Is Mating Alone Enough to Inhibit Infanticide in Male Bank Voles?

Infanticide, the killing of conspecific young, is commonly recognized as an adaptive behavioural strategy enhancing the fitness of the perpetrator. Infanticide is supposed to be inhibited in several male rodent species after mating with a time lag to the time when perpetrators own offspring would be born. This is because males with no parental care do not recognize their own offspring. It has been suggested that copulation alone is enough to inhibit infanticidal behaviour in male rodents. Infanticidal behaviour occurs in more than 50% of male bank voles (Myodes glareolus), and offspring loss because of infanticide may have a great effect on breeding success and population recruitment. In a laboratory experiment, we studied whether infanticidal male bank voles after successful mating stop the killing of pups. Infanticidal males were paired with a female until successful copulation. After the young were born, the males’ infanticidal behaviour was studied from the time of expected birth of own pups until their post‐weaning age. We predicted that mated infanticidal males are inhibited from committing infanticide especially during the time period when pups are less than 10 d old. Against our prediction, 67% of the infanticidal males continued the killing of pups in the age of 3 d. Infanticidal behaviour remained stable, and half of the males were infanticidal still at the age of weaning of pups. Our results are contradictory to previous studies, as we observed no inhibition of infanticide during early life of pups nor increase in infanticide again when their own offspring would have reached the ‘safe’ age and size after weaning. We suggest that mating alone is not sufficient to inhibit infanticide. Thus, we suggest that other cues of the female with whom the male mated with or on her territory are needed for inhibition to occur.     

Mating strategies in dominant meerkats: evidence for extra‐pair paternity in relation to genetic relatedness between pair mates

Rates of extra‐pair paternity (EPP) have frequently been associated with genetic relatedness between social mates in socially monogamous birds. However, evidence is limited in mammals. Here, we investigate whether dominant females use divorce or extra‐pair paternity as a strategy to avoid the negative effects of inbreeding when paired with a related male in meerkats Suricata suricatta, a species where inbreeding depression is evident for several traits. We show that dominant breeding pairs seldom divorce, but that rates of EPP are associated with genetic similarity between mates. Although extra‐pair males are no more distantly related to the female than social males, they are more heterozygous. Nevertheless, extra‐pair pups are not more heterozygous than within‐pair pups. Whether females benefit from EPP in terms of increased fitness of the offspring, such as enhanced survival or growth, requires further investigations.     

Impact of monoecy in the genetic structure of a predominately dioecious conifer species, Araucaria angustifolia (Bert.) O. Kuntze

Understanding the mating system of a tree species is important in genetic conservation and tree breeding strategies because it affects the inbreeding and genetic diversity of the descendant populations. Araucaria angustifolia (Bert.) O. Kuntze is a mainly dioecious species that reproduces through outcrossing. However, some monoecious trees have been identified and they may reproduce through self-fertilization. The objective of this study was to confirm the expected relatedness of full-sibs in outcrossed hand-pollinated progenies of female seed trees, self-sibs of hand self-pollinated monoecious seed trees, and to investigate the mating system of open-pollinated progenies of female and monoecious A. angustifolia trees. To do this, eight microsatellite loci were used to genotype hand- and open-pollinated progenies. Our results show that the relatedness of outcrossed hand-pollinated progenies are true full-sibs and progenies from a selfed monoecious seed tree are self-sibs, which confirms the hand-pollination method used. Open-pollinated female seed trees reproduced only by outcrossing, generating progenies with a mixture of full- and half-sibs. Monoecious seed trees reproduced mainly by xenogamy, generating progenies with mixtures of self-sibs, full-sibs, half-sibs and self-half-sibs. We also found that an increase in the effective number of pollen donors ( $ N_{\text{ep}} $ ) would lead to an increase in the total number of alleles ( $ K $ ) within progenies. Our results also suggest that monecious trees have limited potential to modify the genetic structure through selfed seed production due to the very low estimated selfing rate in these trees and the rare occurrence of these trees in natural populations.     

