Size-dependent mating and gender choice in a simultaneous hermaphrodite, Bulla gouldiana

Simultaneous hermaphrodites are predicted to optimally divide resources between male and female function, which can result in both size-dependent mating behaviors and conflict between potential mates. Predicted strategies include size-assortative mating, conditional exchange of gametes, and mating patterns where relative size affects investment in each sexual role. This study investigated the effect of body size on the mating strategies of a hermaphroditic opisthobranch, Bulla gouldiana. Although individuals were spatially aggregated in the field with high levels of movement and size variation, there was little evidence for predictions. Laboratory experiments, however, revealed complicated effects of mass on the probability and duration of mating, as well as gender choice. Pairs were more likely to mate if they included at least one large animal, with the larger animal typically inseminating the smaller. When both individuals were large, they were more likely to each mate in both sexual roles by switching roles once. Although B. gouldiana did not usually alternate between sexual roles multiple times within mating events, paired individuals behaved similarly (neither or both mating as sperm donors) more often than expected by chance. This suggests some level of reciprocity, which is unlikely to be conditional given rates of unilateral mating. When the larger member of the mating pair inseminated the smaller, the duration of insemination increased with the size of the smaller sperm recipient. Copulations lasted longer in pairs that switched sexual roles than in those that did not switch roles. This study suggests that variation in body size can lead to size-dependent mating patterns, but only some of the patterns in B. gouldiana support theoretical predictions. We review other studies that have addressed similar issues, providing inconsistent mating patterns in sperm-storing hermaphrodites.     

Sperm exchange in a simultaneous hermaphrodite

Many simultaneously hermaphroditic animals cross-inseminate when copulating, even though unilateral sperm exchange is functionally possible. The question is why reciprocity is the rule. This study addresses sperm exchange in a hermaphroditic planarian flatworm, Dugesia polychroa, in which self-fertilisation does not occur. We investigated the availability of self sperm for inseminating a partner, how self sperm affects the likelihood of sperm donation, and whether sperm donation depends on reciprocation by the partner. The amount of self sperm depended on body size, duration of isolation and experimental date, and animals that had more self sperm were more likely to mate. Depletion of allosperm (sperm received from partners) played only an indirect role, suggesting that animals copulate more to donate sperm rather than to replenish allosperm reserves. Among 60 copulating pairs, reciprocal insemination was more common (63.3%) than unilateral transfer (18.3%). A surprising 18.3% did not exchange sperm in either direction. Individuals were more likely to behave like their partners, resulting in more symmetrical matings (either reciprocity or no sperm exchange) than asymmetrical matings (unilateral sperm donation). The amount of self sperm donated during a copulation depended mainly on the amount available before the copulation and not on the amount received from the partner. The results suggest that conditional sperm exchange, or sperm trading, takes place in D. polychroa. Received: 31 May 1997 / Accepted after revision: 1 December 1997     

Male mating effort in a polygynous ungulate

Survival and mating success are key fitness components of mammalian males. Because energy is limited, life history theory predicts trade-offs between current and future reproduction. While many studies have examined fitness trade-off in females, we know little about trade-offs faced by males. In polygynous species, male mating success is largely dependent upon intrasexual competition. Consequently, males have greater uncertainty over the benefits of a given allocation than over its costs, and the correlation between mating effort and success is likely much weaker in males than in females. We analyzed 14 years of data on the mating effort and survival of marked bighorn rams to investigate fitness trade-offs. Dominant rams defended single estrous ewes (“tending”) while subordinates attempted to copulate after separating the tending pair (“coursing”). We estimated the participation in tending and coursing for each ram and the effort in searching for breeding opportunities by each ram each year. We compared these three behavioral indices of male mating effort to demographic parameters, individual characteristics, and both yearly and long-term survival. Mating effort during the rut was unrelated to ram overwinter survival, but longevity was positively correlated with mating effort between 2 and 5 years of age. Persistent variation among rams is likely to explain this pattern, suggesting that in natural populations a few high quality males enjoy both high mating success and high survival.An erratum to this article can be found at     

