Allonursing in tufted capuchin monkeys (Cebus nigritus): milk or pacifier?

Allonursing, the behaviour of females nursing offspring that are not their own, is relatively frequent in capuchin monkeys. Using focal-animal sampling and ad libitum observations we describe the pattern of allonursing in a wild group of tufted capuchins, Cebus nigritus (4 cohorts, 22 infants), at Iguazú National Park, north-eastern Argentina, and test several hypotheses on the adaptive value of allonursing. During 2,351 contact hours with the group (including 4,207 focal-animal samples totalizing 329 h focused on infants) we observed 39 allonursing bouts. Infants were not allonursed more frequently by close kin than by more distant allomothers. Offspring of dominant females were allonursed more frequently than those of low-ranking females. Nursing bouts were longer than allonursing bouts. Our results suggest that allonursing in tufted capuchins has a social function and is not mainly aimed at providing milk to infants.     

Allonursing in Captive Guanacos,Lama guanicoe: Milk Theft or Misdirected Parental Care?

Females in several ungulates transfer milk to non-filial (NF) offspring, in a process known as allonursing. This behavior is less common in monotocous species, including most ungulates, and it has been associated with parasitic behavior of calves or mothers who have lost their own offspring. To examine whether the calves 'steal' milk from the females or whether females fail to discriminate their own calves in guanacos, allonursing behavior was observed. If milk theft drives allonursing, mothers should reject NF offspring, they should search for their own calves, and calves attempting to suckle from alien mothers should adopt parallel (as opposed to the anti-parallel) position during allonursing. Alternatively, if allonursing is caused by mothers unable to discriminate own offspring, mothers are not expected to reject NF offspring, and alien calves should use parallel and antiparallel position similarly when allonursing. Allonursing was investigated during the first 3 mo of lactation in two groups of captive guanacos composed of 15 and 14 mother-calf pairs, respectively. While 40% and 62.5% of mothers in groups 1 and 2 performed allonursing, high individual variation prevailed; some females exhibited this behavior infrequently (4.1% and 6.5 % in groups 1 and 2). The rejection rate to NF nursing attempts was threefold higher than the rejection rate to filial nursing attempts. The occurrence of nursing to NF was associated to a parallel posture by the calves. Our findings suggest that 'milk theft' is a more plausible hypothesis to explain allonursing in guanacos than 'misdirected parental care'.     

Evidence of Reciprocal Allonursing in Reindeer,Rangifer tarandus

The nursing of non‐offspring is referred to as allonursing. Reciprocity is a hypothesized cause of allonursing, but previous studies have not strongly supported or found no evidence in support for this hypothesis. Biological market theory was applied to 25 reindeer (Rangifer tarandus) does and their calves to investigate allonursing reciprocity across bouts and within dyads and assess the diversity of allonursing partners. We also investigated whether variation in allonursing would be associated to relatedness within dyads. We recorded both the occurrence and the duration of 1027 successful allonursing solicitations. All does allonursed, and only three of the 25 calves were not observed being allonursed. Throughout the study, 234 allonursing dyadic pairs were observed. Does allonursed the calves of several does, but allonursing was not distributed evenly among all potential partners. Twenty does were members of at least 1 dyad with a high degree of reciprocity based on the number of allonursing bouts exchanged within the dyad. We found evidence of both relative and absolute allonursing reciprocity at the group level. Across bouts and within dyads, the reciprocal allonursing indexes varied greatly both for frequency and for duration, with an average tendency towards unidirectionality. Evidence of strong reciprocity within dyads was found in 32 dyads for number of allonursing bouts and in 25 dyads for duration of allonursing bouts. Across bouts and within dyads, the number of allonursing bouts received was not influenced by relatedness, allonursing bouts given or absolute rank difference. Allonursing was not interchanged for rank‐related benefits. Our results provide evidence of reciprocal allonursing at the group level, across bouts and within dyads, and reciprocal allonursing among chosen partners. Our results point to the usefulness of applying the biological market theory to allonursing and of considering allonursing as a tradable commodity, traded for itself, among chosen partners.     

Allonursing in captive belugas (Delphinapterus leucas)

This study describes allonursing (females nursing offspring that are not their own) in captive belugas (Delphinapterus leucas). In addition to the calf's mother, two females that were not pregnant or nursing at the time of the calf's birth spontaneously lactated and nursed the male calf intermittently throughout 34 months of his life at the Vancouver Aquarium Marine Science Center. These observations suggest that allonursing may also take place in their wild counterparts and add to existing evidence of alloparental care in this species. Alloparental care, the care of nonoffspring, has been observed in every major mammalian taxon; the protection of calves through alloparental care may be a strong evolutionary benefit. Zoo Biol 29:633–637, 2010. © 2010 Wiley‐Liss, Inc.     

