Corticosterone predicts foraging behavior and parental care in macaroni penguins

Corticosterone has received considerable attention as the principal hormonal mediator of allostasis or physiological stress in wild animals. More recently, it has also been implicated in the regulation of parental care in breeding birds, particularly with respect to individual variation in foraging behavior and provisioning effort. There is also evidence that prolactin can work either inversely or additively with corticosterone to achieve this. Here we test the hypothesis that endogenous corticosterone plays a key physiological role in the control of foraging behavior and parental care, using a combination of exogenous corticosterone treatment, time-depth telemetry, and physiological sampling of female macaroni penguins (Eudyptes chrysolophus) during the brood-guard period of chick rearing, while simultaneously monitoring patterns of prolactin secretion. Plasma corticosterone levels were significantly higher in females given exogenous implants relative to those receiving sham implants. Increased corticosterone levels were associated with significantly higher levels of foraging and diving activity and greater mass gain in implanted females. Elevated plasma corticosterone was also associated with an apparent fitness benefit in the form of increased chick mass. Plasma prolactin levels did not correlate with corticosterone levels at any time, nor was prolactin correlated with any measure of foraging behavior or parental care. Our results provide support for the corticosterone-adaptation hypothesis, which predicts that higher corticosterone levels support increased foraging activity and parental effort.     

Evolution of parental care driven by mutual reinforcement of parental food provisioning and sibling competition

In mammals, altricial birds and some invertebrates, parents care for their offspring by providing them with food and protection until independence. Although parental food provisioning is often essential for offspring survival and growth, very little is known about the conditions favouring the evolutionary innovation of this key component of care. Here, we develop a mathematical model for the evolution of parental food provisioning. We find that this evolutionary innovation is favoured when the efficiency of parental food provisioning is high relative to the efficiency of offspring self-feeding and/or parental guarding. We also explore the coevolution between food provisioning and other components of parental care, as well as offspring behaviour. We find that the evolution of food provisioning prompts evolutionary changes in other components of care by allowing parents to choose safer nest sites, and that it promotes the evolution of sibling competition, which in turn further drives the evolution of parental food provisioning. This mutual reinforcement of parental care and sibling competition suggests that evolution of parental food provisioning should show a unidirectional trend from no parental food provisioning to full parental food provisioning.     

Transmission of parental care behavior in African striped mice, Rhabdomys Pumilio

The expression of behavior, including parental care behavior, is influenced by complex interactions of the genes of an organism and the prevailing environmental conditions. Previously, we showed that the development of paternal, but not maternal, care in the African striped mouse, Rhabdomys pumilio, has a significant nongenetic maternal component. Here, we investigate the genetic component of parental care behavior from parents to offspring. We first measured the duration of parental care behavior of mothers and fathers every second day for 11 days postnatally. Subsequently, one son and one daughter from each of these litters were paired with unrelated mates when they were adults and their parental care behavior scored. Using regression models, we then compared parental care behavior of parents and their adult offspring. The transmission of parental care behavior from striped mouse fathers to sons and from mothers to both sons and daughters did not indicate a genetic component. Instead, we found a patrilineal genetic component for parental care in daughters. The reason for this unusual pattern of inheritance is not known, but this finding complements that of our other studies, showing that the expression of maternal care behavior in adult daughters is also not nongenetically influenced by their mothers. We suggest that, although females are constrained to provide maternal care in different social contexts, maternal care behavior may be influenced genetically by the father.     

Evolution of male parental care and female multiple mating: game-theoretical and two-locus diploid models

Males gain a fitness benefit by mating with many females, whereas the number of progeny per female does not increase as a function of additional mates. Furthermore, males run the risk of investing in the offspring of other males if they provide parental care. Nevertheless, in various species, males provide parental care, and females mate with multiple males. We investigate a game-theoretical model in which females gain a direct benefit by multiple mating from the paternal care they elicit for their offspring. The parameters that directly favor male parental care, such as small cost of paternal care, have indirect positive effects on the evolution of female multiple mating, while they have negative effects in the opposite case. Both traits are more likely to evolve when the number of matings is smaller. The individual-based model of a diploid two-locus, two-allelic genetic model confirms the result.     

Evolution of parental care in dart poison frogs (Amphibia: Anura: Dendrobatidae)

Dendrobatid frogs perform a unique mode of parental care, ranging from egg attendance and tadpole transport to tadpole feeding. It is hypothesized that a behaviour in which the egg attending parent remains with the cluch is the most primitive condition. In more advanced forms or parental care, the male is able to attend several clutches of eggs. Tadpole attendance and feeding, finally, started as deceit; the male induced the female to lay eggs into a bromeliad leaf axil already occupied by a larva. Costs and benefits of the different modes of parental care and possible alternative reproductive tactics are discussed.     

