Alloparental Research Articles

Female Choice and Inter-Sexual Competition for Female Sexual Partners in Japanese Macaques

AbstractObservations of a captive colony of Japanese macaques (Macaca fuscata) were carried out with the goal of documenting (1) competition between males and females for female sexual partners and (2) choice of same-sex sexual partners by females, despite the presence of motivated, opposite-sex alternatives. Data were collected during 21 homosexual consorts hips involving 14 females living in a mixed-sex group of 37 individuals. Intersexual competition for female sexual partners was manifested when a sexually motivated male and female (competitors) simultaneously sought exclusive access to the same infertile or post-conception female (focus of competition). This occurred during male intrusions on female homosexual consortships and counter-challenges by female competitors against intruding males. Inter-sexual competition for female sexual partners took the form of approaches and solicitations directed at the focus of competition, as well as displacements and aggression directed at one's competitor. Females did not acquire alloparental care for their immature offspring from their same-sex consort partners. Thus, female competitors appeared to engaged in potentially risky competition for same-sex sexual partners in the absence of any obvious reproductive benefit (e.g. insemination or alloparental care). Following these interactions, females which were foci of competition chose to mount with the female competitors significantly more often than not.

Parental state and offspring recognition in the biparental cichlid fishPelvicachromis pulcher

Alloparental care was investigated in the biparental West African cichlid,Pelvicachromis pulcherNon-breeding adults typically consumed young conspecifics but this trait was inhibited in both sexes during reproductive attempts. Alien conspecific young were accepted into the brood if they were of a similar age/developmental stage to the parents' own young but not if they were much older or much younger. If not accepted they were consumed by whichever adult located them. Parents separated from their brood for up to 4 days accepted their young on reunion but separation for more than 4 days resulted in the young being consumed. This latter response occurred if chemical stimuli from the young were available during the separation but not if visual stimuli were available. In this latter case parental responsiveness was maintained. Both sexes of this externally fertilizing species appeared to have the same information about their young and showed the same changes in responsiveness and the same discriminatory abilities.

Affiliative relationships between adult males and immature group members in naturally occurring ringtailed lemurs (Lemur catta).

Affiliative relations between adult males and immature group members were studied in three naturally occurring groups of ringtailed lemurs (Lemur catta) over a 12-month period at Beza-Mahafaly Reserve, southwestern Madagascar. No statistically significant difference was found in rates of affiliative interactions between adult males and older immatures (juveniles and adolescents) over reproductive seasons. However, some of the adult males in two focal groups increased their rates of affiliative behaviors with older immatures during the lactation and subsequent 1993 postmigration periods. Female involvement with infants during lactation season, the increasing independence of juveniles and adolescents, and length of male tenure may be factors contributing to such a pattern. Neither adult males nor immatures were significantly responsible for the initiation and maintenance of proximity in male-immature dyadic interactions. Neither dominance rank nor age-class of the adult male affected their rates of affiliative behavior with immatures. The majority of focal males exhibited an interest in infants and occasionally participated in alloparental care. It is suggested that adult males can benefit from affiliative relations with immatures in terms of opportunities for greater spatial centrality in the group, which can lead to enhanced predator protection and greater opportunities to develop affiliative relationships with females. Immatures can benefit from affiliation with males in relation to enhanced predator detection and protection, alloparental care, and opportunities to develop social skills.

The general protected invasion theory: Sex biases in parental and alloparental care

The biases towards eusociality, female workers and maternal care in haplodiploid versus diploid insects may result from the relatively low probabilities that rare mutant, partially dominant alleles promoting these behaviours will be lost by genetic drift in haplodiploid populations (Reeve, 1993). A generalization of this 'protected invasion' theory also predicts that parental and alloparental care will tend to be associated with the homogametic sex in diploid populations if the Y chromosome of the heterogametic sex is absent or largely inert. Sex differences in (allo)parental care (i.e. either parental or alloparental care) should increase with increased asymmetry between the sexes in the fraction of behaviour-influencing loci occurring on their characteristic sex chromosomes. The theory explains the strong predisposition towards female (allo)parental care in mammals, a contrasting tendency towards male (allo)parental care in birds, the propensity for joint male and female (allo)parental care in termites, and biases towards female cooperation in social spiders. The theory also explains the apparent rarity or absence of alloparental care in marsupials, an intriguing consequence of preferential paternal X-chromosome inactivation in this taxon. Thus protected invasion theory possibly provides new insights into the relationship between social structure and the genetic system. The theory does not compete with ecological or kin-selective hypotheses for the advantages of (allo)parental care; indeed, such advantages must exist for protected-invasion biases to operate.

