Modeling spawning strategy for sex change under social control in haremic angelfishes

In haremic angelfishes where protogynous (female to male) sexchange is favored, females have been reported to adopt severaltactics for earlier sex change on the basis of a trade-offbetween reproduction and growth, or survivorship. A recentfield study on Centropyge ferrugatus revealed that femalesreduce spawning frequency in competition with similar-sized neighbors for social dominance. To evaluate the optimal spawningstrategy taken by haremic fishes, we developed an evolutionarilystable strategy model that focuses on their life history andsocial structure based on field data of C. ferrugatus. Theresults of the analysis predict that the spawning frequencywill be low when the mortality rate of females is high comparedwith males, the harem size is large, and there is a moderatedegree of social control. Our model further predicts conditionsunder which females completely stop spawning, as if they havebecome bachelors. Thus, the regulated spawning frequency maybe taken as a strategy to optimize the reproductive successof an individual in response to the available choices for sexchange, social control, and environmental conditions. Socialcontrol would also play an important role in sex change inmany other haremic species.     

Testing a new version of the size-advantage hypothesis for sex change: sperm competition and size-skew effects in the bucktooth parrotfish, Sparisoma radians

A variety of field studies suggest that sex change in animalsmay be more complicated than originally depicted by the size-advantagehypothesis. A modification of the size-advantage hypothesis,the expected reproductive success threshold model, proposesthat sperm competition and size-fecundity skew can stronglyaffect reproductive pay-offs. Size-fecundity skew occurs ifa large female's fecundity is markedly higher than the aggregateof the other members of her social group and, together withpaternity dilution from sperm competition, can produce situationsin which large females benefit by deferring sex change to smallerfemales. Deferral by large females can create sex-size distributionscharacterized by the presence of large females and small sex-changedmales, and it is precisely these distributions that the traditionalsize-advantage model cannot explain. We tested the predictionsof the new model with the bucktooth parrotfish, Sparisoma radians,on coral reefs in St. Croix, U.S. Virgin Islands. Collectionsand spawning observations determined that the local environmentalregime of S. radians is characterized by pervasive sperm competition(accompanying 30% of spawns) and factors that can produce substantialsize-fecundity skew in social groups. Dominant male removalexperiments demonstrate that the largest females in social groupsoften do not change sex when provided an opportunity. Instead,smaller, lower-ranking females change sex when a harem vacancyarises. This pattern of sex change is in contrast to virtuallyall previous studies of social control of sex change in fishes,but provides strong support for the general predictions of theexpected reproductive success threshold model.     

Alternative spawning tactics of female angelfish according to two different contexts of sex change

Social conditions for sex change and reproductive success werestudied in the haremic marine angelfish, Centropyge ferrugatus,in the coral reefs of southern Japan. In this species the largestfemale in a harem changed sex not only after disappearance ofthe dominant male but also occasionally in his presence. Inisolated harems containing two to three females, strict socialcontrol by the dominant male resulted in females changing sexonly after the male disappeared (takeover sex change). In haremsadjacent to each other, however, takeover sex change did notoccur even when one of the males disappeared. Instead, largeharems including more than four females were formed by fusionof two adjacent harems. In such large harems, the dominant malewas unable to socially prevent the largest female from changingsex later to acquire a portion of the harem (harem-fission sexchange). Females in adjacent harems spawned less frequentlyand tended to grow faster than those in isolated harems, probablyto gain an advantage in dominance status over neighbors of similarsize. Thus, females changed spawning frequencies according tothe two different contexts of sex change. The takeover tacticresults in higher fitness than the harem-fission tactic, whichshould be the best in the bad situation of adjacent harems.     

