Sexual selection, natural selection and copulatory patterns in male primates.

Complex copulatory patterns, involving multiple brief intromissions or prolonged single intromissions (PI) occur most frequently among primate species in which females mate with a number of partners (multimale and dispersed mating systems). However, the PI pattern is also confined almost exclusively to arboreal primates - to either smaller-bodied, cryptic, nocturnal species or much larger diurnal forms. Predation pressures may have limited the evolution of the PI pattern, particularly where small-bodied diurnal primates or terrestrial forms are concerned. The available evidence indicates that both sexual selection and natural selection may have influenced the evolution of copulatory patterns.     

Prenatal stress alters reproductive responses of rats in behavioral estrus and paced mating of hormone-primed rats

Adult female offspring of dams exposed to gestational stress (prenatal stress, PNS) may show altered reproductive behavior, exploration in novel environments, and/or social interactions than do their non-PNS counterparts. These behavioral differences may be more readily observed in a seminatural, paced mating paradigm, in which females have greater control of their sexual contacts, than in a standard mating situation. Adult offspring of dams exposed to restraint and lights for 45 min on Gestational Days 14-20 (PNS) were compared with those not subjected to stress (non-PNS, control condition). The motor, reproductive, and sociosexual behaviors of hormone-primed (Experiment 1) or cycling adult offspring in behavioral estrus (Experiment 2) were examined following 20 min of restraint stress under bright lights (postnatal stress). Hormone-primed PNS rats displayed less motor behavior in a novel arena than did non-PNS rats. In a standard mating test, hormone-primed PNS females tended to be more aggressive toward the male than were non-PNS rats. In a seminatural mating situation, hormone-primed PNS females showed increased avoidance behavior, such as longer latencies to the initial intromission, greater return latencies following mounts and intromissions, and more exiting subsequent to mounts and intromissions, than did non-PNS rats. PNS rats in behavioral estrus had decreased incidence and intensity of lordosis, and fewer solicitation behaviors, in both standard or paced mating situations, in which latency to and number of mounts were also increased. Thus, hormone-primed PNS rats exposed to restraint showed more avoidance behaviors in paced mating situations, while cycling PNS rats in behavioral estrus had greater disruption of reproductive responses in standard or paced mating paradigms than did non-PNS control rats.     

Impact of Male Infanticide on the Social Structure of Mountain Gorillas

Infanticide can be a major influence upon the social structure of species in which females maintain long-term associations with males. Previous studies have suggested that female mountain gorillas benefit from residing in multimale groups because infanticide occurs when one-male groups disintegrate after the dominant male dies. Here we measure the impact of infanticide on the reproductive success of female mountain gorillas, and we examine whether their dispersal patterns reflect a strategy to avoid infanticide. Using more than 40 years of data from up to 70% of the entire population, we found that only 1.7% of the infants that were born in the study had died from infanticide during group disintegrations. The rarity of such infanticide mainly reflects a low mortality rate of dominant males in one-male groups, and it does not dispel previous observations that infanticide occurs during group disintegrations. After including infanticide from causes other than group disintegrations, infanticide victims represented up to 5.5% of the offspring born during the study, and they accounted for up to 21% of infant mortality. The overall rates of infanticide were 2–3 times higher in one-male groups than multimale groups, but those differences were not statistically significant. Infant mortality, the length of interbirth intervals, and the age of first reproduction were not significantly different between one-male versus multimale groups, so we found no significant fitness benefits for females to prefer multimale groups. In addition, we found limited evidence that female dispersal patterns reflect a preference for multimale groups. If the strength of selection is modest for females to avoid group disintegrations, than any preference for multimale groups may be slow to evolve. Alternatively, variability in male strength might give some one-male groups a lower infanticide risk than some multimale groups, which could explain why both types of groups remain common.     