Mate choice in Darwin's Finches

Female Geospiza conirostris on Isla Genovesa, Galapagos, pair preferentially with males who have had previous breeding experience. They choose mates on the basis of courtship behaviour and black adult plumage. By mating with experienced black males, they gain a fitness advantage in terms of fledgling production and recruitment of young into the breeding population. Behavioural signs of past breeding experience and black plumage are reliable age- and condition-dependent traits. We suggest that females use conspicuous black plumage to identify old males at a distance, then interactions through courtship to modify initial assessments. Females paired with inferior males may increase the genetic quality of their offspring by extra-pair copulations; results of heritability analysis of morphology are consistent with this suggestion. Females change mates at a frequency of 12–27% per breeding season. They re-pair with males who are generally old, experienced, and hold territories adjacent to the deserted male. Females that re-pair gain a benefit, whereas males who are deserted within a breeding season incur a cost of more than 50% of their future potential production for that season. We conclude that females in choosing males seek reliable indicators of potential parental care, and in addition they may seek indicators of genetic quality.     

Effects of social status, age, and season on androgen and cortisol levels in wild male golden lion tamarins (Leontopithecus rosalia)

This study examines factors affecting androgen and cortisol levels in wild, male golden lion tamarins (Leontopithecus rosalia). Golden lion tamarins are a cooperatively breeding species in which groups often contain two potentially breeding males. Brothers frequently emigrate together and develop a clear dominance hierarchy, but interactions between them are primarily affiliative. Duos in which the males are not related are less stable. In addition, reproductive skew theory predicts that dominant males will be less likely to share reproduction with related subordinates. As such, we predicted that both androgens and cortisol would be higher in subordinate males unrelated to the dominant male. We also predicted that androgens in breeding males would be higher during the mating season than the birth/infant care season, as per Wingfield's "challenge hypothesis" (1990). Fecal samples were collected from 24 males in 14 social groups and assayed by enzyme immunoassay. Androgen levels were higher in breeding males during the mating season, thus supporting the challenge hypothesis. However, while subordinate males unrelated to the dominant male had significantly lower androgens than any other group, cortisol levels were not correspondingly higher. These results suggest that unrelated subordinate males show measurable reproductive suppression and may use strategies such as infantilization to avert aggression from dominant males.     

Selection on ultrasonic call rate in neonatal rats affects low frequency,but not ultrasonic,vocalizations in adults

In this experiment, we studied a rodent model selected over 57 generations for high or low rates of ultrasonic vocalizations (USVs) during maternal separation as pups. We investigated the influence of this breeding on the adult animals’ subsequent vocal output, comparing acoustic variables across developmental stages. We hypothesized that selection on pup USV rate would impact adult USV production without affecting lower frequency calls. Contrary to this hypothesis, we found neither number of USV calls or other acoustic variables to differ among selected adult lines. Instead, we found that pup USV selection mainly affected adults’ low-frequency (human-audible) calls. Furthermore, low-frequency vocalizations did not fully fit a predicted correlation between body weight and fundamental frequency: high line males, although the heaviest on average, did not produce the lowest fundamental frequencies. Our findings suggest that selection for early ultrasonic vocal behaviour pleiotropically results in changes in anatomical production mechanisms and/or neural control affecting low-frequency calls.     

Social status affects the degree of sex difference in the songbird brain

It is thought that neural sex differences are functionally related to sex differences in the behaviour of vertebrates. A prominent example is the song control system of songbirds. Inter-specific comparisons have led to the hypothesis that sex differences in song nuclei size correlate with sex differences in song behaviour. However, only few species with similar song behaviour in both sexes have been investigated and not all data fit the hypothesis. We investigated the proposed structure-function relationship in a cooperatively breeding and duetting songbird, the white-browed sparrow weaver (Plocepasser mahali). This species lives in groups of 2-10 individuals, with a dominant breeding pair and male and female subordinates. While all male and female group members sing duet and chorus song, a male, once it has reached the dominant position in the group, sings an additional type of song that comprises a distinct and large syllable repertoire. Here we show for both types of male-female comparisons a male-biased sex difference in neuroanatomy of areas of the song production pathway (HVC and RA) that does not correlate with the observed polymorphism in song behaviour. In contrast, in situ hybridisation of mRNA of selected genes expressed in the song nucleus HVC reveals a gene expression pattern that is either similar between sexes in female-subordinate male comparisons or female-biased in female-dominant male comparisons. Thus, the polymorphic gene expression pattern would fit the sex- and status-related song behaviour. However, this implies that once a male has become dominant it produces the duetting song with a different neural phenotype than subordinate males.     

