Harsh nutritional environment has positive and negative consequences for family living in a burying beetle.

Harsh environmental conditions in form of low food availability for both offspring and parents alike can affect breeding behavior and success. There has been evidence that food scarce environments can induce competition between family members, and this might be intensified when parents are caring as a pair and not alone. On the other hand, it is possible that a harsh, food-poor environment could also promote cooperative behaviors within a family, leading, for example, to a higher breeding success of pairs than of single parents. We studied the influence of a harsh nutritional environment on the fitness outcome of family living in the burying beetle Nicrophorus vespilloides. These beetles use vertebrate carcasses for reproduction. We manipulated food availability on two levels: before and during breeding. We then compared the effect of these manipulations in broods with either single females or biparentally breeding males and females. We show that pairs of beetles that experienced a food-poor environment before breeding consumed a higher quantity of the carcass than well-fed pairs or single females. Nevertheless, they were more successful in raising a brood with higher larval survival compared to pairs that did not experience a food shortage before breeding. We also show that food availability during breeding and social condition had independent effects on the mass of the broods raised, with lighter broods in biparental families than in uniparental ones and on smaller carcasses. Our study thus indicates that a harsh nutritional environment can increase both cooperative as well as competitive interactions between family members. Moreover, our results suggest that it can either hamper or drive the formation of a family because parents choose to restrain reproductive investment in a current brood or are encouraged to breed in a food-poor environment, depending on former experiences and their own nutritional status.

Associations between fecal cortisol and biparental care in a pair-living primate.

OBJECTIVES: We quantified variation in fecal cortisol across reproductive periods in Azara's owl monkeys (Aotus azarae) to examine physiological mechanisms that may facilitate biparental care. Specifically, we evaluated evidence for the explanation that owl monkeys have hormonal mechanisms to mobilize energy during periods when each sex is investing heavily in reproduction, that is, the gestation period for females and the infant care period for males. MATERIALS AND METHODS: Between 2011 and 2015, we monitored 10 groups of Azara's owl monkeys from a wild population in Formosa, Argentina and collected fecal samples from 26 adults (13 males, 13 females). Using enzyme-linked immunosorbent assays, we quantified fecal cortisol as a proxy for evaluating stress responses, including energetic demands, on both sexes during periods of reproduction and parental care. RESULTS: Male cortisol was lowest during periods when they were caring for young infants (<3 months) compared with periods with older infants or no infant. Female cortisol was elevated during gestation compared with other periods. Mean fecal cortisol in both males and females was lower when an infant was present compared with when females were gestating. DISCUSSION: Our results do not support the hypothesis that owl monkey males have elevated fecal cortisol during periods when they need to mobilize energy to provide intensive infant care. Our findings are also inconsistent with the Maternal Relief hypothesis. However, results from studies measuring fecal cortisol must be interpreted with care and alternative explanations, such as seasonal fluctuations in diet and thermoenergic demands, should be considered when drawing conclusions.

Constrained flexibility of parental cooperation limits adaptive responses to harsh conditions.

Parental care is predicted to evolve to mitigate harsh environments, thus adaptive plasticity of care may be an important response to our climate crisis. In biparental species, fitness costs may be reduced by resolving conflict and enhancing cooperation among partners. We investigated this prediction with the burying beetle, Nicrophorus orbicollis, by exposing them to contrasting benign and harsh thermal environments. Despite measurable fitness costs under the harsh environment, sexual conflict persisted in the form of sex-specific social plasticity. That is, females provided equivalent care with or without males, whereas males with partners deserted earlier and reduced provisioning effort. The interaction of social condition and thermal environment did not explain variation in individual behavior, failing to support a temperature-mediated shift from conflict to cooperation. Examining selection gradients and splines on cumulative care revealed a likely explanation for these patterns. Contrary to predictions, increased care did not enhance offspring performance under stress. Rather, different components of care were under different selection regimes, with optimization constrained due to lack of coordination between parents. We suggest that the potential for parenting to ameliorate the effects of our climate crisis may depend on the sex-specific evolutionary drivers of parental care, and that this may be best reflected in components of care.

Galanin and prolactin expression in relation to parental care in two sympatric cichlid species from Lake Tanganyika.