Cooperative Breeding in Gray Jays: Philopatric Offspring Provision Juvenile Siblings

We present evidence for cooperative breeding in Gray Jays (Perisoreus canadensis), a species characterized by delayed dispersal but long thought not to exhibit the life-history tactic of helping. Our findings to date suggest that the alloparental care of younger siblings by philopatric yearlings is confined to the postfledging period of nutritional dependence. We encourage other workers to investigate whether helping may be confined to this period in other semi-social species as well. Ongoing work is aimed at evaluating the fitness consequences of helping in our study population.

The influence of predators on adoption behaviour in adult convict cichlids (Cichlasoma nigrofasciatum)

The adoption of unrelated young by brood-guarding convict cichlid (Cichlasoma nigrofasciatum) parents is influenced by several factors. Three of these are the risk of intrabrood aggression, the risk of differential predation of their own young, and the trade-off between the benefits of brood dilution and the costs of differential predation. This study introduces the "adoptable fry size hypothesis" model, which synthesizes the findings of earlier studies on each of these factors and details the range of adoptable fry sizes that increase foster brood survival across fry development. The influence of predation risk on the behaviour of parents toward foreign fry of different sizes was examined. Brood-guarding adults approached and mouthed at foreign fry larger than the upper limit of the model least often, but bit at them most often, thus excluding them. As host fry size increased, the number of behaviours directed at foreign fry decreased. Predator number did not significantly influence the size of foreign fry toward which the adults directed their behaviour. However, the overall frequency of these behaviours increased with increasing predator number, confirming previous studies suggesting that alloparental care is motivated by high predation risk.

Babysitting, dive synchrony, and indications of alloparental care in sperm whales

Young sperm whales (Physeter macrocephalus) serially accompany different members of their social group at the surface while the majority of the group is foraging at depth. The presence of a nearby larger whale is likely to increase the survival prospects of the young animal. In studies off the Galapagos Islands, first-year calves were less likely to be seen at the surface alone than were larger whales, and groups containing calves showed less synchronous diving behaviour – shorter intervals with no larger whales at the surface – than those without calves. This difference in diving synchrony was not solely the result of behaviour by individuals assumed to be the mothers of calves (as they spent a disproportionate amount of time accompanying them). Thus babysitting in sperm whales seems to be a form of alloparental care. Its benefit may have been an important factor in the evolution of sociality in female sperm whales.

Brood amalgamation in the Bristle‐thighed Curlew Numenius tahitiensis: process and function

Alloparental care in birds generally involves nonbreeding adults that help at nests or breeding adults that help raise young in communal nests. A less often reported form involves the amalgamation of broods, where one or more adults care for young that are not their own. We observed this phenomenon among Bristle‐thighed Curlew Numenius tahitiensis broods in western Alaska during 1990–1992. Amalgamation of broods generally involved the formation of temporary and extended associations. Temporary associations were formed by the incidental convergence of broods soon after they left their nests. During this period, parents defended distinct brood‐rearing areas, were antagonistic to conspecifics and remained together for less than 3 days. Extended associations formed when chicks were 1–2 weeks old. Here, parents and their broods occupied distinct, but adjacent, brood‐rearing areas and moved around as a unit. Whether a brood participated in either temporary or extended associations or remained solitary appeared to depend on brood density in the immediate area and on hatching date. When chicks were 3–4 weeks old, aggregations of up to ten broods formed wherein young mixed and parents defended a common brood‐rearing area. All broods (n = 48) that survived to fledging joined such aggregations. Alloparental care involved only antipredator defence and was not associated with activities such as feeding and brooding. Most female parents abandoned their broods shortly after the young could fly and when aggregations were forming. The female parent of a pair always deserted its young before or on the same day as the male parent and, in every aggregation, one or two males continued to tend young for about 5 days longer than other male parents. In most cases, adults deserted the young 2–6 days before the young departed the area when about 38 days old. Bristle‐thighed Curlews also formed temporary associations with American and Pacific Golden Plover Pluvialis dominica and Pluvialis fulva, Whimbrel Numenius phaeopus, Bar‐tailed Godwit Limosa lapponica, Western Sandpiper Cal‐idris mauri and Long‐tailed Skua Stercorarius longicaudus. Curlews and other larger bodied species commonly attack‐mobbed predators together, whereas smaller bodied species generally gave alarm calls and circled the predators. For all species, the intensity of antipredator defence by attending adults gradually decreased as young became older and aggregations formed. We suggest that amalgamation of broods among Bristle‐thighed Curlew enhances predator defence, aids in the process of flock formation for migrating young, and allows females and some males to desert their young earlier.

