Multi-male Mating Research Articles

Effects of social and environmental contexts on multi-male mating and mixed paternity in socially monogamous female prairie voles.

With whom and how often to mate are fundamental questions that impact individual reproductive success and the mating system. Relatively few studies have investigated female mating tactics compared with males. Here, we asked how differential access to mates influences the occurrence of mixed paternity and overall reproductive success in socially monogamous female prairie voles (Microtus ochrogaster). We created male- and female-biased sex ratios of prairie voles living in semi-natural outdoor enclosures. We ran paternity analyses to determine the identity and number of mating partners females had and the number of offspring produced. We found that 57.1% of females had litters fathered by two or more males when males outnumbered females, and 87.5% of females had litters with more than one father when females outnumbered males. However, the percentage of mixed paternity and the total number of embryos were not statistically different between social contexts. We determined that female fecundity (i.e. number of embryos) correlated with the number of male fathers in each litter across social contexts. Although our study did not support the hypothesis that social context directly influences female mating decisions, it did suggest that female multi-male mating might lead to increased fertilization success under semi-natural conditions.

Effects of Female Group Size on the Number of Males in Blue Monkey (Cercopithecus mitis) Groups

The number of males per group varies substantially in group-living primates, both between and within species. In blue monkeys (Cercopithecus mitis), males may temporarily join groups during annual mating seasons when sexually receptive females are present. A likely determinant of the number of males per group is female group size (the number of adult females in a group). To clarify the role of female group size in driving variation in the number of males per group, we expanded on earlier observations of a wild population in the Kakamega Forest, Kenya with a larger sample of groups that varied fivefold in female group size. We found considerable flexibility in social organization, with groups experiencing multimale episodes both during and outside mating seasons, some persisting over multiyear periods. The dichotomy between single- and multimale mating seasons was less distinct than previously reported, suggesting greater variation in multimale states. Across 65 group-specific conception periods, female group size strongly influenced how often multiple sexually active females and multiple males were present in a group. The number of sexually active females present on a given day related closely to the number of males in the group that same day, especially during conception periods. Results suggest that males join and remain in larger groups where mating opportunities are greater and costs of joining or staying may be lower than in smaller groups. This longitudinal study highlights intraspecific social variation within and across groups while confirming that female group size influences the number of males.

Battle of the sexes: a multi-male mating strategy helps lionesses win the gender war of fitness

Abstract In species exhibiting infanticide by males, females lose out with high stakes and should adopt preemptive mechanisms, pitching the genders in an evolutionary arms race for maximizing fitness. African lions remain a quintessential model of this gender war, with a coalition of males gaining temporary but exclusive breeding rights over a female group after killing all cubs of former males. However in Asiatic lions, now found as a single population in Gir forests, India, adults live in same-sex groups that interact primarily for mating. Intensive monitoring of 70 adult lions revealed that female groups (n = 9) used exclusive territories, whereas male ranges (n = 11 coalitions) overlapped at areas of intense female use. A social network of mating events (n = 76) indicated that lionesses mated with multiple rival coalitions before conceiving. These neighboring coalitions, although hostile to each other were tolerant toward the same litters, suggestive of confused paternity among them. Given a land-tenure system where lionesses encounter many males capable of killing unfamiliar cubs, multi-male mating buffers cub infanticide and likely diversifies paternal lineages in litters. Consequently, infanticide was observed only when “new” males invaded a female group’s territory. An age-based mate choice was observed in lionesses: maiden breeders chose males having highest range overlaps, whereas experienced females selected peripheral males. The intergender spacing patterns and resultant sexual strategies of lions differ in Asia and Africa probably because of contrasting resource availability, highlighting behavioral plasticity within species inhabiting diverse eco-regions. By mating with multiple males, lionesses safeguard their investments and outdo the males in the war of fitness.

No support for the sexy-sperm hypothesis in the seed beetle: Sons of monandrous females fare better in post-copulatory competition.

