Group augmentation underlies the evolution of complex sociality in the face of environmental instability.

Although kin selection is assumed to underlie the evolution of sociality, many vertebrates-including nearly half of all cooperatively breeding birds-form groups that also include unrelated individuals. Theory predicts that despite reducing kin structure, immigration of unrelated individuals into groups can provide direct, group augmentation benefits, particularly when offspring recruitment is insufficient for group persistence. Using population dynamic modeling and analysis of long-term data, we provide clear empirical evidence of group augmentation benefits favoring the evolution and maintenance of complex societies with low kin structure and multiple reproductives. We show that in the superb starling (Lamprotornis superbus)-a plural cooperative breeder that forms large groups with multiple breeding pairs, and related and unrelated nonbreeders of both sexes-offspring recruitment alone cannot prevent group extinction, especially in smaller groups. Further, smaller groups, which stand to benefit more from immigration, exhibit lower reproductive skew for immigrants, suggesting that reproductive opportunities as joining incentives lead to plural breeding. Yet, despite a greater likelihood of becoming a breeder in smaller groups, immigrants are more likely to join larger groups where they experience increased survivorship and greater reproductive success as breeders. Moreover, immigrants form additional breeding pairs, increasing future offspring recruitment into the group and guarding against complete reproductive failure in the face of environmental instability and high nest predation. Thus, plural breeding likely evolves because the benefits of group augmentation by immigrants generate a positive feedback loop that maintains societies with low and mixed kinship, large group sizes, and multiple reproductives.

Lifetime inclusive fitness effects of cooperative polygamy in the acorn woodpecker.

Although over 50 y have passed since W. D. Hamilton articulated kin selection and inclusive fitness as evolutionary explanations for altruistic behavior, quantifying inclusive fitness continues to be challenging. Here, using 30 y of data and two alternative methods, we outline an approach to measure lifetime inclusive fitness effects of cooperative polygamy (mate-sharing or cobreeding) in the cooperatively breeding acorn woodpecker Melanerpes formicivorus. For both sexes, the number of offspring (observed direct fitness) declined while the number of young parented by related cobreeders (observed indirect fitness effect) increased with cobreeding coalition size. Combining these two factors, the observed inclusive fitness effect of cobreeding was greater than breeding singly for males, while the pattern for females depended on whether fitness was age-weighted, as females breeding singly accrued greater fitness at younger ages than cobreeding females. Accounting for the fitness birds would have obtained by breeding singly, however, lifetime inclusive fitness effects declined with coalition size for males, but were greater for females breeding as duos compared to breeding singly, due largely to indirect fitness effects of kin. Our analyses provide a road map for, and demonstrate the importance of, quantifying indirect fitness as a powerful evolutionary force contributing to the costs and benefits of social behaviors.

Chemical Profiles Differ between Communal Breeding Groups in a Highly Social Bird.

AbstractGregarious species must distinguish group members from nongroup members. Olfaction is important for group recognition in social insects and mammals but rarely studied in birds, despite birds using olfaction in social contexts from species discrimination to kin recognition. Olfactory group recognition requires that groups have a signature odor, so we tested for preen oil and feather chemical similarity in group-living smooth-billed anis (Crotophaga ani). Physiology affects body chemistry, so we also tested for an effect of egg-laying competition, as a proxy for reproductive status, on female chemical similarity. Finally, the fermentation hypothesis for chemical recognition posits that host-associated microbes affect host odor, so we tested for covariation between chemicals and microbiota. Group members were more chemically similar across both body regions. We found no chemical differences between sexes, but females in groups with less egg-laying competition had more similar preen oil, suggesting that preen oil contains information about reproductive status. There was no overall covariation between chemicals and microbes; instead, subsets of microbes could mediate olfactory cues in birds. Preen oil and feather chemicals showed little overlap and may contain different information. This is the first demonstration of group chemical signatures in birds, a finding of particular interest given that smooth-billed anis live in nonkin breeding groups. Behavioral experiments are needed to test whether anis can distinguish group members from nongroup members using odor cues.

A female-biased gene expression signature of dominance in cooperatively breeding meerkats.