Strategic male signalling effort in a desert-dwelling fish

Males often use elaborate courtship displays to attract females for mating. Much attention, in this regard, has been focused on trying to understand the causes and consequences of signal variation among males. Far less, by contrast, is known about within-individual variation in signal expression and, in particular, the extent to which males may be able to strategically adjust their signalling output to try to maximise their reproductive returns. Here, we experimentally investigated male courtship effort in a fish, the Australian desert goby, Chlamydogobius eremius. When offered a simultaneous choice between a large and a small female, male gobies spent significantly more time associating with, and courting, the former, probably because larger females are also more fecund. Male signalling patterns were also investigated under a sequential choice scenario, with females presented one at a time. When first offered a female, male courtship was not affected by female size. However, males adjusted their courtship effort towards a second female depending on the size of the female encountered previously. In particular, males that were first offered a large female significantly reduced their courtship effort when presented with a subsequent, smaller, female. Our findings suggest that males may be able to respond adaptively to differences in female quality, and strategically adjust their signalling effort accordingly.     

The role of body size in early mating behavior in a simultaneous hermaphrodite, <Emphasis Type="Italic">Chelidonura sandrana</Emphasis>

Intraspecific variation in mating behavior is widespread among simultaneous hermaphrodites but its underlying sources remain largely unexplored. In the sea slug Chelidonura sandrana, most matings are reciprocal. However, despite non-conditional sperm exchange and potential polygamy-mediated benefits, 30% of matings end after unilateral insemination. To resolve this apparent inconsistency, we here investigated the effect of body size on the frequency of reciprocal matings by testing the following two hypotheses. First, sex-allocation theory predicts that the likelihood of reciprocity depends on the size difference between mating partners. Second, if both sex functions temporally differ in reaching maturity, reciprocal matings should be more frequent with increasing absolute body size of the smaller partner. The likelihood of reciprocity increased with body size of the smaller partner. Moreover, smaller individuals acted more often as males among unilateral matings. These findings suggest that the ability to donate sperm develops prior to female functionality in C. sandrana.     

Male care and mating effort among Hadza foragers

Paternal care figures prominently in many scenarios of human evolution. Recently, however, such scenarios have been challenged on two scores. First, the level of male contribution may be insignificant. Second, male care may be provided as a form of mating effort, rather than parenting effort. In theory, since men can enhance their Darwinian fitness both by providing care to their own offspring if this raises offspring fitness and by pursuing additional mates if this leads to additional offspring, men should respond to payoffs from both mating and parenting effort. If men respond to payoffs from parenting effort, paternity ought to make a difference. And if men respond to payoffs from mating effort, mating opportunities ought to make a difference. I analyzed the impact of these two factors on variation in male care among the Hadza, a foraging society in Tanzania. Two predictions were tested: (1) biological children will receive more care than stepchildren, and (2) men will provide less care to their biological children as their mating opportunities increase. Both predictions were supported. These results suggest men provide care, in part, as parenting effort, and that they trade off parenting effort for mating effort when they have greater mating opportunities. Received: 21 January 1998 / Received in revised form: 24 January 1999 / Accepted: 1 February 1999     

Alternative male mating tactics in a cichlid, Pelvicachromis pulcher: a comparison of reproductive effort and success

