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.     

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.     

Direct reciprocity stabilizes simultaneous hermaphroditism at high mating rates: A model of sex allocation with egg trading

Simultaneous hermaphroditism is predicted to be unstable at high mating rates given an associated increase in sperm competition. The existence of reciprocal egg trading, which requires both hermaphroditism and high mating rates to evolve, is consequently hard to explain. We show using mathematical models that the presence of a trading economy creates an additional fitness benefit to egg production, which selects for traders to bias their sex allocation toward the female function. This female‐biased sex allocation prevents pure females from invading a trading population, thereby allowing simultaneous hermaphroditism to persist stably at much higher levels of sperm competition than would otherwise be expected. More generally, our model highlights that simultaneous hermaphroditism can persist stably when mating opportunities are abundant, as long as sperm competition remains low. It also predicts that reciprocity will select for heavier investment in the traded resource.     

Paternal investment directly affects female reproductive effort in an insect

Female reproductive effort can be influenced by the quality of her mate. In some species, females increase their reproductive effort by differentially allocating resources after mating with high-quality males. Examination of female reproductive effort in relation to male quality has implications for estimating the evolvability of traits and for sexual-selection models. Accurate quantification of reproductive investment is not possible in many species. Butterflies are an exception, as most nectar-feeding species emerge with almost intact reproductive resources, and in some species males provide nutrients at mating that enhance female fecundity. By manipulating male donations and using radioactive isotopes, we quantified the effect of variation in nutrient provisioning on female reproductive effort in two butterfly species. In the greenveined white butterfly, Pieris napi, females increased their reproductive effort after receiving large male donations. By contrast, in the speckled wood, Pararge aegeria, where males do not provide nutrients, female reproductive effort was independent of male ejaculate. Increased reproductive effort in Pieris napi resulted from the production of more eggs, rather than from investing more resources per egg. In this species donating ability is heritable; hence females laying more eggs after mating with high-donating males benefit both through higher fecundity and through the production of high-donating sons.     

To produce many small or few large eggs: a size-independent reproductive tactic of fish

Summary We demonstrate here the existence of a range of size-independent reproductive tactics in teleostean fish involving the allocation of a size-dependent reproductive effort between fecundity and egg size. Despite considerable evidence that larger eggs and the larvae hatching from them are more likely to survive than smaller ones, we found no evidence of evolutionary trends towards greater egg sizes. Fish with pelagic eggs tend to spawn many, and therefore small, eggs, whereas demersal spawners tend to produce large, and therefore few, eggs. Maximizing egg number should increase the number of eggs hatching in suitable locations in the patchy pelagic environment and, hence, increase the reproductive success of pelagic spawners. On the other hand, the reproductive success of demersal spawners, which reduce the variance in growing conditions experienced by the off spring, should be more dependent on the survival of the individual larvae, which increases as egg size increases.     

Bateman's Principle and Simultaneous Hermaphrodites: A Paradox

Bateman's principle states that reproductive success is limiteda) in females by the resources available for egg production;and b) in males, only by access to females and/or eggs. Theprinciple has been used to generate predictions for two aspectsof hermaphroditism; a) the advantage of hermaphroditism andb) sexual conflict. Comparing these predictions to the empiricaldata offers tests of Bateman's principle. Charnov's predictionthat hermaphroditism would occur under circumstances where Bateman'sprinciple does not apply is found to be largely correct. However,the prediction as to the association of hermaphroditism andlow fixed costs is inconsistent with the data. Alternative explanationsthat predict that hermaphroditism is a strategy for reducingvariance in reproductive success may better explain the data.Probability theory demonstrates that where two strategies haveequal mean fitness, which must be the case for male and femalefunction, the strategy with the lower variance in reproductivesuccess must have higher fitness (Gillespie's principle). Bateman'sprinciple predicts that this will be the female role in hermaphrodites.However, Charnov, assuming Bateman's principle, predicted thatsexual conflict stemming from a preference for the male rolewould be important in hermaphrodite mating systems, creatinga paradox. Many hermaphrodite mating systems are based on conditionalreciprocity with a preferred sexual role indicating sexual conflict.The data demonstrate that the preferred role varies among taxa,contrary to the predictions of Bateman's principle. It has beensuggested that Bateman's principle can explain cases in whichthe female role is preferred (sperm-trading) as involving energyrather than gamete trading. However, energetic considerationssuggest that energy trading would only be adaptive if Bateman'sprinciple does not apply, paradoxically. The gamete tradingmodel, based on the prediction that the role that offers controlof fertilization will be preferred, is more consistent withthe data. Application of Bateman's principle to hermaphroditesleads to contradictory predictions and does not offer the basisfor a coherent theory of sexual selection, as Bateman proposed.     

