Is male-infant caretaking related to paternity and/or mating activities in wild Barbary macaques (Macaca sylvanus)?

In species with a promiscuous mating system, the functions of male-infant caretaking remain unclear in the absence of genetic paternity tests. We tested paternal investment and hypotheses concerning reproductive tactics in wild groups of Barbary macaques, including results of genetic paternity tests. Our study revealed that male-infant caretaking was not related to the probability of paternity. In principle, males could use access to females to estimate paternity. However, we found that mating success was not related to paternity, so males could invest in infants that they had not sired, and caretaking of non-offspring was actually observed. Accordingly, males might be 'deceived' with respect to their paternal investment. In that case, one would expect a positive relation between mating success and the subsequent rate of male caretaking of infants. Such a relation is also lacking, leading to comprehensive rejection of the paternal investment hypothesis in Barbary macaques. By contrast, there was evidence that males showing infant care achieved higher mating frequencies than other males with the mothers of the relevant infants. Thus, male Barbary macaques do not show a 'mate-then-care' pattern, but they do exhibit a 'care-then-mate' pattern.     

The impact of paternity on male–infant association in a primate with low paternity certainty

In multimale groups where females mate promiscuously, male–infant associations have rarely been studied. However, recent studies have shown that males selectively support their offspring during agonistic conflicts with other juveniles and that father's presence accelerates offspring maturation. Furthermore, it was shown that males invest in unrelated infants to enhance future mating success with the infant's mother. Hence, infant care might provide fitness gain for males. Here, we investigate male–infant associations in rhesus macaques (Macaca mulatta), a primate with low paternity certainty as females mate with multiple partners and males ensure paternity less efficiently through mate‐guarding. We combined behavioural data with genetic paternity analyses of one cohort of the semi‐free‐ranging population of Cayo Santiago (Puerto Rico) and recorded affiliative and aggressive interactions between focal subjects and adult males from birth to sexual maturation (0–4 years) of focal subjects. Our results revealed that 9.6% of all interactions of focal subjects involved an adult male and 94% of all male–infant interactions were affiliative, indicating the rareness of male–infant aggression. Second and most interestingly, sires were more likely to affiliate with their offspring than nonsires with unrelated infants. This preference was independent of mother's proximity and emphasized during early infancy. Male–infant affiliation rose with infant age and was pronounced between adult males and male rather than female focal subjects. Overall, our results suggest that male–infant affiliation is also an important component in structuring primate societies and affiliation directed towards own offspring presumably represent low‐cost paternal care.     

Evolution of male parental care and female multiple mating: game-theoretical and two-locus diploid models

Males gain a fitness benefit by mating with many females, whereas the number of progeny per female does not increase as a function of additional mates. Furthermore, males run the risk of investing in the offspring of other males if they provide parental care. Nevertheless, in various species, males provide parental care, and females mate with multiple males. We investigate a game-theoretical model in which females gain a direct benefit by multiple mating from the paternal care they elicit for their offspring. The parameters that directly favor male parental care, such as small cost of paternal care, have indirect positive effects on the evolution of female multiple mating, while they have negative effects in the opposite case. Both traits are more likely to evolve when the number of matings is smaller. The individual-based model of a diploid two-locus, two-allelic genetic model confirms the result.     

Male Tibetan macaques' (Macaca thibetana) choice of infant bridging partners

Adult male Tibetan(Macaca thibetana), Barbary(M. sylvanus), and stump-tailed macaques(M. arctoides) engage in bridging, a ritualized infant-handling behavior. Previous researchers found a bias toward the use of male infants for this behavior, but its function is debated. Explanations include three hypotheses: paternal care, mating effort, and agonistic buffering. We studied a group of habituated, provisioned Tibetan macaques to test whether adult males' affiliative relationships with females predicted their use of an infant for bridging. We also examined biases for sex, age, and individual in males' choice of bridging infant. We collected data via all occurrences, focal animal, and scan methods, from August to September 2011 at the Valley of the Wild Monkeys, China. We found that male infants were significantly preferred over females for bridging, but of three male infants in the group, only one was used by all males, while one male infant was used less often than expected. Adult males had females they were significantly more likely to be proximate to and/or to groom, but these corresponded to the mother of the bridging infant for only one male. Our results are most consistent with the agonistic buffering hypothesis: lower-ranked males used the alpha male's preferred bridging infant in an attempt to regulate their interactions with the alpha.     

