Male sexual attractiveness and aggressiveness in rodents having different mating systems

Male aggressiveness can affect male reproductive success both directly by increasing competitiveness and indirectly through female preference. Assuming that significance of male aggressiveness in species having different mating systems can be different, we studied how male aggressiveness relates to sexual attractiveness in polygynous rodents, the water vole (Arvicola terrestris) and the house mouse (Mus musculus), and in a monogamous species, the steppe lemming (Lagurus lagurus). Our analysis revealed that the relation between odor attractiveness and aggressiveness is nonlinear. In polygynous species, males are more aggressive, so females opt for aggressive, albeit not too aggressive, males. In the monogamous steppe lemming, males show low level of intermale aggressiveness, and the most attractive are slightly aggressive males who have greater reproductive potential.     

Virgin females compete for mates in the male lekking species Ceratitis capitata

Abstract. Aggressive behaviour occurring in intrasexual competition is an important trait for animal fitness. Although female intrasexual aggression is reported in several insect species, little is known about female competition and aggressive interactions in polygynous male lekking species. The interactions of female Mediterranean fruit flies, Ceratitis capitata (a male lekking species), with other females and mating pairs under laboratory conditions are investigated. Mature, unmated (virgin) females are aggressive against each other and against mating pairs, whereas immature females are not. Female aggression against other females decreases dramatically after mating; however, mated females maintain aggression against mating pairs. In addition, higher intrasexual aggression rates are observed for mature, virgin females than for virgin males of the same age. The results show that female aggressiveness is virginity related, suggesting female competition for mates. These findings have important implications for understanding the physiological aspects of a complex social behaviour such as aggression and should stimulate further research on female agonistic behaviour in male lekking mating systems.     

Male competition and its hormonal correlates in Assamese macaques (Macaca assamensis)

In polygynous mammals, where males compete over access to females, the potential of males to monopolize reproductive females largely depends on the spatio-temporal distribution of reproductive females. We investigated mechanisms of male reproductive competition and its hormonal basis in a cercopithecine species with reduced contest potential owing to female reproductive synchrony and concealed ovulation. Over 16 months including two mating seasons we collected 1218 h of observational focal animal data and 1254 fecal samples of 11-12 adult and large subadult male Assamese macaques (Macaca assamensis) living in their natural habitat in Thailand. Androgen output along with aggressive behavior showed a seasonal pattern, with highest values being obtained by all males during the mating season and by those males experiencing acute social challenges, e.g. rank change and dispersal. Individual androgen levels and rates of attacks were linked across the study period, suggesting a promoting function of androgens for aggressive behavior. Dominance rank predicted neither mating success nor androgen levels consistently, indicating a reduced selective advantage of high social status for general mating access. However, high ranking males engaged in extended consortships with reproductive females. Distribution of consortships across males followed a priority of access distribution, with the two top ranking males accounting for 75% of consort activity, suggesting that high social status also carries fitness benefits in a species characterized by low contest potential.     

The Influence of Male Body Size and Social Environment on the Mating Behavior of Phallichthys quadripunctatus (Pisces: Poeciliidae)

In some poeciliid fishes, variation in male size is accompanied by differences in mating behavior. Large males are preferred by females and perform courtship displays followed by copulatory thrusts, whereas small males perform copulatory thrusts with few or no displays. This phenomenon has been described in only a few genera and little is known about mating behavior in other poeciliids. Although Phallichthys quadripunctatus males display size dimorphism that has a genetic component, mating behavior of this species has not been documented. We conducted experiments using socially experienced and socially naive males to characterize the mating behavior of this species and to evaluate potential size-dependent differences in behavior. Males were tested with postpartum (presumably receptive) and midcycle (presumably unreceptive) females in different social environments. Whereas neither size class of P. quadripunctatus males performed courtship displays or altered behavior based on female receptivity, large males performed several reproductive behaviors more frequently than small males. This trend was repeatable and occurred in all social environments examined. Some males also attempted to mate with other males, with small males showing a greater tendency to perform this behavior than large males. The manner in which differences in reproductive activity translate into differences in reproductive success must be examined before inferring sexual selection favoring large males in P. quadripunctatus.     