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.     

Reproductive regulation in the female Japanese minnow, Pseudorasbora parva (Cyprinidae)

The Japanese minnow, Pseudorasbora parva, is a multiple spawner that lays eggs repeatedly during the spawning season. In laboratory aquaria, 19 of 63 females did not spawn, whereas 44 other females laid 167 to 6285 eggs in 1 to 14 mating sequences. Neither fish density nor sex ratio (number of males per female) affected fecundity, but the increase in fish density significantly decreased the growth rate of females. The increase in male length significantly increased fecundity in aquaria which contained only a single male, whereas it decreased female growth rate. These relationships were not evident in aquaria housing three or ten males. Since larger males were more dominant and had larger testes than smaller males, the correlation between fecundity and male size strongly suggests that individual females regulated fecundity to increase their reproductive success.     

Reciprocal egg trading and brood care in a hermaphroditic polychaete worm

Ophryotrocha diadema is a simultaneous hermaphrodite polychaete worm with a brief protandrous phase. Its mating behaviour was investigated in order to elucidate the relationships between mating system and reproductive biology. A genetically determined yellow or white coloration of the eggs and body walls made it possible to distinguish the egg releaser from the fertilizer. The following main features of the mating system were established. (1) Pairs are formed preferentially between simultaneous hermaphrodites, one partner releasing eggs and the other fertilizing them. There is no selfing. (2) The partners attain spawning synchronization by means of close mutual contact during a fairly time-consuming courtship. (3) Partners regularly alternate sex roles, usually with the same partner more than once in succession. (4) Both partners care for their eggs and protect cocoons of neglected eggs spawned by other pairs.     

The effect of mating on female reproduction across hermaphroditic freshwater snails

Sexual conflicts often arise between mating partners because each sex tries to maximize its own reproductive success. One major male strategy to influence a partner's resource allocation is the transfer of accessory gland proteins. This has been shown to occur in simultaneous hermaphrodites as well as in organisms with separate sexes. Although accessory gland proteins affect the investment of resources in both male and female function, we here specifically focus on female investment. In the great pond snail, Lymnaea stagnalis, previous studies found that the accessory gland protein ovipostatin reduced female fecundity by suppressing egg laying in the partner in the short term (days). To investigate whether this reduction in egg laying is a commonly found effect of mating in freshwater snails, we compared egg output for evidence of suppression in isolated and paired snails of eight pulmonate species. Furthermore, we determined whether the suppression of egg laying caused a shift in resource allocation to the eggs. We found that in five of the eight species egg laying was suppressed, with fewer and lighter egg masses being laid when they had access to a mating partner. In mated pairs of L. stagnalis and Biomphalaria alexandrina, allocation of resources to the eggs was altered in opposite ways: individuals of L. stagnalis laid fewer but larger and heavier eggs; individuals of B. alexandrina laid smaller and lighter eggs, with no change in egg numbers. Such changes in the female function are most likely the result of combined effects of receiving accessory gland proteins, and the cost of mating in both male and female roles. Thus, effects of the maternal environment, including the receipt of accessory gland proteins, on offspring investment are not restricted to species with separate sexes.     

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.     

Multiple mating in the traumatically inseminating Warehouse pirate bug, Xylocoris flavipes: effects on fecundity and longevity

Optimal mating frequencies differ between sexes as a consequence of the sexual differentiation of reproductive costs per mating, where mating is normally more costly to females than males. In mating systems where sexual reproduction is costly to females, sexual conflict may cause both direct (i.e. by reducing female fecundity or causing mortality) and indirect (i.e. increased risk of mortality, reduced offspring viability) reductions in lifetime reproductive success of females, which have individual and population consequences. We investigated the direct and indirect costs of multiple mating in a traumatically inseminating (TI) predatory Warehouse pirate bug, Xylocoris flavipes (Reuter) (Hemiptera: Anthocoridae), where the male penetrates the female's abdomen during copulation. This study aimed to quantify the effects of TI on female fecundity, egg viability, the lifetime fecundity schedule, longevity and prey consumption in this cosmopolitan biocontrol agent. We found no difference in the total reproductive output between mating treatments in terms of total eggs laid or offspring viability, but there were significant differences found in daily fecundity schedules and adult longevity. In terms of lifetime reproduction, female Warehouse pirate bugs appear to be adapted to compensate for the costs of TI mating to their longevity.     