Alloparenting in Steller sea lions (<Emphasis Type="Italic">Eumetopias jubatus</Emphasis>): correlations with misdirected care and other observations

Alloparental care is rarely observed in Steller sea lions (Eumetopias jubatus) where maternal care is extended to a single pup for up to 1 year or more. However, we observed 28 allonursing events and one case of adoption at a small breeding rookery in the western Gulf of Alaska between the years 2001 and 2005. Multiparous and primiparous females were observed nursing nonfilial individuals with equal frequency, but primiparous females spent significantly more time nursing nonfilial individuals. Multiparous females allowed allonursing only while sleeping and unaware while most primiparous females were aware that they were allonursing. These results are consistent with the misdirected-care hypothesis suggesting that primiparous (presumably younger) females nurse nonfilial pups due to inexperience, whereas multiparous (presumably older) females are victims of milk stealing during times of inattentiveness. Nonfilial pups were aggressively tossed most often during the pupping season and only by multiparous females, while allonursing events occurred more frequently after the pupping season. Starveling pups were not cared for by any female, but two were attended by a single bull during separate autumn seasons.     

Indiscriminate nursing in communal breeders: a role for genomic imprinting

Abstract In several communally nesting mammal species, females indiscriminately nurse each others' offspring. Previous hypotheses have suggested that the inability to recognize one's own young during lactation is the result of costs incurred from recognition errors. Here, we propose an alternative hypothesis based on sexual conflict theory and genomic imprinting. In polygynous species, males copulate with several females that may later breed communally. Under such conditions, males benefit from indiscriminate nursing of all their offspring and the reduced risk of female infanticide. This may have selected for paternally expressed genes that suppress kin recognition during lactation.     

Direct benefits of choosing a high‐fitness mate can offset the indirect costs associated with intralocus sexual conflict

Intralocus sexual conflict generates a cost to mate choice: high‐fitness partners transmit genetic variation that confers lower fitness to offspring of the opposite sex. Our earlier work in the fruit fly, Drosophila melanogaster, revealed that these indirect genetic costs were sufficient to reverse potential “good genes” benefits of sexual selection. However, mate choice can also confer direct fitness benefits by inducing larger numbers of progeny. Here, we consider whether direct benefits through enhanced fertility could offset the costs associated with intralocus sexual conflict in D. melanogaster. Using hemiclonal analysis, we found that females mated to high‐fitness males produced 11% more offspring compared to those mated to low‐fitness males, and high‐fitness females produced 34% more offspring than low‐fitness females. These direct benefits more than offset the reduction in offspring fitness caused by intralocus sexual conflict, creating a net fitness benefit for each sex to pairing with a high‐fitness partner. Our findings highlight the need to consider both direct and indirect effects when investigating the fitness impacts of mate choice. Direct fitness benefits may shelter sexually antagonistic alleles from selection, suggesting a novel mechanism for the maintenance of fitness variation.     

Mate choice for offspring performance: major benefits or minor costs?

There is considerable disagreement over whether or not gaining viability benefits to offspring could be substantial enough to overcome the costs of female choosiness. A recent review suggested that the ''lek paradox'' might be resolved by large indirect benefits as indicated by highly heritable ornamental traits. We selected males of a wolf spider Hygrolycosa rubrofasciata in relation to their sexual signalling rate (audible drumming). The estimated correlated response in offspring viability was rather small (0.12 s.d.). However, it may be large enough if the costs of being choosy are small. In fact, females mate with better-than-average males just by responding passively to a random drumming signal, and the active choice by females seemed to increase this benefit only slightly. In many mating systems, females obtain better-than-average males as a consequence of intense male–male competition or because of the extraordinary variance in male signalling. The costs of any additional choice may be so minor that female choice for honestly signalling males may evolve even with minute benefits in offspring viability. This may be the general solution to the lek paradox, as most studies report no apparent fitness benefits. Publication bias favouring statistically significant results may have led to an overemphasis on the few studies with large effects.     