The sexy‐sperm hypothesis posits that polyandrous females derive an indirect fitness benefit from multi‐male mating because they increase the probability their eggs are fertilized by males whose sperm have high fertilizing efficiency, which is assumed to be heritable and conferred on their sons. However, whether this process occurs is contentious because father‐to‐son heritability may be constrained by the genetic architecture underlying traits important in sperm competition within certain species. Previous empirical work has revealed such genetic constraints in the seed beetle, Callosobruchus maculatus, a model system in sperm competition studies in which female multi‐male mating is ubiquitous. Using the seed beetle, I tested a critical prediction of the sexy‐sperm hypothesis that polyandrous females produce sons that are on average more successful under sperm competition than sons from monandrous females. Contrary to the prediction of the sexy‐sperm hypothesis, I found that sons from monandrous females had significantly higher relative paternity in competitive double matings. Moreover, post hoc analyses revealed that these sons produced significantly larger ejaculates when second to mate, despite being smaller. This study is the first to provide empirical evidence for post‐copulatory processes favoring monandrous sons and discusses potential explanations for the unexpected bias in paternity.

Male-female interactions in multimale groups of mountain gorillas.

Male-female social interactions may vary according to female receptivity, female parity, and male dominance rank. Such variation may be less apparent in species with one-male mating systems than those with multimale mating systems, as within-group male-male competition and female mate choice are absent. Examining variation in male-female interactions in multimale groups in species with a predominantly one-male mating system may help to shed light on plasticity in behavioral patterns and the evolution of mating systems. In this study, we investigated the effect of female receptivity (i.e., days when mating occurred), female parity, and male dominance rank on the patterns of spatial proximity, grooming, following, and aggression among 34 male-female dyads in four multi-male groups of Virunga mountain gorillas. In addition, as a preliminary investigation of potential physiological costs incurred by females in a mating context (coercion), we tested whether female receptivity and female parity explained variation in immunoreactive glucocorticoid (iGC) levels of females. The amount of time male-female dyads spent in close proximity was significantly higher for parous versus nulliparous females and for high- versus low-ranking males. The rate of male aggression to females did not vary significantly with female parity, male rank, or female receptivity. However, post hoc analysis showed that both proximity and aggression increased for the males that participated in the matings on days that females were receptive. Grooming and following by males occurred infrequently. Neither female receptivity nor parity influenced iGC levels in females, a finding that is more consistent with courtship than coercion of females by males. Overall, our results suggest that males advertise their ability to provide protection to females and their offspring, and females seek out males that can do so.

Bottlenose dolphin (Tursiops truncatus) sperm revisited: Motility, morphology and ultrastructure of fresh sperm of consecutive ejaculates

Computer aided sperm analysis systems allow detailed examination of sperm motility and morphology variables, which are important for the understanding of the spermatology of a species and the development of assisted reproductive techniques. Cetacean biology is too complex to study in the wild and data from captive individuals provide an important alternative for the conservation of these charismatic animals. The present study evaluates ejaculate and sperm characteristics, including sperm motility, kinematic variables and quantitative sperm morphology and ultrastructure, of consecutive ejaculates from Atlantic bottlenose dolphins (Tursiops truncatus). Sperm concentrations and total and progressive motilities were greater in the second than the first ejaculate, with all ejaculates being of very high quality (6.9–1127 × 106/ml sperm concentration, 75% to 91% total motility and 89% to 96% normal sperm). Most sperm in an ejaculate (≥84%) were highly (VCL>150 μm/s) and progressively motile with very few abnormal sperm. The sperm have small heads, a short but very bulky midpiece and a long tail. Detailed sperm morphometrics using CASA indicated there were similarities from one ejaculate to the next. The large mitochondria with extensive cristae mitochondriales are tightly packed in the midpiece resulting in a large midpiece volume. All the semen and sperm characteristics indicate high quality sperm and support the assumption that a multimale mating system is present in T. truncatus.

Screening wild and semi-free ranging great apes for putative sexually transmitted diseases: Evidence of Trichomonadidae infections.

