揭秘鸟类合作繁殖的进化:以青藏高原特有物种地山雀作为模式系统的一项长期努力

鸟类合作繁殖系统的进化机制是行为生态学和进化生态学领域的热点,许多基本理论问题依然悬而未决.青藏高原草甸荒漠气候恶劣、植被贫乏,是地球上独特的生态地理区域.自2004年以来,我们以此极端环境的特有物种地山雀(Parus humilis)为模式系统,探讨合作繁殖系统的特征和适应方式.在掌握合作系统基本结构的基础上,将继续进行长期数据的积累.通过比较帮助者和独立繁殖者的终生适合度,检验亲属选择理论;建立时空尺度上合作繁殖与气候因子的关系,揭露生态压力的作用机制;理清不同种群合作繁殖与婚外父权的关系,阐明遗传单配制作为合作繁殖行为进化的驱动力;联系外源与内源因素,确定合作繁殖物种种群动态的调节机理.地山雀社会系统的神秘需要研究者用不懈的努力去探索.     

Cooperative breeding among Chinese passerines: inference from social behavior,diet, and migratory status

Recent estimates suggest that 9% of bird species are cooperative breeders. However, little is known about the breeding behavior of many species, particularly those in the Indomalayan and Neotropical regions. Our objective was to provide an overview of the prevalence of cooperative breeding among Chinese songbirds. Examination of the social behavior, diet, and migratory status of 55 known cooperative‐breeding species of songbirds in China revealed that 90.9% live in small groups, 89.1% are residents in at least one or all their subspecies, 81.8% are insectivores, and 14.5% are omnivores. In contrast, 58.2% of the 55 species are resident insectivores that live in small groups, 10.9% are resident omnivores that live in small groups, and 12.7% include subspecies that are resident insectivores. We used these combinations of traits of known cooperative breeders and phylogenetic relationships to infer that an additional 106 species of songbirds in China are probable cooperative breeders and 22 species are possible cooperative breeders. Our analysis suggests that a maximum of 27.2% (183 of 674 species) of Chinese passerines are cooperative breeders, with more occurring in subtropical southern China than in temperate northern China. Cooperative breeding is the main breeding system of species in the families Corvidae, Pycnonotidae, and, especially, Timaliidae (105 of 183 species, 57%). Based on our analyses, cooperative breeding might be more common than previously assumed, particularly among species in the families Timaliidae, Corvidae, and Sturnidae, and species in southern, subtropical China. Because most cooperative‐breeding species in our study were either inferred cooperative breeders or possible cooperative breeders, additional study of these species is needed to confirm our results. A better understanding of the prevalence of cooperative breeding in birds will improve our insight into the evolutionary and ecological factors that select for cooperative breeding.     

Female-mediated causes and consequences of status change in a social fish

In highly social species, dominant individuals often monopolize reproduction, resulting in reproductive investment that is status dependent. Yet, for subordinates, who typically invest less in reproduction, social status can change and opportunities to ascend to dominant social positions are presented suddenly, requiring abrupt changes in behaviour and physiology. In this study, we examined male reproductive anatomy, physiology and behaviour following experimental manipulations of social status in the cooperatively breeding cichlid fish, Neolamprologus pulcher. This unusual fish species lives in permanent social groups composed of a dominant breeding pair and 1-20 subordinates that form a linear social dominance hierarchy. By removing male breeders, we created 18 breeding vacancies and thus provided an opportunity for subordinate males to ascend in status. Dominant females play an important role in regulating status change, as males successfully ascended to breeder status only when they were slightly larger than the female breeder in their social group. Ascending males rapidly assumed behavioural dominance, demonstrated elevated gonadal investment and androgen concentrations compared with males remaining socially subordinate. Interestingly, to increase gonadal investment ascending males appeared to temporarily restrain somatic growth. These results highlight the complex interactions between social status, reproductive physiology and group dynamics, and underscore a convergent pattern of reproductive investment among highly social, cooperative species.     

Ecological,Evolutionary and Social Constraints on Reproductive Effort: Are Hoary Marmots Really Biennial Breeders?