Evolution of egg dummies in Tanganyikan cichlid fishes: the roles of parental care and sexual selection

Sexual selection has been suggested to be an important driver of speciation in cichlid fishes of the Great Lakes of Africa, and the presence of male egg dummies is proposed to have played a key role. Here, we investigate how mouthbrooding and egg dummies have evolved in Tanganyikan cichlids, the lineage which seeded the other African radiations, with a special emphasis on the egg dummies. Using modern phylogenetic comparative analyses and a phylogeny including 86% of the 200 described species, we provide formal evidence demonstrating correlated evolution between mouthbrooding and egg dummies in Tanganyikan cichlids. These results concur with existing evidence, suggesting that egg dummies have evolved through sensory exploitation. We also demonstrate that there is a strong evolutionary correlation between the presence of egg dummies and both pre‐ and post‐copulatory sexual selection. Moreover, egg dummy evolution was contingent on the intensity of pre‐ and post‐copulatory sexual selection in Tanganyikan cichlids. In sum, our results provide evidence supporting the hypothesis of egg dummies evolving through sensory exploitation and highlight the role of sexual selection in favouring the evolution and maintenance of this trait.     

Olfaction and parental behavior in ring dove

In the ring dove, several sensory cues emanating from the squab (young) have been shown to be important in maintaining parental care. However, no information exists on the role of olfaction in parental behavior. In the experiments described, the body odor of squabs was artificially altered by application of a fruit-scented substance to its back. This resulted in high mortality of treated squabs by day 7 post-hatching. The body weights of the fruit-scented squabs that died were lower than those of living controls, suggesting that some change in parental feeding had occurred. Behavioral observations also indicated qualitative differences in parental care towards fruit-scented vs control young. Toxicity was ruled out as a cause of squab death since subcutaneous injection of the fruit substance to squabs led to 100% squab survival. High squab mortality following fruit-scent treatment could be prevented by bilateral olfactory nerve cuts in the parents. Taken together, these data suggest that olfactory cues may play a role in parental care in ring doves, and add support to the notion that olfactory cues can influence avian behavior.     

Evolution of parental care in Phodopus: Conflict between adaptations for survival and adaptations for rapid reproduction

SYNOPSIS. Two species of dwarf hamsters are used to developa model of the proximate and ultimate selective forces leadingto the evolution of parental care strategies. One species, Phodopuscampbelli, has been studied extensively as a socially monogamous,biparental species; the other, P. sungorus, rears its youngwithoutmale assistance. The cold, arid habitat occupied by both species has selectedfor shape, insulation, and physiology that provide toleranceof extremely cold ambient temperatures and enhance survivalwhen water availability is limited. At the same time, the smallbody size and highly seasonal environment have selected forrapid maturation and the most compressed reproductive cycleknown in a mammal. Rapid reproduction increases water demandsfor milk production and further stresses water balance becausematernal hyperthermia demands increased evaporative heat loss.Thus, in Phodopus habitat, rapid reproduction requires heattolerance and water availability, which conflict with adaptationsfor survival. In the habitat of P. sungorus, predictable rains allow a breedingseason and females rear litters alone. In P. campbelli, wateravailability is insufficient for solitary reproduction. Instead,male presence alleviates thermoregulatory, and thus water balance,stresses on the female. The result is improved pup survivaland growth. Therefore, an ‘ultimate’ reason forbiparental care in P. campbelli is its harsh environment, anda ‘proximate’ reason is a need to reduce maternalwater demand. Results confirm that independent physiologicalconstraints, in addition to constraints on energy or time investment,can be essential selective pressures in the evolution of mammaliansocial organization and behavior.     

Multiple patterns of parental care

Many animals show multiple patterns of parental care, where more than one of the four basic patterns (biparental care, uniparental care by males or females, or no care) is present within a single population during a single breeding season. We consider three reasons for the existence of multiple patterns of parental care: (1) mixed-strategy behaviours; (2) time-dependent behaviour with parents changing their care decision during the breeding season; and (3) quality differences between individuals leading to different care decisions being made depending on the qualities of both parents. The basic framework we use to investigate these is a two-stage game-theoretical model, and we highlight the importance of including feedback between the parental care decisions made by population members and the probability that a deserting individual will find a new mate. Including this feedback may introduce a nonlinear dependence of the fitness payoffs on the frequencies with which the pure strategies ('care' and 'desert') are played by each of the sexes. This can have important consequences for the existence of evolutionarily stable strategies (ESSs). For example, mixed-strategy ESSs may exist (an outcome forbidden if the feedback is not included) and, in one model, the feedback also prevents uniparental care by either sex from being evolutionarily stable. We also point out that decisions made by animals without dependent offspring can have important consequences for observed parental care behaviour. Copyright 1999 The Association for the Study of Animal Behaviour.     