Our understanding of the hormonal mechanisms underlying parental care mainly stems from research on species with uniparental care. Far less is known about the physiological changes underlying motherhood and fatherhood in biparental caring species. Here, using two biparental caring cichlid species (Neolamprologus caudopunctatus and Neolamprologus pulcher), we explored the relative gene-expression levels of two genes implicated in the control of parental care, galanin (gal) and prolactin (prl). We investigated whole brain gene expression levels in both, male and female caring parents, as well as in non-caring individuals of both species. Caring males had higher prl and gal mRNA levels compared to caring females in both fish species. Expression of gal was highest when young were mobile and the need for parental defense was greatest and gal was lowest during the more stationary egg tending phase in N. caudopunctatus. The onset of parenthood was associated with lower expression of prl and higher expression of gal in N. pulcher, but this pattern was not observed in N. caudopunctatus. Our study demonstrates that gal gene expression is correlated with changes in parental care in two biparental cichlid species and extends both knowledge and taxonomic coverage of the possible neurogenetic mechanisms underlying parental care.

Contribution of males to brood care can compensate for their food consumption from a shared resource.

The sharing of the same food source among parents and offspring can be a driver of the evolution of family life and parental care. However, if all family members desire the same meal, competitive situations can arise, especially if resource depletion is likely. When food is shared for reproduction and the raising of offspring, parents have to decide whether they should invest in self-maintenance or in their offspring and it is not entirely clear how these two strategies are balanced. In the burying beetle Nicrophorus vespilloides, parents care for their offspring either bi- or uniparentally at a vertebrate carcass as the sole food source. The question of whether biparental care in this species offers the offspring a better environment for development compared with uniparental care has been the subject of some debate. We tested the hypothesis that male contribution to biparental brood care has a beneficial effect on offspring fitness but that this effect can be masked because the male also feeds from the shared resource. We show that a mouse carcass prepared by two Nicrophorus beetles is lighter compared with a carcass prepared by a single female beetle at the start of larval hatching and provisioning. This difference in carcass mass can influence offspring fitness when food availability is limited, supporting our hypothesis. Our results provide new insights into the possible evolutionary pathway of biparental care in this species of burying beetles.

Seasonal changes in immune response and reproductive investment in a biparental beetle.

Immunity and reproduction are physiologically demanding processes, therefore trade-offs are expected between these life history traits. Furthermore, investments in these traits are also known to be affected by factors such as sex, body size, individual condition, seasonal changes and parasite infection. The relationship between immunity and reproduction and the effect of other factors on this relationship were investigated in many species, but there are a small number of studies on these patterns in biparental invertebrates. Lethrus apterus is an iteroparous biparental beetle with predominant female care in respect of collecting and processing food for larvae. Males guard the nest built underground and also their mate. Here we investigate how sex, body size, time within the reproductive season and parasite load may influence the relationship between immunocompetence and reproductive investment in this species. In beetles from a natural population we quantified immune response by measuring the encapsulation response, antimicrobial activity of hemolymph, the investment into reproductive tissues by measuring the size of testis follicles in males and total egg size in females, and parasite load by counting the number of mites on the beetles. We found that the encapsulation response is condition-dependent, as large individuals showed significantly higher encapsulation ability than small ones. Antimicrobial capacity was significantly higher in females than in males. In case of antimicrobial activity there was also a seasonal change in the relationship between immunity and reproductive investment, but only under heavy mite load. Reproductive investment was influenced by the interaction between body size and season (in females) and by body size and season (in males). Furthermore in females the interaction between antimicrobial activity and season indicated that reproductive investment increased with antimicrobial activity early in the reproductive season. By investigating the relationship between immunity and reproductive investment in a natural population of a biparental beetle species, we can conclude that investments into these important life history traits are governed by complex interactions between physiological and environmental factors. Our results are discussed in the context of life history evolution, highlighting the role of the assessed factors in shaping trade-offs themselves (in invertebrates).

Neuronal activation in zebra finch parents associated with reintroduction of nestlings.

