Contributions to infant care in captive cotton-top tamarins (Saguinus oedipus): The influence of age,sex, and reproductive status

Marmosets and tamarins are characterized by a reproductive strategy that includes twinning, and a communal rearing system in which infant care is shared among all group members, both breeders and nonbreeding helpers (often older offspring). In order to test some predictions about the extent to which different age-sex classes should invest in infants, contributions to infant carrying and food-sharing by all family members were measured in captive groups of cotton-top tamarins (Saquinus oedipus) ranging in size from 2 to 12 independent individuals. Fourteen litters were observed from birth to 12 weeks. Carrying by mothers decreased steadily over the study period, while carrying by fathers and other offspring increased for 3–5 weeks, then declined. Infants spent more time carried by siblings than by either parent, but parents did more carrying than individual siblings and, also, shared more food with infants. Older siblings contributed more care than younger siblings did. Adult sons carried infants more than adult daughters did, but immature daughters carried more than immature sons did. However, adult daughters actively offered food to infants more than any other class of helper did. These results were interpreted in the light of hypotheses concerning the reproductive and dispersal strategies of callitrichid species.     

Oxytocin changes primate paternal tolerance to offspring in food transfer

Oxytocin facilitates social recognition in rats and mice, onset of maternal behavior in virgin mice and formation of pair bonds without copulation in prairie voles. However, the relationship between this peptide and paternal behavior in primates remains largely unknown. We investigated whether oxytocin affects paternal behavior in common marmosets. In these primates, fathers as well as mothers take care of their infants, and transferring food to the infants is one of their more obvious caretaking behaviors. We tested whether oxytocin and an oxytocin receptor antagonist affect the transfer of food to offspirng by fathers. After intracerebroventricular infusion of the vehicle, oxytocin, or the oxytocin receptor antagonist, the fathers’ behavior, including picking up food, transferring food to the offspring, and refusing to transfer food to the offspring, was analyzed. Compared with the vehicle, oxytocin reduced the frequency of refusal. This was not caused by reduction of appetite. Although the oxytocin receptor antagonist did not change the frequency of refusal behavior of the fathers statistically significant manner, these observations suggest that the tolerance of the adult male marmoset toward its offspring as shown by the transfer of food is increased by oxytocin administered into the central nervous system.     

What happens to offspring when parents are inbred,old or had a poor start in life? Evidence for sex‐specific parental effects

Parental effects on offspring performance have been attributed to many factors such as parental age, size and condition. However, we know little about how these different parental characteristics interact to determine parental effects, or the extent to which their effect on offspring depends on either the sex of the parent or that of the offspring. Here we experimentally tested for effects of variation in parents’ early diet and inbreeding levels, as well as effects of parental age, and for potential interactive effects of these three factors on key aspects of offspring development in the mosquitofish (Gambusia holbrooki). Older mothers produced offspring that were significantly smaller at birth. This negative effect of maternal age on offspring size was still evident at maturation as older mothers had smaller daughters, but not smaller sons. The daughters of older mothers did, however, reach maturity sooner. Paternal age did not affect offspring body size, but it had a complex effect on their sons’ relative genital size. When initially raised on a food‐restricted diet, older fathers sired sons with relatively smaller genitalia, but when fathers were initially raised on a control diet their sons had relatively larger genitalia. The inbreeding status of mothers and fathers had no significant effects on any of the measured offspring traits. Our results indicate that the manifestation of parental effects can be complex. It can vary with both parent and offspring sex; can change over an offspring's life; and is sometimes evident as an interaction between different parental traits. Understanding this complexity will be important to predict the role of parental effects in adaptation.     

The consequences of parental age for development,body mass and resistance to stress in the red flour beetle

The performance of most animals deteriorates with age. Motivated by the inconsistency in the literature regarding the effect of parental age on offspring traits and performance, we studied how parental age affects offspring development time, body mass, and starvation and cold tolerance in the red flour beetle (Tribolium castaneum). Offspring of old parents pupated later and at a higher body mass, and there was a general positive correlation between body mass and starvation tolerance. Despite their higher body mass, offspring of old parents tolerated starvation less well than those of young parents, emphasizing the impaired performance of the former. However, parental age did not affect offspring thermal tolerance and offspring of old parents were not more sensitive to cold shock than those of young parents. We also examined how ageing affects body mass and cold tolerance in the parental generations. By contrast to the effect of ontogeny on thermal tolerance, which is better known, change in thermal tolerance with age is seldom studied and can take different shapes. Old beetles were more sensitive to cold shock than younger beetles. Similar to cold tolerance, body mass decreased with age. In summary, older beetles reflect a worse physiological condition than younger ones. Ageing leads to impaired cold tolerance, lower body mass, lower number of offspring reaching adulthood, and deteriorated performance of the offspring, expressed as a lower starvation tolerance and a longer development time of the offspring. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 305–314.     