Low reproductive success in territorial male Antarctic fur seals (Arctocephalus gazella) suggests the existence of alternative mating strategies

Microsatellites were used to conduct an analysis of paternity of Antarctic fur seals (Arctocephalus gazella) from Bird Island, South Georgia. At most, only 28% of pups at our study site could be assigned a father, even though the majority (approximately 90%) of candidate males within this colony were sampled. The behavioural and genetic evidence from this study suggests that a number of alternative mating strategies may exist within this fur seal population. Holding a land-based territory conferred an advantage to male reproductive success. However, this advantage was much smaller than expected from behavioural observations. At least 70% of fur seal pups born at our study site in a given year are not fathered by males who held a territory or were observed copulating with females in the previous year, implying that there exists a pool of males that seldom venture ashore at this site. To explain this discrepancy we suggest that female choice is an integral component of the Antarctic fur seal mating system and that aquatic mating may play a much larger role in the Antarctic fur seal than previously thought.     

How Do Infanticidal Male Bank Voles (Myodes glareolus) Find the Nest with Pups?

Infanticide, the killing of conspecific young, occurs in most mammal species, like in our study species, the bank vole (Myodes glareolus). Infanticide by adult males is regarded as a strong factor affecting recruitment of young into population. It is considered as an adaptive behaviour, which may increase male fitness via resource gain or an increased access to mates. When an intruder is approaching the nest, the mother should not be present, as her nest guarding is very aggressive and successful. Pups use ultrasonic vocalisation to call their mother when mother leaves nest for foraging but it is not know which cues do infanticidal males use to find the nest with vulnerable pups to commit infanticide? We studied whether the pups' sounds or the olfactory cues of the nest guide the males of known infanticidal behavioural trait towards the nest with vulnerable pups. Four nest boxes in a large indoor arena offered different nesting cues: nest odour, pup vocalisation, both odour and sound or control with no cue. The result showed that infanticidal males were more active in their searching behaviour than non‐infanticidal males and seemed to target the nest providing only acoustic cues. Four of the males, all infanticidal, intruded the nest box. Infanticidal males seem to actively search for nests with vulnerable pups by eavesdropping pup begging calls for absent mother. However, under natural conditions, mother presence and aggressive nest protection may be an effective counter strategy against strange male infanticide. When trapping study voles from the wild, we monitored occurrence of male infanticide across the breeding season from early to late summer. Proportion of infanticidal males was between 25 and 29% of all males tested along the breeding season. Our results suggest that male infanticide seems to cause a stable threat for pup mortality in increasing breeding season density.     

Factors affecting aggressive behaviour of spawning migratory males towards mature male parr in masu salmon Oncorhynchus masou

This study examined whether dominant migratory males (adopting fighter tactics) of the masu salmon Oncorhynchus masou would more aggressively attack large mature male parr (adopting sneaker tactics) as large mature male parr are expected to have the potential to cause a greater decrease in fertilization success. The frequency of aggressive behaviour was not related to the body size of males, and it increased with the frequency of interactions with mature male parr. The fertilization success of mature male parr was much lower than migratory males, and no relationship was observed between fertilization success and aggressive behaviour. The low fertilization success of mature male parr, despite infrequent aggressive behaviour by migratory males, indicates that there might be little benefit for migratory males to attack mature male parr more aggressively according to their body size.     

Socially induced brain differentiation in a cooperatively breeding songbird

Birds living in social groups establish dominance hierarchies, and taking up the dominant position influences behaviour and physiological parameters. In cooperatively breeding white-browed sparrow weavers (Plocepasser mahali), the transition from subordinate helper to dominant breeder male induces the production of a new type of song. This song contains a large number of new syllables and differs in temporal pattern from duet songs produced by all other group members. Here we show that this change in social status of adult males affects the morphology of a behavioural control circuit, the song control system of songbirds that is composed of large neuron populations. The volume of the song control areas HVC and RA and their gene-expression levels depend on males' social status. Dominant males have several times larger testes than subordinates, which is not reflected in circulating androgen and oestrogen levels. Our findings suggest a remarkable differentiation of adult vertebrate brains in relation to changing social cues.     