Recent studies of the brain mechanisms of parental behaviors have mainly focused on rodents. Using other vertebrate taxa, such as birds, can contribute to a more comprehensive, evolutionary view. In the present study, we investigated a passerine songbird, the zebra finch (Taeniopygia guttata), with a biparental caring system. Parenting-related neuronal activation was induced by first temporarily removing the nestlings, and then, either reuniting the focal male or female parent with the nestlings (parental group) or not (control group). To identify activated neurons, the immediate early gene product, Fos protein, was labeled. Both parents showed an increased level of parental behavior following reunion with the nestlings, and no sexual dimorphism occurred in the neuronal activation pattern. Offspring-induced parental behavior-related neuronal activation was found in the preoptic, ventromedial (VMH), paraventricular hypothalamic nuclei, and in the bed nucleus of the stria terminalis. In addition, the number of Fos-immunoreactive (Fos-ir) neurons in the nucleus accumbens predicted the frequency of the feeding of the nestlings. No difference was found in Fos expression when the effect of isolation or the presence of the mate was examined. Thus, our study identified a number of nuclei involved in parental care in birds and suggests similar regulatory mechanisms in caring females and males. The activated brain regions show similarities to rodents, while a generally lower number of brain regions were activated in the zebra finch. Furthermore, future studies are necessary to establish the role of the apparently avian-specific neuronal activation in the VMH of zebra finch parents.

Perceived threat to paternity reduces likelihood of paternal provisioning in house wrens.

Biparental care is a critical and, occasionally, unequally shared obligation that ensures that young survive to maturity. Such care may be complicated in systems in which one parent, typically the male, is unsure of his genetic relatedness to the young. Males may reduce paternal provisioning when full paternity is not assured, as occurs in mating systems in which females engage in extrapair copulations. Moreover, other factors independent of extrapair matings, such as male personality traits, likely also affect the level of paternal care. In this study, we determined the effect of a paternity threat event (i.e., a conspecific or a heterospecific territory intrusion) and male personality (i.e., the level of aggressiveness) on provisioning effort by male house wrens (Troglodytes aedon). Males were more likely to attack a conspecific intruder than a heterospecific intruder. Males that were exposed to a conspecific intruder were less likely to provision young at all. Of those males that did feed the young in their nest, male aggressiveness did not relate to feeding effort. These findings suggest that the likelihood of paternal care is reduced by perceived threats to paternity but that the costs of not feeding potentially multisired young are high and feeding efforts are unrelated to male personality.

Effects of single parenthood on mothers' behavior, morphology, and endocrine function in the biparental California mouse.

Motherhood is energetically costly for mammals and is associated with pronounced changes in mothers' physiology, morphology and behavior. In ~5% of mammals, fathers assist their mates with rearing offspring and can enhance offspring survival and development. Although these beneficial consequences of paternal care can be mediated by direct effects on offspring, they might also be mediated indirectly, through beneficial effects on mothers. We tested the hypothesis that fathers in the monogamous, biparental California mouse (Peromyscus californicus) reduce the burden of parental care on their mates, and therefore, that females rearing offspring with and without assistance from their mates will show differences in endocrinology, morphology and behavior, as well as in the survival and development of their pups. We found that pups' survival and development in the lab did not differ between those raised by a single mother and those reared by both mother and father. Single mothers spent more time in feeding behaviors than paired mothers. Both single and paired mothers had higher lean mass and/or lower fat mass and showed more anxiety-like behavior in open-field tests and tail-suspension tests, compared to non-breeding females. Single mothers had higher body-mass-corrected liver and heart masses, but lower ovarian and uterine masses, than paired mothers and/or non-breeding females. Mass of the gastrointestinal tract did not differ between single and paired mothers, but single mothers had heavier gastrointestinal tract compared to non-breeding females. Single motherhood also induced a flattened diel corticosterone rhythm and a blunted corticosterone response to stress, compared to non-breeding conditions. These findings suggest that the absence of a mate induces morphological and endocrine changes in mothers, which might result from increased energetic demands of pup care and could potentially help maintain normal survival and development of pups.

Effects of short- and long-term cold acclimation on morphology, physiology, and exercise performance of California mice (Peromyscus californicus): potential modulation by fatherhood.