Pelvicachromis pulcher is a small African cichlid which breeds in holes. Males may either reproduce monogamously (pair males), polygynously (harem males), or be tolerated as helpers in a harem territory (satellite males). These helpers share in defence of the territory against conspecifics, heterospecific competitors and predators. There are two male colour morphs that are fixed for life and are apparently genetically determined. These differ in their potential mating strategy. Red morph males may become harem owners, while yellow morph males may become satellite males, and males of both morphs may alternatively pair up monogamously. We compared the reproductive effort and success of these three male reproductive strategies. Effort was measured as attack rates, time expenditure and the risk of being injured or killed when attacking competitors or predators of three sympatric fish species. Reproductive success was measured by observing how many eggs were fertilized by each male when this was possible, and by using genetic markers. The number of fry surviving to independence of parental care was used as a criterion of success. The reproductive success of harem males was 3.3 times higher than that of pair males and 7 times higher than that of the average satellite male. Dominant satellite males, however, were as successful as monogamous pair males, using the measure of fertilized eggs. To our knowledge, this has not been found previously in any fish species. Both harem and pair males had lower parental defence costs per sired offspring, however, than males using the alternative satellite tactic. Defence effort was significantly related to the risk of injury. Received: 17 January 1996 / Accepted after revision: 9 June 1997     

Population dynamics, sex ratio and size at sex change in a protandric simultaneous hermaphrodite, the spiny shrimp Exhippolysmata oplophoroides

One of the main goals of sex allocation theory is understanding sex ratio evolution. However, theoretical studies predicting sex ratios in species with unusual sexual systems, such as protandric simultaneous (PS) hermaphroditism, are rare. In PS hermaphrodites, juveniles first develop into functional males that mature into simultaneous hermaphrodites later in life. Here, we report on the sex ratio (males/males + hermaphrodites) in the PS hermaphroditic shrimp Exhippolysmata oplophoroides. A 2-year study demonstrated that hermaphrodites dominated the population in two different bays. This skewed sex ratio may be explained by limited encounter rates among conspecifics. In agreement with this idea, the density of shrimps was extremely low (≤1 shrimp km⁻²) at the two study sites. Size at sex phase change and sex ratios remained relatively stable through time at the two bays. The stability of these parameters might be explained by the rather steady population structure of this species during the study period. A review of sex ratios in PS hermaphroditic shrimps (Lysmata and Exhippolysmata) revealed considerable variation; some species have male- and others hermaphrodite-skewed sex ratios. The conditions explaining inter- and intra-specific sex ratio variation in protandric simultaneous hermaphroditic species remain to be addressed.     

The false limpet Siphonaria gigas, a simultaneous hermaphrodite, lives in pairs in rock fissures on the Pacific coast of Panama

The pulmonate limpet Siphonaria gigas, a simultaneous hermaphrodite, lives in the mid- to upper-intertidal zone on rocky shores in the tropical Eastern Pacific. Samples along five transects taken in June–July, 2004, on Culebra Point (8º54′N to 79º31′W), Republic of Panama, showed that 71 % of the population occurred in fissures, a significant preference for this habitat. Of 200 adults in 27 fissures, 150 lived side by side in pairs with their shells touching or nearly so, a significant deviation from the number of pairs expected given a random arrangement. Pair frequency did not increase with limpet density suggesting pairing was not an incidental consequence of crowding. Pair living was unknown in the genus Siphonaria, and is very uncommon among simultaneous hermaphrodites. Reproductive synchrony and restrictions on movement due to predation and environmental stress may limit opportunities for encountering and mating with multiple partners favoring pair living in S. gigas.     

Sperm storage and use in laboratory-reared<Emphasis Type="Italic"> Aplysia californica</Emphasis>, a simultaneous hermaphrodite

Aplysia californica, an opisthobranch mollusc, possesses a complex reproductive system that includes a seminal receptacle for the storage of exogenous sperm received from mating. Based on this reproductive anatomy, A. californica should have the ability to maintain and use viable exogenous sperm stores to fertilize multiple eggmasses for extended periods of time. Using controlled matings and careful observation of the development of eggmasses over time, we attempted to quantify A. californicas ability to store and use exogenous sperm following a single mating. On average, A. californica (240.6±31.7 g; mean±SE, n=9) produced 8.8±0.6 eggmasses containing 16.9±2.2×10⁶ fertilized eggs over a period of 22.3±3.6 days following a single mating encounter. The maximum duration an individual A. californica produced fertilized eggs, following a single copulation, was 41 days. The primary factor determining the cumulative number of fertilized eggs produced from a single mating in A. californica was the mass of the sperm recipient (r=0.773, P<0.05, n=9). Our results demonstrated that A. californica are not sperm limited following a single mating as has been suggested for other opisthobranch molluscs by Leonard and Lukowiaks (1991) gamete-trading hypothesis.Communicated by P.W. Sammarco, Chauvin     