Dominance is a primary determinant of social dynamics and resource access in social animals. Recent studies show that dominance is also reflected in the gene regulatory profiles of peripheral immune cells. However, the strength and direction of this relationship differs across the species and sex combinations investigated, potentially due to variation in the predictors and energetic consequences of dominance status. Here, we investigated the association between social status and gene expression in the blood of wild meerkats (Suricata suricatta; n = 113 individuals), including in response to lipopolysaccharide, Gardiquimod (an agonist of TLR7, which detects single-stranded RNA in vivo) and glucocorticoid stimulation. Meerkats are cooperatively breeding social carnivores in which breeding females physically outcompete other females to suppress reproduction, resulting in high reproductive skew. They therefore present an opportunity to disentangle the effects of social dominance from those of sex per se. We identify a sex-specific signature of dominance, including 1045 differentially expressed genes in females but none in males. Dominant females exhibit elevated activity in innate immune pathways and a larger fold-change response to LPS challenge. Based on these results and a preliminary comparison to other mammals, we speculate that the gene regulatory signature of social status in the immune system depends on the determinants and energetic costs of social dominance, such that it is most pronounced in hierarchies where physical competition is important and reproductive skew is large. Such a pattern has the potential to mediate life history trade-offs between investment in reproduction versus somatic maintenance.

Proto-tool use for food processing in wild Arabian babblers: matching processing methods, substrates and prey types.

Cognition is a powerful adaptation, enabling animals to utilise resources that are unavailable without manipulation. Tool use and food processing are examples of using cognition to overcome the protective mechanisms of food resources. Here, we describe and examine the flexibility of proto-tool use (defined as the alteration of an object through object-substrate manipulation) for food processing in a cooperatively breeding bird, the Arabian babbler (Argya squamiceps). Field observations demonstrate that the birds transport different caterpillar species to different substrate types depending on the processing method needed to prepare the caterpillar for eating. Species with toxic setae (e.g. Casama innotata) are transported to be rubbed on rough substrates (e.g. sand) before consumption, while other species (e.g. Hyles livornica) are transported to be pounded against hard substrates until their inner organs are removed and only their external body part is consumed. These results are among the few to describe flexible proto-tool use for food processing in wild animals. They thereby contribute to the taxonomic mapping of proto-tool use and food processing in non-human species, which is a fundamental step to advance comparative studies on the evolution of these behaviours and their underlying cognitive mechanisms.

How does climate change impact social bees and bee sociality?

Climatic factors are known to shape the expression of social behaviours. Likewise, variation in social behaviour can dictate climate responses. Understanding interactions between climate and sociality is crucial for forecasting vulnerability and resilience to climate change across animal taxa. These interactions are particularly relevant for taxa like bees that exhibit a broad diversity of social states. An emerging body of literature aims to quantify bee responses to environmental change with respect to variation in key functional traits, including sociality. Additionally, decades of research on environmental drivers of social evolution may prove fruitful for predicting shifts in the costs and benefits of social strategies under climate change. In this review, we explore these findings to ask two interconnected questions: (a) how does sociality mediate vulnerability to climate change, and (b) how might climate change impact social organisation in bees? We highlight traits that intersect with bee sociality that may confer resilience to climate change (e.g. extended activity periods, diet breadth, behavioural thermoregulation) and we generate predictions about the impacts of climate change on the expression and distribution of social phenotypes in bees. The social evolutionary consequences of climate change will be complex and heterogeneous, depending on such factors as local climate and plasticity of social traits. Many contexts will see an increase in the frequency of eusocial nesting as warming temperatures accelerate development and expand the temporal window for rearing a worker brood. More broadly, climate-mediated shifts in the abiotic and biotic selective environments will alter the costs and benefits of social living in different contexts, with cascading impacts at the population, community and ecosystem levels.

Fitness benefits of alternated chick provisioning in cooperatively breeding carrion crows.