California mice (Peromyscus californicus) differ from most other mammals in that they are biparental, genetically monogamous, and (compared with other Peromyscus) relatively large. We evaluated effects of cold acclimation on metabolic rate, exercise performance, and morphology of pair-housed male California mice, as well as modulation of these effects by fatherhood. In Experiment 1, virgin males housed at 5° or 10 °C for approximately 25 days were compared with virgins housed at standard vivarium temperature of 22 °C. Measures included resting metabolic rate (RMR), maximal oxygen consumption ([Formula: see text]max), grip strength, and sprint speed. In Experiment 2, virgin males housed at 22 °C were compared with three groups of males housed at 10 °C: virgins, breeding males (housed with a female and their pups), and non-breeding males (housed with an ovariectomized, estrogen- and progesterone-treated female) after long-term acclimation (mean 243 days). Measures in this experiment included basal metabolic rate (BMR), [Formula: see text]max, maximal thermogenic capacity ([Formula: see text]sum), and morphological traits. In Experiment 1, virgin males housed at 5° and 10 °C had higher RMR and [Formula: see text]max than those at 22 °C. In Experiment 2, 10 °C-acclimated groups had shorter bodies; increased body, fat, and lean masses; higher BMR and [Formula: see text]sum, and generally greater morphometric measures and organ masses than virgin males at 22 °C. Among the groups housed at 10 °C, breeding males had higher BMR and lower [Formula: see text]max than non-breeding and/or virgin males. Overall, we found that effects of fatherhood during cold acclimation were inconsistent, and that several aspects of cold acclimation differ substantially between California mice and other small mammals.

Polyandrous bee provides extended offspring care biparentally as an alternative to monandry based eusociality.

Parental care behavior evolves to increase the survival of offspring. When offspring care becomes complicated for ecological reasons, cooperation of multiple individuals can be beneficial. There are two types of cooperative care: biparental care and worker (helper)-based care (e.g., eusociality). Although biparental care is common in several groups of vertebrates, it is generally rare in arthropods. Conversely, eusociality is widespread in insects, especially the aculeate Hymenoptera. Here, we present a case of biparental care in bees, in Ceratina nigrolabiata (Apidae, Xylocopinae). Similar to eusocial behavior, biparental care leads to greater brood protection in this species. Male guarding increases provisioning of nests because females are liberated from the tradeoff between provisioning and nest protection. The main benefit of parental care for males should be increased paternity. Interestingly though, we found that paternity of offspring by guard males is extraordinarily low (10% of offspring). Generally, we found that nests were not guarded by the same male for the whole provisioning season, meaning that males arrive to nests as stepfathers. However, we show that long-term guarding performed by a single male does increase paternity. We suggest that the multiple-mating strategy of these bees increased the amount of time for interactions between the sexes, and this longer period of potential interaction supported the origin of biparental care. Eusociality based on monandry was thought to be the main type of extended brood protection in bees. We show that biparental care based on polyandry provides an interesting evolutionary alternative.

Factors that influence the onset of parental care in zebra finches: Roles for egg stimuli and prolactin.

Parental care is a critical component for determining reproductive success both for a current set of offspring but also over the lifetime of the individual. The hormone prolactin has often been implicated as a parental care hormone across taxa but causal relationships have only been strongly demonstrated in mammals and in a few select species of birds. For instance, in mammals, maternal care towards foster pups can be induced by exogenous treatment with prolactin, in concert with other reproductive hormones involved in pregnancy. We aimed to address this causal mechanism in birds by artificially elevating prolactin during the nest building and egg laying stages using vasoactive intestinal peptide (VIP) and then exposing them to foster chicks. We predicted that increasing prolactin would increase brooding and feeding behaviors towards foster chicks compared to the saline control group. Parental behavior towards foster chicks was only shown by individuals who had initiated clutches regardless of treatment. VIP treatment had no effect on parental behavior; however, a positive relationship was found between male and female feeding rates in the VIP but not control group. Our results suggest that both eggs and chicks are sufficient to stimulate foster care, perhaps through endogenous prolactin signalling, while further elevations of prolactin may serve to synchronize parental behaviors between pairs.

Longitudinal Trajectories and Inter-parental Dynamics of Prairie Vole Biparental Care.