Male Competition,Mating Success and Female Choice in a Seasonally Breeding Primate (Erythrocebus patas)

Mammals with restricted breeding seasons often show brief but intense bouts of male competition for mates and male reproductive success has been attributed to male competitive abilities, with the most aggressively successful males able to control access to fertile females, or with females choosing to mate with such males. We studied male competition, mating behaviour and female mate selection in patas monkeys, a primate with a restricted breeding period. We observed two habituated patas groups in Laikipia District, Kenya, during Jun.-Aug. 1983. During the study, one group had a single resident male while the other group had multiple adult males. Within the multimale group, experienced adult males were no more successful than the subadult male. The sole resident male had a significantly higher rate of fights won (p < 0.02) although he did not differ from the multimale group males in rate of aggression or initiation of fights. We found no significant differences in either mating success or female preference based on males' experience or residency. The rates at which males copulated with and were solicited by females were not significantly correlated. We found no evidence of stable dominance ranks among males in the multimale group and aggressive success was not significantly correlated with copulation rate for males in the multimale group. Subadult males were responsible for the majority of copulations observed during the final third of the breeding season. Our observations of this patas population showed a fluid number of males in groups, with the same groups able to shift rapidly from single to multimale structure. This fluidity may result from the large fluctuations in numbers of breeding-age males and females observed over 4 yr of studying this population.     

Copulatory behaviour of the bank voleMyodes glareolus: matings with one and two males do not make a difference

In promiscuous species in which females mate with more than one male during oestrus, males may increase their sperm expenditure or change their copulatory behaviour in response to the risk of sperm competition. I used an experimental approach to investigate the pattern of copulatory behaviour of the bank voleMyodes glareolus Schreber, 1780 depending on whether the female mated with one or two males. The work showed that the copulatory period of the bank vole lasted about 80 minutes and consisted of 4–5 ejaculatory series, with multiple intromissions preceding ejaculation. There were no significant changes in number of intromissions across the first four ejaculatory series, but I did find a relationship between number of intromissions and first ejaculation latency; also, ejaculation latencies grew shorter as the ejaculatory series proceeded. Litter size did not differ significantly between females that mated with one male and those mating with two, nor did the reproductive success of males that mated with the same female. Mating with an oestrus female appears to be advantageous for bank vole males even if they mate as the second one, and the risk of sperm competition did not trigger changes in male copulatory behaviour. The similar durations of the copulatory period and patterns of change of ejaculation latencies during copulations with one and two males point to the role of the female in temporal copulatory behaviour of the bank vole.     

Demographic and reproductive patterns in moustached tamarin monkeys (Saguinus mystax): Implications for reconstructing platyrrhine mating systems

In this paper we address a series of questions concerning reproductive opportunities, kinship, dispersal, and mating patterns in free-ranging moustached tamarin monkeys (Saguinus mystax). Between 1980 and 1990 information on group size, composition, and migration patterns was collected on marked groups of moustached tamarins inhabiting Padre Isla, an island in the Amazon Basin of northeastern Peru. In 1990, 86% of 114 animals residing in 16 social groups were trapped, examined, and released. Mean group size was 7.0, including 2.2 adult males and 2.0 adult females. None of these groups was characterized by a single adult male-female pair. In groups with more than one adult female, only the oldest female produced offspring. An examination of dispersal patterns indicates that transfers between groups were common and fell into several categories, including immigration of individual males and females, simultaneous transfer of pairs of subadult and/or adult males (sometimes relatives) into the same social groups, and group fissioning in which males and females of the splinter group join another small social group. We have no unambiguous cases of 2 adult/subadult females migrating together into the same social group. All 6 groups for which reproductive data were available were characterized by either a polyandrous or polygynous (polygyandrous) mating pattern. The results of this study indicate that moustached tamarins reside in small multimale multifemale groups that are likely to contain both related and unrelated adult group members. Kinship and social ties among males appear to be stronger and more longlasting than kinship and social ties among females. We contend that the modal mating system of moustached and many other tamarins is not monogamous, and offer the possibility that cooperative infant care and mating system flexibility in callitrichines evolved from a polygynous mating pattern. © 1993 Wiley-Liss, Inc.     

