When is a male not a male? Sex recognition and choice in two sex-changing species

For dioecious species, choosing a mate of the same sex can have reproductive costs. For sex-changing animals, however, a lack of sex recognition may not carry a reproductive cost, as pairs that were initially same-sex can become opposite-sex pairs as one partner changes sex. The strength of sex discrimination in sex changers, then, should depend on the duration of mating associations and whether the time of sex change is influenced by social situation (“flexible” sex change). We studied two species of marine snails that change sex from male to female, one with flexible sex change and long-term or permanent mating associations (Crepidula fornicata) and one with short-term pairings and relatively fixed time of sex change (Crepidula convexa), to determine whether either species exhibits sex recognition and whether members of C. convexa show stronger sex discrimination. In laboratory experiments, small males, the choosing animals, were placed with either a male or a female conspecific (no-choice experiments) or given a choice of a male or female (choice experiments). We controlled for shell length in all experiments, as relative size may influence sex change or choice. Males of both species paired more often with females than males, but, as predicted, males of C. convexa showed stronger discrimination: When given a choice, no C. convexa male paired with another male. In contrast, some C. fornicata males always chose other males even when given the choice of a female. These results suggest that sex recognition can be adaptive even for sex changers but demonstrate that the level of sex recognition will depend on other aspects of reproductive behavior.     

Mediating male–male interactions: the role of the UV blue crest coloration in blue tits

Badges of status, usually color patches, are hypothesized to serve as important signals within natural populations by communicating an individual’s fighting ability or aggressiveness before an interaction ever takes place. These signals, which may evolve via sexual and/or social selection, mediate intra-specific competition by influencing the outcome or escalation of contests between individuals. The last 10 years saw the rise of interest in the role of ultraviolet (UV)-based coloration in intra-sexual communication. However, the rare experimental studies that tested this hypothesis found opposite results, which may originate from the different methodological procedures used to assess the badge of status theory. We present here the results of an experiment testing whether male blue tits (Cyanistes caeruleus) respond differently to unfamiliar conspecifics presenting contrasted UV crest coloration. In an aviary, we simultaneously presented two caged blue tits with enhanced (UV+) or reduced (UV−) crest coloration to a focal bird. We found that focal males acted more aggressively towards the UV− males than UV+ males. In addition, focal males fed more often close to males that were similar in brightness or duller than themselves. We conclude that, in blue tits, UV blue crest coloration affects both social and aggressive responses towards unfamiliar individuals, and thus it has some properties of a badge of status.     

Mating skew in Barbary macaque males: the role of female mating synchrony,female behavior,and male–male coalitions

A fundamental question of sexual selection theory concerns the causes and consequences of reproductive skew among males. The priority of access (PoA) model (Altmann, Ann NY Acad Sci 102:338–435, 1962) has been the most influential framework in primates living in permanent, mixed-sex groups, but to date it has only been tested with the appropriate data on female synchrony in a handful of species. In this paper, we used mating data from one large semi-free ranging group of Barbary macaques: (1) to provide the first test of the priority-of-access model in this species, using mating data from 11 sexually active females (including six females that were implanted with a hormonal contraceptive but who showed levels of sexual activity comparable to those of naturally cycling females) and (2) to determine the proximate mechanism(s) underlying male mating skew. Our results show that the fit of the observed distribution of matings with sexually attractive females to predictions of the PoA model was poor, with lower-ranking males mating more than expected. While our work confirms that female mating synchrony sets an upper limit to monopolization by high-ranking individuals, other factors are also important. Coalitionary activity was the main tactic used by males to lower mating skew in the study group. Coalitions were expressed in a strongly age-related fashion and allowed subordinate, post-prime males to increase their mating success by targeting more dominant, prime males. Conversely, females, while mating promiscuously with several males during a given mating cycle, were more likely to initiate their consortships with prime males, thus reducing the overall effectiveness of coalitions. We conclude that high-ranking Barbary macaque males have a limited ability to monopolize mating access, leading to a modest mating skew among them.     

Why do male Callosobruchus maculatus beetles inseminate so many sperm?