Sexual Selection in Black Morph Girardinus metallicus (Pisces: Poeciliidae): Females Can Spot a Winner (But We Cannot)

Male–male competition may interfere with the ability of females to choose mates by interrupting courtship or by favoring highly aggressive males who may damage females during mating attempts. Alternatively, females may benefit by mating with dominant males, and female choice and male–male competition may therefore act in unison. The same traits, including aggressiveness, may indicate male quality to females and to rivals. We investigated sexual selection in the black morph of the endemic Cuban poeciliid fish, Girardinus metallicus, to ascertain the links between morphological and behavioral traits and success in intra‐ and intersexual selection. Males conspicuously exhibit their black ventral surface and gonopodium to females during courtship. Dichotomous choice tests revealed female association preferences for certain males, and those same males were more successful in monopolizing access to females when the fish were allowed to directly interact. Dominant males followed, courted, and copulated with females more than subordinate males within a pair, and it appears that females could either assess dominance based on cues we did not measure, or could influence subsequent mating success by their behavior during the dichotomous choice trials. There was an interaction between black status (i.e., whether the male in each pair had more or less ventral black coloration than the other male in that pair) and dominance, such that low‐black dominant males courted early and then shifted to following females, whereas high‐black dominant males courted far more later in the observation period. These results hint at the importance for sexual selection of the interplay between a static morphological trait (black coloration) and a dynamic behavioral trait (aggressiveness), but the functional significance of the courtship display remains a mystery.     

Sex Differences in Mate Preference Between Two Hybridizing Species of Poeciliid Fish

When hybridization between two species in secondary contact is costly, natural selection should favor pre‐mating isolation barriers. The invasive Gambusia affinis has been introduced to habitats of a closely related species, the endangered Gambusia nobilis. Although other Gambusia species readily hybridize in secondary contact, previous studies in this system found low abundance of hybrids in sympatry. To examine whether hybridization is limited by behavioral pre‐mating isolation that may have evolved in allopatry, I examined each species’ mating preferences using individuals from allopatric populations in male and female visual/olfactory association preference tests as well as open mating tests with and without male–male competition. Gambusia affinis and G. nobilis males had significant association preference for conspecific females in visual/olfactory tests. Only G. nobilis females had statistically significant preference for conspecific males. In open mating tests, males of both species had lower chase times overall when in competition, but there was no difference in number of copulation attempts. Males of both species had higher copulatory success rates with conspecific females when in competition, suggesting females may exert some control over copulation success of males. These results suggest that there are differences in mating preferences between these species. This mate choice may act as a pre‐mating isolating barrier to reduce hybridization in sympatry, a proposed threat to the endangered G. nobilis.     

Size-mediated dominance and aggressive behavior of male Japanese fluvial sculpin Cottus pollux (Pisces: Cottidae) reduce nest-site abundance and mating success of conspecific rivals

Despite growing evidence for plasticity in the mating patterns of nest-holding animals in relation to the changes in nest abundance, the effects of aggressive interaction by dominant males on nest availability for conspecific rivals remains unclear. To quantify the effects of male–male competition on nest-site choice and mating success of the male Japanese fluvial sculpin Cottus pollux, we conducted experiments on 5 males from different 5 size classes under both sufficient and shortage nest-abundance conditions. Nest-choice experiments showed that both male size class and nest-abundance condition had significant effects on the nesting rates of males. Following the nest-choice experiments, 10 gravid females were added in the experimental tanks. Mating experiments revealed that male size, nesting rate before addition of females, and the number of courtship attempts on females were valid variables of male mating success, regardless of nest-abundance conditions. After achieving initial mating success, the largest nesting male exhibited more frequent aggressive interaction with other conspecific males than he did before obtaining eggs in his nest. Our results suggest that size-mediated dominance and aggressive behavior of males may disrupt nest acquisition of other conspecific males, and may consequently result in extreme variation in mating success among males even under sufficient nest-abundance conditions.     