The evolution of avian parental care

A stage model traces key behavioural tactics and life-history traits that are involved in the transition from promiscuity with no parental care, the mating system that typifies reptiles, to that typical of most birds, social monogamy with biparental care. In stage I, females assumed increasing parental investment in precocial young, female choice of mates increased, female-biased mating dispersal evolved and population sex ratios became male biased. In stage II, consortships between mating partners allowed males to attract rare social mates, provided a mechanism for paternity assessment and increased female ability to assess mate quality. In stage III, relative female scarcity enabled females to demand parental investment contributions from males having some paternity certainty. This innovation was facilitated by the nature of avian parental care; i.e. most care-giving activities can be adopted in small units. Moreover, the initial cost of care giving to males was small compared with its benefit to females. Males, however, tended to decline to assume non-partitionable, risky, or relatively costly parental activities. In stage IV, altriciality coevolved with increasing biparental care, resulting in social monogamy. Approaches for testing behavioural hypotheses are suggested.     

雌性动物多次交配行为的机制及进化

雌性动物的后代数量不可能超过她的卵子数。在理论上, 一个生殖季节内, 一次或几次交配就足够使雌性所有卵子受精, 最大化其生殖潜能。但与理论预测相反, 许多物种的雌性经常与同一个或多个雄性发生多次交配。交配通常要付出较高的代价, 所以很难理解为什么雌性动物要反复进行多次交配。本文综述了解释此行为的一些适应性和非适应性假说。从获得直接收益和间接收益二个角度介绍了适应性假说。直接收益主要包括求偶喂食和“彩礼”、受精保证、亲代抚育、生殖刺激和护卫交配权等5 个方面。还着重介绍了多次交配对雌性后代的间接遗传受益, 即获得优质基因、提高后代遗传多样性和遗传互补性3 个假说。非适应性假说包括了遗传相关假说和顺从雄性行为假说。     

Male investment under changing conditions among chacma baboons at Suikerbosrand.

Male investment in infant baboons was measured by frequency of carrying from 1978 through 1985. A series of hypotheses was generated and tested with the carrying data, based on the assumptions that: male baboons have some capacity to estimate likelihood of paternity; where paternity probability is greater, males will invest more, where potential benefits to males or infants are higher, males will invest more. Carrying was affected by probability of paternity, availability of estrous females, season of conception and season of carrying, infant age, subtrooping, and predation risk. Infants were carried by probable fathers, siblings, mothers' siblings, and unrelated "suitors." Male investment increased female reproductive fitness: carried infants were more likely to survive, and mothers of carried infants had shorter interbirth intervals. Males appeared to estimate paternity both by observed copulations by other males and by the likelihood that copulations could have occurred without being observed. Male care of infant baboons may also be affected by female choice among males, the distribution of probable infants in time, male tenure at alpha rank, the number of males per troop, the probability of infanticide, and energy demands. Subtrooping seems to be historically crucial, by initially creating a situation in which some males have high paternity certainty.     

Pair bonding and "the widow effect" in female prairie voles

We conducted field and laboratory experiments with the well-studied monogamous prairie vole, Microtus ochrogaster, to distinguish among three hypotheses for the failure of females that lose their mates to bond with a new male ("the widow effect"). The reproductive value hypothesis predicts that males prefer young to older females because they potentially have a longer reproductive lifespan. The mate rejection hypothesis predicts that females will prevent repairing by aggressively deterring males that might harm their current offspring. The misdirected paternal care hypothesis assumes that females will mate during postpartum estrus and thus will be pregnant and/or nursing young throughout the breeding season; males will avoid pairing with older females to avoid providing care to unrelated offspring and/or because of a delay to the next breeding opportunity. Males associated and bred more with older than young females, allowing us to reject the reproductive value hypothesis. Our results were consistent with the male rejection hypothesis in that females were aggressive toward unfamiliar males. Our results were most consistent with the misdirected paternal care hypothesis in that once females started breeding, they continued to become pregnant and nurse young throughout the study period. Thus, our findings suggest that the potential of misdirected paternal care and delayed mating opportunity in conjunction with the aggressive behavior of females toward unfamiliar males are likely explanations for the lack of repairing for widow females.     