Sexually transmitted diseases (STDs) can persist endemically, are known to cause sterility and infant mortality in humans, and could have similar impacts in wildlife populations. African apes (i.e., chimpanzees, bonobos, and to a lesser extent gorillas) show multi-male mating behavior that could offer opportunities for STD transmission, yet little is known about the prevalence and impact of STDs in this endangered primate group. We used serology and PCR-based detection methods to screen biological samples from wild and orphaned eastern chimpanzees and gorillas (N = 172 individuals, including adults, and juveniles) for four classes of pathogens that either commonly cause human STDs or were previously detected in captive apes: trichomonads, Chlamydia spp., Treponema pallidum (syphilis and yaws), and papillomaviruses. Based on results from prior modeling and comparative research, we expected STD prevalence to be highest in females versus males and in sexually mature versus immature individuals. All samples were negative for Chlamydia, Treponema pallidum, and papillomaviruses; however, a high percentage of wild chimpanzee urine and fecal samples showed evidence of trichomonads (protozoa). Analysis revealed that females were more likely than males to have positive urine—but not fecal—samples; however, there was no evidence of age (sexual maturity) differences in infection status. Sequence analysis of chimpanzee trichomonad samples revealed a close relationship to previously described trichomonads within the genus Tetratrichomonas. Phylogenetic comparisons to archived sequences from multiple vertebrate hosts suggests that many of the chimpanzee parasites from our study are likely transmitted via fecal-oral contact, but the transmission of some Tetratrichomonas sequence-types remains unknown and could include sexual contact. Our work emphasizes that only a fraction of infectious agents affecting wild apes are presently known to science, and that further work on great ape STDs could offer insights for the management of endangered great apes and for understanding human STD origins. Am. J. Primatol. 77:1075–1085, 2015. © 2015 Wiley Periodicals, Inc.

Ultrasonic vocalizations of female Norway rats (Rattus norvegicus) in response to social partners.

In many species of animals, male vocalizations function to attract mating partners and coordinate sexual interactions. Whereas male vocalizations have been well studied in several species, the function of female vocalizations in mating contexts is not fully understood. In Norway rats (Rattus norvegicus), both males and females produce ultrasonic vocalizations (USVs) during sexual encounters with opposite sex partners. The aim of this study was to test the hypothesis that female vocalizations play a role in sociosexual interactions by examining how rates of 50 kHz USV production vary in relation to the sex and gonadal status of the partner, and by examining whether the proportion of frequency modulated (FM) and constant frequency calls differs between these categories of social partner. The results showed that females produced a higher total number of 50 kHz USVs to intact males than castrated males, and produced similar numbers of calls to both categories of females. Females also produced a higher proportion of FM calls to male partners than to female partners, and spent more time in the vicinity of male than female partners, regardless of the partners' gonadal status. Female USVs therefore potentially provide a measure of sexual motivation and may function to promote female mate choice in this species with multimale mating and a high risk of infanticide.

Screening wild and semi-free ranging great apes for putative sexually transmitted diseases: Evidence of Trichomonadidae infections.

Sexually transmitted diseases (STDs) can persist endemically, are known to cause sterility and infant mortality in humans, and could have similar impacts in wildlife populations. African apes (i.e., chimpanzees, bonobos, and to a lesser extent gorillas) show multi-male mating behavior that could offer opportunities for STD transmission, yet little is known about the prevalence and impact of STDs in this endangered primate group. We used serology and PCR-based detection methods to screen biological samples from wild and orphaned eastern chimpanzees and gorillas (N = 172 individuals, including adults, and juveniles) for four classes of pathogens that either commonly cause human STDs or were previously detected in captive apes: trichomonads, Chlamydia spp., Treponema pallidum (syphilis and yaws), and papillomaviruses. Based on results from prior modeling and comparative research, we expected STD prevalence to be highest in females versus males and in sexually mature versus immature individuals. All samples were negative for Chlamydia, Treponema pallidum, and papillomaviruses; however, a high percentage of wild chimpanzee urine and fecal samples showed evidence of trichomonads (protozoa). Analysis revealed that females were more likely than males to have positive urine-but not fecal-samples; however, there was no evidence of age (sexual maturity) differences in infection status. Sequence analysis of chimpanzee trichomonad samples revealed a close relationship to previously described trichomonads within the genus Tetratrichomonas. Phylogenetic comparisons to archived sequences from multiple vertebrate hosts suggests that many of the chimpanzee parasites from our study are likely transmitted via fecal-oral contact, but the transmission of some Tetratrichomonas sequence-types remains unknown and could include sexual contact. Our work emphasizes that only a fraction of infectious agents affecting wild apes are presently known to science, and that further work on great ape STDs could offer insights for the management of endangered great apes and for understanding human STD origins.