For altricial mammalian species, early life social bonds are constructed principally between offspring and their mothers, and the mother-offspring relationship sets the trajectory for offspring bio-behavioral development. In the rare subset of monogamous and biparental species, offspring experience an expanded social network which includes a father. Accordingly, in biparental species fathers also have the potential to influence trajectories of offspring development. Previous semi-natural and laboratory study of one monogamous and biparental species, the prairie vole (Microtus ochrogaster), has given insight into the role that mothers and fathers play in shaping behavioral phenotypes of offspring. Of particular interest is the influence of biparental care in the development of monogamous behavior in offspring. Here, we first briefly review that influence. We then present novel research which describes how parental investment in prairie voles changes across sequential litters of pups, and the extent to which it is coordinated between mothers and fathers. We use approximately 6 years of archival data on prairie vole parenting to investigate trajectories and inter-parent dynamics in prairie vole parenting. We use a series of latent growth models to assess the stability of parental investment across the first 4 l. Our findings suggest that prairie voles display sexually dimorphic patterns of change in parental behavior: mothers' investment declines linearly whereas fathers' pattern of change is characterized by initial decline between litters 1 and 2 with subsequent increase from litters 2 to 4. Our findings also support a conclusion that prairie vole paternal care may be better characterized as compensatory-that is, fathers may compensate for decline in maternal investment. Opposing trends in investment between mothers and fathers ultimately imply stability in offspring investment across sequential litters. These findings, combined with previous studies, generate a hypothesis that paternal compensation could play an important role in maintaining the development of monogamous behavioral phenotypes in individual offspring and across cohorts of those offspring. Understanding longitudinal and inter-individual dynamics of complex social behaviors is critical for the informed investigation of both proximate and ultimate mechanisms that may subserve these behaviors.

The role of intragroup agonism in parent-offspring relationships and natal dispersal in monogamous owl monkeys (Aotus azarae) of Argentina.

Agonistic behaviors are common in many group-living taxa and may serve a variety of functions, ranging from regulating conflicts over reproduction to defending food resources. However, high rates of agonism are not expected to occur among close relatives or individuals in established mating relationships, which are characteristics of monogamous groups. To contribute to our understanding of agonism within socially monogamous groups, we collected behavioral and demographic data from Azara's owl monkeys (Aotus azarae) in the Gran Chaco of Argentina over 14 years. We examined factors related to age, sex, kinship, and behavioral context to evaluate predictions of the hypotheses that agonism functions to regulate dispersal and that it mediates competition for food and/or mates. Intragroup agonism was relatively rare: the group rate was approximately one event every three and a half hours. Rates of agonism were generally similar for both sexes, but there were marked differences among age categories. Agonism performed by adults was more frequently directed at subadults than at younger offspring. In contrast, agonistic interactions involving infants were very rare. Among interactions between adults and subadults, adults were much more frequently the actors than the recipients, suggesting that agonism from adults may influence natal dispersal of subadults. Agonistic events were most frequent during foraging, but also occurred more frequently than expected during bouts of social behavior. Overall, our results suggest that agonism in owl monkeys serves as a mechanism for regulating dispersal, and also likely plays a role in mediating mating and feeding competition.

Searching for hormonal facilitators: Are vasotocin and mesotocin involved in parental care behaviors in poison frogs?

Although the involvement of peptide hormones in parental care behaviors is well investigated in vertebrates, in amphibians the physiological basis of parental care is largely unknown. This is all the more surprising as parental care behaviors in these tetrapods are remarkably diverse. The poison frog Ranitomeya imitator performs biparental care, including clutch guarding, tadpole transportation and nutrient provisioning. Here we tested whether the nonapeptides arginine-vasotocin (AVT) and mesotocin (MT) are involved in clutch guarding and tadpole transportation in these frogs. In ex-sito experiments we injected males and females after clutch deposition and before tadpole transport with AVT and MT, respectively, as well as their antagonist or a control. We measured two types of egg caring behavior (intense and general care) and compared the success rate of tadpole transportation after treatments. Surprisingly we found that AVT did not trigger, but decreased intense egg care behaviors in males and females. However, there was a trend for general care behavior to increase, which might explain the adverse effect regarding intense care. MT did not have an effect on egg caring behaviors, but after administration of this hormone males were less likely to transport their offspring later on. Our results indicate that AVT might be partly involved in egg caring behaviors in R. imitator, while MT does not appear to play any role in behaviors prior to tadpole transportation in males. This implies that other hormones, such as steroids or prolactin are likely to be important for early parental care behaviors in poison frogs.

Biparental care is predominant and beneficial to parents in the burying beetle Nicrophorus orbicollis (Coleoptera: Silphidae).