Infant mortality following male takeovers in wild geladas

Since Sugiyama's [1965] first observations of infanticide, empirical evidence from a multitude of primate species has supported the sexual selection hypothesis-the idea that males enhance their reproductive success by killing nonrelated, unweaned infants to hasten the mothers' return to fertility. Like other primates that live in social groups where paternity certainty is high, the social structure of geladas [Theropithecus gelada] suggests that infanticide by males could enhance their reproductive success. Nevertheless, empirical evidence for infanticide in this species is limited to anecdotal accounts. Using the timing of infant mortality and female reproductive and behavioral data collected across 26 months from a population of geladas living in the Simien Mountains National Park, Ethiopia, we test whether sexually selected infanticide occurs in this species. We also examine two additional hypotheses [noninfanticide hypothesis and generalized aggression hypothesis] for this population. Results suggest that sexually selected infanticide in geladas may, indeed, be a threat to females with dependent infants. First, male takeovers-the most likely time for infanticide-were associated with subsequently elevated rates of infant death [a 32-fold increase] comprising nearly 60% of all infant mortality. Second, females who lost infants during this period returned to fertility more quickly than if infants had lived [IBIs were 50% shorter], and third, all of these females were observed to mate with the new male. We found little to no support for other hypotheses. Finally, these results raise the possibility that anecdotal reports [from previous studies and this study] of pregnancy termination, accelerated weaning, and deceptive sexual swellings may represent female counterstrategies to male infanticide in geladas.     

Multiple mating and repeated copulations: effects on male reproductive success in red flour beetles

In many insects, both sexes mate multiple times and females use stored sperm for fertilizations. While males frequently engage in two distinct behaviours, multiple mating (with different females) and repeated copulations (with the same female), the reproductive consequences of these behaviours for males have been quantified for only a few species. In this study, males of the red flour beetle, Tribolium castaneum, were found to be capable of mating with as many as seven different virgin females within 15 min. Across sequential copulations with virgin females, there was no decline in either male insemination success or average female progeny production over 48 h. However, when males copulated with previously mated females, there was a significant decline in male paternity success across sequential copulations, possibly due to male sperm depletion. In separate experiments, T. castaneum males were found to engage in two to six repeated copulations with the same, individually marked female. These repeated copulations did not increase male insemination success, short-term female fecundity, or male paternity success. Repeated copulations may possibly play a role in sperm defence. This study indicates that males may frequently engage in multiple matings, but these additional matings may lead to diminishing male reproductive returns.     

A theoretical study on the evolution of male parental care and female multiple mating: effects of female mate choice and male care bias

Male parental care and female multiple mating are seen in many species in spite of the cost they entail. Moreover, they even coexist in some species though polyandry, by reducing paternity confidence of caregiving males, seems to hinder the evolution of paternal care. Previous studies have investigated the coevolutionary process of paternal care and polyandry under various simplifying assumptions, including random mating and random provision of male care. We extend these models to examine possible effects of female mate choice and male care bias, assuming that (a) monandrous females mate preferentially with caregiving males while polyandrous females compromise their preference in order to mate with multiple males and (b) caregiving males tend to direct their care to offspring of monandrous females. Our models suggest that both the female preference and the male bias always favor caregiving males while they may not always facilitate the evolution of monandry.     

Strategic male mating effort and cryptic male choice in a scorpionfly

In animal species with high male mating effort, males often find themselves in a dilemma: by increasing their mating effort, the gain from each copulation increases but simultaneously reduces available resources and, thus, the opportunity for future copulations. Therefore, we expect males to spend less reproductive resources on matings that provide low reproductive potential, thereby saving resources for future copulations, possibly with high-quality females, a sort of cryptic male choice. However, the strength of the trade-off between investment in a current mating and resources available for future matings must not be the same for all males. Males with relatively high mating costs should allocate their limited resources more cautiously than males with more plentiful resources. Here, we examine this prediction in the scorpionfly Panorpa cognata. Prior to copulation, males produce a large salivary mass on which females feed during copulation. We show that the production of larger salivary masses leads to longer copulations. Moreover, the size of the salivary gland and salivary mass increases with increasing male condition. However, males in poor condition make a relatively higher mating investment than males in good condition. We therefore expect male condition to influence cryptic male choice. In accordance with our hypothesis, only males in poor condition choose cryptically, producing larger salivary masses in copulations with females of high fecundity.     