Copulatory Plug Displacement Evidences Sperm Competition in Lemur catta

Male displacement of copulatory (sperm) plugs from female vaginas provides further evidence for sperm competition in ring-tailed lemurs (Lemur catta), a gregarious prosimian species with a multimale, multifemale mating system. During two mating seasons, I studied two groups of free-ranging ring-tailed lemurs on St. Catherines Island, GA, USA. I observed 22 mating pairs in which males achieved penile intromission. Copulatory plug displacement by males occurred in 9 cases. Plugs were displaced during copulation by male penes upon withdrawl following deep vaginal thrusting. In every case of copulatory plug displacement, the male displacing a plug mated to ejaculation with the estrous female. In a mating system in which females typically mate with more than one male during estrous, often in succession, copulatory plug displacement may function to disrupt or preclude other males' successful insemination of estrous females. The effects of sperm plug displacement on paternity in Lemur catta are unknown, as no study had heretofore documented copulatory plug displacement in this species. The first-male mating advantage suggested for Lemur catta should be re-evaluated where mating order is known, and copulatory plug displacement during mating, or lack thereof, is identified. Because there is a tendency for first-mating males to mate-guard for longer periods of time in Lemur catta, the latency period between the first mate's ejaculation and that of subsequent mates may be an important determinant of male fertilization success.     

Female rats exhibit a conditioned place preference for nonpaced mating

Paced, but not nonpaced, mating behavior is reported to induce a conditioned place preference (CPP) in female rats. Contrary to these previous findings, Experiment 1 showed that female rats that received 15 intromissions from a single male rat during each of five conditioning sessions exhibited a CPP for the compartment associated with mating when the intromissions were delivered via a paced or nonpaced paradigm. Experiment 2 demonstrated that nonpaced mating induced a CPP when a single male delivered the 15 intromissions but not when the male was replaced following ejaculation and a new male allowed to complete the requisite number of intromissions. These findings invite reevaluation of the reinforcing aspects of mating behavior in female rats.     

Assortative Mating by Size in the American Rubyspot Damselfly (<Emphasis Type="Italic">Hetaerina americana</Emphasis>)

Assortative mating refers to the non-random nature of mating patterns between certain males and females. Thus, males and females may associate negative- or positively, based on different traits. Amongst these associations, assortative mating by size is one of the most common patterns found in natural populations of animals. Two main hypotheses have been proposed to account for the occurrence of assortative mating by size. First, it may be the result of mechanical, temporal, or physiological constraints. Second, it may occur in response to direct or indirect selection on mating preferences. Here we investigate whether the American rubyspot damselfly exhibits true assortative mating by size. Males of this species exhibit high levels of male-male competition, as they compete over territories, to which females are attracted for copulation. There is a documented large male body size advantage: the largest males are better able to hold their territories and thus secure more copulations. Our major results show that i) mated males are more likely to be larger than unmated males, whereas mated and unmated females tend to have similar body sizes; ii) H. americana exhibits true assortative mating by size; as such, this pattern is not driven by seasonal changes in the body sizes of males and females. We suggest that this mating pattern occurs in this species given the advantages of large male size, and the advantages of large female body size (i.e. higher fecundity). We believe that males may be able to evaluate a female’s reproductive value and exert mate choice.     

Male copulatory patterns in the lesser bushbaby (Galago moholi) in captivity

I observed seven pairs of sexually mature, captiveGalago moholi during the females’ ovarian cycles to determine the pattern of male copulatory behavior and its relationship to female receptivity. In this species, a copulatory lock was not apparent, a variety of thrusting patterns was displayed, and the male was capable of ejaculating following a single mount and intromission and may have ejaculated more than once during the 30-min test. Male mating indices did not differ significantly on consecutive days of the mating period, though declines in certain mating latencies on the second and third days of mating suggested increased female receptivity. Mating indices did not differ notably between the first and the second copulation within a test, though both showed some differences compared to the third copulation. InG. moholi, male copulatory behavior is typical of a prosimian species with a dispersed — nongregarious — mating system, in which copulation has a single prolonged intromission that extends into the postejaculatory period. This is characteristic of species in which more than one male has access to an estrous female.     

