The immunological function of allosuckling

Young mammals are unable to mount an efficient immune response against invading pathogens. Until their immune system is mature mothers transmit to their young immunological compounds during lactation. Given that genetic and foster mothers can assume this protective role, we propose that young mammals may gain immunological benefits by suckling more than one nursing female, a behaviour referred to as "allosuckling". This hypothesis has so far not been considered as a potential explanation for the propensity of young mammals to suckle foster mothers. However, pathogen transmission through milk during allosuckling may reduce the immunological net benefit that young gain, and furthermore allosuckling may increase pathogen transmission between foster and genetic mothers implying costs of allosuckling for all participants. Here, we develop the immunological function of allosuckling hypothesis (IFA) as a potential explanation for intra-and interspecific variation in allosuckling frequency. We present published experimental evidence for the assumption that immunological benefits of allosuckling depend on the immunological status of the offspring, the foster and the genetic mothers. Finally, we give predictions arising from the IFA hypothesis and propose that the IFA may provide a new explanation as to why neonates suckle various females and why foster females often refuse to nurse nonoffspring.     

Nursing Synchronization and Milk Ejection Failure as Maternal Strategies to Reduce Allosuckling in Pair-Housed Sows (Sus scrofa domestica)

Non‐offspring nursing (allosuckling) is costly for lactating females. It is reasonable to assume, therefore, that mechanisms have evolved to control the frequency of allosuckling. It is suggested that the synchronization of nursing between females could be such a mechanism. The aim of this study was to investigate whether nursing synchronization is related to the timing of nursing behaviour of paired sows and the behaviour of alien piglets in relation to allosuckling. Specifically, we predicted that: (i) nursing synchronization will increase if there is a real risk of allosuckling compared with a situation where there is none, (ii) nursing synchronization indeed reduces allosuckling and, therefore, those nursings with allosuckling attempts will be less closely synchronized than those without allosuckling attempts and (iii) in non‐synchronized nursings, the sows will more often employ another strategy to reduce allosuckling, namely, they will make the nursings non‐nutritive by not releasing milk. Ten pairs of sows and their litters were used in this study. For each pair, the two sows were housed individually until their litters were weaned; however, their litters had access to both sows from day 11 post‐partum. The behaviour of the 10 pairs of sows with their litters was videotaped for 6 h on days 10, 11, 17 and 24 post‐partum. The frequency of allosuckling attempts, non‐nutritive nursings and allosuckling during milk ejection was analysed for every pair for every day of observation. The observed frequency of nursing synchronization was high. The median interval between the start of a nursing within one pair of sows was 32 s. The first prediction was supported as synchronization became significantly tighter when piglets were given the possibility to allosuckle on day 11 [Cochran–Mantel–Haenszel (CMH) statistics, p < 0.0001]. The second prediction was also supported; the nursings were less closely synchronized when there were allosuckling attempts (CMH statistics, p < 0.05). Of all nursings, 36% had an allosuckling attempt; however, only 17% resulted in real allosuckling. Evidence in favour of the third prediction was also found as non‐nutritive nursings were more frequent in non‐synchronized nursings (CMH statistics, p < 0.05). Finally, real allosuckling during milk ejection was unrelated to the degree of nursing synchronization, as in less synchronized nursings, the sows responded to allosuckling attempts by not releasing milk. Our results suggest that sows are not able to completely suppress allosuckling; however, they can reduce its frequency through nursing synchronization and non‐nutritive nursings.     

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'.     

Suckling and Allosuckling in Captive Fallow Deer (Dama dama,Cervidae)

Suckling and allosuckling were studied in relation to the age and sex of fawns in a captive population of fallow deer (Dama dama) showing a high rate of allosuckling (73% of the suckling bouts). No difference occurred between the sexes in either the duration or frequency of suckling and allosuckling. The frequency of suckling bouts decreased rapidly during the first four weeks of life while the frequency of allosuckling bouts increased rapidly between the second and the third week and remained constant until the conclusion of the observations (11th week of life). Birth date affected allosuckling, with late-born fawns performing fewer and shorter allosuckling bouts. The lack of a negative relationship between suckling and allosuckling frequencies failed to confirm the hypothesis that allosuckling allows fawns to complete their milk requirements on foster mothers. Both inbreeding and crowding could explain the absence of particular relationship between fawns and foster mothers.     