Social relations between fathers and offspring in a captive group of rhesus monkeys (Macaca mulatta)

Analysis of social relations between adult males and immatures of known paternity in a captive group of rhesus monkeys (Macaca mulatta) revealed that fathers and offspring associated significantly more than other male-immature dyads. This association was highly variable, however, and there was no evidence of active preference for or investment in offspring by fathers. The tendency of offspring to approach fathers more often than other males appeared to account for the pattern of selective association. Preferential father-offspring association occurred whether or not mothers were in proximity to fathers, but mothers' associations with males did predict their offspring's, especially for the younger juveniles and the infants. It is possible that long-term social relationships between mothers and fathers lead to father-offspring association, but a year-to-year pattern of shifting mating preferences in the group weakens this hypothesis.     

Higher risk of seizures in offspring of mothers than of fathers with epilepsy.

Seizure risk has consistently been found to be higher in offspring of mothers than of fathers with epilepsy. This pattern cannot be explained by any simple genetic model. The present study examined the possibility that the pattern arises from differences between affected mothers and fathers in the characteristics of their epilepsy that influence offspring seizure risk. The study population comprised 687 offspring of parents with epilepsy from the Rochester-Olmsted County Record Linkage Project. Cumulative incidences of unprovoked seizures to age 25 were 8.7% and 2.4% in offspring of affected mothers and fathers, respectively. Cox proportional hazards analysis was used to calculate rate ratios (RRs) for unprovoked seizures in offspring. In the univariate analysis, risk of unprovoked seizures was higher if the affected parent was the mother (RR = 2.8, 95% confidence interval [ci] 1.1-7.2) or if the parent's onset was before age 20 (RR = 2.5, 95% ci 1.1-5.9), but there was no effect on offspring risk of either parent's etiology (idiopathic vs. remote symptomatic) or parent's seizure type (generalized vs. partial). These findings were not substantially changed in the multivariate analysis. Thus, differences between affected mothers and fathers in these characteristics did not account for the higher risk in offspring of affected mothers. Anticonvulsant use during pregnancy was not associated with increased offspring seizure risk.(ABSTRACT TRUNCATED AT 250 WORDS)     

Sex differences in biparental care as offspring develop: a field study of convict cichlids (<Emphasis Type="Italic">Amatitlania siquia</Emphasis>)

Parental investment theory states that parents should contribute more to older offspring. Differences between the sexes also influence how each parent contributes to offspring in biparental species. Here, we examined a naturally occurring population of biparental convict cichlids in Costa Rica to determine how each parent cared for offspring during two distinct offspring development stages. Consistent with the predictions of the reproductive value hypothesis, we hypothesized that the levels of parental contribution would be relative to the value that each parent places on a brood. We predicted that female parents would contribute more than male parents because female convict cichlids have lower future reproductive success than males. Additionally, we predicted that both parents should contribute more to older offspring, either due to the young’s increased susceptibility to predation (i.e., the vulnerability hypothesis) or because of the longer period of time parents have been interacting with older offspring (i.e., feedback hypotheses). This increase in investment by males should coincide with a change in the coordination of care between parents. Detailed observations of parental pairs in their natural habitat supported these predictions. Females contributed more to broods than males and were relatively unaffected by offspring age while males spent significantly more time with older, free-swimming fry. Additionally, males tended to leave younger offspring more than females did, and were more likely to do so consecutively with younger offspring. This suggests that the coordination of duties between parents changes as parental investment changes. Overall, these data support both the reproductive value and the vulnerability hypotheses, but not necessarily the feedback hypothesis.     

Chemical mediation of reciprocal mother–offspring recognition in the Southern Water Skink (Eulamprus heatwolei)

Abstract Kin recognition has been demonstrated to play an important role in the social structure of a wide range of animals. Most studies to date have examined parent–offspring recognition only in species that provide offspring with direct parental care, however, there are several advantages to parent–offspring recognition even in the absence of direct parental care. In this study we investigated reciprocal mother–offspring recognition in the Australian scincid lizard Eulamprus heatwolei, a species that does not show direct parental care. We examined whether neonates could discriminate between their mothers and unrelated females, and whether females could discriminate between their offspring and unrelated neonates, via chemical cues, using retreat site selection experiments. We conducted trials when neonates were 1 and 4 weeks old to investigate whether responses are maintained as neonates age. We found that both neonates and mothers could discriminate between related and unrelated individuals when neonates were 1 week old. Mothers were more likely to take refuge under tiles treated with the odours of their own offspring, while neonates spent less time in areas treated with the odours of unrelated females. At 4 weeks of age, mothers no longer exhibited discriminatory behaviour between their offspring and unrelated neonates, while neonates were more likely to associate with the odour of any female over the odourless control. We hypothesize that reciprocal mother–offspring recognition in E. heatwolei reduces interference competition between mothers and their offspring and also may be important in habitat selection and territory establishment.     