Paternity and the evolution of male parental care

It is generally believed that level of paternity (the proportion of zygotes in a brood that were fertilized by the male providing parental care) has an important role in the evolution of parental care. We have used population genetics models to investigate this role. The models indicate that only in mating systems where a parental male “sacrifices” promiscous matings can paternity influence the evolution of male parental care. This is because level of paternity can reflect the number of opportunities for these promiscuous fertilizations. For example, high paternity can mean few opportunities and therefore a low cost for paternal care.Certain behaviors may preadapt a species for the evolution of male parental care because they decrease the costs of providing care. For example, in fish species where male care has evolved from spawning territories, the very establishment of territories may have precluded males from gaining promiscuous matings, thereby eliminating the promiscuity costs and facilitating the evolution of care. Without a promiscuity cost, level of paternity will not have influenced the evolution of male care in fishes.Because paternity has limited influence in the evolution of male care, differences in reliability of parentage between males and females are unlikely to explain the prevalence of female care. Our analysis suggests that paternity differences between species cannot serve as a general explanation for the observed patterns of parental care behavior.     

Sexual selection favours male parental care, when females can choose

Explaining the evolution of male care has proved difficult. Recent theory predicts that female promiscuity and sexual selection on males inherently disfavour male care. In sharp contrast to these expectations, male-only care is often found in species with high extra-pair paternity and striking variation in mating success, where current theory predicts female-only care. Using a model that examines the coevolution of male care, female care and female choice; I show that inter-sexual selection can drive the evolution of male care when females are able to bias mating or paternity towards parental males. Surprisingly, female choice for parental males allows male care to evolve despite low relatedness between the male and the offspring in his care. These results imply that predicting how sexual selection affects parental care evolution will require further understanding of why females, in many species, either do not prefer or cannot favour males that provide care.     

Value of male remating and functional sterility in redback spiders

In the Australian redback spider, Latrodectus hasselti, males typically use their paired copulatory organs (palps) to copulate twice with a single female then sacrifice themselves to their cannibalistic mates in a strategy that increases their paternity in that one mating, but leads to death. This type of terminal investment in one mating is predicted only if the expected value of future matings is low for males relative to the value of repeated mating with the same female. In this laboratory study, we quantified the reproductive value of mating more than once with the same female (repeated mating) and mating with more than one female (multiple mating) for male redback spiders. We tested two natural selection hypotheses for repeated mating, sperm limitation and reproductive insurance, but found no support for either hypothesis. We show that, in the absence of sperm competition or cannibalism, male lifetime reproductive output is the same whether a male copulates once, twice, or several times with a given female. Repeated mating does not increase the probability of successful fertilization, nor does it increase the number of offspring produced in successful matings. Although male repeated mating is not favoured because of increased fertility of mates, other studies suggest it may be important in sperm competition. Here we show that the relative reproductive value of the first two copulations is very high for redback males because they are functionally sterile after each palp has been used once; nonvirgin males are unable to father offspring. Functional sterility and repeated mating by male redbacks may be favoured by the same factors that lead to male sacrifice behaviour: ecological constraints on multiple mating combined with competitive benefits of maximal investment in the first mating. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Can females gain extra paternal investment by mating with multiple males? A game theoretic approach

Although females may require only one mating to become inseminated, many female animals engage in costly mating with multiple males. One potential benefit of polyandrous mating is gaining parental investment from multiple males. We developed two game theoretic models to explore this possibility. Our first model showed that male care of multiple females' offspring evolves when male help substantially increases offspring fitness, future mating opportunity is limited, and group size is small. In our second model, we assumed that males invest in the offspring of former mates and evaluated the fitness consequences of female monogamous and polyandrous mating strategies. Females benefit only from limited polyandry, that is, mating with several males. Polyandry is discouraged because females must share male investment with other polyandrous females, and paternal care is likely to experience diminishing returns. Females may enhance their access to male investment by competing with rival females and monopolizing investment, however. The results support the argument that females can gain paternal investment by mating with several males in small social groups (e.g., dunnocks Prunella modularis). The results do not support the argument that females can gain paternal investment from pronounced multiple mating in large social groups, however, as observed in many primate species.     