Correlates of male mating success in great bustard leks: the effects of age, weight, and display effort

We examined how mating success varied in relation to age, weight, body size, and display behavior among great bustard Otis tarda males. The estimated mating success was strongly skewed, with 45% of adult males being involved in copulation attempts and only 9.7% actually seen copulating successfully. Unlike most birds, body size continued increasing in great bustards several years after reaching sexual maturity. Age, weight, and display effort were all significant and independent predictors of male mating success. The higher display effort involved performing longer full-display bouts. Older males could detach from the male flock earlier in the season as well as on each day and spend longer seasonal and daily periods displaying as solitary birds, which contributed to increase their mating success. In contrast, males weighing more did not invest more in display, which suggests that they could be recognized as dominants by other males and selected by females through assessment of their plumage sexual traits. In contrast to most other bird species, the system described for great bustards resembles that found in some lek-mating ungulates, where social rank is a complex trait determined by both age and mass, and as in these mammals, it suggests that sexual selection continues to favor a high male weight in this extremely sexually dimorphic species.     

Bateman gradients in a promiscuous mating system

The Bateman gradient is increasingly used to measure sexual selection and characterize mating systems. In a landmark paper, Arnold and Duvall (Am Nat 143:317–348, 1994) formulated predictions about the relationships between sex-specific Bateman gradients and the major types of mating system. In promiscuous species, gradients are expected to be strong and similar in both sexes. Current support for this prediction however remains equivocal as reported male gradients are almost constantly steeper than female gradients. Here, we estimated Bateman gradients in a wild population of Eastern chipmunks (Tamias striatus) over two reproductive seasons characterized by extreme levels of promiscuity and unbiased operational sex ratios. We found significant and positive Bateman gradients for both sexes. The gradients were not different among sexes suggesting that the strength of sexual selection was similar for males and females. The opportunity for selection was also particularly strong for a promiscuous species and not different among sexes. Our results thus support the predicted Bateman gradients for a promiscuous mating system.     

Large donors transfer more sperm,but depletion is faster in a promiscuous hermaphrodite

Males are limited in sperm and seminal fluid, which can lead to prudent sperm allocation across consecutive matings. While sperm depletion is usually considered a population characteristic, we investigated an individual size-related variation in sperm depletion in the promiscuous sea slug Chelidonura sandrana. We found that sperm counts substantially declined across four successive copulations, indicating sperm depletion. Sperm depletion occurred at a disproportionally fast rate in larger sperm donors. Based on our finding of body size-dependent sperm depletion, we further investigated whether this translates into prudent sperm allocation across ejaculates. We found no evidence that slugs adjusted the number of delivered sperm in response to partner body weight, a tight proxy of fecundity. Instead, sperm counts increased with sperm donor body weight. Sperm donation independent of partner body size and—as found in previous work—partner novelty leaves scope for currently unidentified traits like the sperm competition environment to affect male sperm allocation. Alternatively, we propose that, in C. sandrana, a low optimal male mating rate close to the female optimum as indicated by our data may ultimately render indiscriminate sperm allocation the most beneficial male mating strategy.     