Maternal condition and offspring sex ratio in polygynous ungulates: a case study of bighorn sheep

The Trivers and Willard model (TWM) predicts that for sexuallydimorphic polygynous mammals, mothers able to provide a highlevel of care should bias offspring sex ratio in favor of sons.Contradictory results of empirical studies, however, suggestthat selective pressures for adaptive offspring sex ratio varywith species and environmental conditions. We report the resultsof a 29-year study of marked bighorn sheep (Ovis canadensis)in a population that underwent wide changes in density and wheremost females were weighed each year. Lamb sex ratio was independentof absolute ewe mass and yearly deviations from individual orpopulation average mass, but there was a nonsignificant trendtowards fewer males being born at high population density. Bighornsheep satisfy all the assumptions of the TWM but not its prediction:lamb sex ratio is independent of maternal ability to providecare. Recent hypotheses to explain the lack of relationshipbetween maternal condition and offspring sex in ungulates areunlikely to apply to bighorn sheep. We suggest that the TWMmay only apply when social rank strongly affects the abilityto provide maternal care. Those circumstances are likely tooccur for only a few species and within a narrow range of environmentalconditions.     

Sex change in either direction by growth-rate advantage in the monogamous coral goby, Paragobiodon echinocephalus

The size-advantage model predicts the evolution of sex changeif the relative reproductive success of the sexes changes withsize or age. In the goby (Paragobiodon echinocephalus) the largesttwo fish, a male and a female matched by size, breed monogamouslyin each host coral. Because the female fecundity and male abilityof egg care increase with body size in a similar way, no size-fecundityadvantage exists. However, we found both protogyny and infrequentprotandry in a natural population of this species in Okinawa.New pairs were often formed after movement between host coralsand also sex change or sex differentiation of one or both members.In most new pairs males were larger than females, and femalesgrew much faster than their mates until breeding (growth-rateadvantage). The smaller member of a new pair should be the femalethat grows faster, because the smaller limits the reproductivesuccess of the pair. To form such a pair, the goby changed sexaccording to the sex and relative size of a new mate, as a status-dependentconditional strategy. The growth-rate advantage predicts predominanceof protogyny, but movement between host corals provides opportunitiesalso for protandry.     

Physical interactions facilitate sex change in the protogynous orange-spotted grouper,Epinephelus coioides

Sex change in teleost fishes is commonly regulated by social factors. In species that exhibit protogynous sex change, such as the orange-spotted grouper Epinephelus coioides, when the dominant males are removed from the social group, the most dominant female initiates sex change. The aim of this study was to determine the regulatory mechanisms of socially controlled sex change in E. coioides. We investigated the seasonal variation in social behaviours and sex change throughout the reproductive cycle of E. coioides, and defined the behaviour pattern of this fish during the establishment of a dominance hierarchy. The social behaviours and sex change in this fish were affected by season, and only occurred during the prebreeding season and breeding season. Therefore, a series of sensory isolation experiments was conducted during the breeding season to determine the role of physical, visual and olfactory cues in mediating socially controlled sex change. The results demonstrated that physical interactions between individuals in the social groups were crucial for the initiation and completion of sex change, whereas visual and olfactory cues alone were insufficient in stimulating sex change in dominant females. In addition, we propose that the steroid hormones 11-ketotestosterone and cortisol are involved in regulating the initiation of socially controlled sex change.     

Sexual selection explains sex-specific growth plasticity and positive allometry for sexual size dimorphism in a reef fish

In 1950, Rensch noted that in clades where males are the larger sex, sexual size dimorphism (SSD) tends to be more pronounced in larger species. This fundamental allometric relationship is now known as ‘Rensch''s rule’. While most researchers attribute Rensch''s rule to sexual selection for male size, experimental evidence is lacking. Here, we suggest that ultimate hypotheses for Rensch''s rule should also apply to groups of individuals and that individual trait plasticity can be used to test those hypotheses experimentally. Specifically, we show that in the sex-changing fish Parapercis cylindrica, larger males have larger harems with larger females, and that SSD increases with harem size. Thus, sexual selection for male body size is the ultimate cause of sexual size allometry. In addition, we experimentally illustrate a positive relationship between polygyny potential and individual growth rate during sex change from female to male. Thus, sexual selection is the ultimate cause of variation in growth rate, and variation in growth rate is the proximate cause of sexual size allometry. Taken together, our results provide compelling evidence in support of the sexual selection hypothesis for Rensch''s rule and highlight the potential importance of individual growth modification in the shaping of morphological patterns in Nature.     