Male Callosobruchus maculatus F. (Coleoptera: Bruchidae) inseminate more sperm than females can effectively store in their spermathecae. This study examines the adaptive significance of excess sperm transfer by measuring components of male and female reproductive success in response to manipulating the number of sperm inseminated. The number of sperm transferred during copulation was reduced from 56,000 ±4,462 to 8,700±1,194 by sequentially mating males to virgin females. Reducing the number of sperm inseminated by the first male to mate had no effect on the extent of sperm precedence, but reducing the number of sperm inseminated by the second male resulted in a significant reduction in the extent of sperm precedence. When large numbers of sperm are inseminated the remating refractory period of females is increased. These results indicate that males transferring large numbers of sperm during copulation have a two-fold advantage at fertilization; they are more effective at preempting previously stored sperm and they are likely to father more offspring by delaying the time of female remating. The transfer of excess sperm does not appear to serve as nonpromiscuous male mating effort; the number of eggs laid, their fertility and the subsequent survival of zygotes were unaffected by manipulating the number of sperm inseminated. The underlying mechanisms of sperm precedence were also examined. Simple models of sperm displacement failed to accurately predict the patterns of sperm precedence observed in this species. However, the results do not provide conclusive evidence against the models but rather serve to highlight our limited understanding of the movement of sperm within the female's reproductive tract.     

Is male rhesus macaque red color ornamentation attractive to females?

Male sexually selected traits can evolve through different mechanisms: conspicuous and colorful ornaments usually evolve through intersexual selection, while weapons usually evolve through intra-sexual selection. Male ornaments are rare among mammals in comparison to birds, leading to the notion that female mate choice generally plays little role in trait evolution in this taxon. Supporting this view, when ornaments are present in mammals, they typically indicate social status and are products of male-male competition. This general mammalian pattern, however, may not apply to rhesus macaques (Macaca mulatta). Males of this species display conspicuous skin coloration, but this expression is not correlated to dominance rank and is therefore unlikely to have evolved due to male-male competition. Here, we investigate whether male color expression influences female proceptivity toward males in the Cayo Santiago free-ranging rhesus macaque population. We collected face images of 24 adult males varying in dominance rank and age at the peak of the mating season and modeled these to rhesus macaque visual perception. We also recorded female sociosexual behaviors toward these males. Results show that dark red males received more sexual solicitations, by more females, than pale pink ones. Together with previous results, our study suggests that male color ornaments are more likely to be a product of inter- rather than intra-sexual selection. This may especially be the case in rhesus macaques due to the particular characteristics of male-male competition in this species.     

Prostaglandin F2α facilitates female mating behavior based on male performance

Hormones play an important role in the regulation of reproductive behavior. Here, we examined the effects of the fatty acid derivative prostaglandin F2α (PGF2) on female sexual behavior as well as the interaction between PGF2-induced mating behavior with male courtship display in the lek-breeding African cichlid fish, Astatotilapia burtoni. In a two-way choice paradigm, we found that nonreproductive females preferred to associate with smaller, less aggressive males over larger, more aggressive males. However, PGF2-treated females dramatically reversed their preference to larger males. In a second experiment, PGF2 treatment dramatically increased sexual behavior in nonreproductive females as measured by time spent in the bower of the stimulus male, even when the female and the stimulus male were separated by a transparent divider. This effect was even more pronounced when the stimulus males were exposed to the putative female pheromone 17α,20β-progesterone (17α,20β-P). Under full-contact conditions, only PGF2-treated females visited a stimulus male’s bower, where they even displayed circling behavior usually only seen during spawning. Interestingly, male performance prior to PGF2 treatment predicted female sexual response. Our study demonstrates the importance of PGF2 in the control of female reproductive behavior in interaction with male performance.     