Parentage and the evolution of parental behavior

Parentage is the proportion of juveniles in a brood that areoffspring of potential care givers. We analyzed how reductionsin parentage affect the evolution of parental behavior usinga static optimization model. The main benefit of parental effortwas an increase in the survival of offspring, and the main costswere reduced opportunities to seek additional matings or toparasitize neighbors and or reduced survival. Both the costsand benefits included terms for relatedness to young. The effectof parentage depended on (1) whether parents responded in ecologicaltime (facultative response) or in evolutionary time (nonfacultativeresponse), (2) whether the cues enabling assessment of parentagepermitted discrimination among offspring, and (3) whether parentagewas the same among different groups of juveniles (unrestricted)or varied between them (restricted). When parents did not knowtheir own parentage and mean parentage was the same for allmatings, reduced parentage affected the costs and benefits equally,so, as in several previous models, there was no effect on theoptimal level of parental effort. Parentage did affect optimalparental effort when mean parentage to the present brood differedfrom that to young from alternative or future matings. Loweredparentage reduced optimal parental effort when the cost of parentingwas missed opportunities for extrapair copulations or broodparasitism or when parentage was consistently higher in alternativeor future matings. Nonlinear changes in parentage with age gavecomplex trajectories of parental care, with individuals of differentages having similar parentage but exhibiting different levelsof parental effort. Correlations between parentage and othervariables in the model (such as opportunities for additionalmatings) sometimes masked, but never eliminated, the effectsof parentage. When parents could discriminate their own youngin a brood, overall parental effort was reduced, but nepotismwas increased. When parents could not discriminate their ownoffspring but had general cues about average parentage to thebrood, effects varied depending on the costs and benefits ofparental behavior. When parental behavior was costly to caregivers, parentage had more effect than when parenting was notcostly. Likewise, parentage had less effect when care greatlyincreased offspring survival than when care was less necessary.Our analyses reconcile conflicting results from previous modelsand suggest a general framework for analyzing parental behaviorwithin populations and among higher taxonomic groups.     

The evolution of parental care

Our understanding of parental care behavior can be significantly advanced through the application of Williams's Principle, which states that reproduction has not only a benefit but also a cost to lifetime fitness. My laboratory has formalized Williams's Principle into the relative value theorem and found that its application to fishes, the taxa with the most diverse patterns of parental care, can help to explain which sex provides care and how much. In fishes, it is often the male that provides parental care, not because the male obtains greater benefits from this care, but probably because he pays fewer costs. Fish dynamically adjust their investment into parental care according to the number of offspring in their brood, past investment, genetic relatedness, and alternative mating opportunities, all of which affect the value of current offspring relative to potential future offspring. These results may also help us understand the joy and the challenges of parental care in humans.     

Reproductive behavior of Helmeted Guinea Fowl (Numida meleagris): Mating system and parental care

Social behavior of free-ranging domestic Helmeted Guinea Fowl was studied in Spring Mills, Pennsylvania, and Nantucket, U.S.A., and in a flock of wild Helmeted Guinea Fowl near Kimberley, South Africa. The general pattern of mating behavior was for males to first associate sequentially with one to several females. After 4–6 weeks of short-term associations, one male and one female typically paired and remained in close association throughout the breeding season. Males courtship-fed their mates and guarded them during egg laying and incubation. Females incubated alone. Both parents brooded the young during the first 12 days after hatching.     

鱼类亲代抚育行为的研究进展

亲代抚育行为（parental care behavior）是指动物对其后代或其亲缘后代提供保护和养育的所有活动,属于本能行为的一种,广泛存在于动物界之中。鱼类在其为数不多的科中充分发展了几乎所有类型的亲代抚育行为,因而成为研究该行为的最佳物种之一。随着威廉斯原理（Williams’s Principle）的提出和应用,人们对鱼类亲代抚育行为的探索逐步由定性向定量发展,普遍认同了在鱼类进化中,雄性抚育模式得以占据支配地位的缘由并非是因为雄性在抚育活动中获得了较多的利益,而是由于在获取相同利益时雄性损失的未来投资成本较雌性低的观点。近年来的研究证实,在亲代抚育过程中存在着某种动态调整机制,其中四个比较关键的影响因素分别为：亲本所抚育的子代数量、亲本先前的投资、亲本与被抚育子代间的遗传关联度和亲本未来的交配机会。     

The phylogeny of parental care in fishes

This paper tests the hypothesis that in the evolution of parental care, taxa of bony fish should only exhibit certain transitional states (where a transition is defined by the occurrence of at least two types of parental care within a genus or family). These are those between no parental care and male care, male care and biparental care, biparental care and female care, and female care and no parental care. A review of the teleost literature reveals 21 transitions. All of these agree with the hypothesized transitions and, in some cases, the direction of evolution is inferred by simple pedigree analysis.     