The influence of simulated exploitation on Patella vulgata populations: protandric sex change is size‐dependent

Grazing mollusks are used as a food resource worldwide, and limpets are harvested commercially for both local consumption and export in several countries. This study describes a field experiment to assess the effects of simulated human exploitation of limpets Patella vulgata on their population ecology in terms of protandry (age‐related sex change from male to female), growth, recruitment, migration, and density regulation. Limpet populations at two locations in southwest England were artificially exploited by systematic removal of the largest individuals for 18 months in plots assigned to three treatments at each site: no (control), low, and high exploitation. The shell size at sex change (L₅₀: the size at which there is a 50:50 sex ratio) decreased in response to the exploitation treatments, as did the mean shell size of sexual stages. Size‐dependent sex change was indicated by L₅₀ occurring at smaller sizes in treatments than controls, suggesting an earlier switch to females. Mean shell size of P. vulgata neuters changed little under different levels of exploitation, while males and females both decreased markedly in size with exploitation. No differences were detected in the relative abundances of sexual stages, indicating some compensation for the removal of the bigger individuals via recruitment and sex change as no migratory patterns were detected between treatments. At the end of the experiment, 0–15 mm recruits were more abundant at one of the locations but no differences were detected between treatments. We conclude that sex change in P. vulgata can be induced at smaller sizes by reductions in density of the largest individuals reducing interage class competition. Knowledge of sex‐change adaptation in exploited limpet populations should underpin strategies to counteract population decline and improve rocky shore conservation and resource management.     

Do mothers prefer helpers or smaller litters? Birth sex ratio and litter size adjustment in cotton-top tamarins (Saguinus oedipus)

Sex allocation theory has been a remarkably productive field in behavioral ecology with empirical evidence regularly supporting quantitative theoretical predictions. Across mammals in general and primates in particular, however, support for the various hypotheses has been more equivocal. Population‐level sex ratio biases have often been interpreted as supportive, but evidence for small‐scale facultative adjustment has rarely been found. The helper repayment (HR) also named the local resource enhancement (LRE) hypothesis predicts that, in cooperatively breeding species, mothers invest more in the sex which assists with rearing future offspring and that this bias will be more pronounced in mothers who require extra assistance (i.e., due to inexperience or a lack of available alloparents). We tested these hypotheses in captive cotton‐top tamarins (Saguinus oedipus) utilizing the international studbook and birth records obtained through a questionnaire from ISIS‐registered institutions. Infant sex, litter size, mother's age, parity, and group composition (presence of nonreproductive subordinate males and females) were determined from these records. The HR hypothesis was supported over the entire population, which was significantly biased toward males (the “helpful” sex). We found little support for helper repayment at the individual level, as primiparous females and those in groups without alloparents did not exhibit more extreme tendencies to produce male infants. Primiparous females were, however, more likely to produce singleton litters. Singleton births were more likely to be male, which suggests that there may be an interaction between litter size adjustment and sex allocation. This may be interpreted as supportive of the HR hypothesis, but alternative explanations at both the proximate and ultimate levels are possible. These possibilities warrant further consideration when attempting to understand the ambiguous results of primate sex ratio studies so far.     

Fledgling sex ratios in relation to brood size in size-dimorphic altricial birds

In six species of dimorphic raptors (females larger than males)and one passerine (males larger than females), the sex ratioat fledging varied systematically with brood size at fledging.In all species the strongest bias toward the smaller sex wasestablished in the largest as well as the smallest broods; amore even distribution of males and females was observed inbroods of intermediate size. We explored a specific differentialmortality explanation for this sex ratio variation. Our hypothesispostulates that variation in mortality is caused by differencesin food demand between broods of the same size, due to theirsex composition. Data from the marsh harrier Circus aeruginosuson gender-related food demand and overall nestling mortalitywere used to predict the frequency of surviving males and femalesat fledging, assuming an even sex ratio at hatching and randommortality with respect to both sexes within broods. The modelquantitatively fits the marsh harrier data well, especiallyin broods originating from large dutches. Although we anticipatethat other mechanisms are also involved, the results supportthe hypothesis of sex-ratio-dependent mortality, differentialbetween broods, as the process generating the observed brood-sizedependence of fledgling sex ratios in sexually dimorphic birds.     