Parenting strategies can be flexible within a species, and may have varying fitness effects. Understanding this flexibility and its fitness consequences is important for understanding why parenting strategies evolve. Here, we investigate the fitness consequences of flexible parenting in the burying beetle Nicrophorus orbicollis, a species known for its advanced provisioning behaviour of regurgitated vertebrate carrion to offspring by both sexes. We show that even when a parent is freely allowed to abandon the carcass at any point in time, biparental post-hatching care is the most common pattern of care adopted in N. orbicollis. Furthermore, two parents together raised more offspring than single parents of either sex, showing that the presence of the male can directly influences parental fitness even in the absence of competitors. This contrasts with studies in other species of burying beetle, where biparental families do not differ in offspring number. This may explain why biparental care is more common in N. orbicollis than in other burying beetles. We suggest how fitness benefits of two parents may play a role in the evolution and maintenance of flexible biparental care in N. orbicollis.

Paternal care and litter size coevolution in mammals.

Biparental care of offspring occurs in diverse mammalian genera and is particularly common among species with socially monogamous mating systems. Despite numerous well-documented examples, however, the evolutionary causes and consequences of paternal care in mammals are not well understood. Here, we investigate the evolution of paternal care in relation to offspring production. Using comparative analyses to test for evidence of evolutionary associations between male care and life-history traits, we explore if biparental care is likely to have evolved because of the importance of male care to offspring survival, or if evolutionary increases in offspring production are likely to result from the evolution of biparental care. Overall, we find no evidence that paternal care has evolved in response to benefits of supporting females to rear particularly costly large offspring or litters. Rather, our findings suggest that increases in offspring production are more likely to follow the evolution of paternal care, specifically where males contribute depreciable investment such as provisioning young. Through coevolution with litter size, we conclude that paternal care in mammals is likely to play an important role in stabilizing monogamous mating systems and could ultimately promote the evolution of complex social behaviours.

Age and sex-specific mortality of wild and captive populations of a monogamous pair-bonded primate (Aotus azarae).

In polygynous primates, a greater reproductive variance in males have been linked to their reduced life expectancy relative to females. The mortality patterns of monogamous pair-bonded primates, however, are less clear. We analyzed the sex differences in mortality within wild (NMales = 70, NFemales = 73) and captive (NMales = 25, NFemales = 29) populations of Azara's owl monkeys (Aotus azarae), a socially and genetically monogamous primate exhibiting biparental care. We used Bayesian Survival Trajectory Analysis (BaSTA) to test age-dependent models of mortality. The wild and captive populations were best fit by the logistic and Gompertz models, respectively, implying greater heterogeneity in the wild environment likely due to harsher conditions. We found that age patterns of mortality were similar between the sexes in both populations. We calculated life expectancy and disparity, the latter a measure of the steepness of senescence, for both sexes in each population. Males and females had similar life expectancies in both populations; the wild population overall having a shorter life expectancy than the captive one. Furthermore, captive females had a reduced life disparity relative to captive males and to both sexes in the wild. We interpret this pattern in light of the hazards associated with reproduction. In captivity, where reproduction is intensely managed, the risks associated with gestation and birth are tempered so that there is a reduction in the likelihood of captive females dying prematurely, decreasing their overall life disparity.

Direct benefits of mate choice: a meta-analysis of plumage colour and offspring feeding rates in birds.

Mate choice is generally costly to the choosy sex, so fitness benefits must counterbalance these costs. Genetic benefits of choice are widely examined and have received overall support. Direct benefits such as high quality parental care by highly ornamented individuals are widely assumed to be important but are less frequently tested, theoretically debated, and their support in the recent literature is unknown. Furthermore, in taxa where both sexes provide care, the preferential investment of the partner in relation to ornamentation may reduce own investment and modify apparent parental care quality. In a phylogenetically controlled meta-analysis, we collated correlative results from birds concerning parental plumage coloration and the nestling feeding rates of the ornament bearer and its partner. Overall evidence was weak for signalling of parental care quality and somewhat stronger for preferential partner investment. Surprisingly, the sex of the signaller and the type of plumage colour seemed to exert weak effects on the signalling of parental care quality. Finally, there was a group of cases with opposite relationships of care and ornamentation in the two parties. We found that this group arose predominately from preferential partner investment in relation to ornamentation, with concomitant, but weaker, reduction of own investment. We conclude that the effect of partner investment on parental care indication seems system-specific and needs further study.