Paternal care effects outweigh gamete-mediated and personal environment effects during the transgenerational estimation of risk in fathead minnows

Background Individuals can estimate risk by integrating prenatal with postnatal and personal information, but the relative importance of different information sources during the transgenerational response is unclear. The estimated level of risk can be tested using the cognitive rule of risk allocation, which postulates that under consistent high-risk, antipredator efforts should decrease so that individual metabolic requirements can be satisfied. Here we conduct a comprehensive study on transgenerational risk transmission by testing whether risk allocation occurs across 12 treatments that consist of different maternal, paternal, parental care (including cross-fostering) and offspring risk environment combinations in the fathead minnow Pimephales promelas, a small cyprinid fish with alloparental care. In each risk environment, we manipulated perceived risk by continuously exposing individuals from birth onwards to conspecific alarm cues or a control water treatment. Using 2810 1-month old individuals, we then estimated shoaling behaviour prior to and subsequent to a novel mechanical predator disturbance. Results Overall, shoals estimating risk to be high were denser during the prestimulus period, and, following the risk allocation hypothesis, resumed normal shoaling densities faster following the disturbance. Treatments involving parental care consistently induced densest shoals and greatest levels of risk allocation. Although prenatal risk environments did not relate to paternal care intensity, greater care intensity induced more risk allocation when parents provided care for their own offspring as opposed to those that cross-fostered fry. In the absence of care, parental effects on shoaling density were relatively weak and personal environments modulated risk allocation only when parental risk was low. Conclusions Our study highlights the high relative importance of parental care as opposed to other information sources, and its function as a mechanism underlying transgenerational risk transmission.

Association of social group with both life-history traits and brain size in cooperatively breeding birds

Social group is associated with life-history traits and can predict brain size variation in cooperative primates and some other mammal groups, but such explicit relationships remain enigmatic in cooperatively breeding birds. Indeed, some compositions of social group in cooperative species (e.g., helper number and group size) would affect the fitness of breeders by providing alloparental care. Here, we conducted comparative tests of the relationship between the social group and both life-history traits and brain size across 197 species of cooperatively breeding birds using phylogenetically controlled comparative analyses. We did not find any correlations between helper numbers and both life-history traits and brain size. However, we found that maximum group size was positively associated with clutch size. Moreover, average group size has positive associations with body mass and relative brain size. Our findings suggest that helper numbers cannot promote variation in relative brain size, while larger groups may predict bigger brains in cooperatively breeding birds.

Developmental environment shapes honeybee worker response to virus infection

The consequences of early-life experiences are far reaching. In particular, the social and nutritional environments that developing animals experience can shape their adult phenotypes. In honeybees, larval nutrition determines the eventual social roles of adults as reproductive queens or sterile workers. However, little is known about the effects of developmental nutrition on important adult worker phenotypes such as disease resilience. In this study, we manipulated worker developmental nutrition in two distinct ways under semi-natural field conditions. In the first experiment, we restricted access to nutrition via social isolation by temporarily preventing alloparental care. In the second experiment, we altered the diet quality experienced by the entire colony, leading to adult bees that had developed entirely in a nutritionally restricted environment. When bees from these two experiments reached the adult stage, we challenged them with a common bee virus, Israeli acute paralysis virus (IAPV) and compared mortality, body condition, and the expression of immune genes across diet and viral inoculation treatments. Our findings show that both forms of early life nutritional stress, whether induced by lack of alloparental care or diet quality restriction, significantly reduced bees’ resilience to virus infection and affected the expression of several key genes related to immune function. These results extend our understanding of how early life nutritional environment can affect phenotypes relevant to health and highlight the importance of considering how nutritional stress can be profound even when filtered through a social group. These results also provide important insights into how nutritional stress can affect honeybee health on a longer time scale and its potential to interact with other forms of stress (i.e. disease).

Habitat Quality Determines Dispersal Decisions and Fitness in a Beetle – Fungus Mutualism