Field evidence for bi-directional sex change in the polygynous gobiid fish Trimma okinawae

The social condition of bi-directional sex change in the gobiid fish Trimma okinawae was investigated at Akamizu Beach, Kagoshima, Japan. Social groups of T. okinawae usually consisted of a large male and one or more smaller females. The number of females in the group was positively correlated with male body size and groups were usually separated from each other by 1–3 m. In total, 22 instances of female-to-male sex change and three instances of male-to-female sex change were observed during the 16 months that social groups were monitored. Two individuals changed sex twice: female to male and back to female. Female-to-male sex change occurred when the male disappeared from a group. Either the largest remaining female changed sex to male or a large female from another group immigrated and changed sex to male. Larger individuals appear to benefit from becoming male because they can monopolize the breeding opportunities with several females, as reported in other protogynous fishes. Sex change from male-to-female only occurred when a solitary male joined another group as a subordinate. Mortality rates are high in these small fish, therefore joining another group and reproducing as a female is likely to increase the reproductive value of a solitary male.     

Drivers of protogynous sex change differ across spatial scales

The influence of social demography on sex change schedules in protogynous reef fishes is well established, yet effects across spatial scales (in particular, the magnitude of natural variation relative to size-selective fishing effects) are poorly understood. Here, I examine variation in timing of sex change for exploited parrotfishes across a range of environmental, anthropogenic and geographical factors. Results were highly dependent on spatial scale. Fishing pressure was the most influential factor determining length at sex change at the within-island scale where a wide range of anthropogenic pressure existed. Sex transition occurred at smaller sizes where fishing pressure was high. Among islands, however, differences were overwhelmingly predicted by reefal-scale structural features, a pattern evident for all species examined. For the most abundant species, Chlorurus spilurus, length at sex change increased at higher overall densities and greater female-to-male sex ratios at all islands except where targeted by fishermen; here the trend was reversed. This implies differing selective pressures on adult individuals can significantly alter sex change dynamics, highlighting the importance of social structure, demography and the selective forces structuring populations. Considerable life-history responses to exploitation were observed, but results suggest potential fishing effects on demography may be obscured by natural variation at biogeographic scales.     

Sex allocation and nestling survival in a dimorphic raptor: does size matter?

Fisher's theory predicts equal sex ratios at the end of parentalcare if the costs and benefits associated with raising eachsex of offspring are equal. In raptors, which display variousdegrees of reversed sexual size dimorphism (RSD; females thelarger sex), sex ratios biased in favor of smaller males areonly infrequently reported. This suggests that offspring ofeach sex may confer different fitness advantages to parents.We examined the relative returns associated with raising eachsex of offspring of the brown falcon Falco berigora, a medium-sizedfalcon exhibiting RSD (males approximately 75% of female bodymass) and subsequent sex ratios. Female nestlings hatched eitherfirst or second did not receive more food nor did they hatchfrom larger eggs or remain dependent on parents for longer periodsthan male offspring from these hatch orders. Together with previousstudies this result indicates that even in markedly dimorphicspecies, the required investment to raise the larger sex islikely to be less than that predicted by body size differencesalone. Moreover, among last-hatched nestlings, both sexes faceda reduced food allocation and suffered a slower growth rateand thus final body size, with a concurrent increased probabilityof mortality. For last-hatched females the reduction in foodallocation was more marked, with complete mortality of all last-hatchedfemale nestlings monitored in this study. Once independent,males of any size but only larger females are likely to be recruitedinto the breeding population. The sex-biased food allocationamong last-hatched offspring favoring males thus reflects therelative returns to parents in raising a small member of eachsex.     