Experimental test of socially mediated sex change in a protandric simultaneous hermaphrodite,the marine shrimp<Emphasis Type="Italic"> Lysmata wurdemanni</Emphasis> (Caridea: Hippolytidae)

In Lysmata wurdemanni, individuals begin benthic life in a male phase (MP) but later change to a female phase (FP) with female external morphology, but with both male and female reproductive capacity (protandric simultaneous hermaphroditism). Previous studies have demonstrated that the size (timing) of sex change varies considerably in natural populations. We experimentally tested for social mediation of sex change by rearing male-phase individuals (MPs) in both large and small social groups with different sexual and size composition. In the large group experiment, speed of sex change was inversely related to the abundance of female-phase individuals (FPs) in the group (sex-ratio induction). Increased allocation to female function (more rapid change to FP) may occur when male mating opportunities are lower because the simultaneous-hermaphrodite FP can immediately reproduce as a female while maintaining male mating capacity. When FPs are abundant, delayed sex change might be adaptive because the costs of female reproduction are considerable. An MP may gain reproductively by increased growth before changing to FP at a larger size (fewer but much larger broods). Size-ratio induction of sex change by small MPs was suggested but not confirmed. Experimental results from small groups (1–2 individuals) were qualitatively similar but not as conclusive as those from large groups. The number and complexity of social interactions in large groups may be necessary to stimulate labile sex change in this species. In L. wurdemanni, sex change may be influenced not only by abiotic factors related to breeding [Bauer (2002) Biol Bull 203:347–357] but also by social factors in certain demographic situations.Communicated by K. Lindström     

Multiple mating opportunities boost protandry in a pied flycatcher population

Protandry, the earlier arrival of males than females to breeding areas, is widespread in birds, but its underlying mechanisms are far from well understood. The two, not mutually exclusive most highly supported hypotheses to explain avian protandry postulate that it has evolved from intrasexual male competition to acquire the best territories (“rank advantage” hypothesis) and/or to maximize the number of mates (“mate opportunity” hypothesis). We studied for two consecutive years the relative importance of both hypotheses in a population of pied flycatchers (Ficedula hypoleuca), a territorial songbird with a mixed mating strategy. We measured territory quality using a long-term dataset on nest occupation and breeding output, and we used molecular techniques to assess male fitness across the range of social and genetic mating options. Territory quality was unrelated to breeding date and had no influence on extra-pair paternity or social polygynous events. However, males breeding early increased their chances of becoming socially polygynous and/or of attaining extra-pair paternity and, as a consequence, increased their total reproductive success. These results support the “mate opportunity” hypothesis, suggesting that sexual selection is the main mechanism driving protandry in this population.     

Costs of courtship and mating in a sexually cannibalistic orb-web spider: female mating strategies and their consequences for males

The costs of courtship and mating may include increased risks of predation, the transmission of pathogens, and a loss of foraging opportunities. Thus, a female's decision to tolerate a courting male will depend upon how these costs offset the benefits of mating, which will depend on her reproductive and nutritional status. While these costs may be similar for mated and unmated females, the benefits of mating will be less for mated than virgin females. However, the cost of lost foraging opportunities may be higher for females with fewer nutritional reserves necessary for forming eggs. We examined how these costs and benefits influence the courtship and mating behaviour of male and female orb-web spiders, Argiope keyserlingi. In the field, females on webs that also contained a courting male intercepted fewer prey items per hour than females on webs without a male. In the laboratory, the presence of a courting male at the hub also attracted mantid predators to the web, increasing the risk of predation for both male and female. Staged mating experiments in the laboratory revealed that the frequency of female attacks and pre-copulatory cannibalism was greater among mated than virgin females. Feeding history did not affect aggression in virgin females but, among mated females, food-deprived spiders attacked and cannibalized males more frequently than sated females and only the latter ever remated. These differences in female behaviour influenced male mating strategies. Choice experiments demonstrated that males preferred to venture onto the silk threads of virgin rather than those of mated females. Similar patterns of mate selectivity were observed in the field; females with narrow abdomens attracted more males to the webs than females with broad abdomens, and copulations were observed more frequently among females with narrow abdomens. These smaller females are likely to be virgins that have recently molted. Males that preferentially mate with virgin females will not only avoid potentially fatal attacks but also obtain, on average, a higher fertilization success.     