Non-offspring nursing in social carnivores: minimizing the costs

We compare the nursing behavior of two species, African lions(PanfheraLeo) and spotted hyenas(Crocuta Craig Packer crocuta), and showthat non-offspring nursing is much less common in hyenas thanlions. Hyenas spend less time with their cubs, are more alertduring the suckling attempts of cubs, and more frequently resistthe attempts of non-offspring. Vigilance against milk theftmay therefore influence the distribution of non-offspring nursingacross species. Our detailed study of non-offspring nursingin lions shows that females preferentially nurse their own offspringand that cubs are more surreptitious when attempting to sucklefrom other females. Non-offspring nursing in lions is most commonwhen the costs are lowest. First, non-offspring nursing is morecommon among close kin. Second, females with small litters,and presumably more milk to spare, give a higher proportionof their nursing to non-offspring. Third, females give a higherproportion of their nursing to non-offspring as their own cubsgrow older and need less milk. Cubs reared in créchesdo not appear to gain more milk that cubs raised alone, andfemales do not show any evidence of reciprocity in nursing oneanother's offspring. We suggest that non-offspring nursing inlions occurs as a by-product of the females' communal defenseof their cubs against infanticide.     

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.     

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.     

Effects of hypergravity exposure on plasma oxytocin concentration in pregnant and lactating rat dams

Rat dams and offspring were exposed to 1.5-g, 1.75-g or 2.0-g hypergravity (hg) from Gestational day [G] 11 until Postnatal day [P] 10. To ascertain the role of maternal factors in reduced postnatal body weights of offspring developed in hg, the dams' lactational hormones were measured. Oxytocin (OT), the major hormone responsible for milk ejection, was reduced in hg dams whereas prolactin (Prl), involved in milk production, was unchanged. Video analyses of nursing behavior revealed that hg dams spent more time nursing relative to 1-g controls. We hypothesized impaired milk transfer from dam to pup, however pup body weight gains following a discrete suckling episode were comparable across conditions. Changes in lactational hormones and nursing behavior by dams exposed to hg do not account for reduced body masses of their offspring.     

Effects of prolactin deficiency during the early postnatal period on the development of maternal behavior in female rats: Mother's milk makes the difference

During early life, prolactin (PRL) ingested by the pups through the milk participates in the development of neuroendocrine, immunological and reproductive systems. The present study tested whether a deficiency in PRL in the dam's milk during early lactation affected the offspring in terms of the maternal responsiveness in the sensitization paradigm and behavioral response to a novel environment in the offspring. Thus, lactating rats were injected (sc) on postnatal days (PND) 2–5 with bromocriptine (125 μg/day), bromocriptine + ovine PRL (125 μg + 300 μg/day), or vehicle. As juveniles (at PND 24) or adults (PND 90–100), one female from each litter was exposed to 5 foster pups continuously for 8 days and their maternal responsiveness was recorded. Female offspring were also tested in an open field arena. Adult, but not juvenile, female offspring of bromocriptine-treated mothers showed an increased latency to become maternal, in comparison to latencies displayed by the offspring of control mothers. Furthermore, the proportion of adult, but not juvenile, offspring of bromocriptine-treated mothers that became maternal was lower than that showed by the offspring of vehicle-treated mothers. In comparison to female offspring of vehicle-treated mothers, female offspring of bromocriptine-treated mothers spent less time hovering over the pups (as juvenile females), body licking (as both juvenile and adult females), and in close proximity to pups (as adult females) during the maternal behavior test. Simultaneous administration of ovine PRL and bromocriptine reversed almost all the negative effects of bromocriptine. These data suggest that maternally-derived PRL participates during the early postnatal period in the development of neural systems that underlie the control of maternal behavior.     