Microhabitat heterogeneity influences offspring sex allocation and spatial kin structure in possums

1. Sex allocation theory predicts that where dispersal is sex biased, the fitness consequences of producing male or female offspring are mediated by resource availability and maternal competitive ability. Females in poorer condition are expected to favour dispersing offspring to minimize resource competition with kin. Environmental heterogeneity may drive spatial variation in sex allocation through resource competition-related benefits to females and territory quality benefits to dispersing or philopatric offspring. 2. Here, we demonstrate that microhabitat heterogeneity can drive extremely fine-scale spatial heterogeneity in offspring sex allocation. Female bobucks (Trichosurus cunninghami) in temperate rainforest were more likely to produce male offspring than those in surrounding Eucalyptus forest. 3. A maternal physiological effect was identified, in that females of lower body mass were more likely to produce male offspring. This finding is consistent with resource competition predictions, in that smaller females are expected to have poorer competitive ability. 4. Genetic spatial autocorrelation analysis identified males as the more dispersing sex. Furthermore, overproduction of males by mothers in the rainforest habitat was geographically concordant with reduced philopatry, as inferred from spatial genetic analysis. This provides empirical validation of dispersal-related explanations of offspring sex allocation: that production of offspring of the dispersing sex minimizes the potential for resource competition with kin. 5. Spatial variation in dispersal via sex allocation responses to environmental heterogeneity can potentially contribute to spatial patterns in population dynamics.     

The Neuroendocrine Function of Allosuckling

In mammals, females occasionally nurse offspring that are not their own. The function of allosuckling for foster females remains puzzling given that lactation is energetically costly and augments the risk of pathogen transmission. Current hypotheses suggest that allosuckling is not adaptive resulting from misguided parental behaviour, females reciprocate by nursing each other's offspring, females nurse preferentially related offspring for inclusive fitness benefits, females involved in allosuckling events evacuate extra milk or improve their maternal skills. These hypotheses received only little empirical evidence, and a recent review suggested that they are not mutually exclusive and do not exclude alternatives. Based on the established fact that teat stimulation by neonates leads to an elevated production of prolactin, I develop the hypothesis called ‘neuroendocrine function of allosuckling’ (NFA). The hypothesis postulates that the nursing of alien offspring allows females to increase and/or maintain prolactin concentration in the case own offspring do not stimulate their teats enough. This neurohormone enhances immunocompetence, the immunological quality and the quantity of milk whilst reducing female's fertility. The NFA suggests that via teat stimulation by the genetic offspring, and if necessary by foster ones, females can optimally adjust prolactin concentration, as both hypo‐ and hyper‐prolactinaemia entail physiological and immunological costs. The hypothesis does not only provide an explanation as to why females may nurse alien offspring but is also useful to understand the consequences of allosuckling. Indeed, even if mothers do not nurse alien offspring to control their prolactin production, allosuckling will alter the concentration of this crucial neurohormone.     

Co-operative Rearing by Slender-tailed Meerkats (Suricata suricatta) in the Southern Kalahari

Slender-tailed meerkats or suricates, Suricata suricatta, are small, gregarious and largely insectivorous mongooses which inhabit the arid and semi-arid areas of southern Africa. We describe four elements of co-operative rearing of the young: 1. babysitting at the den; 2. creching on foraging trips; 3. provisioning with prey items away from the den; and 4. allonursing , including spontaneous lactation. Individual band members differed markedly in contributions to co-operative rearing. All adults and yearlings guarded the den and helpers actively defended young against predators. Breeders babysat significantly less than did non-breeding adults. Differences in age–sex class contributions were also evident in creching behaviour. The feeding of kittens by provisioners extended from soon after their first emergence from the den at 2–3 wk of age to effective foraging independence at 10–12 wk. Breeding females initially contributed little care other than nursing. Allonursing occurred in six of 25 closely observed litters, including three incidents of spontaneous lactation when subordinates nursed the young of higher-ranking females. Such co-operation is likely to be critical to the survival of these highly sociable mongooses in a semi-arid environment such as the Kalahari where food availability can fluctuate enormously.     