Sexual Selection, Epistasis and Species Boundaries in Sympatric Hawaiian Picture-winged Drosophila

The Hawaiian picture-winged flies in the genus Drosophila are a spectacular example of rapid evolutionary diversification in which sexual selection is considered an important mechanism for reproductive isolation and speciation. We investigated the behavioral reproductive isolation of two closely related and sympatric Hawaiian picture-winged Drosophila species, D. silvestris and D. heteroneura, which are known to hybridize in nature and produce viable and fertile hybrids. We compared the mating success of parental, F1 and backcross males in pairings with D. heteroneura females. The F1 males were produced by mating D. heteroneura males with D. silvestris females, and the backcross males were produced by mating F1 females with D. heteroneura males. The mating success of backcross males paired with D. heteroneura females were significantly reduced relative to that of parental and F1 males. This reduced mating success occurred primarily at a late stage of courtship where female choice of mate may be important. Two- and three-gene models demonstrate that epistasis involving a few genes could account for the observed variation in male mating success. These results are consistent with negative epistasis in the backcross generation and support the importance of sexual selection and negative epistasis in the evolution and maintenance of these species.     

`Little Chipmunk' Syndrome? Male Body Size and Dominance in Captive Yellow‐Pine Chipmunks (Tamias amoenus)

In mammals, large males are often assumed to have higher mating success because they have greater success at contest competition. This relationship is often used to explain the prevalence of male-biased sexual size dimorphism in mammals. However, in many small vertebrates, large individuals are not always dominant. Using staged dyadic encounters, we examined the relationship between male body size and social dominance in captive male yellow-pine chipmunks ( Tamias amoenus ), a species with female-biased sexual size dimorphism. The yellow-pine chipmunk has a mating system in which males participate in mating chases and dominant males may have an advantage in acquiring matings with oestrous females. Captive male chipmunks were aggressive in only 28% of 144 paired encounters; however, several lines of evidence indicated that smaller chipmunks were dominant over large chipmunks: (1) small males were dominant in more dyads than large males; (2) within dyads, dominant males were smaller than subordinate males; and (3) small males performed more aggressive behaviour than large males. These results are not consistent with the prediction that large males are typically dominant. If large chipmunks are able to gain matings with females because of qualities other than dominance (such as the ability to successfully find and/or chase receptive females), then the costs of aggression to large chipmunks may outweigh any potential benefits. Small males, but not large males, may improve their mating success by being aggressive.     

Pre‐ and postcopulatory sexual selection favor aggressive,young males in polyandrous groups of red junglefowl

A challenge in evolutionary biology is to understand the operation of sexual selection on males in polyandrous groups, where sexual selection occurs before and after mating. Here, we combine fine‐grained behavioral information (>41,000 interactions) with molecular parentage data to study sexual selection in replicated, age‐structured groups of polyandrous red junglefowl, Gallus gallus. Male reproductive success was determined by the number of females mated (precopulatory sexual selection) and his paternity share, which was driven by the polyandry of his female partners (postcopulatory sexual selection). Pre‐ and postcopulatory components of male reproductive success covaried positively; males with high mating success also had high paternity share. Two male phenotypes affected male pre‐ and postcopulatory performance: average aggressiveness toward rival males and age. Aggressive males mated with more females and more often with individual females, resulting in higher sexual exclusivity. Similarly, younger males mated with more females and more often with individual females, suffering less intense sperm competition than older males. Older males had a lower paternity share even allowing for their limited sexual exclusivity, indicating they may produce less competitive ejaculates. These results show that—in these populations—postcopulatory sexual selection reinforces precopulatory sexual selection, consistently promoting younger and more aggressive males.     