Allopaternal care in the redlip blenny

Territorial male Ophioblennius atlanticus atlanticus were found to switch to experimentally deserted nests of other males and adopt their fry. This alloparental care appears to aid in

Nest switching and alloparental care in colonial white storks

White stork,Ciconia ciconia, chicks were observed to abandon their natal nests prior to independence and to be adopted by neighbouring foster parents in approximately 40% of broods at three breeding colonies. Nest switching coincided with a decrease in feeding rates by parents and an increase in aggression by siblings triggered by the flight exercises of nestmates, and mainly affected the eldest chicks in larger broods. Chicks that abandoned their natal nests moved into broods containing both fewer and younger chicks, and thus experienced a decrease in aggression rate compared with their natal broods. Adopted chicks may also have increased their food intake as a consequence of nest switching. Resident chicks suffered from lower feeding rates during adoption and had lower mass increments than chicks in non-fostering broods of comparable age and size. Both adults and chicks were highly aggressive against trespassing chicks. The probability of aggression was a good predictor of the extent of fostering across different brood sizes, suggesting that defence by residents was effective at preventing adoption. Residents appeared not to recognize kin but were capable of aggressive discrimination against non-familiar chicks. Fostering behaviour in this species can be understood as the equilibrial outcome of an intraspecific ‘co-evolutionary’ arms race between kleptoparasitic chicks and fostering host adults with weak selection pressures for both parties.

Helping non-relatives: a role for deceit?

In birds and mammals with ‘helpers-at-the-nest’, some individuals not only feed unrelated offspring, but also compete to do so. Non-adaptive explanations for alloparental care do not predict competition for access to offspring that, in its most extreme form, can include kidnapping young from adjacent territories. A common adaptive explanation holds that allofeeding promotes a ‘social bond’, with non-relatives. This proximate hypothesis does not explain why the recipient later cooperates with or helps at the nest of its former benefactor. An extension of this hypothesis posits that, by helping to care for unrelated young, individuals may take advantage of a kin-recognition mechanism based on associations learned by nestlings while being fed. The deceived young later may offer assistance according to its perceived relatedness to the former helper. This mechanism, termed kinship deceit, may be a form of bet-hedging in cooperative breeding systems where mortality is high, where breeders can benefit from contributions by helpers, and where helpers normally assist relatives.

Biparental care in Djungarian but not Siberian dwarf hamsters ( Phodopus)

Parental behaviour was directly observed during two 30-min bouts on each of the first 18 days after birth for both Djungarian, P. campbelli, and Siberian, P. sungorus, dwarf hamster litters. Results were consistent with predictions based on earlier studies that demonstrated a positive impact of paternal presence on pup survival in P. campbelli, but not P. sungorus. The presence of the father or an aunt significantly decreased, by about half, the proportion of time that pups were alone in P. campbelli. Because brief parental absences were unlikely to result in pup cooling, analyses also considered only those absences that were 3 min or longer. By those criteria, P. campbelli pups housed with a second adult were rarely alone. In contrast, the father had little impact on the parental care received by pups in P. sungorus. Phodopus sungorus males were rarely alone in the nest with the pups, whereas both fathers and aunts in P. campbelli were alone with the pups significantly more often than the mother from mid-lactation until weaning. This behaviour reflected temporal coordination between the behaviour of the adults. Pups were left alone less often than expected based on the independent behaviour of each adult. Because there was no reason to expect alloparental care by aunts in the wild, the presence of a second adult, rather than specific parental behaviour by that adult, may be the essential component of increased pup survival. Limited observations of male parental care in the wild demonstrated that significant paternal care could occur in P. campbelli. Both field and laboratory data, however, suggest that biparental care would be facultative and adaptive under certain environmental conditions (e.g. extreme temperatures) but not all.