Biennial breeding is a rare life-history trait observed in animal species living in harsh, unproductive environments. This reproductive pattern is thought to occur in 10 of 14 species in the genus Marmota, making marmots useful model organisms for studying its ecological and evolutionary implications. Biennial breeding in marmots has been described as an obligate pattern which evolved as a mechanism to mitigate the energetic costs of reproduction (Evolved Constraint hypothesis). However, recent anecdotal evidence suggests that it is a facultative pattern controlled by annual variation in climate and food availability (Environmental Constraint hypothesis). Finally, in social animals like marmots, biennial breeding could result from reproductive competition between females within social groups (Social Constraint hypothesis). We evaluated these three hypotheses using mark-recapture data from an 8-year study of hoary marmot (Marmota caligata) population dynamics in the Yukon. Annual variation in breeding probability was modeled using multi-state mark-recapture models, while other reproductive life-history traits were modeled with generalized linear mixed models. Hoary marmots were neither obligate nor facultative biennial breeders, and breeding probability was insensitive to evolved, environmental, or social factors. However, newly mature females were significantly less likely to breed than older individuals. Annual breeding did not result in increased mortality. Female survival and, to a lesser extent, average fecundity were correlated with winter climate, as indexed by the Pacific Decadal Oscillation. Hoary marmots are less conservative breeders than previously believed, and the evidence for biennial breeding throughout Marmota, and in other arctic/alpine/antarctic animals, should be re-examined. Prediction of future population dynamics requires an accurate understanding of life history strategies, and of how life history traits allow animals to cope with changes in weather and other demographic influences.     

Neuroendocrine control in social relationships in non-human primates: Field based evidence

Primates maintain a variety of social relationships and these can have fitness consequences. Research has established that different types of social relationships are unpinned by different or interacting hormonal systems, for example, the neuropeptide oxytocin influences social bonding, the steroid hormone testosterone influences dominance relationships, and paternal care is characterized by high oxytocin and low testosterone. Although the oxytocinergic system influences social bonding, it can support different types of social bonds in different species, whether pair bonds, parent-offspring bonds or friendships. It seems that selection processes shape social and mating systems and their interactions with neuroendocrine pathways. Within species, there are individual differences in the development of the neuroendocrine system: the social environment individuals are exposed to during ontogeny alters their neuroendocrine and socio-cognitive development, and later, their social interactions as adults. Within individuals, neuroendocrine systems can also have short-term effects, impacting on social interactions, such as those during hunting, intergroup encounters or food sharing, or the likelihood of cooperating, winning or losing. To understand these highly dynamic processes, extending research beyond animals in laboratory settings to wild animals living within their natural social and ecological setting may bring insights that are otherwise unreachable. Field endocrinology with neuropeptides is still emerging. We review the current status of this research, informed by laboratory studies, and identify questions particularly suited to future field studies. We focus on primate social relationships, specifically social bonds (mother-offspring, father-offspring, cooperative breeders, pair bonds and adult platonic friendships), dominance, cooperation and in-group/out-group relationships, and examine evidence with respect to the ‘tend and defend’ hypothesis.     

The ecology of cooperative breeding behaviour

Ecology is a fundamental driving force for the evolutionary transition from solitary living to breeding cooperatively in groups. However, the fact that both benign and harsh, as well as stable and fluctuating, environments can favour the evolution of cooperative breeding behaviour constitutes a paradox of environmental quality and sociality. Here, we propose a new model – the dual benefits framework – for resolving this paradox. Our framework distinguishes between two categories of grouping benefits – resource defence benefits that derive from group‐defended critical resources and collective action benefits that result from social cooperation among group members – and uses insider–outsider conflict theory to simultaneously consider the interests of current group members (insiders) and potential joiners (outsiders) in determining optimal group size. We argue that the different grouping benefits realised from resource defence and collective action profoundly affect insider–outsider conflict resolution, resulting in predictable differences in the per capita productivity, stable group size, kin structure and stability of the social group. We also suggest that different types of environmental variation (spatial vs. temporal) select for societies that form because of the different grouping benefits, thus helping to resolve the paradox of why cooperative breeding evolves in such different types of environments.     

Reduction of Foraging Work and Cooperative Breeding

Using simple stochastic models, we discuss how cooperative breeders, especially wasps and bees, can improve their productivity by reducing foraging work. In a harsh environment, where foraging is the main cause of mortality, such breeders achieve greater productivity by reducing their foraging effort below full capacity, and they may thrive by adopting cooperative breeding. This could prevent the population extinction of cooperative breeders under conditions where a population of lone breeders cannot be maintained.     