Grey seal, Halichoerus grypus, energetics: females invest more in male offspring

Grey seal females transfer large amounts of energy to their pups during the brief lactation period. The costs of lactation have been measured using weight changes of mother and pup pairs. Large females come ashore to give birth earlier in the season and lose weight more rapidly than smaller females. The sex ratio of Grey seal pups born is skewed towards males in the early part of the breeding season. Male pups are larger at birth and gain weight more rapidly than female pups, and their mothers show a correspondingly faster rate of weight loss than mothers of female pups. The energy costs of gestation and lactation to a Grey seal mother are 31 GJ for male pups and2–8 GJ for female pups. Males are therefore 10% more costly in energy terms to raise to weaning. Because, on average, large females arrive at breeding sites before smaller animals, biased results on weight changes would be obtained from methods which do not use repeated weighings. We suggest that the high efficiencies of lactation estimated for Harp seals compared with other phocid seals could be accounted for by such a bias.     

Philopatry, Site Fidelity and Local Kin Associations within Grey Seal Breeding Colonies

Abstract Colonially breeding animals such as grey seals typically have a discrete number of breeding sites. The extent to which offspring are philopatric (return to breed at their natal site) and the prevalence of philopatry by sex of pup has fundamental consequences for the social and genetic structure within and between each colony.
Grey seals born and marked by tagging and cohort brands at colonies on North Rona, Outer Hebrides since 1960 and at the Isle of May, Firth of Forth since 1981 have shown philopatry. Overall re-sight rates of 1620 pups tagged at North Rona and 1667 pups at the Isle of May ranged from 0 to 17%. Although most evidence of philopatry relates to females, males at each colony displayed philopatry. In addition, females born at N. Rona pupped closer to their natal sites than would be expected by chance (p = 0.005), providing evidence of fine scale natal site fidelity. Females born at the Isle of May did not show the same degree of fine scale natal site fidelity, but there was considerable individual variation. The spatial scale of philopatry shown by seals differed according to the local area within each island. Fidelity of known adult females to pupping sites at both colonies was high. In addition, we found an instance of mother and daughter pupping together away from the daughter's natal site.
These data: (i) provide evidence of philopatry in both sexes at each site; (ii) describe occurrences of fine scale philopatry at both sites; (iii) show that mothers and offspring occupied the same areas on the colony, suggesting the possibility of highly related groups within colonies, which would provide conditions for kin-specific altruistic behaviours; (iv) suggest the possibility of individual or kin recognition, even though contact between mothers and offspring has been thought to cease after the 18 d lactation period.     

Weak polygyny in California sea lions and the potential for alternative mating tactics

Female aggregation and male territoriality are considered to be hallmarks of polygynous mating systems. The development of genetic parentage assignment has called into question the accuracy of behavioral traits in predicting true mating systems. In this study we use 14 microsatellite markers to explore the mating system of one of the most behaviorally polygynous species, the California sea lion (Zalophus californianus). We sampled a total of 158 female-pup pairs and 99 territorial males across two breeding rookeries (San Jorge and Los Islotes) in the Gulf of California, Mexico. Fathers could be identified for 30% of pups sampled at San Jorge across three breeding seasons and 15% of sampled pups at Los Islotes across two breeding seasons. Analysis of paternal relatedness between the pups for which no fathers were identified (sampled over four breeding seasons at San Jorge and two at Los Islotes) revealed that few pups were likely to share a father. Thirty-one percent of the sampled males on San Jorge and 15% of the sampled males on Los Islotes were assigned at least one paternity. With one exception, no male was identified as the father of more than two pups. Furthermore, at Los Islotes rookery there were significantly fewer pups assigned paternity than expected given the pool of sampled males (p<0.0001). Overall, we found considerably lower variation in male reproductive success than expected in a species that exhibits behavior associated with strongly polygynous mating. Low variation in male reproductive success may result from heightened mobility among receptive females in the Gulf of California, which reduces the ability of males to monopolize groups of females. Our results raise important questions regarding the adaptive role of territoriality and the potential for alternative mating tactics in this species.     