Female/Female Competition in European Badgers Meles meles: Effects on Breeding Success

We present data on the effects of female/female competition on the reproductive success of European badgers Meles meles in Britain. While a single, dominant female usually suppresses reproduction in other female group members, elsewhere up to four females may breed successfully in each group. Across Britain, the mean number of breeding females per social group decreases in populations living at high latitudes, where food availability and population density are relatively low. Within our study population in southern England, the number of breeding females in each social group increased with the quality of the group territory. In our study population, all females aged 3 years and older became pregnant, but a proportion of females lost their litters during gestation or around the time of birth. The proportion of females that lost their litters was higher in larger groups. However, mean litter size at weaning remained roughly constant despite variation in the number of females lactating, and preweaning cub mortality appeared to be low. Females tended to disperse away from very large groups, and may have increased their chances of breeding in this way. These results suggest that females competed for breeding status, but that there was little competition among females thereafter. The characteristics of females that produced cubs successfully differed between the 2 years when this study was carried out. Only females in relatively good condition bred successfully following a very dry summer, when food availability was low. However, when food availability was high, following a wet summer, females were in better condition on average and breeding success appeared to be related to social status. We suggest that this reflected a difference in the structure of competition between the two years. In contrast with the situation in other social carnivores, reproductive suppression in badgers appears to be a response to female/female competition for resources, rather than a need for co-operative care of the young. Although alloparental care occurred in at least one badger population, this population had the lowest, rather than the highest, level of reproductive suppression.

Alloparental care in the marine sculpinAlcichthys alcicornis (Pisces: Cottidae): Copulating in conjunction with paternal care

The elkhorn sculpinAlcichthys alcicornis spawns and subsequently copulates, and the eggs are then cared for by the male. DNA fingerprinting was used to determine the paternity of males for the clutches guarded by them. When a female was mated with 4 males in succession in aquaria, males did not fertilize the eggs spawned just before copulation unless the female was unimpregnated but fathered the eggs spawned by the female later. In the field, near the end of the breeding season, males were genetically unrelated to the clutches in their territories. We concluded that males guard non-kin eggs for the opportunity to copulate and to fertilize the future clutches of their mates.

Helping is costly to young birds in cooperatively breeding white-winged choughs

Cooperative breeding among birds is at its most extreme in white-winged choughs ( Corcorax melanorhamphos ). Choughs have never been observed to breed successfully without helpers, and reproductive success increases linearly across all group sizes (maximum = 16). Further, helpers contribute to every aspect of reproduction, including nest building and incubation. Here we show that the contribution of young helpers (one year old and less) to incubation depends on the group in which they live. In small groups (3-5 birds), young helpers contribute as much to incubation as older birds, but in large groups they contribute little. In large groups, help increases sharply with age. Old birds contribute equally, regardless of group size. Although choughs generally do not lose body mass over incubation, young helpers lose mass in proportion to the amount of incubation they perform, independent of any effect of group size. This provides evidence that helpers in cooperatively breeding birds suffer costs from providing help additional to the costs incurred from remaining philopatric. It also demonstrates that the needs of the group influence whether young birds provide help.

Alloparental care and the influence of father presence on juvenile prairie voles, Microtus ochrogaster

Abstract. The influence of fathers on alloparental behaviour of juvenile prairie voles was studied in a semi-natural environment. Juveniles were observed throughout the lactation period either in the presence of both parents and litter or with the mother and litter only. Juveniles remained in the natal nest after the birth of a subsequent litter and displayed alloparental care including huddling over, making contact with, and grooming younger siblings. The presence of fathers influenced the behaviour of juveniles. Juveniles spent more time in the natal nest in contact with younger siblings and less time engaged in passive-alone behaviour (resting on all four feet outside the nest away from other animals) when housed with both parents than with mothers only. This effect was stronger in male juveniles. Developmental changes in alloparental care coinciding with the growth of pups were observed only in the two-parent condition. Younger pups also developed more rapidly when fathers were present.

Haplodiploidy, eusociality and absence of male parental and alloparental care in Hymenoptera: a unifying genetic hypothesis distinct from kin selection theory

