Cooperative Breeding Research Articles

Neurodevelopmental timing and socio-cognitive development in a prosocial cooperatively breeding primate (Callithrix jacchus).

Primate brain development is shaped by inputs received during critical periods. These inputs differ between independent and cooperative breeders: In cooperative breeders, infants interact with multiple caregivers. We study how the neurodevelopmental timing of the cooperatively breeding common marmoset maps onto behavioral milestones. To obtain structure-function co-constructions, we combine behavioral, neuroimaging (anatomical and functional), and neural tracing experiments. We find that brain areas critically involved in observing conspecifics interacting (i) develop in clusters, (ii) have prolonged developmental trajectories, (iii) differentiate during the period of negotiations between immatures and multiple caregivers, and (iv) do not share stronger connectivity than with other regions. Overall, developmental timing of social brain areas correlates with social and behavioral milestones in marmosets and, as in humans, extends into adulthood. This rich social input is likely critical for the emergence of their strong socio-cognitive skills. Because humans are cooperative breeders too, these findings have strong implications for the evolution of human social cognition.

Lifetime fitness benefits of breeding site fidelity and low costs of inbreeding permit inbreeding tolerance in an avian cooperative breeder.

Inbreeding, or breeding with close relatives, often decreases individual fitness, but mate choice in many species can increase inbreeding risk. Inbreeding is more likely in species with limited dispersal, such as cooperative breeders where non-parental individuals-often offspring from previous broods-provide parental care and frequently breed close to home. We leverage 32 years of data from a population of Florida Scrub-Jays ( Aphelocoma coerulescens ), an avian cooperative breeder, to investigate whether mate choice, and its lifetime fitness outcomes, affects inbreeding tolerance. We find that both sexes show a stronger preference for geographically closer rather than less related mates. While female-biased dispersal mitigates inbreeding risk when pairing for the first time, limited movement away from the breeding territory by both sexes for later pairings (following mate death or divorce) results in higher relatedness between mates than expected under random mating. Males paired with close relatives and females that move longer distances experience equivalently reduced lifetime reproductive success. Fitness benefits of breeding site fidelity and relatively low fitness costs of inbreeding thus permit inbreeding tolerance in Florida Scrub-Jays. Understanding how and why mate choice contributes to inbreeding is crucial for informed conservation action for endangered species like the Florida Scrub-Jay.

Big data and artificial intelligence-aided crop breeding: Progress and prospects.

The past decade has witnessed rapid developments in gene discovery, biological big data (BBD), artificial intelligence (AI)-aided technologies, and molecular breeding. These advancements are expected to accelerate crop breeding under the pressure of increasing demands for food. Here, we first summarize current breeding methods and discuss the need for new ways to support breeding efforts. Then, we review how to combine BBD and AI technologies for genetic dissection, exploring functional genes, predicting regulatory elements and functional domains, and phenotypic prediction. Finally, we propose the concept of intelligent precision design breeding (IPDB) driven by AI technology and offer ideas about how to implement IPDB. We hope that IPDB will enhance the predictability, efficiency, and cost of crop breeding compared with current technologies. As an example of IPDB, we explore the possibilities offered by CropGPT, which combines biological techniques, bioinformatics, and breeding art from breeders, and presents an open, shareable, and cooperative breeding system. IPDB provides integrated services and communication platforms for biologists, bioinformatics experts, germplasm resource specialists, breeders, dealers, and farmers, and should be well suited for future breeding.

Cooperative and Solitary Mobbing to Defend Offspring in Wild Gray Mouse Lemurs, Microcebus murinus

ABSTRACTGray mouse lemur, Microcebus murinus, mothers either cooperatively breed plurally with kin or breed solitarily. We describe the first observations of cooperative and solitary mobbing to defend offspring by wild cooperative breeding gray mouse lemur mothers in Kirindy Forest, Western Madagascar. We observed four groups of cooperatively breeding mothers and their offspring daily between 18:00 and 04:00 from January 1 to 15, 2023. Cooperative mobbing was observed twice, and solitary mobbing by a single cooperative breeding mother was observed once. There was one Malagasy tree boa, Sanzinia madagascariensis, per mobbing event. Mothers solitarily mobbed by directly approaching within 1 m of the boa, walking and changing distance while within 1 m of the boa. In addition to the solitary mobbing behaviors, cooperatively mobbing mothers approached the boa together from the same or different directions or alternated, and they gathered around the boa. Mothers collaborated in the context of offspring defense from predators and performed different complementary tasks: mobbing while another provided alloparental care by guarding the offspring of the association, that is, babysitting. Mothers performed similar mobbing behaviors and occasionally synchronized in time or coordinate in time and in space to approach from different directions and gather around the boa. Mothers did not come in contact with the boas during mobbing but kept a distance of at least 20 cm. On two mobbing events, the boa rose up with its head facing the mobbing mothers and climbed down the tree after the mobbing. Cooperative mobbing to defend offspring likely evolved by kin selection but reciprocity and an interaction between kin selection and reciprocity cannot be ruled out, since gray mouse lemur mothers cooperatively breed with kin and basically allonurse reciprocally.