Internest sex-ratio variation and male brood survival in the ant Pheidole pallidula

Sex allocation in social insects has become a general modelin tests of inclusive fitness theory, sex-ratio theory, andparent-offspring conflict. Several studies have shown that colonysex ratios are often bimodally distributed, with some coloniesproducing mainly females and others mainly males. Sex specializationmay result from workers assessing their relatedness to malebrood versus female brood, relative to the average worker-relatednessasymmetry in other colonies of their population. Workers thenadjust the sex ratio in their own interest This hypothesis assumesthat workers can recognize the sex of the brood in their colonyand selectively eliminate males. We compared the primary sexratio (at the egg stage) and secondary sex ratio (reproductivepupae and adults) of colonies in the ant Pheidole pallidula.There was a strong bimodal distribution of secondary sex ratios,with most colonies producing mainly reproductives of one sex.In contrast, there was no evidence of a bimodal distributionof primary sex ratios. The proportion of haploid eggs producedby queens was 0.35 in early spring and decreased to about 0.1in summer. Male eggs also were present in virtually all fieldcolonies sampled in July, although eggs laid at this time ofyear never give rise to males. All male brood is, therefore,selectively eliminated beginning in July and continue to beeliminated through the rest of the year. Finally, the populationsex-ratio investment was female-biased. Together, these resultsare consistent with the hypothesis that workers control thesecondary sex ratio by selectively eliminating male brood inabout half the colonies, perhaps those with high relatednessasymmetry.[Behav Ecol 7: 292–298 (1996)]     

Social Reversal of Sex‐Biased Aggression and Dominance in a Biparental Cichlid Fish (Julidochromis marlieri)

In biparental species, aggression, dominance, and parental care are typically sexually dimorphic. While behavioral dimorphism is often strongly linked to gonadal sex, the environment—either social or ecological—may also influence sex‐biased behavior. In the biparental cichlid fish Julidochromis marlieri, the typical social environment for breeding pairs consists of large females paired with smaller males. While both sexes are capable of providing territory defense and parental care, the larger female provides the majority of defense for the pair, while the smaller male remains in the nest guarding their offspring. We examine the contributions of sex and relative mate size to these sex‐biased behaviors in monogamous J. marlieri pairs. Both female‐larger and male‐larger pairs were formed in the laboratory and were observed for territorial aggression (against conspecifics and heterospecifics), dominance, and parental care. In female‐larger pairs, territorial aggression and intra‐pair dominance were female‐biased, while in male‐larger pairs this bias was reversed. For both pairing types, the presence of an intruder amplified sex differences in territorial aggression, with the larger fish always attacking with greater frequency than its mate. Though less robust, there was evidence for plasticity of sex‐bias for some egg care related behaviors in the inverse direction. Our study suggests that relative mate size strongly influences the sex bias of aggression and dominance in J. marlieri and that this aspect of the social environment can override the influence of gonadal sex on an individual's behavior. The remarkable plasticity of this species makes Julidochromis an exciting model that could be used to address the relationship between proximate and ultimate mechanisms of behavioral plasticity.     

Experience does not alter alternative mating tactics in the burying beetle Nicrophorus vespilloides

Alternative male mating tactics are widespread, but the cuesthat determine which tactic is adopted remain unclear. Sizeis commonly associated with alternative mating tactics, butit is not known how individuals gauge their size effectively,especially given that size is relative and frequency dependent.One possibility is that interactions with conspecifics are usedto assess size, relative to potential competitors, and thusfine-tune tactics. Success in mating might also influence matingtactics given that this should indicate the potential availabilityof mates in the population. We tested these ideas in the buryingbeetle Nicrophorus vespilloides, examining whether individualsuse the outcome of larval or adult interactions as cues to adjustthe tactics used to acquire mates. Male N. vespilloides employ2 tactics; search for a carcass, a resource required for reproduction,or release a pheromone (call) to attract a mate. Males are plasticin the amount of time they invest in each tactic, and in a relatedspecies (Nicrophorus orbicollis), male size influences the tacticadopted. We examine the potential effects of parental care,sibling competition, relative size within a brood, and adultexperience of agonistic interactions and mating on tactic adoption.Absolute size was consistently the best predictor of callingrate, with smaller males calling more often than larger males.We suggest that the lack of a response to adult cues may reflectunpredictability in the occurrence of social interactions orstable size distributions in this population.     