The effects of male–male contests and female eavesdropping on female mate choice and male mating success in the jumping spider, <Emphasis Type="Italic">Thiania bhamoensis</Emphasis> (Araneae: Salticidae)

In experiments that comprised of three phases (fight, choice, and mating) under “seen” and “unseen” conditions, we examined the effects of the outcomes of male–male contests and female eavesdropping on female mate choice and male mating success in the fighting spider, Thiania bhamoensis (Salticidae). The results revealed female eavesdropping on agonistic interactions. Females that had watched an aggressive interaction showed no distinctive preference for the winner over the loser, but they preferred the loser when they had not observed a fight. Winners, however, achieved a greater mating success than did losers during the mating phase. Gaining access to females was based on the insistence of the winners in courtship in terms of the number of quivers, rather than on the fighting behavior of the males. Hence, the outcome of male–male contests may not be an important determinant of a male’s mating success in T. bhamoensis. Instead, courtship display plays an important role in determining the success of male mating in this species. This study also suggests that female mate preference may not be a good indicator of eventual female mate choice and male mating success. Thus, a causal relationship between female mate preference and male mating success cannot be inferred. Joanna P. Y. Chan, Pei Rong Lau, and Ai Jie Tham contributed equally.     

Chelipeds are the real weapon: cheliped size is a more effective determinant than body size in male–male competition for mates in a hermit crab

To understand the evolution of weapons, we must understand both their functions and relative importance compared to body size in determining fighting success. Many decapod crustaceans develop disproportionately large chelipeds for their body size and use them as a weapon in agonistic interaction. There are, however, examples where weapons are merely signals of resource holding potential (RHP) and the RHP is actually determined by body size. We investigated the function and relative efficacy of body size and major cheliped size in male–male contests for females in the hermit crab Diogenes nitidimanus. Contests over females took two forms: (1) males preemptively guarded females and opponents did not fight with the guarding male. Cheliped size contributed significantly to the settlement of these contests and probably functioned as a visual signal for the opponents. (2) Guarding males engaged in physical combat with an opponent. In these cases, both body and cheliped sizes affected contest outcomes. The effect size for cheliped size was as strong, or stronger, than that for body size. These results suggest that large chelipeds have evolved as a true weapon and are effective in escalated fights for resources. Therefore they are also efficient visual signals for settling contests with only display. Our results are a rare example that clearly demonstrate that weapons are a more important determinant of fights than body size when both body and weapon size affect resource acquisition.     

Does it matter that male beaugregory damselfish have a mate preference?

Male beaugregory damselfish (Stegastes leucostictus) spent more time courting larger females in both two-choice and single presentations. Female size was significantly correlated with gonad weight. We also verified that female fecundity was extremely variable within a natural population. We found that male reproductive success was highly correlated with both clutch size and clutch number. However, clutch size was not significantly correlated with clutch number, indicating that males that received larger clutches did not receive more egg clutches. Furthermore, there was no difference between the number of offspring produced by males that mated with the largest females and by males that mated with the most females. Thus, although males preferred larger females, males produced similar numbers of offspring by mating with large females or mating with many females. Received: 7 March 1997 / Accepted after revision: 1 November 1997     

Function of the major cheliped in male–male competition in the hermit crab <Emphasis Type="Italic">Pagurus nigrofascia</Emphasis>

Functions of the major cheliped in pagurid hermit crabs have been studied in fights for shells. The major cheliped often shows sexual size dimorphism, suggesting that sexual selection favors the development of the male major cheliped. The function of the major cheliped in male–male competition was examined in Pagurus nigrofascia collected from April to June 2009 on the intertidal rocky shore in southern Hokkaido, Japan (41°N, 140°E). Sexual size dimorphism of the major cheliped was observed, and precopulatory guarding males had larger major chelipeds than solitary ones. Guarding males used the major cheliped to deter intruders during competitive interactions. Males without a major cheliped were disadvantaged even if they were larger than opponents and had ownership. Cheliped size affected the outcomes of contests between similar sized males. This suggests that the male major cheliped in P. nigrofascia protects mates from competitors and, consequently, enhances male mating success. Sexual selection may favor the development of the major cheliped in male pagurids.     

Surplus territory contenders in male red-winged blackbirds: where are the desperados?