Sweet mama: affiliative interactions are related to the reproductive success of dominant female Alpine marmots (Marmota marmota)

AbstractSociality is a complex phenomenon, able to influence multiple traits of an individual life history. In group-living mammals, sociality is likely to play a major role in the reproductive success of individuals. Here we investigate how sociality traits are associated to reproductive success in female Alpine marmots (Marmota marmota), a highly social and cooperative breeding ground squirrel distributed in the European Alps. We used social network analysis to calculate sociality metrics and hurdle generalized linear mixed models (hurdle GLMMs) to model the relationship between sociality metrics and reproductive success of individually tagged female Alpine marmots. Our results showed that centrality of a reproductive female within her social group and the number of social partners are positively related to reproductive success, while agonistic behavior was not related with reproduction. Our results highlight the importance of affiliative interactions with other group members in cooperative breeders, suggesting that in such systems female fitness could be more related to social cohesion than to costs of agonistic behaviors to maintain dominance status.

Life-history and genetic relationships in cooperatively breeding dwarf mongoose groups.

Cooperatively breeding societies show distinct interspecific variations in social and genetic organization. Long-term studies provide invaluable data to further our understanding of the evolution and maintenance of cooperative breeding but have also demonstrated how variation exists within species. Here we integrate life-history, behavioural and genetic data from a long-term study of dwarf mongooses Helogale parvula in South Africa to document mating, breeding, dispersal and relatedness patterns in this population and compare them to those found in a Tanzanian population at the other extreme of the species' range. Our genetic data reveal high levels of reproductive skew, above that expected through observational data. Dispersal was male-biased and was seen more frequently towards the onset of the breeding season, but females also regularly switched between groups. These patterns of breeding and dispersal resulted in a genetically structured population: individuals were more related to groupmates than outsiders, apart from the unrelated dominant pair, ultimately resulting in reduced inbreeding risk. Our results also demonstrate that dwarf mongooses are largely consistent in their social structure across their sub-Saharan distribution. This work demonstrates the direct and indirect pathways to reproductive success for dwarf mongooses and helps to explain the maintenance of cooperative breeding in the species.

Androgen-mediated maternal effects and trade-offs: postnatal hormone development, growth, and survivorship in wild meerkats.

Mammalian reproductive and somatic development is regulated by steroid hormones, growth hormone (GH), and insulin-like growth factor-1 (IGF-1). Based largely on information from humans, model organisms, and domesticated animals, testosterone (T) and the GH/IGF-1 system activate sexually differentiated development, promoting male-biased growth, often at a cost to health and survivorship. To test if augmented prenatal androgen exposure in females produces similar developmental patterns and trade-offs, we examine maternal effects in wild meerkats (Suricata suricatta), a non-model species in which adult females naturally, albeit differentially by status, express exceptionally high androgen concentrations, particularly during pregnancy. In this cooperative breeder, the early growth of daughters predicts future breeding status and reproductive success. We examine effects of normative and experimentally induced variation in maternal androgens on the ontogenetic patterns in offspring reproductive hormones (androstenedione, A4; T; estradiol, E2), IGF-1, growth from pup emergence at 1 month to puberty at 1 year, and survivorship. Specifically, we compare the male and female offspring of dominant control (DC or high-T), subordinate control (SC or lower-T), and dominant treated (DT or blocked-T) dams, the latter having experienced antiandrogen treatment in late gestation. Meerkat offspring showed sex differences in absolute T and IGF-1 concentrations, developmental rates of A4 and E2 expression, and survivorship - effects that were sometimes socially or environmentally modulated. Atypical for mammals were the early male bias in T that disappeared by puberty, the absence of sex differences in A4 and E2, and the female bias in IGF-1. Food availability was linked to steroid concentrations in females and to IGF-1, potentially growth, and survival in both sexes. Maternal treatment significantly affected rates of T, E2, and IGF-1 expression, and weight, with marginal effects on survivorship; offspring of DT dams showed peak IGF-1 concentrations and the best survivorship. Maternal effects thus impact offspring development in meerkats, with associated trade-offs: Whereas prenatal androgens modify postnatal reproductive and somatic physiology, benefits associated with enhanced competitiveness in DC lineages may have initial costs of reduced IGF-1, delay in weight gain, and decreased survivorship. These novel data further confirm the different evolutionary and mechanistic pathways to cooperative breeding and call for greater consideration of natural endocrine variation in both sexes.