Beginning with Hamilton ( J. theor. Biol. 7, 1-52 (1964)), evolutionary biologists have attempted to explain the apparent predisposition for the haplodiploid Hymenoptera to evolve both eusociality and female workers. As an alternative to kin selective, pre-adaptational, or ecological explanations for this association, I propose a new genetic hypothesis, the protected invasion hypothesis : dominant alleles for maternal care in finite haplodiploid populations are more resistant to loss from genetic drift than are paternal-care alleles in haplodiploid populations or than are either maternal or paternal-care alleles in diploid populations. Similarly, dominant alleles for female alloparental care in finite haplodiploid populations are more resistant to loss from genetic drift than are male alloparental alleles in haplodiploid populations or than are (male or female) alloparental alleles in diploid populations. A Markov model of phenotypic evolution describing the step-wise progress of a population toward one of two adaptive peaks demonstrates that even small differences in fixation probabilities among these alleles can translate into large differences in the long-run probabilities of observing the corresponding parental or alloparental strategies. Thus the protected invasion hypothesis immediately explains all of the peculiar social features of the haplodiploid Hymenoptera, namely: (i) the overwhelmingly greater tendency for maternal care than paternal care in Hymenoptera; (ii) the greater propensity for eusociality (alloparental sibling care) in Hymenoptera than in diploid insects; and (iii) the greater likelihood for females than males to become alloparents (workers) in the Hymenoptera. The hypothesis also correctly predicts (iv) the apparently higher frequency of paternal care in diploid species than in haplodiploid species, and (v) the lack of a sex-bias among workers of eusocial diploid species. The protected invasion hypothesis is distinct from relatedness-based explanations and provides a more comprehensive explanation for the repeated appearance of the distinctive social structures of the Hymenoptera than does the kin selection model. I show that the bias toward eusociality in Hymenoptera is produced by protected invasion effects even when there is no female-biased sex ratio and no asymmetry between a female’s relatedness to its siblings and to its own offspring. In addition, protected invasion effects create a bias for female versus male workers within the Hymenoptera even when there is no asymmetry between a female’s and male’s relatedness to its siblings. Furthermore, protected invasion effects create a bias toward eusociality in haplodiploid versus diploid populations even when the queen mates an indefinite number of times and there is no difference between haplodiploid and diploid colonies in the relatednesses of workers to their tended brood. Finally, the protected invasion hypothesis explains a phenomenon that cannot be explained by kin selection theory: the surprising overwhelming preponderance of maternal over paternal care in the Hymenoptera (because male and female parents have the same mean relatedness to their offspring when the female mates singly). An important implication of the protected invasion hypothesis is that synergistic co-operation among siblings is more likely to evolve in haplodiploid than in diploid species.

Effect of Familiarity With the Mother and Kinship On Infanticidal and Alloparental Behaviour in Virgin House Mice

AbstractExperienced male and female house mice encountering a newborn pup can display indifference, parental or infanticidal behaviour. Characteristics of the pup such as sex and strain do not seem to influence the likelihood of infanticide, in contrast to attributes of the adult subjects (age, sex, strain, sexual experience, previous cohabitation with the mother, reproductive condition). This study investigated the effect of kinship and/or familiarity with the mother on male and female behaviour towards pups. The subjects were 100-day-old Swiss-Webster virgin male and female mice. After 24 hours of isolation, a 24-36 hrs old pup was introduced into their home-cage and their behaviour was recorded for 15 min. Male and female mice killed related as well as unrelated pups. Females killed fewer offspring of females with whom they had cohabited until 3 weeks before the study, in comparison with the offspring of completely unfamiliar females. When females were exposed to the offspring of females of comparable familiarity but different relatedness, they devoted more parental behaviour towards more related pups. This suggests that, even if familiarity plays a major role in determining females' behaviour, kin recognition occurs and is responsible for differences in alloparental care distribution. The behavioural strategies adopted by male and female mice are interpreted on the basis of differences in activity range of the sexes within a deme (breeding group).

Alloparental Care in Free-Ranging Lemur catta at Berenty Reserve, Madagascar

Alloparental care was examined in three free-ranging groups of Lemur catta. Group members of all age/sex classes were found to participate to varying degrees in alloparental care of infants, and some types of care were performed significantly more frequently by animals of particular age/sex classes. Adult males, previously reported not to interact with infants, were found to groom and play with them occasionally. Rank or sex of the infant did not affect the amount of alloparental care it received. It is suggested that individuals of all age/sex classes can benefit from receiving or performing alloparental care. Infants can develop social skills and receive protection from alloparents; mothers gain free time to forage and rest; prereproductive females can learn parental skills; all adult females and prereproductive animals are aiding kin by alloparental care, and adult males, by interacting with infants, may have the opportunity to establish a relationship with the mother which could enhance future reproductive success.

Brood amalgamation and alloparental care in the Least Sandpiper, Calidris minutilla

Least Sandpipers (Calidris minutila) were studied on the Queen Charlotte Islands, British Columbia, over five breeding seasons. Brood amalgamation and care of foreign chicks occur regularly, though at low incidence, among the approximately 90 breeding pairs there. Such behavior is probably important to chick survival and has little impact on adult fitness. Brood amalgamation and alloparental care appear to be widespread in calidridine sandpipers.