Summary We tested whether payoff asymmetries could explain why floater red-winged blackbirds seldom escalate contests to acquire territories. We removed territorial male \ldowners\rd and allowed floater replacements to claim territories. We then released owners to see how three currencies of payoff asymmetries (replacement occupancy) owners' likelihood and speed of reclaiming their territories (owner success). Neither the duration of an owner's internment nor the amount of time that a floater replacement had held the territory affected owner success (Figs. 1 and 2). Owner success was also not affected by the number of neighbors that they had (Fig. 3). Finally, owner success was the same irrespective of whether or not he was the likely sire of offspring on the territory, or the size of his harem (Fig. 4). Although these results are consistent with the proposal that payoff asymmetries will be irrelevant in contests for valuable resources, they are inconsistent with the proposal's corollary that excluded individuals should become \lddesperados\rd and escalate or even fight to the death in contests for those resources. Expected payoffs for passive acquisition of territories in this species may be higher than from a more aggressive desperado strategy.Correspondence to: P.J. Weatherhead     

Site fidelity of male Galápagos sea lions: a lifetime perspective

Knowledge about the distribution of resources can lead to the development of spatial preferences and long-term site fidelity. Individuals are expected to choose sites that best suit their needs. However, dominant individuals restrict movements of less competitive ones. Accordingly, one may expect spatial preferences to differ with regard to individual characteristics and to change over time. We investigated lifetime changes of site fidelity patterns with regard to reproductive success in male Galápagos sea lions (Zalophus wollebaeki). Showing a high degree of natal philopatry in the first 2 years of life, non-territorial males pass through a stage of fidelity to their natal colony where they develop preferences for areas outside prime breeding areas. Variation in the degree of spatial preferences was not associated with age or size, characteristics linked to an individual’s dominance status. For non-territorial males, roaming proved to be an adequate strategy to gain reproductive success. Only the most competitive males established territories in areas preferentially visited by females. They had a high probability to return to breeding areas where they successfully reproduced in previous seasons. Overall, the results reveal lifetime changes in site fidelity with regard to male status. The degree of site fidelity observed within the colony suggests familiarity and thus a high degree of tolerance among individuals using the same areas. This seems to facilitate attendance in the colony and thus the possibility to prospect for oestrus females.     

Reproductive consequences of male body mass and aggressiveness depend on females’ behavioral types

Relatively few investigations explicitly test for concordant versus conflicting selection pressures from intrasexual versus intersexual selection. Here, we examine the effects of male body mass and behavioral type (BT) on reproductive success in the spider Anelosimus studiosus, with emphasis placed on the potential interaction between intrasexual and intersexual selection influences. Female A. studiosus exhibit either an aggressive-active or docile-passive BT, both of which co-occur in multifemale colonies. Males, in contrast, exhibit a more continuous distribution of behavioral tendencies. We investigated the male traits favored by females in five trial types: one docile female, one aggressive female, four docile females, four aggressive females, and two docile and two aggressive females. Male reproductive success was estimated by the number eggs produced by females following staged mating trials. In previous work, it was established that large aggressive males are favored in male–male contests, an intrasexual effect. However, large aggressive males were not universally favored here. We failed to detect an effect of male body mass or aggressiveness on reproductive success in trials with all docile females; however, in situations involving aggressive females, large aggressive males experienced diminished reproductive success relative to small docile males. Large, aggressive males were also more likely to be attacked and killed by aggressive females in the first 20 min of staged encounters and were more likely to be found dead after 72 h of unobserved interactions. Taken together, our data suggest that the reproductive consequences of male traits differ based on (1) the aspect of sexual selection being considered (intrasexual versus intersexual) and (2) the BT of their prospective mates: large aggressive males enjoy advantages in intrasexual selection and when courting docile females and small docile males experience reduced risk of cannibalism and increased reproductive success with aggressive females.     