Egalitarian cooperation linked to central oxytocin levels in communal breeding house mice

Relationships between adult females are fundamental to understanding diversity in animal social systems. While cooperative relationships between kin are known to promote fitness benefits, the proximate mechanisms underlying this are not well understood. Here we show that when related female house mice (Mus musculus domesticus) cooperate to rear young communally, those with higher endogenous oxytocin levels have more egalitarian and successful cooperative relationships. Sisters with higher oxytocin concentrations in the paraventricular nucleus (PVN) of the hypothalamus weaned significantly more offspring, had lower reproductive skew and spent more equal proportions of time in the nest. By contrast, PVN oxytocin was unrelated to the number of weaned offspring produced in the absence of cooperation, and did not vary in response to manipulation of nest site availability or social cues of outgroup competition. By linking fitness consequences of cooperation with oxytocin, our findings have broad implications for understanding the evolution of egalitarian social relationships.

The effects of human-caused mortality on mammalian cooperative breeders: a synthesis.

Human-caused mortality can be pervasive and even highly selective for individuals in groups of cooperative breeders. Many studies of cooperative breeders, however, do not address human-caused mortality. Similarly, studies focused on the effects of human-caused mortality on wildlife populations often do not consider the ecology of cooperative breeders. We searched the literature and identified 58 studies where human-caused mortality affected a group characteristic, vital rate, or population state of a cooperative breeder. Of studies reporting population growth or decline, 80% reported a link between human-caused mortality and population declines in cooperative breeders. Such studies often did not identify the mechanism behind population declines, but 28% identified concurrent declines in adult survival and another 21% reported concurrent declines in recruitment or reproduction. There was little overlap between the cooperative breeding and human-caused mortality literatures, limiting our ability to accrue knowledge. Future work would be beneficial if it (i) identified the vital rate(s) causing population declines, (ii) leveraged management actions such as lethal removal to ask questions about the ecology of group-living in cooperative breeders, and (iii) used insights from cooperative breeding theory to inform management actions and conservation of group-living species.

Intraspecific variation in group structure arises due to environmentally-mediated directional dispersal in a cooperative breeder.

Many cooperatively breeding species live in groups with complex structure-large group sizes, low and variable kin structure, and multiple breeding pairs. Since these mixed-kin groups typically form because of immigration of unrelated individuals of both sexes in addition to limited offspring dispersal, differences in patterns of dispersal can generate variation in group structure, even within the same species or population. Here, we examine how environmentally mediated dispersal patterns influence variation in group structure in the plural breeding superb starling (Lamprotornis superbus), an avian cooperative breeder that inhabits a spatiotemporally variable savanna environment and forms mixed-kin groups with variable group sizes and more than one breeding pair per group. Using 4068 genome-wide polymorphic loci and fine-scale, remotely sensed ecological data from 22 groups sampled across a nearly 200 km2 environmental gradient in central Kenya, we find evidence of not only frequent and long-distance dispersal in both sexes (low isolation-by-distance and weak genetic structure), but also directional dispersal from small groups in lower quality habitat with low normalised difference vegetation index (NDVI) to large groups in higher quality habitat with high NDVI. Additionally, we find stronger genetic structure among groups in lower quality habitat, and higher genetic diversity and lower relatedness of groups in higher quality habitat. Previous work using long-term data from groups in the same population has shown that groups with lower relatedness are larger and have more breeding pairs. Long-distance, directional dispersal to maximise individual fitness can thus lead to smaller and simpler kin-based social groups in lower quality habitat, but larger and more complex mixed-kin groups in higher quality habitat. Such intraspecific, within-population variation in group structure, including variation in kin structure of social groups, could have profound implications for the relative importance of the evolutionary mechanisms (i.e. direct vs. indirect fitness benefits) underlying the formation of cooperative societies.