Female Gryllus vocalis Field Crickets Gain Diminishing Returns from Increasing Numbers of Matings

Although female insects generally gain reproductive benefits from mating frequently, females do not mate unlimited numbers of times. This study asks whether the limit on female mating rate is imposed by trade‐offs between reproduction and survival. Female Gryllus vocalis were given the opportunity to mate 5, 10, or 15 times with novel males, and the effects on daily fecundity (egg production), fertility (proportion of eggs that were fertilized), and female post‐experimental longevity were measured. Females that mated 10 times laid more eggs and had a higher proportion of fertile eggs than females that mated 5 times. However, females that mated 15 times did not lay significantly more eggs or have a higher proportion of fertile eggs than females that mated 10 times. Although number of matings did not affect the date that females laid their last egg, mating more times was associated with a prolonged period of laying fertile eggs. Number of matings did not affect female post‐experimental longevity. Thus, there was no trade‐off between female reproductive effort and survival, even when females mated very large numbers of times. When females were allowed to mate ad libitum, the average number of times that females mated was greater than the number of times that confers maximal fitness. The lack of cost to mating explains why females might be willing to mate beyond the point of diminishing reproductive returns.     

The cost of peripheral males in a brook trout mating system

A focus on the reproductive contributions of males displaying alternative life histories has neglected the role of size-dependent peripheral males in salmonine mating systems. We documented mating behaviour of brook trout Salvelinus fontinalis, including observations of spawning, over two breeding seasons to determine the mating costs of peripheral males to dominant males (kleptogamy) and females (egg cannibalism). For males and females, the mating costs of peripheral males were substantial because more than half (56%) of all observed brook trout spawnings involved peripheral males. Males that paired with large females experienced a greater incidence of kleptogamy due to increased numbers of peripheral males present. Large males face a conflict when mating in that they prefer to spawn with large females; however, these same females attract numerous males against which the dominant male cannot defend. From paternity studies, we estimated that males that had peripheral males participate in spawning may fertilize, on average, equal numbers of eggs compared to males spawning solely with a smaller female. Females that paired with relatively smaller males had significantly more eggs eaten by peripheral males than females that paired with relatively larger males. Latency to spawn by females increased when paired with a relatively small male, and resulted in females obtaining a larger spawning partner. The observed patterns of size-assortative mating, kleptogamy and cannibalism are discussed in relation to mate choice for this population of brook trout. Copyright 1999 The Association for the Study of Animal Behaviour.     

Effects of age at mating of both sexes on female longevity and fecundity performance in Ophraella communa LeSage (Coleoptera: Chrysomelidae)

Life-history strategies of animals are governed by fitness-related trait trade-offs. In particular, the age at which either one of the two sexes copulate has been shown to affect insect reproductive output and longevity. This suggests that trade-offs between longevity and reproduction might drive the choice of a mating partner based on their age and ultimately such choices might select for different life-histories. Although several studies indicate that female age at mating dictates subsequent insect longevity, fecundity, and egg hatch rate, it is unclear how male age at copulation affects these life-history traits. In this study, we simultaneously investigated the effects of female and male age on female fecundity, eggs hatch rate, and adult longevity in Ophraella communa LeSage (Coleoptera: Chrysomellidae), the primary biological control agent of the invasive common ragweed, Ambrosia artemisiifolia L. We found that young mature females lived significantly longer when they were mated with older males. Maximum female fecundity and subsequent egg hatch rate occurred when young females mated with 3-day-old males. On the other hand, females lived longer when mating with an older male. These findings are in accordance with the cost-of-reproduction concept.     

The effect of male mating history on paternal investment, fecundity and female remating in the seed beetle Callosobruchus maculatus

1. In many organisms, males provide nutrients to females via ejaculates that can influence female fecundity, longevity and mating behaviour. The effect of male mating history on male ejaculate size, female fecundity, female longevity and female remating behaviour in the seed beetle Callosobruchus maculatus was determined.
2. The quantity of ejaculate passed to females declined dramatically with successive matings. Despite the decline, a male's ability to fertilize a female fully did not appear to decline substantially until his fourth mating.
3. When females multiply mated with males of a particular mated status, the pattern of egg production was cyclic, with egg production increasing after mating. Females multiply mated to virgins had higher fecundity than females mated to non-virgins, and females mated to twice-mated males had disproportionately increased egg production late in their life.
4. Females that mated to multiple virgins, and consequently laid more eggs, experienced greater mortality than females mated only once or mated to non-virgins, suggesting that egg production is costly, and rather than ameliorating these costs, male ejaculates may increase them by allowing or stimulating females to lay more eggs.
5. Females mating with non-virgin males remated more readily than did females mated to virgins. Females given food supplements were less likely to remate than females that were nutritionally stressed, suggesting that females remate in part to obtain additional nutrients.     