Fertility assurance through extrapair fertilizations and male paternity defense

Extrapair paternity has been observed in many formally monogamous species. Male pursuit of extrapair fertilizations is explained by the advantages of having offspring that receive essential paternal care from other males. Since females are capable of exercising a degree of control over the post-copulatory sperm competition, extrapair paternity cannot persist unless it confers fitness benefits on cuckolding females. Thus, extrapair paternity involves cooperation between mated females and extrapair males. On the other hand, paired males frequently exhibit strategies that minimize their loss of paternity and/or conserve paternal investment if paternity is lost. Hence, extrapair attributes of diverse species and populations reported in the literature are particular solutions of evolutionary games involving gender-specific cuckolding/anti-cuckolding strategies. Here we use methods of evolutionary game theory to study the role of male paternity guarding strategies in situations where females seek extrapair fertilizations for reasons of genetic compatibility and/or in pursuit of genetic diversity for their offspring. Our results indicate that in these circumstances pursuit of extrapair fertilizations is the only evolutionary stable female strategy. Males, on the other hand, have two, mutually exclusive, evolutionary stable strategies: full time pursuit of extrapair fertilizations and a compromise strategy wherein they protect in-pair paternity during their mate's fertile periods and pursue extrapair paternity the rest of the time. The relative merits of these two strategies are determined by the efficiency of male in-pair paternity defense, breeding synchrony, fitness advantages of extrapair over in-pair offspring, and the intensity of competition for extrapair fertilizations from floater males.     

Female hunger can explain variation in cannibalistic behavior despite male sacrifice in redback spiders

Male Australian redback spiders (Latrodtctus hasselti Thorell:Theriidae) place their abdomens directly over their mate's mouthpartsduring copulation, increasing the likelihood of sexual cannibalism.Male sacrifice may be adaptive because cannibalized males increasetheir paternity relative to those that are not eaten. Despitemale sacrifice behavior, however, up to 50% of laboratory matingsmay end without sexual cannibalism. Here, I report a similarpattern in the field, where males were not cannibalized in 35%of observed matings (6/17). I examined variation in female cannibalisticbehavior by evaluating the following three hypotheses for theoccurrence of cannibalism from the female perspective: (1) themistaken identity hypothesis proposes that females sometimescannibalize males because they mistake them for prey, (2) themate rejection hypothesis predicts that females cannibalizemales who are unacceptable as mates, and (3) the feeding opportunismhypothesis predicts that hungry females are more likely to becannibalistic Field observations refuted die first two hypotheses:females recognized males as potential mates (i.e., nonprey),and cannibalized and noncannibalized males were not phenotypicallydifferent. The feeding opportunism hypothesis was supported.In staged field matings, cannibalistic females were hungrierthan their noncannibaUstic counter-parts. Moreover, a logisticregression analysis indicated that hunger was a significantpredictor of cannibalism. Because redback males are below thetypical prey size that females accept, well-fed females areless likely to consume their mates, despite the vulnerable matingposture. These results indicate that, although males facilitatesexual cannibalism, their fate may depend on the female's physicalcondition.     

Emasculation to plug up females: the significance of pedipalp damage in Nephila fenestrata

Female multiple mating selects for male adaptations that maximizefertilization success in a context of sperm competition. Whilemale mating strategies usually reflect a trade-off between presentand future reproduction, this trade-off is largely removed insystems where the maximum number of matings for males is verysmall. Selection may then favor extreme mechanisms of paternityprotection that amount to a maximal investment in a single mating.Males in several arthropod taxa break off parts of their copulatoryorgans during mating, and it has frequently been suggested thatmutilated males can thus secure their paternity. Nevertheless,such a mechanism has rarely been confirmed directly. Here westudy the golden orb spider Nephila fenestrata, which has amating system with potentially cannibalistic, polyandrous females,and males that are often functionally sterile after mating withone female only. We show that males in this species can indeedprotect their paternity by obstructing the female's genitalopenings with fragments of their copulatory organs.     

Males of the orb-web spider Argiope bruennichi sacrifice themselves to unrelated females

Costs of inbreeding can lead to total reproductive failure and inbreeding avoidance is, therefore, common. In classical sex roles with no paternal care, the selective pressure to avoid inbreeding is mostly on the female, which carries the higher costs. In some orb-web spiders, this situation is very different because females are polyandrous and males are monogynous or at most bigynous. Additionally, females of many entelegyne orb weavers are thought to bias paternity post-copulatorily towards a desired mate. This increases the selective pressure on males to adjust their investment in a mating with regard to the compatibility to a female.Here, we examine whether genetic relatedness influences mating behaviour in the orb-web spider Argiope bruennichi. We mated either a sibling or a non-sibling male to a female in single copulation trials and compared copulation duration, cannibalism rate and female fecundity.Our experiment revealed that males prolonged their copulation duration and were cannibalized more frequently when mating with a non-sibling female. Males mating with a sibling female were more likely to escape cannibalism by copulating briefly, thus presumably increasing their chances of re-mating with a more compatible female. This suggests that males can adaptively adjust their investment relating to the compatibility of a female.