Delayed dispersal of sexually mature offspring is a fundamental component of cooperative breeding. In ambrosia beetles, female offspring temporarily remain in their natal nest and refrain from reproduction, instead investing in alloparental care. Previous work has demonstrated a link between helping behaviour and the increased need for pathogen defence, arising from their close association with fungal cultivars. In the ambrosia beetle Xyleborinus saxesenii, mature female offspring can effectively fight pathogen infections and manage the microbial composition within the nest by adjusting the frequency of different hygienic and nest maintenance behaviours. This suggests a potential to respond flexibly to the ecology of their nest, which calls for a better understanding of the connection between behaviour and the microbial community thriving within their nests. Here, we studied the significance of the mutualistic fungus garden composition for the beetles’ nest ecology and fitness by experimentally varying substrate quality. We found that the vertically transmitted ambrosia fungus garden is composed of at least two fungus mutualist species and a wide variety of other microbes varying in their relative abundance. This is strongly affected by the moisture content of the substrate, which in nature depends on the age and type of wood. We found that the mutualist fungi complement each other in terms of dryness-resistance, allowing the beetles to utilise a broad range of substrates over prolonged time during which the wood gradually desiccates. Under suboptimal humidity conditions, the interaction between host and multiple fungus species has important ramifications for the behaviour of philopatric helpers, including their alloparental investment, sibling cannibalism and the timing of dispersal. Rearing five generations of beetles consecutively in dry substrate resulted in transgenerational effects on philopatry and alloparental care, probably mediated through the dominance of a particular fungus species that was driven by the experimental habitat condition. Interestingly, the nests of these selection lines produced much more offspring after five generations than any first-generation nest, which may have reflected increased egg laying by non-dispersing daughters. Our study highlights the importance of considering the interactions between the microbial community and their insect hosts for understanding social evolution in cooperatively breeding beetles.

Care-giver identity impacts offspring development and performance in an annually social bumble bee

Background The developmental fates of offspring have the potential to be influenced by the identity of their care-givers and by the nature of the care that they receive. In animals that exhibit both parental and alloparental care, such as the annually eusocial insects, the influence of care-giver identity can be directly assessed to yield mechanistic and evolutionary insights into the origins and elaboration of brood care. Here, we performed a comparative investigation of maternal and worker brood care in bumble bees, a pollinator group where mothers (queens) rear the first offspring in the nest, and then daughters (workers) assume this role upon their emergence. Specifically, we compared the effects of queen and worker brood care on offspring development and also offspring performance, for a set of traits related to sensory biology, learning, and stress resistance. Results We found that queen-reared workers were smaller-bodied than worker-reared offspring, suggesting that bumble bee queens influence body size determination in their offspring. We also found that queen-reared workers were more resistant to starvation, which might be beneficial for early nesting success. These maternal influences could not be explained by feeding rate, given that we detected a similar offspring feeding frequency in both queens and workers. Conclusion Bumble bee queens have a unique influence on the development of the first offspring in the nest, which they rear, relative to worker-reared workers. We propose that bumble bee brood care has been shaped by a suite of evolutionary and ecological factors, which might include a maternal influence on traits that promote survival of incipient colonies.

Non-kin adoption in the common vampire bat

Individual animals across many different species occasionally ‘adopt’ unrelated, orphaned offspring. Although adoption may be best explained as a by-product of adaptive traits that enhance parental care or promote the development of parental skills, one factor that is possibly important for the likelihood of adoption is the history of cooperative interactions between the mother, adopted offspring and adopter. Using 652 h of behavioural samples collected over four months, we describe patterns of allogrooming and food sharing before and after an instance of non-kin adoption between two adult female common vampire bats ( Desmodus rotundus ) that were captured from distant sites (340 km apart) and introduced to one another in captivity. The first female died from an illness 19 days after giving birth. The second female groomed and regurgitated food to the mother more often than any other group member, then groomed, nursed and regurgitated food to the orphaned, female pup. The substantial increase in alloparental care by this female after the mother's death was not observed among the 20 other adult females that were present in the colony. Our findings corroborate previous reports of non-kin adoption in common vampire bats and are consistent with the hypothesis that non-kin adoption can be motivated, in part, by a history of cooperative interactions.

Alloparental care in glassfrogs: males care for unrelated clutches only when associated with their own

Parental care is costly, thus theory predicts that parents should avoid caring for unrelated offspring. However, alloparenting has been reported in many taxa because it may increase the caregiver mating success or offspring survival. We experimentally investigated the existence of allopaternal care in two glassfrog species, Hyalinobatrachium chirripoi and Centrolene peristicta, and discussed possible costs and benefits. Males mated with multiple females and cared for clutches, while continued to call. In the field, we randomly placed unrelated clutches in the territory of males already caring for their clutches and in the territory of non-attending males. Attending males adopted unrelated clutches, whereas non-attending males abandoned their territories. Once males adopted unrelated offspring, they cared for all clutches in a similar frequency and gained new clutches. Alloparenting was context-dependent, as only males already caring for their clutches adopted unrelated ones. We suggest that steroid hormonal levels might mediate the adoption of unrelated offspring by attending males. Additionally, our results suggest that males do not directly discriminate between related and unrelated offspring. Alloparenting has been widely investigated in different vertebrates, except for amphibians. Thus, our study sheds light on the roles of alloparenting for offspring survival and mating success in this group.