Determinants of female fecundity in a simultaneous hermaphrodite: the role of polyandry and food availability

Classical sexual selection theory assumes that the reproductive success of females is primarily limited by the resources available for egg production rather than by the number of mating partners. However, there is now accumulating evidence that multiple mating can entail fitness costs or benefits for females. In this study we investigated the effect of polyandry (i.e., the mating with different mating partners) and food availability on the reproductive output of the female sex function in an outcrossing simultaneous hermaphrodite, the free-living flatworm Macrostomum lignano. We exposed virgin worms to different group sizes, a treatment that has previously been shown to affect the level of polyandry in this species. Moreover, we manipulated the food availability throughout the subsequent egg laying period, during which the worms were kept in isolation. The number of offspring produced was used as an estimate of female fecundity. We found that food availability, but not group size, had a significant effect on female fecundity. Additionally, female fecundity was positively correlated with the number of stored sperm in the female sperm-storage organ at the time of isolation, but it was not correlated with body or ovary size of the worms. Our results suggest that female fecundity in M. lignano is primarily determined by the resources available for egg production, and not by the level of polyandry, confirming classic sexual selection theory for simultaneous hermaphrodites.     

Do male two-spotted gobies prefer large fecund females?

A male mating preference for large females may be expected whenfemale size is correlated with fecundity. We tested for sucha preference in a fish, the two-spotted goby (Gobiusculus flavescens,Gobiidae), for which a male preference for colorful femaleshas been demonstrated. We offered males a choice between twostimulus females of different size, controlling for female colorand stage of egg maturation. We also analyzed the relationshipbetween size and fecundity (total number of eggs in the clutch)by allowing females of different size to spawn in a controlledenvironment. Female length explained 37% of the variation infecundity, but males showed only a weak preference for largefemales. We compared the coefficient of variation (CV) in fecunditybetween female two-spotted gobies and other fish species forwhich male preferences for large females have been reported.The CV in fecundity in the two-spotted goby was among the lowest.We suggest that the low variation limits the potential fecunditybenefit to be gained by a male selecting females on the basisof size alone. Our study emphasizes the importance of the variationin partner quality for the direction and the strength of matepreferences, as suggested by theoretical models.     

Multiple mating of male and female codling moth (Lepidoptera: Tortricidae) in apple orchards treated with sex pheromone

Studies were conducted with codling moth, Cydia pomonella L., to evaluate the mating status of male and female moths in apple, Malus domestica (Borkhausen), orchards treated with and without sex pheromone dispensers. Laboratory studies first examined the effect of multiple mating of male and female moths on female fecundity and egg fertility. Females that had mated three times had a significantly higher fecundity than singly mated moths. Sequential mating by male moths had no effect on the fecundity of female moths or egg fertility. However, male moth age did impact female fecundity, with significantly fewer eggs laid after mating with virgin 1- versus 3-d-old males. The mean size of the first spermatophore transferred by males was significantly larger than all subsequent spermatophores. Classifying spermatophores based on size was used in field sampling to categorize the mating status of the female's partner. The proportion of mated females with small spermatophores (partner had previously mated) was significantly higher in treated versus untreated orchards. The proportion of female moths caught in traps baited with pear ester that were virgin was low (相似文献   

Fitness advantage from nuptial gifts in female fireflies

Abstract 1. In many insects, males provide nuptial gifts to females in the form of spermatophores, sperm-containing structures produced by male accessory glands.
2. The work reported here examined the influence of both spermatophore number and spermatophore size on female reproductive output in two related firefly beetles, Photinus ignitus and Ellychnia corrusca (Coleoptera: Lampyridae). Based on differences in adult diet, male spermatophores were predicted to increase female reproductive output to a greater extent in P. ignitus than in E. corrusca .
3. Female fecundity was significantly higher in triply mated females than in singly mated females in both species, with no difference between mating treatments in female lifespan or egg hatching success. No effects of second male spermatophore size on fecundity, lifespan, or egg hatching success were detected in either species.
4. These results suggest a direct fitness advantage from multiple mating for females in both species, although enhanced fecundity may be due either to allocation of spermatophore nutrients to eggs or to other substances transferred within the spermatophore acting as oviposition stimulants.