation. We discuss the implications of condition‐dependent sex allocation for the evolution of sexually selected traits in simultaneous hermaphrodites.     

Bigger testes increase paternity in a simultaneous hermaphrodite,independently of the sperm competition level

Hermaphroditic animals face the fundamental evolutionary optimization problem of allocating their resources to their male vs. female reproductive function (e.g. testes and sperm vs. ovaries and eggs), and this optimal sex allocation can be affected by both pre‐ and post‐copulatory sexual selection. For example, local sperm competition (LSC) – the competition between related sperm for the fertilization of a partner's ova – occurs in small mating groups and can favour a female‐biased sex allocation, because, under LSC, investment into sperm production is predicted to show diminishing fitness returns. Here, we test whether higher testis investment increases an individual's paternity success under sperm competition, and whether the strength of this effect diminishes when LSC is stronger, as predicted by sex allocation theory. We created two subsets of individuals of the simultaneously hermaphroditic flatworm Macrostomum lignano – by sampling worms from either the highest or lowest quartile of the testis investment distribution – and estimated their paternity success in group sizes of either three (strong LSC) or eight individuals (weak LSC). Specifically, using transgenic focal individuals expressing a dominant green‐fluorescent protein marker, we showed that worms with high testis investment sired 22% more offspring relative to those with low investment, corroborating previous findings in M. lignano and other species. However, the strength of this effect was not significantly modulated by the experienced group size, contrasting theoretical expectations of more strongly diminishing fitness returns under strong LSC. We discuss the possible implications for the evolutionary maintenance of hermaphroditism in M. lignano.     

Insemination success discrepancy between long-term and short-term copulations in the provisioning shield bug, Parastrachia japonensis (Hemiptera: Cydnidae)

The duration of copulation in the gregarious shield bug, Parastrachia japonensis Scott (Hemiptera: Cydnidae), is of two types, the far more prevalent short-term copulation (average, 15 s) and the long-term coupulation (average, 23 min). Both types were thought to be equally effective in inseminating females. Recent evidence has suggested that there is, in fact, a discrepancy in insemination success between the two duration types of copulations. We carried out manipulated field studies to clarify the difference in insemination success between the two duration types and to determine whether there is some physical or physiological variability in females or males that might affect female receptivity to a long-term copulation. The findings indicated that, although a small percentage of short-term copulations resulted in some sperm transfer, long-term copulations were a far more effective way for males to inseminate females. Further, females experiencing long-term copulations were found to be at a slightly more advanced stage of ovarian development than those experiencing only short-term copulations, and may be deciding whether a long-term copulation occurs. Male size does not appear to affect copulation duration. It is concluded that the long-term type of copulation is the actual effective copulation duration in this species and the objective of all females. Possible factors that might contribute to the prevalence of these two copulation durations are discussed. Received: June 21, 1999 / Accepted: September 6, 1999     

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.     

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.     

Sex allocation and reproductive success in the andromonoecious perennial Solanum carolinense (Solanaceae). I. Female

Relative allocation of resources to growth vs. reproduction has long been known to be an important determinant of reproductive success. The importance of variation in allocation to different structures within reproductive allocation is somewhat less clear. This study was designed to elucidate the importance of allocation to vegetative vs. reproductive functions, and allocation within reproductive functions (sex allocation), to realized female success in an andromonoecious plant, Solanum carolinense. Allocation measurements were taken on plants in experimental arrays exposed to natural pollination conditions. These measurements included total flower number, the proportion of flowers that were male, flower size, and vegetative size. Flower number explained the majority of the variation among individuals in their success-that is, there was strong selection for increased flower production. There was also selection to decrease the proportion of flowers that were male, but neither flower size nor vegetative size (a measure of overall resource availability) were direct determinants of female success. After Bonferroni corrections for multiple comparisons, most phenotypic correlations among the traits measured were nonsignificant. Thus, in this andromonoecious species there is not a strong relationship between resource availability (vegetative size) and female success, and female success is instead determined by the relative production of the two different flower types.     

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.