Offspring sex ratio in a communal breeding bird is male‐biased when pre‐breeding rainfall is low

Offspring sex ratios may deviate from parity when the fitness benefits of producing male or female offspring vary. We tested for sex ratio bias in smooth‐billed anis Crotophaga ani, a communal laying cuckoo with low within‐group relatedness and high offspring dispersal. One male group member performs nocturnal incubation and sires more offspring than other males in the group, suggesting males may have greater reproductive variance than females. We hypothesized that pre‐breeding rainfall influences food availability and offspring sex ratio, predicting that breeding females skew production towards the sex with higher reproductive variance (males) in high food years. Females may also adjust sex ratio across the hatching order to increase survival of the more competitive sex, especially when clutches are larger and within‐brood competition is higher. As adults, male smooth‐billed anis are larger than females, so we assumed male nestlings are more competitive than females and predicted a male‐bias in first hatched chicks in larger broods. Contrary to our first prediction, offspring sex ratio was male biased when pre‐breeding rainfall was lower. In partial support of our second prediction, marginally more first hatched chicks were male in larger broods. To our knowledge, this is the first evidence of offspring sex ratio bias in a communal laying bird species. Future work in this system will attempt to uncover the mechanisms by which co‐breeding females adjust offspring sex ratio and test alternative hypotheses to explain male‐biased offspring sex ratios under different conditions.

Digest: Cooperative breeding strategies in birds are shaped by avian predator richness.

Despite their prevalence, family-living and cooperative breeding in birds have received little examination as to how and why they vary across species. Investigating the evolution of these social systems, Bliard et al. (2024) found that the presence of avian predators is associated with birds' social systems, with increases in predator presence corresponding to multiple shifts from non-family-living to cooperative breeding. Phylogenetic comparative analyses indicate that factors outside the breeding season can be selected for family-living and cooperative breeding.

Domestication as the evolution of interspecies cooperative breeding.

We propose that domestication is the result of interspecies cooperative breeding. Considering domestication as an outcome of cooperative breeding can explain how domestication occurs in both plants and animals, encompass cases of domestication that do not involve humans, and shed light on why humans are involved in so many domesticatory relationships. We review the cooperative breeding model of human evolution, which posits that care of human infants by alloparents enabled the evolution of costly human brains and long juvenile development, while selecting for tolerance of strangers. We then explore how human cooperation in the protection and provisioning of young plants and animals can explain the evolution of domestication traits such as changes in development; loss of aggressive, defensive, and bet-hedging aspects of the phenotype; and increased fertility. We argue that the importance of cooperative breeding to human societies has made humans especially likely to enter into interspecies cooperative breeding relationships.

Does sentinel presence improve foraging success? A study in a cooperative breeder

Abstract In various cooperative breeding species, a group member often sentinels from a prominent position that enables early detection of approaching predators, and then utters alarm calls to which the other group members react immediately. We tested in the cooperatively breeding Arabian babbler (Argya squamiceps), whether in the presence of a sentinel the other group members forage for longer or more effectively. In natural observations, in different distances from shelter and in different group sizes, we found no effect of sentinel presence on foraging time. Likewise, in a giving-up density (GUD) experiment with artificial food patches containing mealworms in each of 3 different distances from shelter, fewer mealworms were consumed further from shelter, but irrespective of whether a sentinel was present or not during foraging. While foragers react to a sentinel’s alarm calls when a predator approaches, our findings indicate that Arabian babbler foragers do not improve their foraging efficiency due to the sentinel’s presence. Combined with previous studies on the Arabian babbler, these findings reinforce the conclusion that in this species the sentinel is “selfish” and benefits from early detection of predators. These results contrast with those from other cooperative breeders in which sentinels utter calming calls and foraging efficiency increases when sentinels are present. We, therefore, suggest that similar sentinel behavior may serve different sentinel systems and functions in different cooperative breeders.

Genetic diversity of the critically endangered Blue‐crowned laughingthrush (Garrulax courtoisi)

AbstractTo evaluate the genetic quality and provide available management strategies for Blue‐crowned laughingthrush (BCLT), fifteen polymorphic microsatellite loci were developed and applied. The genetic diversity of wild individuals was indicated to be higher than the two captive populations. The average number of alleles (5.50 ± 0.317), the number of effective alleles (3.417 ± 0.222), observed heterozygosity (0.828 ± 0.04), and genetic differentiation index (0.028 ± 0.007) of 64 wild individuals showed high genetic diversity despite drastic bottleneck and low genetic differentiation. The number of effective migrants (22.737 ± 8.318) indicated the intriguing wintering grounds may be surrounded by the breeding sites where the syncheimadia occurred in Wuyuan. Efficient conservation, winter flocking, and cooperative breeding may facilitate gene exchange and inclusive fitness. We recommend that monitoring concentrated distribution areas for BCLT should be strengthened, and geographical barriers, interference types, and the inner mechanism of distribution patterns should be further explored.

Gazing Strategies among Sentinels of a Cooperative Breeder Are Repeatable but Unrelated to Survival.