Rapid establishment of teat order and allonursing in wild boar (Sus scrofa)

Transfer of milk is the fundamental common characteristic of mammalian reproduction, but species differ considerably with respect to nursing strategies. The consequences of teat orders and allonursing have been studied intensively in domestic pigs. However, whether similar nursing strategies also exist in wild boar, the ancestor of domestic pigs is so far not known. The occurrence of allonursing in wild boar is only described anecdotally, and the question whether a teat order is established has not yet been investigated. Studying suckling behaviour of 29 piglets from six primiparous wild boar females in a semi‐natural environment we found a surprisingly fast development of a rigid teat order among littermates, which established within 2.2 hr after birth. This suggests strong fitness benefits of this phenomenon that may ultimately explain the evolution and maintenance of this trait. We further found a strong synchrony of oestrus and delivery among the females of a group, as well as the occurrence of allonursing. By determining the amount of allonursing for the first time quantitatively, we demonstrate the importance of this trait and its presumably pivotal role for juvenile survival under truly natural conditions.     

An experimental test for body size‐dependent effects of male harassment and an elevated copulation rate on female lifetime fecundity and offspring performance

Many studies investigate the benefits of polyandry, but repeated interactions with males can lower female reproductive success. Interacting with males might even decrease offspring performance if it reduces a female's ability to transfer maternal resources. Male presence can be detrimental for females in two ways: by forcing females to mate at a higher rate and through costs associated with resisting male mating attempts. Teasing apart the relative costs of elevated mating rates from those of greater male harassment is critical to understand the evolution of mating strategies. Furthermore, it is important to test whether a male's phenotype, notably body size, has differential effects on female reproductive success versus the performance of offspring, and whether this is due to male body size affecting the costs of harassment or the actual mating rate. In the eastern mosquitofish Gambusia holbrooki, males vary greatly in body size and continually attempt to inseminate females. We experimentally manipulated male presence (i.e., harassment), male body size and whether males could copulate. Exposure to males had strong detrimental effects on female reproductive output, growth and immune response, independent of male size or whether males could copulate. In contrast, there was a little evidence of a cross‐generational effect of male harassment or mating rate on offspring performance. Our results suggest that females housed with males pay direct costs due to reduced condition and offspring production and that these costs are not a consequence of increased mating rates. Furthermore, exposure to males does not affect offspring reproductive traits.     

Offspring kidnapping with subsequent shared nursing in Antarctic fur seals

Non-offspring maternal care should be common in phocids, but their occurrence would be uncommon among otariids due to the high costs of raising offspring, particularly lactation, and an efficient recognition system that allow for accurate recognition during the frequent mother–pup re-associations. However, non-offspring maternal care has been documented in some otariid species. While the phenomenon in general is not novel among the colonially breeding seals, the exclusive care to a single pup by two lactating females for an extended time is a behavior scarcely documented in natural population. In an extension of this allonursing care, we document the first case of the kidnapping of a pup with subsequent shared nursing in Antarctic fur seal including data on the effect of this interaction on the pup’s growth. While all other lactating females nursed exclusively their own pups, the shared nursing was advantageous for the pup because he grew noticeably larger (in weight and axillary girth) than other of his cohort, particularly after 50 days. This advantage would have been influenced by the asynchrony of the foraging cycle of the biological and foster mother, which resulted in a higher attendance on shore than any other male pups. Although several explanations have been hypothesized for allolactation in mammals, our observations suggest a misguided parental care, associated with recognition errors by the foster mother whose pup was stillborn.     

The indirect benefits of mating with attractive males outweigh the direct costs

The fitness consequences of mate choice are a source of ongoing debate in evolutionary biology. Recent theory predicts that indirect benefits of female choice due to offspring inheriting superior genes are likely to be negated when there are direct costs associated with choice, including any costs of mating with attractive males. To estimate the fitness consequences of mating with males of varying attractiveness, we housed female house crickets, Acheta domesticus, with either attractive or unattractive males and measured a variety of direct and indirect fitness components. These fitness components were combined to give relative estimates of the number of grandchildren produced and the intrinsic rate of increase (relative net fitness). We found that females mated to attractive males incur a substantial survival cost. However, these costs are cancelled out and may be outweighed by the benefits of having offspring with elevated fitness. This benefit is due predominantly, but not exclusively, to the effect of an increase in sons' attractiveness. Our results suggest that the direct costs that females experience when mating with attractive males can be outweighed by indirect benefits. They also reveal the value of estimating the net fitness consequences of a mating strategy by including measures of offspring quality in estimates of fitness.     

Inbreeding avoidance in rhesus macaques: Whose choice?