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.     

Population differences in female resource abundance, adult sex ratio, and male mating success in Dendrobates pumilio

In this study I examined the relationship among abundance ofreproductive resources, population density, and adult sex ratioin the strawberry dart-poison frog, Dendrobates pumilio, andhow these variables in turn influence the mating system, malereproductive success, and sexual selection. I studied the matingbehavior in two populations of D. pumilio living in a primaryand secondary rainforest on the Caribbean slope of Costa Rica.The abundance of tadpole-rearing sites (reproductive resourcesfor females) was approximately 10-fold higher in the secondary forest. Accordingly, the population density was higher and theadult sex ratio was strongly female biased in the secondaryforest, whereas the adult sex ratio was even in the primaryforest. The female-biased sex ratio was associated with a higherlevel of polygyny and higher male mating and reproductive successin the secondary forest. In contrast, the level of polyandrydid not differ between habitats. As expected, the opportunityfor sexual selection on male mating success was lower in thesecondary forest, the habitat with high female density. Inconclusion, my results suggest that ecological variables suchas resource availability have a great impact on the matingsystem and sexual selection through their effect on population structure. Moreover, the results of this study give furtherevidence that the opportunity for sexual selection is influencedby the adult sex ratio and hence by the operational sex ratioin a population.     

Synergistic effects of olfactory and tactile cues in short‐range mate finding of Ophraella communa

Sensory signals between individuals are important in short‐range mate finding. The purpose of our experiments was to verify the roles of different sensory cues in mate orientation and discrimination in Ophraella communa LeSage (Coleoptera: Chrysomelidae) adults. Sex discrimination and sensory deprivation tests (i.e., depriving the olfactory and/or visual senses of either or both sexes by coating with paint) were conducted in the laboratory. Male O. communa were able to locate and recognize conspecifics using olfactory cues prior to physical contact, but could not discriminate the opposite sex prior to physical contact. When the olfaction of male O. communa was deprived by painting antennae, males spent significantly longer times seeking mates in the arena. Copulation duration did not differ significantly among treatments. Thus, the mating process of O. communa adults was mediated by contact cues, but not by olfactory cues. The percentages of successful mating, searching duration, and copulation duration were all unaffected by visual deprivation, i.e., when the eyes of either or both sexes were covered by black paint. The function of visual cues was thus negligible in the mate‐finding process of O. communa adults. Overall, these results suggested that orientation and discrimination of the opposite sex by O. communa is dependent on the synergy between olfactory and tactile cues.     

Local population density and group composition influence the signal‐preference relationship in Enchenopa treehoppers (Hemiptera: Membracidae)

Many animals exhibit social plasticity – changes in phenotype or behaviour in response to experience with conspecifics that change how evolutionary processes like sexual selection play out. Here, we asked whether social plasticity arising from variation in local population density in male advertisement signals and female mate preferences influences the form of sexual selection. We manipulated local density and determined whether this changed how the distribution of male signals overlapped with female preferences – the signal preference relationship. We specifically look at the shape of female mate preference functions, which, when compared to signal distributions, provide hypotheses about the form of sexual selection. We used Enchenopa binotata treehoppers, a group of plant‐feeding insects that exhibit natural variation in local densities across individual host plants, populations, species and years. We measured male signal frequency and female preference functions across the density treatments. We found that male signals varied across local social groups, but not according to local density. By contrast, female preferences varied with local density – favouring higher signal frequencies in denser environments. Thus, local density changes the signal–preference relationship and, consequently, the expected form of sexual selection. We found no influence of sex ratio on the signal–preference relationship. Our findings suggest that plasticity arising from variation in local group density and composition can alter the form of sexual selection with potentially important consequences both for the maintenance of variation and for speciation.