Simulation of the population dynamics and social structure of the Virunga mountain gorillas

An agent-based model was developed to simulate the growth rate, age structure, and social system of the endangered mountain gorillas (Gorilla beringei beringei) in the Virunga Volcanoes region. The model was used to compare two types of data: 1) estimates of the overall population size, age structure, and social structure, as measured by six censuses of the entire region that were conducted in 1971-2000; and 2) information about birth rates, mortality rates, dispersal patterns, and other life history events, as measured from three to five habituated research groups since 1967. On the basis of the research-group data, the "base simulation" predicted a higher growth rate than that observed from the census data (3% vs. 1%). This was as expected, because the research groups have indeed grown faster than the overall population. Additional simulations suggested that the research groups primarily have a lower mortality rate, rather than higher birth rates, compared to the overall population. Predictions from the base simulation generally fell within the range of census values for the average group size, the percentage of multimale groups, and the distribution of females among groups. However, other discrepancies predicted from the research-group data were a higher percentage of adult males than observed, an overestimation of the number of multimale groups with more than two silverbacks, and an overestimated number of groups with only two or three members. Possible causes for such discrepancies include inaccuracies in the census techniques used, and/or limitations with the long-term demographic data set obtained from only a few research groups of a long-lived species. In particular, estimates of mortality and male dispersal obtained from the research groups may not be representative of the entire population. Our final simulation addressed these discrepancies, and provided a better basis for further studies on the complex relationships among individual life history events, group composition, population age structure, and growth rate patterns.     

Effect of Mating Activity and Dominance Rank on Male Masturbation Among Free‐Ranging Male Rhesus Macaques

The adaptive function of male masturbation is still poorly understood, despite its high prevalence in humans and other animals. In non‐human primates, male masturbation is most frequent among anthropoid monkeys and apes living in multimale–multifemale groups with a promiscuous mating system. In these species, male masturbation may be a non‐functional by‐product of high sexual arousal or be adaptive by providing advantages in terms of sperm competition or by decreasing the risk of sexually transmitted infections. We investigated the possible functional significance of male masturbation using behavioral data collected on 21 free‐ranging male rhesus macaques (Macaca mulatta) at the peak of the mating season. We found some evidence that masturbation is linked to low mating opportunities: regardless of rank, males were most likely to be observed masturbating on days in which they were not observed mating, and lower‐ranking males mated less and tended to masturbate more frequently than higher‐ranking males. These results echo the findings obtained for two other species of macaques, but contrast those obtained in red colobus monkeys (Procolobus badius) and Cape ground squirrels (Xerus inauris). Interestingly, however, male masturbation events ended with ejaculation in only 15% of the observed masturbation time, suggesting that new hypotheses are needed to explain masturbation in this species. More studies are needed to establish whether male masturbation is adaptive and whether it serves similar or different functions in different sexually promiscuous species.     

Group mating among Norway rats II. The social dynamics of copulation: Competition,cooperation, and mate choice

The social interactions within groups of Norway rats (Rattus norvegicus) had a strong impact on the individual pattern of copulation which, in turn, affects sperm precedence and the probability of implantation in this species. Males alternated uninterrupted ejaculatory series, augmenting each others' copulatory investment. Females took turns mating after receiving an intromission, collectively potentiating the males' copulatory behaviour; increasing the number of oestrous females increased the number of intromissions and ejaculations achieved by each male but did not affect the amount of copulation experienced by each female. These turn-taking patterns within each sex provided the opportunity to change partners and permitted the emergence of different sex-typical patterns of copulation. Furthermore, the dominant male contributed more intromissions and tended to give each female more ejaculations than the subordinates did. Dominant males were also more likely to inhibit the subordinates' sperm transport. Females competed among themselves for the opportunity to mate with a male as he approached ejaculation and were likely to protect more of the dominant male's sperm transport than the subordinate male's.     

Random size‐assortative mating despite size‐dependent fecundity in a Neotropical amphibian with explosive reproduction