EFFECTS OF SOCIAL AND EXTRA‐PAIR MATING ON SEXUAL SELECTION IN BLUE TITS (CYANISTES CAERULEUS)

The contribution of extra‐pair paternity (EPP) to sexual selection has received considerable attention, particularly in socially monogamous species. However, the importance of EPP remains difficult to assess quantitatively, especially when many extra‐pair young have unknown sires. Here, we combine measurements of the opportunity for selection (I), the opportunity for sexual selection (I_S), and the strength of selection on mating success (Bateman gradient, β_SS) with a novel simulation of random mating tailored to the specific mating system of the blue tit (Cyanistes caeruleus). In a population where social polygyny and EPP are common, the opportunity for sexual selection was significantly stronger and Bateman gradients significantly steeper for resident males than for females. In general, success with the social mate(s) contributed most to variation in male reproductive success. Effects of EPP were small, but significantly higher than expected under random mating. We used sibship analysis to estimate the number of unknown sires in our population. Under the assumption that the unknown sires are nonbreeding males, EPP reduced the variance in and the strength of selection on mating success, a possibility that hitherto has not been considered.     

The Haremic Mating System and Mate Choice in the Wide-Eyed Flounder, Bothus podas

The social structure and reproductive behaviour of the wide-eyed flounder, Bothus podas, was studied in the coastal waters around the Azorean Islands. Both sexes are territorial throughout the year. Adult males defend large territories, which include several smaller female territories. Intraspecific agonistic behaviour was frequent and differed between sexes: males were more aggressive towards other males, while females were only aggressive towards each other and juveniles. During the reproductive season and only at dawn, territorial males court and mate successively with females in their territories, and females seem to show mating fidelity to their dominant male. Such territoriality and mating patterns indicate a haremic social system in the wide-eyed flounder. In order to identify potential factors influencing female mate choice acting on this haremic system, we examined male mating success and some of its potential correlates. We found no evidence for female preference for any of the males' physical or territory characteristics. However, courtship effort was strongly correlated with the total number of attempted and successful spawnings, indicating that females seem to mate preferentially with males that court them more vigorously. Thus, our data suggest that courtship plays an important role in determining male mating success in the wide-eyed flounder and, that it may possibly serve as an honest indicator of male `quality' for female choice.     

SEXUAL SELECTION AGAINST HYBRIDS BETWEEN SYMPATRIC STICKLEBACK SPECIES: EVIDENCE FROM A FIELD EXPERIMENT

Sexual selection against viable, fertile hybrids may contribute to reproductive isolation between recently diverged species. If so, then sexual selection may be implicated in the speciation process. Laboratory measures of the mating success of hybrids may underestimate the amount of sexual selection against them if selection pressures are habitat specific. Male F₁ hybrids between sympatric benthic and limnetic sticklebacks (Gasterosteus aculeatus complex) do not suffer a mating disadvantage when tested in the laboratory. However, in the wild males choose different microhabitats and parental females tend to be found in the same habitats as conspecific males. This sets up the opportunity for sexual selection against male hybrids because they must compete with parental males for access to parental females. To test for sexual selection against adult F₁ hybrid males, we examined their mating success in enclosures in their preferred habitat (open, unvegetated substrate) where limnetic males and females also predominate. We found significantly reduced mating success in F₁ hybrid males compared with limnetic males. Thus, sexual selection, like other mechanisms of postzygotic isolation between young sister species, may be stronger in a wild setting than in the laboratory because of habitat-specific selection pressures. Our results are consistent with, but do not confirm, a role for sexual selection in stickleback speciation.     