In most bird species, parents raise offspring cooperatively. In some cases, this cooperation extends to helpers-at-the-nest who assist the breeders with a range of tasks. While cooperative food provisioning might merely arise incidentally, as a result of the efforts of carers that act independently from each other, recent studies suggest that birds may coordinate by taking turns in visiting the nest. However, evidence that such coordination emerges because individuals actively respond to each other's behaviour is controversial, and the potential benefits of carers' alternation remain unknown. We addressed this knowledge gap by analysing a multiyear dataset for cooperatively breeding carrion crows Corvus corone, comprising 8693 nest visits across 50 groups. Our results reveal that turn-taking does occur in this species and that all group members, regardless of their sex and social role (breeder/helper), tend to alternate at the nest with other carers rather than to make repeat visits. Importantly, we found that the body mass of nestlings increased significantly with the degree of carers' alternation, possibly because well-coordinated groups provided food at more regular intervals. Using earlier monitoring data, the observed increase in body mass is predicted to substantially boost postfledging survival rates. Our analyses demonstrate that alternation in nestling provisioning has measurable fitness benefits in this study system. This raises the possibility that cooperatively breeding carrion crows, as well as other bird species with similarly coordinated brood provisioning, exhibit specialized behavioural strategies that enable effective alternation.

En la mayoría de las especies de aves, los padres cooperan entre sí en el cuidado de sus crías. En algunos casos, la cooperación se extiende a individuos ayudantes que asisten a los reproductores en diferentes tareas. El aprovisionamiento cooperativo de las crías puede darse simplemente como resultado del esfuerzo de cuidadores que actúan de forma independiente, pero estudios recientes sugieren que las aves pueden coordinarse, tomando turnos a la hora de visitar el nido. Sin embargo, las evidencias de que dicha coordinación ocurre porque los individuos realmente responden al comportamiento de los demás es controvertida, y los potenciales beneficios de la alternancia al nido son desconocidos. Nosotros abordamos estos aspectos analizando una base de datos plurianual en la corneja negra Corvus corone, que incluye 8693 visitas al nido en 50 grupos. Nuestros resultados revelan que se produce toma de turnos en esta especie y que todos los miembros del grupo, independientemente del sexo y del estatus social (reproductor / ayudante), tienden a alternarse al nido con otros cuidadores, en vez de repetir visitas. Más importante aún, encontramos que la masa corporal de los polluelos aumentaba de forma significativa al aumentar el grado de coordinación de los cuidadores, posiblemente porque los grupos mejor coordinados aprovisionaban las crías a intervalos más regulares. Basándonos en datos anteriores, pudimos calcular que el incremento observado en masa corporal predice un aumento sustancial de la tasa de supervivencia de los volanderos. Nuestros análisis demuestran, por lo tanto, que la alternancia al nido tiene beneficios medibles en eficacia biológica. Esto conlleva la posibilidad de que las cornejas negras cooperativas, al igual que otras especies de aves con aprovisionamiento coordinado de las crías, exhiban estrategias comportamentales especializadas que permitan una eficiente alternancia al nido.

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.

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.

Impacts of the COVID-19 pandemic on population management in AZA.

Soon after the onset of the COVID-19 pandemic, almost all Association of Zoos and Aquariums (AZA) facilities closed to the public. Resulting cost-saving and safety measures led some facilities to temporarily cease or reduce animal breeding and/or transfers. We surveyed AZA facilities and Species Survival Plan® (SSP) Coordinators for AZA's cooperative population management programs to evaluate how widespread these decisions were, if impacts varied by taxa, and how the AZA community navigated related challenges during the pandemic. We found that 60% of responding facilities did not suspend breeding and 22% did not suspend transfers. About 50% of responding zoos increased their reliance on ground transportation to move animals, while aquariums reported no change to transportation methods. SSP Coordinators reported the main reason why breeding decreased, regardless of taxa, was due to canceled or delayed transfers. The reasons transfers decreased differed by taxa, such as limited financial resources and lack of access to air transportation. The majority of respondents for both surveys stated transfers were the greatest challenge they faced. To address this, facilities utilized alternative transportation methods and worked closely with nearby zoos and aquariums for the movement of animals, while SSP Coordinators issued alternative transfer recommendations. If another pandemic or other widespread facility closure occurs, our research highlights the importance of communication, collaboration, and flexibility to fulfill breeding and transfer recommendations to maintain sustainable zoo and aquarium populations.