Providing parental care entails variable mating opportunity costs for male Temminck’s stints

Males of many species theoretically face a fitness tradeoff between mating and parental effort, but quantification of this is rare. We estimated the magnitude of the mating opportunity cost paid by incubating male Temminck’s stints (Calidris temminckii), taking advantage of uniparental care provided by both sexes in this species. “Incubating males” provide all care for an early clutch, limiting subsequent mating possibilities. “Non-incubating” males include males that failed to obtain, lost to predation, or actively avoided incubating clutches. These males were free to pursue extrapair copulations and to mate with females laying later clutches, which females usually incubate themselves. Male incubation classes did not differ in measures of quality, and many individuals changed classes between years, suggesting the use of conditional reproductive tactics. However, specialist non-incubators may also exist. Using microsatellites to assign parentage, we compare males’ total fertilizations and the subset “free of care” fertilizations between incubation classes. Incubators were more likely to gain at least one fertilization per season and averaged one more per season than non-incubators. However, successful non-incubators were more likely to gain “free of care” fertilizations, averaging two more than successful incubators. The relative success of male incubation classes also changed with local sex ratios. With higher female proportions, non-incubators gained disproportionately more offspring, suggesting that the use of tactics should be partly determined by the availability of potentially incubating females. Overall, we estimate the opportunity cost of incubating to be 13–25 % of the potential annual reproductive output.     

Female choice on male quantitative traits in lizards — why is it so rare?

Female choice on the basis of male traits has been described in an array of taxa but has rarely been demonstrated in reptiles. In the sand lizard (Lacerta agilis), and possibly in other non-territorial reptiles, a male's contribution to a female's fitness is restricted to his genes. In order to choose males of high genetic quality, females have to trade the fitness gain against the costs of active choice. In a Swedish population of sand lizards, long-lived males sired offspring with higher embryonic survival compared to offspring sired by short-lived males. In spite of this female sand lizards did not mate selectively with older and/or larger males. There appeared to be mo reliable cues to male longevity; age-specific male body size was highly variable. Furthermore, estimates of male nuptial coloration did not covary with ectoparasite load and, hence, females cannot use male coloration as a cue to heritable resistance to pathogenic parasite effects. When cues to male genetic quality are poor, or inaccurate, and males make no parental investment, we predict that female choice will be rare. Sand lizard females mating with many partners lay clutches with higher hatching success. Thus, females may obtain good genes for their young by multiple mating, thereby avoiding costs associated with mate choice.     

The lexicon of love: what cues cause size-assortative courtship by male garter snakes?

Cues that females use to select potential mates have attracted substantial research effort, but the criteria for male mate choice remain very poorly known. Red-sided garter snakes ( Thamnophis sirtalis parietalis) court and mate in large aggregations around overwintering dens in southern Manitoba, Canada. Both courtship and mating are size-assortative: small male snakes court small as well as large females, whereas larger males court only large females. This system provides a unique opportunity to assess the cues that males use in selecting mates, and in particular the mechanisms that generate a size-related shift in mate preference. Experiments in which we manipulated body sizes and scents showed that both vision and scent (sex pheromones) were important. Large males directed intense courtship only when the stimulus provided both visual and chemical (skin lipid) evidence of large body size. Small males were much less discriminating in both respects. Thus, size-assortative mating in this system is generated not by larger males excluding their smaller rivals from the largest females (as has been reported in other reptile species), but by a size-related shift in the visual and pheromonal cues that elicit courtship. Males of some species may thus show complex patterns of mate choice, with the cues that stimulate courtship differing even among males within a single population based on traits such as age or body size.     

Same-sex pair-bonds are equivalent to male–female bonds in a life-long socially monogamous songbird

Same-sex sexual behaviors are well documented in both captive and wild animals. In monogamous species, these behaviors are often exclusive, each individual having only one same-sex partner. A bias in sex ratio has been proposed as a social context yielding same-sex pair-bonding, but this hypothesis has rarely been tested. Focusing on a life-long pair-bonding songbird, the zebra finch Taeniopygia guttata, we tested whether same-sex pairing results from a shortage of individuals of the opposite sex. By experimentally skewing the sex ratio towards members of one sex, we observed a greater proportion of same-sex pair-bonds of that sex. Moreover, we assessed whether the quality and stability of social interactions were equivalent in same-sex and male–female pairs. Male–male and female–female same-sex bonds display the same behavioral characteristics as male–female ones: they are intense, highly selective, and stable affinitive relationships involving the same behavioral displays already described in wild birds. Moreover, same-sex male bonds were sufficiently strong not to split up when individuals were given the opportunity to reproduce with females. Because the pair-bond in socially monogamous species represents a partnership that may give advantages for survival (e.g., resources defense, fighting against predators, etc.), we propose that same-sex pairing in the zebra finch may result from the pressure to find a social partner.     