Cooperative breeding in birds: a comparative test of the life history hypothesis

In approximately 3.2% of bird species individuals regularly forgo the opportunity to breed independently and instead breed cooperatively with other conspecifics, either as non-reproductive ''helpers'' or as co-breeders. The traditional explanation for cooperative breeding is that the opportunities for breeding independently are limited owing to peculiar features of the species'' breeding ecology. However, it has proved remarkably difficult to find any common ecological correlates of cooperative breeding in birds. This difficulty has led to the ''life history hypothesis'', which suggests that the common feature of cooperatively breeding birds is their great longevity, rather than any particular feature of their breeding ecology. Here, we use a comparative method to test the life history hypothesis by looking for correlations between life history variation and variation in the frequency of cooperative breeding. First, we find that cooperative breeding in birds is not randomly distributed, but concentrated in certain families, thus supporting the idea that there may be a common basis to cooperative breeding in birds. Second, increases in the level of cooperative breeding are strongly associated with decreases in annual adult mortality and modal clutch size. Third, the proportion of cooperatively breeding species per family is correlated with a low family-typical value of annual mortality, suggesting that low mortality predisposes cooperative breeding rather than vice versa. Finally, the low rate of mortality typically found in cooperatively breeding species is associated with increasing sedentariness, lower latitudes, and decreased environmental fluctuation. We suggest that low annual mortality is the key factor that predisposes avian lineages to cooperative breeding, then ecological changes, such as becoming sedentary, further slow population turnover and reduce opportunities for independent breeding. As the traditional explanation suggests, the breeding habitat of cooperatively breeding species is saturated, but this saturation is not owing to any peculiar feature of the breeding ecology of cooperative breeders. Rather, the saturation arises because the local population turnover in these species is unusually slow, as predicted by the life history hypothesis.     

Kin selection, not group augmentation, predicts helping in an obligate cooperatively breeding bird

Kin selection theory has been the central model for understanding the evolution of cooperative breeding, where non-breeders help bear the cost of rearing young. Recently, the dominance of this idea has been questioned; particularly in obligate cooperative breeders where breeding without help is uncommon and seldom successful. In such systems, the direct benefits gained through augmenting current group size have been hypothesized to provide a tractable alternative (or addition) to kin selection. However, clear empirical tests of the opposing predictions are lacking. Here, we provide convincing evidence to suggest that kin selection and not group augmentation accounts for decisions of whether, where and how often to help in an obligate cooperative breeder, the chestnut-crowned babbler (Pomatostomus ruficeps). We found no evidence that group members base helping decisions on the size of breeding units available in their social group, despite both correlational and experimental data showing substantial variation in the degree to which helpers affect productivity in units of different size. By contrast, 98 per cent of group members with kin present helped, 100 per cent directed their care towards the most related brood in the social group, and those rearing half/full-sibs helped approximately three times harder than those rearing less/non-related broods. We conclude that kin selection plays a central role in the maintenance of cooperative breeding in this species, despite the apparent importance of living in large groups.     

Evolutionary routes to non-kin cooperative breeding in birds

Cooperatively breeding animals live in social groups in which some individuals help to raise the offspring of others, often at the expense of their own reproduction. Kin selection—when individuals increase their inclusive fitness by aiding genetic relatives—is a powerful explanation for the evolution of cooperative breeding, particularly because most groups consist of family members. However, recent molecular studies have revealed that many cooperative groups also contain unrelated immigrants, and the processes responsible for the formation and maintenance of non-kin coalitions are receiving increasing attention. Here, I provide the first systematic review of group structure for all 213 species of cooperatively breeding birds for which data are available. Although the majority of species (55%) nest in nuclear family groups, cooperative breeding by unrelated individuals is more common than previously recognized: 30% nest in mixed groups of relatives and non-relatives, and 15% nest primarily with non-relatives. Obligate cooperative breeders are far more likely to breed with non-kin than are facultative cooperators, indicating that when constraints on independent breeding are sufficiently severe, the direct benefits of group membership can substitute for potential kin-selected benefits. I review three patterns of dispersal that give rise to social groups with low genetic relatedness, and I discuss the selective pressures that favour the formation of such groups. Although kin selection has undoubtedly been crucial to the origin of most avian social systems, direct benefits have subsequently come to play a predominant role in some societies, allowing cooperation to persist despite low genetic relatedness.     

Cooperative breeding in oscine passerines: does sociality inhibit speciation?

Cooperative breeding in birds is much more prevalent than has been previously realized, occurring in 18.5% of oscine passerines known to have biparental care, and is the predominant social system of some ancient oscine clades. Cooperation is distributed unevenly in clades that contain both cooperative and pair breeders, and is usually confined to a few related genera in which it can be ubiquitous. Cooperative clades are species poor compared with pair-breeding clades, because pair breeders evolve migratory habits, speciate on oceanic islands and are more likely to have distributions spread across more than one biogeographic region. These differences reflect the increased capacity for colonization by pair breeders because their young disperse. Thus cooperative breeding has macroevolutionary consequences by restricting rates of speciation and macroecological implications by influencing the assembly of island and migrant faunas.     