Costs and benefits of parental care in eastern kingbirds

We manipulated brood sizes of eastern kingbirds (Tyrannus tyrannus)to measure the costs and benefits of parental care and to testwhether kingbirds showed evidence of individual optimizationof reproductive effort. We found that the number of feedingtrips (trips/h) increased and that per capita feeding rates(trips/nestling/h) declined as brood size increased. The declinein per capita feeding rates was mostly due to high feeding rateto broods of one: parents made roughly equal number of tripsto feed each nestling in broods of two to five. Nonetheless,nestling mass declined with brood size, probably because largebroods were fed more small prey. Nestling condition (mass adjustedfor structural size) differed only between broods of one andfive. After controlling for effects of brood size, feeding rateshad no supplementary influence on either nestling size or condition,but productivity and feeding rate were positively and significantlyrelated. Adult male condition did not vary with brood size,manipulated brood size, or total feeding rate, but declinedas the pair's per capita feeding rates increased. In addition,males that returned to breed were in better condition beforeleaving for migration than those that failed to return. Femalecondition tended to decline, and the probability of returningto breed dropped when broods were enlarged. However, femalecondition was independent of the probability of returning. Ourresults show that high feeding rates were costly, but that theycarried benefits (greater productivity). Some evidence for individualoptimization of reproductive effort existed: variability innestling and adult female condition were better explained bychanges in brood size than by the actual number of young inthe nest. However, most evidence supported the alternative thatincreased brood size was equally costly for all birds     

The effect of paid parental leave on breastfeeding,parental health and behavior

Little is known about the effects of paid parental leave (in particular fathers’ quotas) on parental health and involvement. In this paper, we exploit a reform that took place in the Canadian province of Quebec to address that important topic. In 2006, Quebec opted out of the federal plan and established its own parental insurance plan, named the Quebec Parental Insurance Plan (QPIP). This program has lowered the eligibility criteria, increased income replacement and introduced fathers’ quotas. Using three data sets, we investigate the impact of the QPIP on breastfeeding and parental health and behavior. Our results show that the reform increased breastfeeding duration. The results also suggest that the policy had limited positive effects on parental health and parenting practices.     

Hormonal correlates of parental behavior in male rats

Groups of seven intact male Long-Evans hooded rats were housed with pups for 1, 7, 14, or 22 days and their parental behavior was recorded each day. All but one male showed parental behavior. Twenty-eight control males were housed without pups. At the end of each observation period the males were decapitated and their trunk blood was collected for hormone analysis by radioimmunoassay. Males with pups had lower prolactin levels than control males on all 4 days but did not differ in leutinizing hormone, follicle-stimulating hormone, or testosterone levels from males without pups. Both prolactin and testosterone levels were correlated positively with the frequency of parental behavior, suggesting that the males which are behaviorally the most responsive to infants are also hormonally the most responsive.     

Innovative parental care in a myrmecophageous mammal

Male bat-eared foxes, Otocyon megalotis, are known to contribute extensively to parental care. Yet, the exact roles that males and females play in raising offspring remain relatively unexplored. Here, we describe interactions between adult foxes and their presumed offspring based on a pilot study on three family groups of a wild population in South Africa. We report the first recorded instance of dung provisioning observed in canids. A male bat-eared fox provided dung to his offspring during a foraging trip, presumably to give them access to the ensconced insects. Further, this male provisioned the young foxes with large, live insects. Similar to other researchers, we never observed provisioning by females, but the females in this population did interact socially with their young in addition to suckling. We emphasize the importance of anecdotal reports of novel behavioural responses in wild canids, as an accumulation of such evidence may reveal patterns of innovative behaviour presently unrecognized in this family.     

The evolution of avian parental care

A stage model traces key behavioural tactics and life-history traits that are involved in the transition from promiscuity with no parental care, the mating system that typifies reptiles, to that typical of most birds, social monogamy with biparental care. In stage I, females assumed increasing parental investment in precocial young, female choice of mates increased, female-biased mating dispersal evolved and population sex ratios became male biased. In stage II, consortships between mating partners allowed males to attract rare social mates, provided a mechanism for paternity assessment and increased female ability to assess mate quality. In stage III, relative female scarcity enabled females to demand parental investment contributions from males having some paternity certainty. This innovation was facilitated by the nature of avian parental care; i.e. most care-giving activities can be adopted in small units. Moreover, the initial cost of care giving to males was small compared with its benefit to females. Males, however, tended to decline to assume non-partitionable, risky, or relatively costly parental activities. In stage IV, altriciality coevolved with increasing biparental care, resulting in social monogamy. Approaches for testing behavioural hypotheses are suggested.