Molecular assessment of mating strategies in a population of Atlantic spotted dolphins.

Similar to other small cetacean species, Atlantic spotted dolphins (Stenella frontalis) have been the object of concentrated behavioral study. Although mating and courtship behaviors occur often and the social structure of the population is well-studied, the genetic mating system of the species is unknown. To assess the genetic mating system, we genotyped females and their progeny at ten microsatellite loci. Genotype analysis provided estimates of the minimum number of male sires necessary to account for the allelic diversity observed among the progeny. Using the estimates of male sires, we determined whether females mated with the same or different males during independent estrus events. Using Gerud2.0, a minimum of two males was necessary to account for the genetic variation seen among progeny arrays of all tested females. ML-Relate assigned the most likely relationship between offspring pairs; half or full sibling. Relationship analysis supported the conservative male estimates of Gerud2.0 but in some cases, half or full sibling relationships between offspring could not be fully resolved. Integrating the results from Gerud2.0, ML-Relate with previous observational and paternity data, we constructed two-, three-, and four-male pedigree models for each genotyped female. Because increased genetic diversity of offspring may explain multi-male mating, we assessed the internal genetic relatedness of each offspring’s genotype to determine whether parent pairs of offspring were closely related. We found varying levels of internal relatedness ranging from unrelated to closely related (range -0.136–0.321). Because there are several hypothesized explanations for multi-male mating, we assessed our data to determine the most plausible explanation for multi-male mating in our study system. Our study indicated females may benefit from mating with multiple males by passing genes for long-term viability to their young.

First report of satellite males during breeding in Leptodactylus latrans (Amphibia, Anura)

The occurrence of satellite males is a common behaviour across anuran taxa. Satellite males take peripheral positions to calling males and adopt tactics in an attempt to intercept females that are attracted to calling males to increase their own mating success. Satellite males could have an inexpensive form of mate-locating, avoiding predators, and saving energy. Furthermore, this strategy could play an important role in the genetic structure of populations. The genus Leptodactylus consists of approximately 70 described species that are widely distributed in South America. The literature on the biology of this genus is extensive; however, we found only two reports on the existence of multi-male mating behavior in the genus ( L. chaquensis and L. podicipinus ). Herein, we report intrasexual competition in the form of satellite behavior in Leptodactylus latrans , where multiple satellite males were observed in close vicinity to a calling male.

On the socio-sexual behaviour of the extinct Ursid Indarctos arctoides: an approach based on its baculum size and morphology.

The fossil bacula, or os penis, constitutes a rare subject of study due to its scarcity in the fossil record. In the present paper we describe five bacula attributed to the bear Indarctos arctoides Depéret, 1895 from the Batallones-3 site (Madrid Basin, Spain). Both the length and morphology of this fossil bacula enabled us to make interpretative approaches to a series of ecological and ethological characters of this bear. Thus, we suggest that I. arctoides could have had prolonged periods of intromission and/or maintenance of intromission during the post-ejaculatory intervals, a multi-male mating system and large home range sizes and/or lower population density. Its size might also have helped females to choose from among the available males.

Why do female mice mate with multiple males?

Females often show multi-male mating (MMM), but the adaptive functions are unclear. We tested whether female house mice (Mus musculus musculus) show MMM when they can choose their mates without male coercion. We released 32 females into separate enclosures where they could choose to mate with two neighboring males that were restricted to their own territories. We also tested whether females increase MMM when the available males appeared unable to exclude intruders from their territories. To manipulate territorial intrusion, we introduced scent-marked tiles from the neighboring males into males' territories, or we rearranged tiles within males' own territories as a control. Each female was tested in treatment and control conditions and we conducted paternity analyses on the 57 litters produced. We found that 46 % of litters were multiply sired, indicating that multiple paternity is common when females can choose their mates. Intrusion did not increase multiple paternity, though multiple paternity was significantly greater in the first trial when the males were virgins compared to the second trial. Since virgin male mice are highly infanticidal, this finding is consistent with the infanticide avoidance hypothesis. We also found that multiple paternity was higher when competing males showed small differences in their amount of scent marking, suggesting that females reduce MMM when they can detect differences in males' quality. Finally, multiple paternity was associated with increased litter size but only in the intrusion treatment, which suggests that the effect of multiple paternity on offspring number is dependent on male–male interactions.