Application of paternity discrimination by DNA polymorphism to the analysis of the social behavior of primates

Paternity in many primate species cannot be established reliably on behavioral grounds. For instance, Japanese macaques (Macaca fuscata) have a multi-male group structure and promiscuous mating patterns. On the other hand, accurate evaluation of male reproductive success is needed to analyze primate behavior. DNA finger-printing techniques were applied to 2 captive groups of Japanese macaques in the Primate Research Institute of Kyoto University for identification of paternity. Also, mating behavior of a captive group was observed in order to compare the reproductive success of each male with that expected on the basis of his observed mating activity. The number of offspring of full adult males was not related to their social rank although the number of copulations with ejaculation was highly correlated with their social rank. Monitoring of the female sexual cycles from the plasma profiles of gonadotropins and ovarian hormones suggested that males could not choose females at days of ovulation. The results of two-free-ranging wild troops, like those of the captive groups, indicated that high-ranking males could not monopolize the paternity of offspring. The results of paternity discrimination in Japanese macaques were compared with results from patas monkeys (Erythrocebus patas) in a discussion of social structure and male reproductive success. Some aspects of polymorphism detection techniques are also discussed.     

Potentially infanticidal behavior in the Amazon river dolphin (<Emphasis Type="Italic">Inia geoffrensis</Emphasis>)

Infanticide by males is a phenomenon common in species in which the reproductive output of large numbers of females can be monopolized by a small number of males. It is thought to increase a male’s fitness, at the expense of the fitness of the infant’s parents, by bringing females into season more quickly. Infanticide by males has been recorded in just three cetacean species. We report aggressive behavior suggestive of infanticide in a fourth, the Amazon river dolphin (Inia geoffrensis). We observed and photographed a series of attacks on a neonate Amazon river dolphin by a large male, with apparent protective behavior by the mother. Although infanticide was not confirmed, the forceful, aggressive behaviors were highly suggestive of infanticidal behavior and represent another important data point for comparative studies of infanticide in mammals. Amazon river dolphins may have a polygynous, polyandrous, or promiscuous mating system, the latter two of which are not the norm in species in which the reproductive output of large numbers of females are monopolized by a small number of males. However, sexual dimorphism, high rates of aggression by males, socio-sexual object-carrying displays by males, and a long interbirth interval suggest that successful male Amazon river dolphins may be able to monopolize a large proportion of mating opportunities, and it is plausible that male dolphins can improve their reproductive success by bringing females into estrous sooner by killing the offspring of other males.     

Effect of male-to-male aggressiveness and feed-restriction during rearing on sexual behaviour and aggressiveness towards females by male domestic fowl

This experiment was one part of a larger study investigating problems of aggression towards females by male broiler breeder fowl. To investigate causal mechanisms, we were interested in determining (1) if feed-restriction during rearing affects behaviour towards females at sexual maturity and (2) if aggressiveness towards females is correlated with general levels of aggressiveness. We compared broiler breeder males with commercial laying strain males, which were either fed ad libitum or were feed-restricted during the rearing phase, and with game strain males, bred for fighting. Differences in behaviour were determined by observing males during interactions with small groups of females.Laying strain males did not behave aggressively towards females, whether feed-restricted or fed ad libitum during rearing. Despite genetic selection for fighting ability, game strain males also were not aggressive towards females. Conversely, broiler breeder males displayed significantly higher levels of aggression towards females than did feed-restricted laying strain males (P<0.02). Broiler breeder males were rough with females during mating, whereas laying strain and game strain males were not. Females struggled more frequently during mating attempts by broiler breeder males (P<0.002) and interfered frequently when these males attempted to mate with other females.From our results, we conclude that (1) feed-restriction during rearing has little effect on the sexual and aggressive behaviour of laying strain males at maturity and (2) selection for aggressiveness has not resulted in males which are more aggressive to females. Aggression towards females appears to be a unique problem occurring in broiler breeder male strains and not a function of feed-restriction.     