Environmental quality mediates the ecological dominance of cooperatively breeding birds.

Although social species as diverse as humans and ants are among the most abundant organisms on Earth, animals cooperate and form groups for many reasons. How these different reasons for grouping affect a species' ecological dominance remains unknown. Here we use a theoretical model to demonstrate that the different fitness benefits that animals receive by forming groups depend on the quality of their environment, which in turn impacts their ecological dominance and resilience to global change. We then test the model's key predictions using phylogenetic comparative analysis of >6500 bird species. As predicted, we find that cooperative breeders occurring in harsh and fluctuating environments have larger ranges and greater abundances than non-cooperative breeders, but cooperative breeders occurring in benign and stable environments do not. Using our model, we further show that social species living in harsh and fluctuating environments will be less vulnerable to climate change than non-social species.

Fitness Costs of Female Competition Linked to Resource Defense and Relatedness of Competitors.

AbstractFemale reproductive success is often limited by access to resources, and this can lead to social competition both within and between kin groups. Theory predicts that both resource availability and relatedness should influence the fitness consequences of social competition. However, testing key predictions requires differentiating the effects of these two factors. Here, we achieve this experimentally by manipulating the social environment of house mice, a facultative communal breeding species with known kin discrimination ability. This allows us to investigate (1) the reproductive costs of defending a limited resource in response to cues of social competition and (2) whether such costs, or their potential mitigation via cooperative behavior, are influenced by the relatedness of competitors. Our results support the hypothesis that resource defense can be costly for females, potentially trading off against maternal investment. When the availability of protected nest sites was limited, subjects (1) were more active, (2) responded more strongly to simulated territory intrusions via competitive signaling, and (3) produced smaller weaned offspring. However, we found no evidence that the propensity for kin to cooperate was influenced by the relatedness of rivals. Communal breeding between sisters occurred independently of the relatedness of competitors and communally breeding sisters weaned fewer offspring when competing with unrelated females, despite our study being designed to prevent infanticide between kin groups. Our findings thus demonstrate that female competition has fitness costs and that associating with kin is beneficial to avoid negative fitness consequences of competing with nonkin, in addition to more widely recognized kin-selected benefits.

Behavioural, demographic and fitness consequences of social instability in cooperatively breeding dwarf mongoose groups.

Social instability frequently arises in group-living species, but the potential costs have rarely been investigated in free-living cooperative breeders, especially across different timeframes. Using natural observations, body mass measurements and life-history data from dwarf mongooses (Helogale parvula), we determined the short- and long-term consequences of a change in one of the dominant breeding pairs. We found that a new breeder led to alterations in both collective and individual behaviours (i.e. increases in communal scent-marking, engagement in intergroup interactions, sentinel activity and within-group grooming), as well as reduced body mass gain, further demographic changes and decreased reproductive success (i.e. fewer pups surviving to adulthood). The effects were particularly apparent when it was the female breeder who changed; new female breeders were younger than more experienced counterparts. Our findings support the idea that stability and cooperation are strongly linked and provide potential reasons for previously documented health and fitness benefits of social stability.

Ecogeography of group size suggests differences in drivers of sociality among cooperatively breeding fairywrens.

Cooperatively breeding species exhibit a range of social behaviours associated with different costs and benefits to group living, often in association with different environmental conditions. For example, recent phylogenetic studies have collectively shown that the evolution and distribution of cooperative breeding behaviour is related to the environment. However, little is known about how environmental variation may drive differences in social systems across populations within species, and how the relationship between environmental conditions and sociality may differ across species. Here, we examine variation in social group size along a steep environmental gradient for two congeneric cooperatively breeding species of fairywrens (Maluridae) and show that they exhibit opposing ecogeographic patterns. Purple-backed fairywrens, a species in which helpers increase group productivity, have larger groups in hot, dry environments and smaller groups in cool, wet environments. By contrast, superb fairywrens, a species with helpers that do not increase group productivity despite the presence of alloparental care, exhibit the opposite trend. We suggest differences in the costs and benefits of sociality contribute to these opposing ecogeographical patterns and demonstrate that comparisons of intraspecific patterns of social variation across species can provide insight into how ecology shapes social systems.