Does the cost of polygyny in house wrens include reduced male assistance in defending offspring?

Summary This study investigated whether reduced male aid in defending offspring potentially reduces the fitness of females choosing already-mated males in the house wren (Troglodytes aedon), a small, territorial songbird. Frozen snakes were placed at 23 nests of monogamously mated males and 12 secondary nests of bigamously mated males. All presentations were made during incubation stages of females attending focal nests. Snakes were placed at nests of secondary females when nests of their primary counterparts contained young 5–9 days old. Males are most attentive to primary nests during this period and should therefore be relatively inattentive to secondary mates and nests. Nevertheless, an equal proportion of monogamous and bigamous males discovered snakes within 15 min, and mean time to discovery, when discovery occurred, did not differ with nest status. Monogamous and bigamous males were also equally likely to attack snakes physically once discovered. Monogamous males appeared no more likely to discover snakes than bigamous males for two main reasons. First, although monogamous males were near focal nests (i.e., < 10 m) more often than bigamous males, monogamous males tended to stay out of view of nests for long periods. In contrast, bigamous males always went immediately to focal nests upon arriving in their vicinity. Second, about one-third of monogamous males in this study spent much of their time during trials at the far edges of their territories advertising for secondary mates. Our experiment suggests that reduced male aid in defending nests against small, diurnal predators probably does not contribute to the cost of polygyny in house wrens. Correspondence to: L.S. Johnson     

Does mating experience of male house crickets affect their behavior to subsequent females and female choice?

Male mating experience was shown to play an important role in settling conflicts between males; however, little is known about whether and how prior access to females influences male behavior during intersexual interactions and female choice itself. Here, I experimentally test this relationship in the house cricket (Acheta domesticus) by combining one-on-one interaction between the male and female with direct comparison of males by the female, but precluding aggression between males. I found that solitary males were more active during subsequent courtship displays than paired males, suggesting the detrimental effect of mating on courtship performance. At the same time, females spent significantly more time close to solitary males or playbacks of male's natural courtship songs, and responded positively to the condition of males, ignoring body size of males. In contrast, females responded similarly to computer-modified playbacks of courtship songs of solitary and paired males with standardized rate of phrases and amplitudes; however, when females were additionally allowed to contact with anesthetized males they spent more time close to bigger males, irrespective of the acoustic parameters of courtship songs. These results show that although females were able to differentiate between many behavioral and morphological characteristics of males, including voluntary and intrinsic ones, they preferred traits conditional upon the costliness of male's displays. In addition, mating experience appeared to be a crucial factor in the choice of a particular costly mating strategy by males.     

Are nest characters of importance when choosing a male in the fifteen-spined stickleback (Spinachia spinachia)?

Male fifteen-spined sticklebacks (Spinachia spinachia) build their nests by wrapping epiphytic algae around macroalgae and securing them with secretional threads. In this study, I show that female fifteen-spined stickleback prefer males which have built their nests above the surrounding vegetation. High-located nests are safer, because they are less likely to attract egg-predators such as shore crabs (Carcinus maenas). Thus, I found that shore crabs more rapidly find eggs in nests built close to the bottom than in nests well above the it. Moreover, male-male competition could be an additional explanation as to why males build nests high up. Thus, my field results suggest that the closer the males were to a neighbour, the higher they built. Larger males were also found to have larger territories but male size did not correlate with the height of the nest above the surrounding vegetation. Females showed no preference for nest size, regardless of the presence of egg-predators. However, they tended to choose nests that had no egg-predators in the vicinity over nests with egg-predators close by. Female choosiness for certain nest characters may provide one explanation for the evolution of male care in this species. Received: 29 December / 1999 Revised: 18 April 2000 / Accepted: 28 May 2000