Food Sharing in Pied Bare-Faced Tamarins (Saguinus bicolor bicolor): Development and Individual Differences

We investigated food sharing behavior in 5 litters of pied bare-faced tamarins (Saguinus bicolor bicolor)—8 infants, from 3 families—from 5 to 26 weeks of age. The frequency of sharing by parents in response to infant begging increased steadily from the age of 5 weeks to 16 weeks, and then declined. Offering of food by adults without prior infant begging occurred at very low frequencies throughout observations (1.5% of total items transferred). On average, infants received approximately equal amounts of food from transfers from others and by self feeding until about 20 weeks, after which self feeding began to predominate. Begging success—the proportion of infant begs which resulted in food sharing—remained relatively constant over time, at 60–70%. Overall, therefore, the frequency of food sharing seemed to be governed by changes in infant rather than adult behavior. There were individual differences between adults in their response to infant begging, but two of three fathers transferred significantly more food to infants than mothers did. The results of this study emphasize the existence of specific and individual differences in food-sharing behavior, which must be taken into account in explaining its importance in the reproductive strategies of the Callitrichidae.     

Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae)

It is widely recognized that maternal phenotype can have important effects on offspring, but paternal phenotype is generally assumed to have no influence in animals lacking paternal care. Nonetheless, selection may favour the transfer of environmentally acquired condition to offspring from both parents. Using a split-brood, cross-generational laboratory design, we manipulated a key environmental determinant of condition - larval diet quality - of parents and their offspring in the fly Telostylinus angusticollis, in which there is no evidence of paternal provisioning. Parental diet did not affect offspring survival, but high-condition mothers produced larger eggs, and their offspring developed more rapidly when on a poor larval diet. Maternal condition had no effect on adult body size of offspring. By contrast, large, high-condition fathers produced larger offspring, and follow-up assays showed that this paternal effect can be sufficient to increase mating success of male offspring and fecundity of female offspring. Our findings suggest that both mothers and fathers transfer their condition to offspring, but with effects on different offspring traits. Moreover, our results suggest that paternal effects can be important even in species lacking conventional forms of paternal care. In such species, the transfer of paternal condition to offspring could contribute to indirect selection on female mate preferences.     

Food Transfer Among Adult Lion Tamarins: Mutualism,Reciprocity or One-Sided Relationships?

Tamarins (Callitrichidae) are cooperative breeders. Groups typically contain only two or three breeding individuals and subordinate group members are reproductively suppressed. Nonreproductive individuals, which are usually the offspring of the group's breeding members, delay dispersal while providing care to infant siblings. Callitrichid breeder-infant and helper-infant relationships have been well studied but empirical studies regarding the dynamics of breeder-helper relationships are sparse. I examined food-transfer interactions among parents and natal adults in 7 groups of captive lion tamarins, Leontopithecus spp., to test whether relationships are maintained by mutualism or reciprocity or are to the benefit of one side of a dyad. Individuals that had recently received food from a group member most frequently released food to the previous donor as their next act of transfer. Conversely, food transfer was not dependent on symmetrical relationships within groups over a time frame of several weeks. These results suggest that mutualism plays a role in the maintenance of food-transfer relationships but reciprocity does not. However, there is evidence for a reciprocal relationship between grooming and food transfer in one group. Subadults and adults living in their natal groups transferred proportionally more food to mothers than to oppositely-sexed subadult and adult siblings. Thus, individuals most likely to receive aggression preferentially released food to individuals most likely to inflict injury upon them. Although these results support the coercion hypothesis, they may suggest alternatively that food transfer by helpers to breeding adults is driven by inclusive fitness considerations.     