Sexual selection theory predicts that, when body size is correlated with fecundity, there should be fitness advantages for mate choice of the largest females. Moreover, because larger males are expected to monopolise the largest females, this should result in an assortative mating based on body size. Although such patterns could be expected in both explosive and prolonged breeders, non‐assortative mating should be more widespread in species under time constraints. However, patterns of sexual selection are largely unexplored in explosive breeding species, and contrasting patterns have been found previously. We expect that the active choice of partners may be particularly risky when the time period during which sexual partners are available is severely limited. Therefore, to avoid missing an entire reproductive act, males and females should pair irrespective of traits, such as body size. We tested this hypothesis by investigating the mating patterns of the Pacific horned toad, Ceratophrys stolzmanni, a short‐lived fossorial species inhabiting Neotropical dry forests. This species is particularly adequate to test our prediction because it reproduces explosively over the course of a single night per year. Although the number of eggs laid was proportional to the size of females, and individuals of both sexes showed variation in body size, there was no assortative mating based either on size, body condition or age of mates. Egg size was not influenced by either female size or clutch size. The larger body size of females compared to males is likely due to fecundity selection, that is, the selective pressure that enhances reproductive output. Although we cannot dismiss the possibility that individuals could select their partners based on other criteria than those related to size or age, the results fit well our prediction, showing that the explosive breeding makes improbable an active choice of partners in both sexes and therefore favours a random mating pattern.     

Social organization of the golden brown mouse lemur (Microcebus ravelobensis)

Our study provides the first data on the social organization of the golden brown mouse lemur, a nocturnal primate discovered in northwestern Madagascar in 1994. The study was carried out in two 6-month field periods during the dry season, covering time before and during the mating season. The spatial and temporal distributions of the sexes in the population were investigated by mark/recapture and radiotelemetry. Focal observations and the determination of sleeping associations provided further insights into the sociality of this solitary forager. High intra- and intersexual home-range overlaps occurred throughout the study. In general, individuals of both sexes had spatial access to more than one conspecific of the same and the opposite sex. We found no indication for spatial monopolization of females by certain males. These results suggest a dispersed multimale/multifemale system with a promiscuous mating pattern. Individuals showed temporal stability in their home range locations and interacted regularly with conspecifics. Five sleeping groups were identified during the study period: one female group and four mixed-sex groups. Even though sleeping sites were changed frequently, sleeping-group compositions remained stable over time. Thermoregulatory constraints are the most likely explanation for sleeping-group composition with members of both sexes in this species. Mixed-sex sleeping groups can be described as the basic social unit within this dispersed multimale/multifemale society.     

Expression of FOS, EGR-1, and ARC in the amygdala and hippocampus of female rats during formation of the intromission mnemonic of pseudopregnancy

Pseudopregnancy (PSP) in the female rat is a neuroendocrine condition that is induced by repeated and intermittent vaginocervical stimulation received during mating and involves the expression of bicircadian prolactin surges and cessation of normal estrous cyclicity for 10-12 days postmating. The temporal patterning and number of intromissions received by the female are critical for PSP initiation, and thus, short-term encoding of VCS occurs during transduction of intromissions into PSP. In this experiment, we characterized and compared the mating-induced neural activation patterns within amygdalar and hippocampal regions using expression of the immediate early genes FOS, EGR-1, and ARC. Cycling female rats mated on proestrus received 15 or 5 intromissions under paced or nonpaced mating conditions. High numbers of intromissions during nonpaced mating or low numbers received during paced mating are sufficient to induce PSP, while five nonpaced intromissions and mounts without intromission are insufficient. Here we demonstrate that the CA1 region of the hippocampus was selectively sensitive to PSP-sufficient but not PSP-insufficient mating stimulation by showing significant effects of paced mating for all three IEGs. Paced mating also stimulated the expression of ARC within the basolateral, cortical, and central nuclei of the amygdala. The posterodorsal medial amygdala also showed selective EGR-1 responses to PSP-sufficient mating stimulation. There was no effect of hemisphere on IEG expression. The postmating expression profiles of these IEGs provide evidence that limbic areas involved in encoding and consolidation of memory are involved in initiating the neuroendocrine memory of PSP.     

Sexual Strategies of a North American ‘Tarantula’ (Araneae: Theraphosidae)

Despite their general notoriety and popularity as pets, little is known of the behavioural ecology of ‘tarantulas’ or theraphosid spiders. We studied a theraphosid of the Arizona deserts, Aphonopelma sp., to determine behavioural events crucial to successful courtship and mating. Males search for spatially scattered females and, at short range, may detect females by substrate-borne cues. When two males are present with a single female, no direct competition such as aggression is observed. Both males may mate with a single female in rapid succession, with no evidence of post-copulatory mate guarding. Despite the potential for sexual cannibalism, courtship and mating behaviour patterns exhibit few aggressive elements and males nearly always survive sexual encounters with females. The mating system of this Aphonopelma species may best be described as a type of scramble-competition polygyny, in which the ability of males to locate receptive females is an important determinant of mating success in males. Multiple mating by females renders predictions concerning fertilization success uncertain, due to the possibility of sperm competition and ‘cryptic’ female mate choice.     