Evidence for a reproductive sharing continuum in cooperatively breeding mammals and birds: consequences for comparative research.

Extreme reproductive skew occurs when a dominant female/male almost monopolizes reproduction within a group of multiple sexually mature females/males, respectively. It is sometimes considered an additional, restrictive criterion to define cooperative breeding. However, datasets that use this restrictive definition to classify species as cooperative breeders systematically overestimate reproductive skew by including groups in which reproduction cannot be shared by definition (e.g. groups with a single female/male). Here, we review the extent of reproductive sharing in 41 mammal and 37 bird species previously classified as exhibiting alloparental care and extreme reproductive skew, while only considering multi-female or multi-male groups. We demonstrate that in groups where unequal reproduction sharing is possible, extreme reproductive skew occurs in a few species only (11/41 mammal species and 12/37 bird species). These results call for significant changes in datasets that classify species' caring and mating system. To facilitate these changes, we provide an updated dataset on reproductive sharing in 63 cooperatively breeding species. At the conceptual level, our findings suggest that reproductive skew should not be a defining criterion of cooperative breeding and support the definition of cooperative breeding as a care system in which alloparents provide systematic care to other group members' offspring.

Queen fecundity, worker entourage and cuticular chemistry in the ant Formica fusca.

Cooperative breeding entails conflicts over reproductive shares that may be settled in different ways. In ants, where several queens simultaneously reproduce in a colony, both queens and workers may influence the reproductive apportionment and offspring quality. Queens may vary in their intrinsic fecundity, which may influence the size of the worker entourage attending individual queens, and this may eventually dictate the reproductive output of a queen. We tested whether the reproductive success of queens is affected by the size of their worker entourage, their fecundity at the onset of the reproductive season, and whether the queen cuticular hydrocarbon profile carries information on fecundity. We show that in the ant Formica fusca both queen fecundity and egg hatching success increase with the size of their entourage, and that newly hatched larvae produced by initially highly fecund queens are smaller. Furthermore, higher relatedness among workers increased queen fecundity. Finally, the queens that received a large worker entourage differed in the cuticular chemistry from those that received a small worker entourage. Our results thus show that workers play a pivotal role in determining queen fitness, that high intracolony relatedness among workers enhances the overall reproductive output in the colony, and that queen fecundity is reflected in their cuticular hydrocarbon profile.

Effects of meteorological conditions on brood care in cooperatively breeding carrion crow and consequences on reproductive success.

Meteorological stressors (e.g., temperature and rain shortage) constrain brood provisioning in some bird species, but the consequences on reproductive success have been rarely quantified. Here we show, in a cooperatively breeding population of carrion crow Corvus corone in Spain, that individual feeding rates decreased significantly with rising air temperatures both in breeders and helpers, while lack of rain was associated with a significant reduction in the effort of the male helpers as compared to the other social categories. Group coordination, measured as the degree of alternation of nest visits by carers, was also negatively affected by rising temperature. Furthermore, we found that the body condition of the nestlings worsened when temperatures were high during the rearing period. Interestingly, the analysis of a long-term data set on crow reproduction showed that nestling body condition steadily deteriorated over the last 26-years. Although many factors may concur in causing population changes, our data suggest a possible causal link between global warming, brood caring behaviour and the decline of carrion crow population in the Mediterranean climatic region of Spain.

Should sons breed independently or help? Local relatedness matters.