Begging for information: mother-offspring food sharing among wild Bornean orangutans

Transfer of solid food from mothers or other adults to dependent offspring is commonly observed in various primate species and both nutritional and informational benefits have been proposed to explain the function of such food sharing. Predictions from these hypotheses are tested using observational data on wild orangutans (Pongo pygmaeus wurmbii) at Tuanan, Central Borneo, Indonesia. In 1,145 hr of focal observation and 458 recorded food interactions between four pairs of females with offspring it was found that virtually all transfers were initiated by the offspring and that younger infants solicited food more often and did so for a greater variety of items than older offspring. All offspring primarily solicited food that was difficult to process, i.e., inaccessible to them. Furthermore, the amount of food solicitation was negatively correlated with ecological competence. Hence food sharing seemed to be related to an offspring's skill level, as suggested by the informational hypothesis. In contrast, offspring did not solicit high-quality items more than low-quality items and food sharing did not peak around the age of weaning, as predicted by the nutritional hypothesis. Mothers were usually passively tolerant, allowing offspring to take food but hardly ever provisioned. Parent-offspring conflict concerning food sharing was only observed well after weaning. Thus, by taking food directly from the mother, young orangutans were able to obtain information about the affordances and nutritional value of food items that were otherwise out of their reach and could familiarize themselves with the mother's diet. In species such as orangutans or other apes, characterized by a broad diet that requires extractive foraging, informational food transfer may be vital for an immature to acquire complex feeding skills and adult diet.     

Unequal food distribution among great egret Ardea alba nestlings: parental choice or sibling aggression?

In broods of great egrets Ardea alba and other birds with siblicidal nestlings, the first-hatched brood members generally secure far more food than do their juniors. This feeding advantage could be caused by parental favoritism, or by seniors attacking and thereby dominating their juniors. We investigated these possibilities by comparing how fathers and mothers allocated food among their offspring when chicks were free to fight versus when they were physically separated by a Plexiglas barrier. When free to fight, dominant nestlings received significantly more food than did their subordinates. When nestlings were separated, mothers, but not fathers, delivered significantly more food per meal to the β (second-ranked) chick than to other nestlings. This is the first experimental evidence of differential feeding by parents in a species with aggressive nestlings.     

Pre-hatching maternal effects inhibit nestling humoral immune response in the tawny owl Strix aluco

Although evidence is accumulating that mothers can transfer antibodies to their offspring, little is known about the consequences of such a transfer to the offspring immune system. Because maternal antibodies are effective only during a short period of time after their transfer to offspring, one hypothesis is that maternal antibodies provides a transitory antigen-specific protection to offspring, thus lessening the need for offspring to mount their own humoral immune response towards these specific antigens. In birds, this scenario predicts that offspring immune response towards a specific antigen is inhibited to a larger extent in hatchlings than in older nestlings. We tested this hypothesis in tawny owls Strix aluco by cross-fostering clutches between nests and then challenging siblings with a vaccine either two times (at 4- and 11-d-old) or only one time at 11-d-old to compare the strength of the humoral response between nestlings born from mothers with naturally high and low levels of antibodies against this vaccine. Because maternal antibodies are expected to be effective only during a short period of time after hatching, we predict that maternal antibodies should inhibit the immune response of nestlings vaccinated from the fourth day after hatching more than in nestlings vaccinated only at a later age. As expected, the inhibitory effect of maternal antibodies was stronger in nestlings vaccinated soon after hatching than in siblings injected at a later age. Therefore, in wild avian populations pre-hatching maternal effects may confer offspring with a transitory immune protection in the first days following hatching.     

Family break-up in Black and Red Kites Milvus migrans and M. milvus: is time of independence an offspring decision?

I observed the natural process of family break-up in 13 families of Black Kites Milvus migrans and five families of Red Kites M. milvus in which fledglings had been individually marked. In other broods, I performed experiments which modified the parental investment fledglings received by supplementing nests of both species with food or transferring Black Kite chicks to nests with younger or older chicks of the same species.
The time of family break-up in the Black Kite is mainly an offspring decision which is not affected by an artificial increase of parental investment. The duration of the post-fledging period was not increased in Black Kites that were given supplementary food. Chicks transferred to nests with a younger chick did not extend the post-fledging period, nor did chicks transferred to nests with an older chick shorten the post-fledging period. In Red Kites, parental investment seemed to have more influence on the timing of the family break-up. Red Kite adults invested less as parents than did Black Kites during the post-fledging dependence period, and in nests where supplementary food was given, Red Kite fledglings stayed attached for a longer period.     