Prosocial behaviour emerges independent of reciprocity in cottontop tamarins

The cooperative breeding hypothesis posits that cooperatively breeding species are motivated to act prosocially, that is, to behave in ways that provide benefits to others, and that cooperative breeding has played a central role in the evolution of human prosociality. However, investigations of prosocial behaviour in cooperative breeders have produced varying results and the mechanisms contributing to this variation are unknown. We investigated whether reciprocity would facilitate prosocial behaviour among cottontop tamarins, a cooperatively breeding primate species likely to engage in reciprocal altruism, by comparing the number of food rewards transferred to partners who had either immediately previously provided or denied rewards to the subject. Subjects were also tested in a non-social control condition. Overall, results indicated that reciprocity increased food transfers. However, temporal analyses revealed that when the tamarins'' behaviour was evaluated in relation to the non-social control, results were best explained by (i) an initial depression in the transfer of rewards to partners who recently denied rewards, and (ii) a prosocial effect that emerged late in sessions independent of reciprocity. These results support the cooperative breeding hypothesis, but suggest a minimal role for positive reciprocity, and emphasize the importance of investigating proximate temporal mechanisms underlying prosocial behaviour.     

Territorial aggression does not feed back on testosterone in a multiple-brooded songbird species with breeding and non-breeding season territoriality,the European stonechat

Testosterone mediates reproductive behaviours in male vertebrates. For example, breeding season territoriality depends on testosterone in many species of birds and in some, territorial interactions feed back on testosterone concentrations. However, the degree to which territorial behaviour and testosterone are associated differs even between species with seemingly similar life histories, especially between species that also defend territories outside the breeding season. Here, we investigate the link between territorial behaviour and testosterone in European stonechats. Previous studies found that territorial aggression in stonechats depends on testosterone in a breeding, but not in a non-breeding context. We investigated whether stonechats show a rise in testosterone during simulated territorial intrusions (STI) during the breeding season. Post-capture testosterone concentrations of males caught after an STI were not higher than those of males caught in a control situation regardless of breeding stage. However, most of the males would have been able to mount a testosterone response because the same individuals that did not increase testosterone during the STI showed a substantial increase in testosterone after injections of gonadotropin-releasing hormone (GnRH). GnRH-induced and post-capture testosterone concentrations were positively correlated and both decreased with successive breeding stages. Further, territory owners with a short latency to attack the decoy expressed higher post-capture testosterone concentrations than males with a longer latency to attack the decoy. Thus, there is no evidence for behavioural feedback on testosterone concentrations during male-male interactions in stonechats. In combination with previous studies our data suggest that testosterone functions as an on/off switch of high intensity territorial aggression during the breeding season in stonechats. The among-species variation in the androgen control of territorial behaviour may be only partly a result of environmental differences. Instead, potential differences in how territoriality evolved in different species may have influenced whether and how a reproductive hormone such as testosterone was co-opted into the mechanistic control of territorial behaviour.     

Female Intrasexual Territoriality and its Potential Adaptive Significance: The Pampean Grassland Mouse as an Ecological Model Species

Territorial behaviour in female small mammals has been proposed as a mechanism to defend limited ecological resources or their pups against conspecific infanticidal or predators. Female territorial behaviour very often is associated with reproductive activity due to the fact that frequency and intensity of aggression are exhibited mainly when females are pregnant or lactating. In vole and mice species, female territoriality would be a counterstrategy to prevent the killing of their pups by conspecific breeding females. To study whether female territoriality is a strategy for pups or nest defence against infanticidal breeding females, and whether time invested in nursing young affects aggressive response of mothers, we used the Pampean grassland mouse (Akodon azarae) as an ecological model species. We conducted resident–intruder tests between lactating females. Differences in residency time (48 vs. 72 h) of focal females in their home territory were also included in the analysis. In all cases, the pups of both resident and intruder mothers were placed with the nesting material from their reproductive cages. Resident mothers were always more aggressive than intruders and they were even more aggressive when they spent more time nursing their pups. Contrarily, intruder females exhibited the greatest values of submissive behaviours. Our results show that female territoriality of A. azarae would represent a strategy to protect pups from potentially infanticidal females. We discuss the extent of female intrasexual territoriality and its potential adaptive significance in relation to strategies which lead to increase their reproductive success.     