A case of allosuckling in wild guanacos (<Emphasis Type="Italic">Lama guanicoe</Emphasis>)

Although allosuckling, the lactation of non-filial offspring, can be a costly behavior, it has been reported in several species across a wide range of mammalian orders. Monotocous species such as ungulates exhibit this behavior less frequently than polytocous species, and most cases have been reported among captive specimens. A case of allosuckling of a free-ranging guanaco (Lama guanicoe) calf is reported. Allosuckling observed in this species may represent opportunistic behavior by the calf, supporting the “milk theft” hypothesis.     

Kin Recognition and Maternal Care under Restricted Feeding in House Mice (Mus domesticus)

This study tests the hypothesis that female house mice (F1 generation of wild caught Mus domesticus) should preferentially invest in own offspring if confronted with young of different degrees of relatedness. The maternal behaviour of females with litters of 4 own and 4 unrelated alien young (cross-fostered at day 1 of lactation) was analysed during a lactation period of 22 days both under ad libitum and under restricted feeding (food was restricted by 20%). Cross-fostering and restricted feeding had no effect on the amount of time spent nursing until weaning. Under both feeding conditions the females did not differ in their maternal behaviour towards own and alien young: there were no significant differences either in the amount of time spent nursing own versus alien pups or in the time spent licking own versus alien young. Weight gain of own and alien = wild littermates did not differ significantly in mixed litters and was similar both under ad libitum and under restricted feeding. Such indiscriminate behaviour might be adaptive if female house mice prefer to communally nest with a relative and thus improve their inclusive fitness by investing in own and related offspring in a communal nest. Under moderate restricted feeding females could not wean the entire litter but reduced litter size by cannibalizing on average 2.7 pups (75% of the pups were killed when they were 4–8 days old). Females with cross-fostered litters killed as many own as alien young. This suggests that females cannot discriminate between own and unrelated young if cross-fostering takes place at day 1 of lactation. Besides testing kin recognition abilities, the experiments also allow analysis of the weaning strategy of females under food shortage. Under restricted feeding, body weight of the females was significantly lower during middle lactation than under ad libitum feeding. Weaning weight of young in reduced litters under food restriction (9–10 g) did not differ significantly from weaning weight of young in litters of 7–10 young, but was lower than that of young in similar sized litters (litter size 6), under ad libitum feeding. The maternal behaviour of cannibalizing some young under food shortage can be interpreted as a weaning strategy which results in the largest number of offspring that can be raised to a minimal weaning weight of 9–10 g. Such a weaning strategy might represent a favourable trade-off between number and size of young produced.     

Fostering in an African rodent, Saccostomus campestris (Cricetidae)

Fostering was studied in females of an African rodent Saccostomus campestris , the pouched mouse, which, contrary to most other rodents, is a solitary species. Females will only tolerate their own offspring and other adults are viciously attacked at all times except during the short period of pro-oestrus, when a male will be temporarily accepted.
Alien pups (n = 857) of different age-groups (0–30 days) were introduced to lactating females (n = 191) with their own pups (n = 1053) of different age-groups (0–20 days) over a period of three years. The total number of pups per female was made up to 10 (e.g. 7 own + 3 alien or 4 own + 6 alien).
The 'foster mother' readily accepted and successfully reared alien pups provided they were less than 21 days of age when introduced. Weaned alien pups, introduced when 25 or 30 days old, were viciously attacked by the foster mother and had to be removed, althoughin the breeding colony, pups that were allowed to remain with their mother after weaning were not attacked. It appears that up to weaning-age, female Saccostomus campestris may not distinguish between may not distinguis between their own and alien offspring, but rather between suckling and weaned pups.     

Differential Growth of Own and Alien Pups in Mixed Litters of Mice: A Role for Genomic Imprinting?