Male genital length and mating status differentially affect mating behaviour in an earwig

Phenotypic variation in male genitalia may affect copulation behaviour, which can have important fitness consequences for males. Male genitalia commonly possess traits that increase male control over copulation, but in species where females control mating, a poor functional understanding often prevents insight into the processes responsible for such effects. Here, I investigate the effect of male genital length on copulation behaviour in the earwig Euborellia brunneri, where both sexes exhibit extremely elongated genitalia that correspond in shape. This model system is particularly suitable because pairs mate repeatedly and females can limit both the number and duration of copulations. I used both virgin and mated males and females in a double-mating design because longer male genitalia confer benefits in sperm competition. Consistent with a greater predicted male mating effort in mated females, the duration of individual copulations increased, but this traded off against mating frequency as cumulative mating duration remained unchanged. In contrast, male genital length increased both individual and cumulative mating duration, regardless of mating status. This difference suggests that, while males may modify copulation duration in response to mating status, females facultatively adjust mating frequency to prevent mating excessively or express preferences for increased male genital length. Notably, this study demonstrates that male genital phenotypes that are successful in sperm competition also enjoy female-mediated mating benefits.     

Nest distribution affects behaviour and mating success in a marine fish

The distribution of breeding resources, such as nest sites, can have a pronounced impact on a population by affecting the proportion of individuals that succeed to breed and hence, the variation in reproductive success. Aggregation of important resources can lead to resource monopolisation by a limited number of individuals and thus affect the intensity of sexual selection. In this study, we tested, by contrasting two experimental treatments (dispersed vs. aggregated), how nest distribution affects: (1) mating behaviour, (2) male nest occupation and mating success, and (3) reproductive success and the opportunity for selection. We used the two-spotted goby (Gobiusculus flavescens), a small marine fish with a resource-based mating system, as our model species. When nests were aggregated, a larger proportion of the males behaved aggressively, fewer males succeeded in occupying a nest, fewer males became mated, and those males that mated received fewer eggs from spawning females. These effects resulted in a higher variance in reproductive success and hence, a higher opportunity for selection (I _rs ), in the aggregated treatment. We suggest that the results are a direct consequence of males defending a territory around their nest, preventing competitively inferior males from breeding. However, we found no significant selection differentials for body length or condition of males in either treatment. Our results support the hypothesis that aggregation of essential resources like nests promotes resource monopolisation. In species facing highly clumped nesting resources in the wild, monopolisation may negatively impact population productivity but could lead to strong selection on traits that promote male competitive ability.     

Male mating opportunities affect sex allocation in a protrandric-simultaneous hermaphroditic shrimp

Sex allocation theory predicts phenotypic adjustments by individuals in their investments into the male and female reproductive function in response to environmental conditions. I tested for phenotypically plastic shifts in sex allocation in a protandric simultaneous hermaphrodite, in which individuals mature and reproduce as males first, and later in life, as simultaneous hermaphrodites. I predicted that initially maturing males should adjust the timing of maturation as hermaphrodites according to male mating opportunities mediated by population size of hermaphrodites. In a first experiment, males maintained with only one hermaphrodite reduced the time they spent as males in comparison to males maintained with no conspecifics, presumably because total reproductive output is maximized by two individuals being simultaneous hermaphrodites when the mating system is a pair. Conversely, males maintained in groups with two or more hermaphrodites increased the time they spent as males in comparison to single males. This delay in maturation was not an effect of resource depletion with increasing shrimp density because the growth rate of males did not differ among most of the experimental treatments. One hypothesis to explain this social mediation of sex allocation is that the smaller males are more successful in mating as males than are the larger hermaphrodites: it will pay reproductively for males to delay maturation as hermaphrodites in large but not in small groups. In agreement with this notion, a second experiment demonstrated that smaller males were four times more successful than were larger hermaphrodites in inseminating shrimps reproducing as females. The informative cue that males may use to perceive different group sizes deserves further attention.