Old‐male paternity advantage is a function of accumulating sperm and last‐male precedence in a butterfly

Old‐male mating advantage has been convincingly demonstrated in Bicyclus anynana butterflies. This intriguing pattern may be explained by two alternative hypotheses: (i) an increased aggressiveness and persistence of older males during courtship, being caused by the older males' low residual reproductive value; and (ii) an active preference of females towards older males what reflects a good genes hypothesis. Against this background, we here investigate postcopulatory sexual selection by double‐mating Bicyclus anynana females to older and younger males, thus allowing for sperm competition and cryptic mate choice, and by genotyping the resulting offspring. Virgin females were mated with a younger virgin (2–3 days old) and afterwards an older virgin male (12–13 days old) or vice versa. Older males had a higher paternity success than younger ones, but only when being the second (=last) mating partner, while paternity success was equal among older and younger males when older males were the first mating partner. Older males produced larger spermatophores with much higher numbers of fertile sperm than younger males. Thus, we found no evidence for cryptic female mate choice. Rather, the findings reported here seem to result from a combination of last‐male precedence and the number of sperm transferred upon mating, both increasing paternity success.     

Mating success in the spittlebug Cercopis sanguinolenta (Scopoli, 1763) (Homoptera, Cercopidae): the role of body size and mobility

In insects, a sexual size dimorphism commonly occurs, with larger females. However, as a deviation from this general rule, larger males are found in some species. In these species often sexual selection for large males has been presumed. The spittlebug Cercopis sanguinolenta exhibits a distinct sexual size dimorphism with larger males. Mating behaviour was studied in a field population in respect to mating success of males and females. The aim of this study was to examine the mechanisms that lead to the observed non-random mating pattern. The results showed a mating pattern without size-assortative mating. A correlation was found between mating success and body size in males. In females no such correlation was found. The mobility of males depends on their body size and mobility is high only when females are present. However, in an analysis of covariance it was found that male mating success is not correlated with mobility, when controlled for body size. The mating system of the spittlebug was classified as scramble competition polygyny. Electronic Publication     

Mating Success in the Polyandrous Social Wasp Vespula maculifrons

The mating decisions made by social insect males and females profoundly affect the structure of colonies and populations. However, few studies have used experimental approaches to understand mating behavior and mate choice in social insect taxa. This study investigated mating success in the polyandrous social wasp Vespula maculifrons. Mating trials were designed to test predictions that characteristics of body size and colony‐of‐origin would affect mating success. We first investigated if size differences existed among individuals and found that males from different colonies differed significantly in the size of nine morphological traits. However, male trait size was not significantly associated with male mating success. In contrast, females from different colonies differed significantly in only six of the nine measured traits, and four of these traits were associated with successful mating behaviors. Specifically, the correlated traits of gaster length, third tergum length, antennal length, and total length were positively associated with female mating success. Thus, long females experience mating advantages over females that are short. We also found that males and females from one particular colony displayed significantly greater mating activity than individuals from other colonies. Thus, the colony from which individuals originate plays an important role in determining mating success. Finally, our experiments failed to detect any evidence of nestmate avoidance during the mating trials. Overall, our data suggest that social insect reproductives may experience differential mating success based on their phenotype or developmental environment.     

The effects of male harassment on mating duration in the seed bug,Togo hemipterus

Harassment on mating pairs by solitary males is usually considered an attempt by the male to (1) take over the female, (2) guard the female against further insemination (when the solitary male has previously copulated with this female), or (3) influence mating duration. Paired males of a seed bug repel harassment on mating pairs by solitary males by firmly grasping females using their legs and/or genital claspers; in this way, mating duration is prolonged. Male fertilization success increases as mating duration increases. Males of the seed bug, Togo hemipterus (Scott) (Heteroptera: Lygaeidae), use seminal substances to inhibit female remating. These substances induce protracted female refractory periods and are transferred to the females in a time‐dependent manner. Consequently, mating duration has important effects on fitness in this species. We observed harassment on T. hemipterus mating pairs by solitary males, and examined conflicts between paired and solitary males over mating duration. None of the solitary males were able to take over a mating female, and this may be due to the unique male genital structure in this species. All conflicts over mating duration resulted in wins by the paired males over the solitary males. Paired males prolonged mating durations, whereas severe harassment on mating pairs by solitary males shortened durations. We show that even though there is no immediate reward for the solitary male (i.e., it is unable to take over the mating female), this harassment behavior may be adaptive.