Variable mode of estrus affects female decision for multiple mating

Investigating patterns of variation in mating strategies may shed light on their evolutionary importance as well as their impact on the strength and shape of sexual selection. Multimale mating (polyandry) and mate choice are intensely studied subjects in the area of sexual selection, but little is known about intraspecific patterns of variation that may respond to dynamic cost-benefit balances. In a laboratory study, we investigated the mating behavior of female bank voles (Myodes glareolus) with distinctly different time and energy budgets: They were either in cycling estrus (CE) or postpartum estrus (PPE) shortly after delivery. Postpartum mating is highly constrained by time and energy due to maternal commitments to the newborn litter. All females had a free and simultaneous choice among 4 males that differed in scent-marking frequency (indicator of dominance) and body mass. We show that females in CE engaged significantly more often in multimale mating than females in PPE. Additionally, PPE females mated with males that scent marked more, whereas CE females seemingly mated indiscriminately. We discuss our findings in light of time and energy budgets of females and also consider alternative explanations such as pup protection against infanticidal males or physiological constraints to estrus modes.

Observed infanticides following a male immigration event in black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico

This study describes two cases of directly observed and one case of nearly observed infanticide after an adult male immigrated into a multimale-multifemale group of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico. The immigrant male entered the group alone, injured the central adult male, presumably evicted the noncentral adult male, and killed all three young infants present over the course of three consecutive days in February 2010. Three weeks after the infanticide events, the three adult females who lost their infants were observed to sexually solicit and copulate with both the infanticidal male and the injured central male. Multimale mating is an effective reproductive strategy that females employ to confuse paternity and reduce the risk of infanticide, but the extent to which promiscuous mating after infanticide events is part of a counterstrategy in this species is still unknown. More cases of infanticide will need to be observed to assess the degree to which infanticide avoidance shapes the social system of the black howler monkey.

Chest staining variation as a signal of testosterone levels in male Verreaux's Sifaka

Male Verreaux's sifaka ( Propithecus verreauxi) exhibit variation in the staining of chest hair in association with the activity of the sternal gland. Scent-marking behavior and social relationships have been shown to vary with the state of chest staining. Research on other mammals suggests that sternal gland activity is modulated by testosterone. The goal of this study was to examine the relationship among fecal testosterone, testes mass, and chest staining in sifaka. I predicted that for sifaka (1) testosterone and testes mass are positively correlated, (2) stained males have higher testosterone and larger testes than clean-chested males, (3) testes mass is greater during the mating season than the birth season, and (4) testes mass is comparable to species with multimale mating systems. Eighty fecal samples were collected from eight adult males in five social groups in the Kirindy Mitea National Park of Madagascar during the mating season and analyzed using enzyme immunoassays. Males were captured during the mating season and the subsequent birth season to measure body mass and testes size and to document chest staining. Stained males had significantly higher fT and larger testes mass than clean-chested males. Testes mass was significantly greater during the mating season than the birth season for all males. However, the stained males exhibited less testes mass reduction during birth season than clean-chested males. These results suggest that the activity of the sternal gland is regulated by testosterone and that sexual selection has shaped male morphological variation in Verreaux's sifaka.

Female multiple mating and paternity in free-ranging North American red squirrels

Multimale mating (MMM) is common in female mammals, but our understanding of its evolutionary significance in this taxon lags behind that in others (e.g. invertebrates and birds). To date, the majority of research on mammalian MMM has been conducted under laboratory conditions, and the extent to which these findings have relevance for natural populations is little known. We quantified MMM in a free-ranging population of North American red squirrels, Tamiasciurus hudsonicus , and investigated its hypothesized influences and consequences. We observed 85 mating chases, representing 62 individual females, over three mating seasons and calculated standardized indexes of MMM and number of copulations. Extrinsic elements of mating chases (i.e. an index of the number of attending males and date) explained variation in MMM, while traits of the females (age and pre-oestrous body mass) did not correlate with MMM. Hypotheses of cryptic direct benefit (fertility assurance and infanticide avoidance) were not supported because MMM did not influence pregnancy rate, litter size or nest fate. There was also no correlation between MMM and offspring quality, multiple paternity or litter allelic diversity, and therefore, no support for hypotheses of genetic benefit. In addition to not accruing observable benefits to MMM, females did not incur a detectable cost, thus rendering MMM selectively neutral. Rather, in line with traditional explanations, female mating behaviour in red squirrels appears to be a passive response to selection on multifemale mating in males.