Female mice are said to be unable to distinguish own from alien offspring and will indiscriminately nurse each other's young in communal nests. Here, we present results of a split‐litter experiment that tested whether offspring growth was affected depending on whether they were nursed by their own or unrelated foster mothers. Pups of reciprocal crosses between C57/B6 and CBA/Ca strains were fostered in mixed litters that consisted half of their natural siblings and half of unrelated littermates of the reciprocal genotype. Analysing the relative growth of the two pup types showed that offspring gained proportionally more weight when nursed by their own mothers than their cross‐fostered litter mates during the period from day 15 until weaning, during which maternal provisioning effort contributes to pup weight gain. Before day 15 of the pups’ life, however, we found no advantage of being nursed by biological mothers, and we suggest that this may be due to the effects of paternally expressed genes in young that mask their maternal identity, thus favouring indiscriminate nursing of all young in a communal nest.     

Testing why the sex of the maternal parent affects seedling survival in a gynodioecious species

In gynodioecious plants, seed offspring from hermaphrodites often perform less well than those from females. This lower performance sometimes can be attributed to inbreeding by hermaphrodites or to relatively greater provisioning of individual seeds by females. However, these hypotheses are not explanatory when only outcrossing occurs and when individual seeds of the two morphs are equally well provisioned. Three hypotheses may explain the lower fitness of seed offspring from hermaphrodites in such cases. The morphology hypothesis states that the opportunity for gametophytic selection is lower within flowers of hermaphrodites compared to flowers on females, because the perfect flowers of hermaphrodites are relatively short-styled. The cytotype hypothesis states that the performance difference is directly caused by an individual's cytotype, whose frequency in the population may differ for the two sex morphs. The pleiotropy hypothesis states that negative pleiotropic effects of nuclear restorer alleles or alleles hitchhiking with them are expressed more often by offspring from hermaphrodites. We performed two experiments using the gynodioecious plant Silene acaulis to contrast these hypotheses. In our first experiment we contrasted the morphology and pleiotropy hypotheses by performing controlled pollinations and subsequently planting seeds in both the greenhouse and field. Hermaphrodites of S. acaulis can produce both pistillate and perfect flowers, which allowed us to determine whether flower morphology affects offspring survivorship independent of the sex of the maternal parent. We found that neither seed mass nor germination differed between seeds from females and hermaphrodites. Offspring from pistillate flowers on hermaphrodites did not differ significantly in their survival compared to offspring from perfect flowers on hermaphrodites, but had lower survivorship compared to offspring from pistillate flowers on females, refuting the morphology hypothesis. In a second experiment, we compared offspring survival of full-sibling pairs of females and hermaphrodites (who shared the same cytoplasm) to contrast the cytotype and pleiotropy hypotheses. We found that seed offspring from females and hermaphrodites that shared the same cytoplasm differed in their survival, which is counter to the prediction of the cytotype hypothesis. In both experiments, the sex of the maternal parent significantly affected offspring survival, with seed offspring from hermaphrodites surviving less well than those from females. These results support the pleiotropy hypothesis. We conclude by discussing alternative ways of thinking about negative pleiotropic effects of nuclear restorers or "the cost of restoration."     

Plasma prolactin concentrations in breeding pied flycatchers (Ficedula hypoleuca) with an experimentally prolonged brooding period

This experiment explored the stimulatory effect of brooding newly hatched young on plasma prolactin concentration in male and female pied flycatchers, Ficedula hypoleuca. By exchanging offspring between nestboxes, one group of parents was exposed to 1- to 3-day-old nestlings for 12 days. Females in this group continued night-time brooding during these 12 days. The females, but not the males (who do not participate in brooding nestlings), after 6 days had higher plasma prolactin concentrations than control birds which had shown a 50% reduction in night-time brooding at this stage. By Day 12, however, prolactin concentration had decreased to the same level as in control birds, even though these females were still brooding 3-day-old nestlings. Female flycatchers given 3-day-old nestlings on the day their own eggs hatched showed an earlier reduction in night-time brooding and an earlier decrease in plasma prolactin than did control birds. An early decrease in prolactin was also seen in the males of this experimental group.     