Matrilineal genetic structure within and among populations of the cooperatively breeding common marmoset,Callithrix jacchus

Common marmosets are members of the family Callitrichidae, South American primates characterized by highly social group living and cooperative breeding. In this study we analysed 1112 base pairs (bp) of the mitochondrial control region in 59 Callithrix jacchus individuals, sampled mainly from two geographically distinct field sites in N.E. Brazil. Analysis of molecular variation revealed a highly significant genetic structuring of haplotypes between social groups and between populations. Examination of matrilineal genetic structure within social groups revealed that seven of nine recorded breeding pairs were from different maternal lineages, indicating assortative mating and outbreeding. In addition to the breeders, at least six of 10 groups contained adult individuals from different matrilines, with five haplotypes present in one social group of nine animals. Groups of mixed lineages raise questions about potential reproductive conflicts of interest, and the extent of kin-selected altruism in the evolution and maintenance of cooperative breeding in this species.     

Environmental variability uncovers disruptive effects of species' interactions on population dynamics

How species respond to changes in environmental variability has been shown for single species, but the question remains whether these results are transferable to species when incorporated in ecological communities. Here, we address this issue by analysing the same species exposed to a range of environmental variabilities when (i) isolated or (ii) embedded in a food web. We find that all species in food webs exposed to temporally uncorrelated environments (white noise) show the same type of dynamics as isolated species, whereas species in food webs exposed to positively autocorrelated environments (red noise) can respond completely differently compared with isolated species. This is owing to species following their equilibrium densities in a positively autocorrelated environment that in turn enables species–species interactions to come into play. Our results give new insights into species'' response to environmental variation. They especially highlight the importance of considering both species'' interactions and environmental autocorrelation when studying population dynamics in a fluctuating environment.     

Human‐modified habitats change patterns of population genetic structure and group relatedness in Peter's tent‐roosting bats

Although coloniality is widespread among mammals, it is still not clear what factors influence composition of social groups. As animals need to adapt to multiple habitat and environmental conditions throughout their range, variation in group composition should be influenced by adaptive adjustment to different ecological factors. Relevant to anthropogenic disturbance, increased habitat modification by humans can alter species’ presence, density, and population structure. Therefore, it is important to understand the consequences of changes to landscape composition, in particular how habitat modification affects social structure of group‐forming organisms. Here, we combine information on roosting associations with genetic structure of Peter's tent‐roosting bats, Uroderma bilobatum to address how different habitat characteristics at different scales affect structure of social groups. By dividing analyses by age and sex, we determined that genetic structure was greater for adult females than adult males or offspring. Habitat variables explained 80% of the variation in group relatedness (mainly influenced by female relatedness) with roost characteristics contributing the most explained variation. This suggests that females using roosts of specific characteristics exhibit higher relatedness and seem to be philopatric. These females mate with more males than do more labile female groups. Results describe ecological and microevolutionary processes, which affect relatedness and social structure; findings are highly relevant to species distributions in both natural and human‐modified environments.     

Behaviour and breeding biology of the cooperatively breeding Grey-backed Fiscal Shrike Lanius excubitorius in Kenya

Grey-backed Fiscal Shrikes Lanius excubitorius were studied over a 2j year period near Lake Naivasha, Kenya. Grey-backs are cooperative breeders, with group sizes ranging from two to II. Only one pair breeds per group, with all other group members aiding in the rearing of young. The study population ranged from 64 to 79 individuals that occurred in from 13 to 16 groups. Non-breeding helpers made up to 66% of the population, with male helpers being more numerous overall than females. The annual survival rate was 65%, with no differences detected between the survival of males and females, or of breeders and helpers. Only male helpers were observed to acquire breeding status within the natal territory. Some female helpers acquired breeding positions in territories adjacent to their natal territories. Group territorial displays occurred throughout the year but were most pronounced prior to breeding during rainy periods. Reproductive success was very low, with only 14.5% of the recorded breeding attempts leading to fledged young. Large groups (four or more birds) had greater reproductive success than small groups, but many factors other than, or in addition to, group size may have influenced this pattern. The breeding male contributed the most food to the incubating female and to the nestlings. Male helpers and the breeding female contributed more to nestlings than did female helpers. Observations on the post-fledging period indicate that socialization and establishment of dominance may be of importance in group-living species living in a restricted ecological and social setting.     