In cooperatively breeding birds, why do some individuals breed independently but others have to help at home? This question has been rarely addressed despite its fundamental importance for understanding the evolution of social cooperation. We address it using 15 years of data from Tibetan ground tits Pseudopodoces humilis where helpers consist of younger males. Since whether younger males successfully breed depends critically on their chances to occupy territories nearby home, our analytic strategy is to identify the determinants of individual differences in gaining territory ownership among these ready-to-breed males. Across widowed, last-year helper and yearling males, an age advantage was evident in inheriting resident territories, occupying adjacent vacancies and budding off part of adjacent territories, which left some last-year helpers and most yearling males to take the latter two routes. These males were more likely to acquire a territory if they were genetically related to the previous or current territory owners; otherwise they remained on natal territories as helpers. The relatedness effect can arise from the prior residence advantage established in the preceding winter when younger males followed their parents to perform kin-directed off-territory forays. Our research highlights the key role of local kinship in determining younger males' territory acquisition and thus their fate in terms of independent reproduction versus help. This finding provides insight into the formation of kin-based, facultative cooperative societies prevailing among vertebrates.

Egg components and offspring survival vary with group size and laying order in a cooperative breeder.

Prenatal resource allocation to offspring can be influenced by maternal environment and offspring value, and affect offspring survival. An important pathway for flexible maternal allocation is via egg components such as nutrients and hormones. In cooperative breeders, females with helpers may increase resource allocation to eggs-'differential allocation'-or reduce it-'load-lightening'. Yet, helper effects on egg composition have been poorly studied. Moreover, it is unknown how helpers' presence modulates laying order effects on egg content and survival. Here, we investigated how maternal allocation varied with group size and laying order in the cooperatively breeding sociable weaver (Philetairus socius). We estimated interactive effects of helpers and laying order on allocation to egg mass, yolk nutrients-yolk mass, proteins, lipids, carotenoids, vitamin A and vitamin E-and hormones-testosterone, androstenedione, and corticosterone. Results concurred with the 'differential allocation' predictions. Females with more helpers produced later-laid eggs with heavier yolks and more lipids, and laid eggs overall richer in lipids. Proteins, antioxidants, and hormones were not found to vary with helper number. We then analyzed how helper number modulated laying order effects on survival. Females with more helpers did not specifically produce later-laid eggs with higher survival, but eggs laid by females with more helpers were overall more likely to fledge. These findings show that some egg components (yolk mass, lipids) can positively vary according to females' breeding group size, which may improve offspring fitness.

Genomic signatures and evolutionary history of the endangered blue-crowned laughingthrush and other Garrulax species.

BACKGROUND: The blue-crowned laughingthrush (Garrulax courtoisi) is a critically endangered songbird endemic to Wuyuan, China, with population of ~323 individuals. It has attracted widespread attention, but the lack of a published genome has limited research and species protection. RESULTS: We report two laughingthrush genome assemblies and reveal the taxonomic status of laughingthrush species among 25 common avian species according to the comparative genomic analysis. The blue-crowned laughingthrush, black-throated laughingthrush, masked laughingthrush, white-browed laughingthrush, and rusty laughingthrush showed a close genetic relationship, and they diverged from a common ancestor between ~2.81 and 12.31 million years ago estimated by the population structure and divergence analysis using 66 whole-genome sequencing birds from eight laughingthrush species and one out group (Cyanopica cyanus). Population inference revealed that the laughingthrush species experienced a rapid population decline during the last ice age and a serious bottleneck caused by a cold wave during the Chinese Song Dynasty (960-1279 AD). The blue-crowned laughingthrush is still in a bottleneck, which may be the result of a cold wave together with human exploitation. Interestingly, the existing blue-crowned laughingthrush exhibits extremely rich genetic diversity compared to other laughingthrushes. These genetic characteristics and demographic inference patterns suggest a genetic heritage of population abundance in the blue-crowned laughingthrush. The results also suggest that fewer deleterious mutations in the blue-crowned laughingthrush genomes have allowed them to thrive even with a small population size. We believe that cooperative breeding behavior and a long reproduction period may enable the blue-crowned laughingthrush to maintain genetic diversity and avoid inbreeding depression. We identified 43 short tandem repeats that can be used as markers to identify the sex of the blue-crowned laughingthrush and aid in its genetic conservation. CONCLUSIONS: This study supplies the missing reference genome of laughingthrush, provides insight into the genetic variability, evolutionary potential, and molecular ecology of laughingthrush and provides a genomic resource for future research and conservation.