Whether nonhuman primates avoid copulating with close kin living in their social group is controversial. If sexual aversion to relatives occurs, it should be stronger in females than in males because of females' greater investment in each offspring and hence greater costs resulting from less viable offspring. Data presented here show that adult male rhesus macaques breeding in their natal groups at Cayo Santiago experienced high copulatory success, but copulated less with females of their own matrilineages than with females of other matrilineages. Adult females were never observed to copulate with males of their own matrilineage during their fertile periods. Although natal males sometimes courted their relatives, examination of two measures of female mate choice showed that females chose unrelated natal males over male kin. Female aversion to male kin was specific to the sexual context; during the birth season, females did not discriminate against their male relatives in distributing grooming. Evolved inbreeding avoidance mechanisms probably produce different outcomes at Cayo Santiago than in wild rhesus macaque populations. Gender differences in sexual aversion to relatives may be partly responsible for differences between studies in reported frequency of copulations by related pairs. © 1993 Wiley-Liss, Inc.     

Limited indirect fitness benefits of male group membership in a lekking species

In group living species, individuals may gain the indirect fitness benefits characterizing kin selection when groups contain close relatives. However, tests of kin selection have primarily focused on cooperatively breeding and eusocial species, whereas its importance in other forms of group living remains to be fully understood. Lekking is a form of grouping where males display on small aggregated territories, which females then visit to mate. As females prefer larger aggregations, territorial males might gain indirect fitness benefits if their presence increases the fitness of close relatives. Previous studies have tested specific predictions of kin selection models using measures such as group‐level relatedness. However, a full understanding of the contribution of kin selection in the evolution of group living requires estimating individuals' indirect fitness benefits across multiple sites and years. Using behavioural and genetic data from the black grouse (Tetrao tetrix), we show that the indirect fitness benefits of group membership were very small because newcomers joined leks containing few close relatives who had limited mating success. Males' indirect fitness benefits were higher in yearlings during increasing population density but marginally changed the variation in male mating success. Kin selection acting through increasing group size is therefore unlikely to contribute substantially to the evolution and maintenance of lekking in this black grouse population.     

New colony formation in the "highly inbred" eusocial naked mole-rat: outbreeding is preferred

If the adaptive significance of sexual reproduction derivesfrom genetic recombination, then sexual organisms that severelyinbreed minimize the benefits of sexuality without fully escapingits costs. Local populations of the eusocial naked mole-ratare extremely genetically uniform, and colonies have the highestinbreeding coefficient known for wild mammals. Because non-breedingworkers cooperate to rear the queen's offspring, researchershave speculated that the inclusive fitness benefits of closerelatedness outweigh the benefits of genetic recombination,thus leading to the adaptive avoidance of outbreeding. However,I show that in laboratory colonies in which each individualhad an equal number of familiar siblings and unfamiliar distantkin (UDK) as potential mates, mating pairs were significantlymore likely to consist of UDK. Some form of kin recognitionmust have been used in order for this pattern to result. Aggressionwas not mitigated by relatedness, however, as both fightingand cooperation occurred as frequently between siblings as betweenUDK. By studying the early stages of colony development I wasable to investigate correlations between physical characteristicsof workers and success in attaining breeding status. I alsoobserved allonursing, hitherto unseen in this species, and suggestthat it is less likely to occur later in colony development.     

Does experimentally altered plumage ornamentation of female passerines influence nestling quality? A test in female tree swallows

It is widely recognized that female animals in a variety of taxa display ornamental traits, such as elaborate plumage, but elucidating whether such traits evolve by selection or genetic correlation remains a challenge because more ornamented females are often found to produce low‐quality offspring. While resource trade‐offs between the production of ornaments and offspring may underlie this negative relationship, it is not an adequate explanation for species where the timing of production of ornaments and offspring does not overlap. Instead, costs associated with engaging in agonistic interactions with conspecifics, which maintains the honesty of signals of quality, may also reduce resources available to invest in offspring. In this study, we enhanced and reduced the plumage brightness of female tree swallows (Tachycineta bicolor) relative to controls to test whether social costs associated with displaying bright plumage is a potential mechanism underlying the observation that more ornamented females produce low‐quality nestlings. Our results showed that nestlings reared by females in the enhanced plumage brightness treatment were structurally smaller, having shorter lengths of the combined head and bill than nestlings in the reduced plumage brightness treatment, and tended to grow their head and bills more slowly than nestlings in the reduced and control plumage brightness treatments. Nestlings in the enhanced plumage brightness treatment also tended to gain mass more slowly than nestlings in control treatment. Overall, that females with enhanced plumage brightness produced structurally smaller nestlings provides evidence that social costs paid by females may lead to the production of low‐quality offspring and should be considered in future studies.