Different effects of paternal trans-generational immune priming on survival and immunity in step and genetic offspring

Paternal trans-generational immune priming, whereby fathers provide immune protection to offspring, has been demonstrated in the red flour beetle Tribolium castaneum exposed to the insect pathogen Bacillus thuringiensis. It is currently unclear how such protection is transferred, as in contrast to mothers, fathers do not directly provide offspring with a large amount of substances. In addition to sperm, male flour beetles transfer seminal fluids in a spermatophore to females during copulation. Depending on whether paternal trans-generational immune priming is mediated by sperm or seminal fluids, it is expected to either affect only the genetic offspring of a male, or also their step offspring that are sired by another male. We therefore conducted a double-mating experiment and found that only the genetic offspring of an immune primed male show enhanced survival upon bacterial challenge, while phenoloxidase activity, an important insect immune trait, and the expression of the immune receptor PGRP were increased in all offspring. This indicates that information leading to enhanced survival upon pathogen exposure is transferred via sperm, and thus potentially constitutes an epigenetic effect, whereas substances transferred with the seminal fluid could have an additional influence on offspring immune traits and immunological alertness.     

State-dependent parental care in the Antarctic petrel: responses to manipulated chick age during early chick rearing

Life histories are state-dependent, and an individual's reproductive decisions are determined by its available resources and the needs of its offspring. Here we test how a chick's needs for food and protection influence parental decisions in the Antarctic petrel, Thalassoica antarctica , where the parents, due to their long breeding lifespan, are expected to give priority to their own needs before those of the young. We exchanged one-day-old chicks with four-day-old chicks and studied how the parents subsequently provided care to the chick. The duration of the guarding period was adjusted, and parents left older chicks earlier and younger chicks later compared to controls. Three mechanisms were responsible for the adjustments. 1) Parents with an older chick co-ordinated fewer guarding spells whereas parents with a younger chick co-ordinated more guarding spells. 2) At the last guarding spell, i.e. where a parent left the chick alone before the partner returned, less time was spent with older chicks, and more time with younger chicks. 3) Foraging trip duration was shortened by parents given older chicks and prolonged by parents given younger chicks, probably in response to the chick's food demand. Hence, the parents responded quickly to the altered needs of the chick. Parents with high body mass guarded longer and were better able to co-ordinate the guarding spells compared to lighter parents. In conclusion, Antarctic petrels adjust reproductive decisions to their own, their mate's, and their chick's state, and they seem to respond to the chick's needs for both food and protection.     

Transgenerational effects of parental larval diet on offspring development time, adult body size and pathogen resistance in Drosophila melanogaster

Environmental conditions experienced by parents are increasingly recognized to affect offspring performance. We set out to investigate the effect of parental larval diet on offspring development time, adult body size and adult resistance to the bacterium Serratia marcescens in Drosophila melanogaster. Flies for the parental generation were raised on either poor or standard diet and then mated in the four possible sex-by-parental diet crosses. Females that were raised on poor food produced larger offspring than females that were raised on standard food. Furthermore, male progeny sired by fathers that were raised on poor food were larger than male progeny sired by males raised on standard food. Development times were shortest for offspring whose one parent (mother or the father) was raised on standard and the other parent on poor food and longest for offspring whose parents both were raised on poor food. No evidence for transgenerational effects of parental diet on offspring disease resistance was found. Although paternal effects have been previously demonstrated in D. melanogaster, no earlier studies have investigated male-mediated transgenerational effects of diet in this species. The results highlight the importance of not only considering the relative contribution each parental sex has on progeny performance but also the combined effects that the two sexes may have on offspring performance.     

Cyanobacterial protease inhibitors lead to maternal transfer of increased protease gene expression in Daphnia

Protease inhibitors (PIs) have frequently been found in cyanobacterial blooms and have been shown to affect the major herbivore Daphnia by decreasing growth and inhibiting gut protease activity. However, it has been shown that a clone of Daphnia is able to respond to dietary PIs by increasing its protease gene expression. Such an inducible response might be maternally transferred to the next generation. Therefore, we tested a tolerant clone for maternal transfer of protease gene expression. When exposed to the trypsin inhibitor-producing cyanobacterium Microcystis aeruginosa PCC7806 Mut, Daphnia mothers and their untreated newborns showed an increase in trypsin gene expression compared to naïve mothers grown on control food and their offspring. The maternally transferred increase in gene expression was accompanied by a higher somatic growth rate of the offspring generation from exposed mothers compared to offspring from naïve mothers. This higher growth rate compensated for the lower dry mass of newborns from exposed mothers and led to the same fitness as observed in the offspring of naïve mothers. In nature, clones that can maternally transfer increased protease gene expression should have an advantage over clones that cannot. The selection for such more tolerant clones by naturally occurring PIs might lead to microevolution of natural Daphnia populations, and to local adaptation in the long term. This is the first study to show an adaptive maternal transfer of increased target gene expression in an ecological context.