Effect of Local Density of Males on the Occurrence of Multimale Mating in Gray-sided Voles (Myodes rufocanus)

Multiple paternity may vary in frequency within populations because of changes in density. We investigated the occurrence of multiple paternity in an enclosed population of gray-sided voles (Myodes [formerly Clethrionomys] rufocanus) while focusing on the effect of density. We determined parentage from microsatellite DNA loci and mark-recapture livetrapping data. Breeding males had home ranges that covered several home ranges of reproductive females and overlapped with those of intrasexual competitors throughout the breeding season. We captured 918 weaned voles (454 females and 464 males) from 215 litters. Litters sired by multiple males (mainly 2 males) were observed throughout the breeding season, and the proportion of litters with multiple sires was 23.2% (50/215). The proportion of litters showing multiple paternity was strongly positively correlated with local density of males around estrous females. Mating success of males was related to body mass of males for mating occasions with a single sire and those with multiple sires. Taken together, our results suggest that multimale mating occurs because dominant males cannot deter subordinates from access to their mates when local density of males is high.

No effect of group size on sex allocation in a protandric-simultaneous hermaphroditic shrimp

Lysmata wurdemanni is a protandric-simultaneous hermaphroditic shrimp. Individuals reproduce as males first and late in life as simultaneous hermaphrodites. I examined whether sex allocation (resources devoted to ova vs sperm) varies with group size in shrimps that have just matured as hermaphrodites. Focal males were reared with different numbers of hermaphrodites (1, 2, 5 or 10). Sperm stored in the ejaculatory ducts and eggs brooded underneath the abdomen were retrieved and weighted immediately after focal shrimps matured as hermaphrodites. Hermaphrodites should invest more into sperm with increasing group size to cope with more intense sperm competition. The proportion of focal shrimps that lost their first clutch of eggs after maturing as hermaphrodites increased with group size. This suggests male gender preferences by hermaphrodites experiencing large group sizes. No differences in sex allocation among group sizes were recorded for shrimps that did not lose their first clutch of eggs. Thus, group size does not affect sex allocation in terms of ova and sperm mass. This lack of phenotypic plasticity might be explained if sperm competition is not important in L. wurdemanni. It should not pay in terms of fitness for shrimps to produce and inseminate female-role hermaphrodites with large amounts of sperm when full paternity is assured in the absence of multi-male mating. In agreement with this idea, a second experiment demonstrated that female-role hermaphrodites invariably mated only once with a single other shrimp.

Genetic relatedness of mates does not predict patterns of parentage in North American red squirrels

Previously limited to laboratory studies, the deleterious effects of inbreeding are now being revealed in a number of wild systems. Female North American red squirrels, Tamiasciurus hudsonicus, show high levels of multimale mating and little to no overt precopulatory mate selection. We hypothesized that the negative repercussions of inbreeding should select for a female's ability to select sperm from more distantly related males. Consequently, successful sires should be less genetically related to the female than are unsuccessful males. We tested this hypothesis using both an analysis of absolute success among all copulating males and also relative success of sires within multiply sired litters. Pairwise genetic relatedness and paternity were determined through molecular analysis of tissue samples collected from reproductive females, copulating males and resultant offspring. In contrast to other systems, we found no evidence that the genetic similarity of mates predicts patterns of parentage in red squirrels. Genetic relatedness did not predict whether a copulating male would sire any offspring, and relative success of sires within multiply sired litters was unrelated to their relatedness to the dam of the litter. Furthermore, selection for inbreeding avoidance mechanisms may be minimal, as there were no observable negative fitness repercussions to inbreeding. We detected no relationship between the genetic relatedness of an offspring's parents and its neonatal mass, growth rate or survival to reproductive age. In red squirrels, we found no evidence of parentage patterns based on genetic similarity of mates, and this phenomenon may be less universal than previously thought.