Do "sperm trading" simultaneous hermaphrodites always trade sperm?

Sperm trading can be a mechanism to solve the conflict oversex roles in hermaphrodites with copulation, sperm competition,and sperm digestion. If present, sperm donation depends on spermreceipt, resulting in conditional reciprocal inseminations.Conditional reciprocity can involve three traded commodities:penis intromissions on a yes-or-no basis, intromission durations(indicating ejaculate size), or sperm transfer. If present,animals that refuse to donate (cheaters) should be desertedby their partner or receive smaller ejaculates. We tested whetherany of these commodities is traded in the simultaneously hermaphroditicsea slug, Chelidonura sandrana. Matings involve a stereotypicsingle sex role alternation. As a result, reciprocity was morefrequent than expected under random mating, supporting tradingof penis intromissions. Contrary to the predictions under tradingof ejaculate sizes, intromission durations were not balancedbetween mating partners. To test trading of sperm transfer itself,we interrupted the sperm groove that transports sperm into thepenis during copulation. Treated animals (experimental cheaters)could still copulate normally but could not transfer sperm.When paired to a cheater, sham-treated control animals did notrespond to the absence of sperm receipt, neither by desertionnor by shortening intromission. We thus reject trading of inseminationdurations and sperm transfer in C. sandrana. Although tradingof intromissions may be present, we discuss why reciprocityin this species may also be a by-product of the mutual willingnessof both partners to donate as well as receive sperm, and notan indicator of sperm trading.     

Seasonal Effects on Reconciliation in Macaca fuscata yakui

Dietary composition may have profound effects on the activity budgets, level of food competition, and social behavior of a species. Similarly, in seasonally breeding species, the mating season is a period in which competition for mating partners increases, affecting amicable social interactions among group members. We analyzed the importance of the mating season and of seasonal variations in dietary composition and food competition on reconciliation in wild female Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Yakushima macaques are appropriate subjects because they are seasonal breeders and their dietary composition significantly changes among the seasons. Though large differences occurred between the summer months and the winter and early spring months in activity budgets and the consumption of the main food sources, i.e., fruits, seeds, and leaves, the level of food competition and conciliatory tendency remained unaffected. Conversely, conciliatory tendency is significantly lower during the mating season than in the nonmating season. Moreover, conciliatory tendency is lower when 1 or both female opponents is in estrous than when they are not. Thus the mating season has profound effects on reconciliation, whereas seasonal changes in activity budgets and dietary composition do not. The detrimental effects of the mating season on female social relationships and reconciliation may be due to the importance of female competition for access to male partners in multimale, multifemale societies.     

Demographic Changes over Thirty Years in a Red Howler Population in Venezuela

During a 30-year span (1969–1999) the annual growth rate of a Venezuelan red howler (Alouatta seniculus) population fluctuated irregularly, but its size increased, remained stable for a short while, and finally declined sharply. The increase took place in three stages, and began as an increase in the size of established groups. The next two stages of population increase were due to the formation of new groups and their subsequent increases in size. These two stages likely occurred because of habitat regeneration, which increased the areas where newly formed groups could establish home ranges. The population decline of 74% was most likely due to disease. However, new groups died out more rapidly than established groups, indicating that food shortages, especially in recently regenerated areas, may also have contributed to the population crash. The food shortages could have been caused by unpredictable periods of drought, which may explain the irregular size fluctuations of the study population. Since many howler species show irregular size fluctuations and sharp declines, their demographic features may reflect adaptations to unpredictable events like droughts and disease epidemics. On this premise we explain the preponderance of unimale groups and female-biased birth sex ratios at low densities and the dispersal of both sexes as adaptations for increasing a population rapidly after a decline. Within the population, mortality of small juvenile females was higher in multimale than in unimale groups, though medium juvenile and older immature females were better represented in multimale than in unimale groups. These results may be explained in terms of group composition and the mating systems in red howlers.