Vigilance is a common behavioural adaptation to increase the chances of detecting predators before it is too late to escape. Behavioural traits are often repeatable among individuals over the long term, suggesting differences in personality. Earlier studies have documented individual consistency in the time allocated to vigilance. However, little is known about individual consistency in the ways vigilance is achieved from one moment to another and whether different patterns of vigilance among individuals are associated with survival. We aimed to determine whether sentinels of a cooperative breeder showed individual consistency in their vigilance and if individual variation was related to annual survival. During sentinel bouts from vantage points, Florida scrub-jays (Aphelocoma coerulescens) turn their heads from side to side to monitor their surroundings. Over three field seasons, we found that the head-turning frequency was repeatable in breeders but not in juveniles or non-breeding helpers. The moderate repeatability in breeders was not related to survival. Our results suggest that the head-turning frequency in sentinels of the Florida scrub-jay is repeatable in breeders but not in less experienced juveniles or helpers and, therefore, likely becomes more repeatable as individuals age. The assumption that individual variation in vigilance is related to survival was unsupported in our study and requires further study.

Within‐group sex ratios predict growth of social mole‐rats

AbstractGroups of wild animals can vary considerably in their composition, including in the proportion of group members who are male or female, that is the within‐group sex ratio. Variation in within‐group sex ratios can arise from active adjustment of litter sex ratios by mothers, from sex differences in mortality, dispersal and immigration, or from stochastic variation in recruitment. Variation in the within‐group sex ratio can have consequences for within‐group competition and can affect individual life histories throughout development. In this paper, we explore which processes may generate variation in within‐group sex ratios in wild Damaraland mole‐rats (Fukomys damarensis), a singular cooperative breeder. We investigate whether within‐group sex ratios predict the growth, body condition and philopatry of individuals. We show that although the population‐level sex ratio is balanced, skewed within‐group sex ratios are common, particularly among small groups. Our data suggests that stochastic variation in the sex of recruits explains natural variation in the sex ratio of wild groups. Non‐breeding individuals in groups with a sex ratio biased towards their own sex grow more slowly than individuals in groups biased towards the opposite sex, suggesting that intra‐sexual competition may decrease growth rates. We suggest that the costs of competition may contribute to the large variation in growth observed in social mole‐rat groups.

Lifetime reproductive characteristics of gray wolves

Abstract Female and male cooperative breeders can use different strategies to maximize reproduction and fitness over their lifetimes. Answering questions about fitness in cooperative breeders requires long-term studies as well as complete data on group composition and size which can be exceedingly difficult to obtain. Using a long-term genetic data set of complete group pedigrees, I asked how lifetime reproductive characteristics of female and male gray wolves (Canis lupus) differed. I predicted that genetic relatedness to helpers would be higher for females than males due to philopatric behavior of female wolves, group size would be similar between the sexes, females would inherit breeding positions from within groups more often than males due to differences in dispersal strategies between the sexes, males would have more lifetime mates and produce more young than females because of polygamy, and females would breed for more years than males due to the likelihood that females would still breed (with a new partner) after a mate died or was expelled from the group. I documented complete lifetime breeding histories for 11 male and 18 female wolves in Idaho, United States, 2008 to 2018. Genetic relatedness to helpers, group size, number of mates, pups, and years breeding did not differ between the sexes. Females, however, inherited breeding positions within groups far more often than males. Individuals who secured breeding positions generally reproduced for 2 seasons and commonly had more than 1 partner during their lifetimes if they were able to maintain their breeding position longer. Direct fitness varied greatly within female and male breeding wolves.

Cooperative Breeding by Golden Eagles (Aquila chrysaetos) in Colorado

Cooperative Breeding by Golden Eagles (Aquila chrysaetos) in Colorado

Family living and cooperative breeding in birds are associated with the number of avian predators.

Cooperative breeding occurs when individuals contribute parental care to offspring that are not their own. Numerous intra- and interspecific studies have aimed to explain the evolution of this behavior. Recent comparative work suggests that family living (i.e., when offspring remain with their parents beyond independence) is a critical stepping stone in the evolution of cooperative breeding. Thus, it is key to understand the factors that facilitate the evolution of family living. Within-species studies suggest that protection from predators is a critical function of group living, through both passive benefits such as dilution effects and active benefits such as prosocial antipredator behaviors in family groups. However, the association between predation risk and the formation and prevalence of family groups and cooperative breeding remains untested globally. Here, we use phylogenetic comparative analyses including 2,984 bird species to show that family living and cooperative breeding are associated with increased occurrence of avian predators. These cross-species findings lend support to previous suggestions based on intraspecific studies that social benefits of family living, such as protection against predation, could favor the evolution of delayed dispersal and cooperative breeding.