Male reproductive strategy and the importance of maternal status in the Antarctic fur seal Arctocephalus gazella

Abstract. Although mammalian mating systems are classically characterized in terms of male competition and polygyny, it is becoming increasingly apparent that alternative male strategies and female choice may play important roles. For example, females who mate with males from a dominant dynasty risk producing inbred offspring. Many pinnipeds are highly polygynous, but in some species alternative male strategies such as aquatic mating appear to be important, even when behavioral observations suggest strong polygyny. Here, we analyze male reproductive success in the Antarctic fur seal Arctocephalus gazella , an otariid described behaviorally as being highly polygynous, by combining a microsatellite paternity analysis spanning seven consecutive breeding seasons with detailed behavioral data on both sexes. Territorial males fathered 59% of 660 pups analyzed from our study colony. Male reproductive skew was considerable, with a quarter of all paternities assigned to just 12 top individuals on a beach where mean annual pup production was 635. Most males were successful for only a single season, but those able to return over successive years enjoyed rapidly increasing success with each additional season of tenure. We found no evidence of alternative male reproductive tactics such as aquatic or sneaky terrestrial mating. However, paternity was strongly influenced by maternal status. Females observed on the beach without a pup were significantly less likely to conceive to a sampled territorial male than equivalent females that did pup. In addition, their pups carried combinations of paternal alleles that were less likely to be found on the study beach and exhibited lower levels of shared paternity. Thus, from a territorial male's perspective, not all females offer equal opportunities for fertilization.     

Male dominance,paternity, and relatedness in the Jamaican fruit-eating bat (Artibeus jamaicensis)

We analysed variation at 14 nuclear microsatellite loci to assess the genetic structure, relatedness, and paternity of polygynous Jamaican fruit-eating bats. A total of 84 adults captured in two caves exhibited little genetic differentiation between caves (FST = 0.008). Average relatedness among adult females in 10 harem groups was very low (R = 0.014 +/- 0.011), providing no evidence of harem structure. Dominant and subordinate males shared paternity in large groups, while dominant and satellite males shared paternity in smaller groups. However, our results suggest that male rank influences paternity. Dominant males fathered 69% of 40 offspring, followed by satellite (22%) and subordinate males (9%). Overall adult male bats are not closely related, however, in large harem groups we found that subordinate and dominant males exhibited relatedness values consistent with a father-offspring relationship. Because dominant and subordinate males also sired all the pups in large groups, we propose that their association provides inclusive fitness to them.     

Territorial intrusions and copulation patterns in red kites, Milvus milvus, in relation to breeding density

Two main paternity assurance strategies are generally found in birds: mate guarding and frequent copulations. The latter is expected particularly in species such as raptors that cannot guard their mates efficiently because of ecological constraints, such as frequent courtship feeding. I investigated the prelaying behaviour of red kites, in which the males courtship feed. I compared pair behaviour in situations of varying breeding density and simulated male territorial intrusions by presenting decoys. Males' certainty of paternity was likely to decrease with increasing breeding density, because of the proximity of other males and more frequent male territorial intrusions during the presumed fertile period. The percentage of time spent by males within their breeding territory during the prelaying period was positively related to the number of close breeding neighbours, suggesting territory surveillance and mate guarding. The kites copulated frequently and over a long period. Copulation frequency prior to and during laying increased with breeding density, and in isolated pairs in response to simulated male territorial intrusions. The results support the idea of paternity assurance through frequent copulations during the presumed fertile period of the female, and suggest that early copulation activity is related to functions other than fertilization, such as pair bonding or mate assessment. Copyright 2000 The Association for the Study of Animal Behaviour.