The male and female perspective in the link between male infant care and mating behaviour in Barbary macaques

Infant care from adult males is unexpected in species with high paternity uncertainty. Still, males of several polygynandrous primates engage in frequent affiliative interactions with infants. Two non‐exclusive hypotheses link male infant care to male mating strategies. The paternal investment hypothesis views infant care as a male strategy to maximize the survival of sired offspring, while the mating effort hypothesis predicts that females reward males who cared for their infant by preferably mating with them. Both hypotheses predict a positive relationship between infant care and matings with a particular female. However, the paternal investment hypothesis predicts that increased matings come before infant care whereas the mating effort hypothesis predicts that infant care precedes an increase in matings. Both hypotheses are usually tested from the perspective of the proportion of matings and care that individual females engage in and receive, rather than from the perspective of the care and mating behaviour of individual males. We tested the relationships between care and mating from both female and male perspectives in Barbary macaques. Mating predicted subsequent care and care predicted subsequent mating when viewed from the male but not the female perspective. Males mainly cared for infants of their main mating partners, but infants were not mainly cared for by their likely father. Males mated more with the mothers of their favourite infants, but females did not mate more with the main caretakers of their infants. We suggest that females do not choose their mating partners based on previous infant care, increasing paternity confusion. Males might try to increase paternal investment by distributing the care according to their own instead of female mating history. Further, males pursue females for mating opportunities based on previous care.     

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.     

Milk intake and production curves and allosuckling in captive Iberian red deer, Cervus elaphus hispanicus

In two experiments, we compared milk intake (assessed by weighing calves before and after suckling) and milk production (by hand milking hinds) in Iberian red deer both when calves sucked their mothers together (group-suckling experiment) and when mother and offspring were isolated (isolation-suckling experiment). In both experiments, the general lactation curve for calves increased to a peak and then decreased (type I, standard lactation curve in mammals), whereas the curve for hinds decreased from the start (type II). However, in the experiment on group suckling, calves ingested 17.2% more milk than that produced by their mothers from weeks 6 to 20. In both isolation- and group-suckling experiments, hinds showed an overproduction of milk decreasing from weeks 1 to 5. This decreasing overproduction coincides with a similar trend in calf mortality reported in the literature and might thus be aimed at ensuring calves have sufficient nutrients when mortality is highest. In addition, allosuckling observations in the group-suckling experiment showed an inverse relationship between milk production and percentage of allosucking attempts. Allosucking attempts were also more frequent after the milk overproduction period. Both findings suggest that allosuckling is a response to compensate for a reduced maternal milk supply. Copyright 2000 The Association for the Study of Animal Behaviour.     

Heterochrony and the evolution of poecilogony: generating larval diversity

Poecilogony is the production of more than one type of young within a single species of marine invertebrate. We chose a poecilogonous polychaete to investigate potential differences in morphogenesis among offspring that are polymorphic in dispersal potentials (planktonic, benthic) and trophic modes (planktotrophy, adelphophagy). Differences in morphogenesis occur and are strongly influenced by maternal type. Females that provide extra-embryonic nutrition (as nurse eggs; type III females) also produce offspring with an accelerated onset of juvenile traits, relative to planktotrophic offspring of females that do not provide extra-embryonic nutrition (type I females). Thus, progeny of some females appear morphologically preadapted for a benthic lifestyle. Surprisingly, differences in phenotype among offspring do not parallel offspring ecotype, as offspring with early onset of juvenile traits (III) are ecologically bimodal. Some Type III offspring eat the nurse eggs (adelphophagy), have accelerated development, and hatch as benthic juveniles. In contrast, their siblings hatch as small, planktotrophic, dispersive larvae that are morphologically similar to their type III siblings, but ecologically similar to Type I planktotrophic larvae. We propose that poecilogony evolved through sequence heterochrony in morphogenesis with accelerated onset of juvenile traits in type III offspring. In addition, we suggest that heterochrony in life-history events (hatching, metamorphosis) also occurs, thereby generating offspring that are dimorphic in both phenotype and ecotype. Over time, selection acting on different levels of ontogeny (morphogenesis vs. dispersal) may balance this polymorphism and allow poecilogony to persist.     

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.