Preservation of winter social dominance status in Brent Geese Branta bernicla bernicla within and across winters

Dominant and subordinate individuals in a group may benefit from the stability of the social dominance organisation, avoiding excessive waste of time and energy in aggressive interactions and reducing injury risks. Nevertheless, the likely evolutionary incentive for individuals to become, and furthermore to stay, dominant may destabilise such dominance hierarchies. In this context, the relative importance of fixed (e.g. sex, morphological size) and fluctuating (e.g. body condition, mating status, reproductive success, social unit size) traits influencing the establishment and preservation of dominance relationships could play a key role in group structure. We investigated the relative role of fixed and fluctuating traits on social status in Dark-bellied Brent Geese Branta bernicla bernicla which form large fairly unstable groups both within and across winters. We compared individual dominance scores of ringed Brent Geese during four consecutive winters. Brent Geese conserved their dominance score within a given winter irrespective of their age but were generally unable to conserve it across consecutive winters. As winter dominance scores correlated best with social unit size, dominance status thus appeared to be mostly a by-product of a fluctuating trait: breeding success in the previous summer. When we considered only adults that had the same social unit size during two consecutive winters, we observed a significant preservation of dominance scores. This result suggests that a fixed trait such as sex or morphological size may still play a role in setting dominance status.     

Different Responses to Reward Comparisons by Three Primate Species

Background

Recently, much attention has been paid to the role of cooperative breeding in the evolution of behavior. In many measures, cooperative breeders are more prosocial than non-cooperatively breeding species, including being more likely to actively share food. This is hypothesized to be due to selective pressures specific to the interdependency characteristic of cooperatively breeding species. Given the high costs of finding a new mate, it has been proposed that cooperative breeders, unlike primates that cooperate in other contexts, should not respond negatively to unequal outcomes between themselves and their partner. However, in this context such pressures may extend beyond cooperative breeders to other species with pair-bonding and bi-parental care.

Methods

Here we test the response of two New World primate species with different parental strategies to unequal outcomes in both individual and social contrast conditions. One species tested was a cooperative breeder (Callithrix spp.) and the second practiced bi-parental care (Aotus spp.). Additionally, to verify our procedure, we tested a third confamilial species that shows no such interdependence but does respond to individual (but not social) contrast (Saimiri spp.). We tested all three genera using an established inequity paradigm in which individuals in a pair took turns to gain rewards that sometimes differed from those of their partners.

Conclusions

None of the three species tested responded negatively to inequitable outcomes in this experimental context. Importantly, the Saimiri spp responded to individual contrast, as in earlier studies, validating our procedure. When these data are considered in relation to previous studies investigating responses to inequity in primates, they indicate that one aspect of cooperative breeding, pair-bonding or bi-parental care, may influence the evolution of these behaviors. These results emphasize the need to study a variety of species to gain insight in to how decision-making may vary across social structures.     

Urban and coastal breeding lesser black-backed gulls (Larus fuscus) segregate by foraging habitat

Despite urbanization's general erosion of biodiversity, towns and cities provide novel opportunities for some species. During the 20th century, gulls (Laridae) colonized urban areas around the world where they flourished. At the same time, some coastal populations declined. The reasons for this difference are not fully understood, partly because little is known about any ecological differences between urban and non-urban gulls, such as their foraging ecology. Here we compare the movement ecology and habitat selection of Lesser Black-backed Gulls Larus fuscus graellsii breeding at two neighbouring colonies – one urban and one coastal – in north-west England. We used bird-borne GPS loggers to first compare colony-level movement behaviour and habitat selection and then investigated individual-level habitat use. We observed clear colony-level habitat segregation: urban breeders preferentially foraged in urban areas whereas coastal breeders foraged primarily in coastal habitats and avoided urban areas. Coastal breeders also had larger core and home-ranges than urban breeders, possibly due to differences in colony size. However, we also found inter-individual differences in habitat use, which may have important management implications. These findings suggest a link between nesting and foraging ecology, and thus management or environmental change altering food availability will impact gulls at the coastal and urban sites differently.     

Anticipated effects of abiotic environmental change on intraspecific social interactions

Social interactions are ubiquitous across the animal kingdom. A variety of ecological and evolutionary processes are dependent on social interactions, such as movement, disease spread, information transmission, and density-dependent reproduction and survival. Social interactions, like any behaviour, are context dependent, varying with environmental conditions. Currently, environments are changing rapidly across multiple dimensions, becoming warmer and more variable, while habitats are increasingly fragmented and contaminated with pollutants. Social interactions are expected to change in response to these stressors and to continue to change into the future. However, a comprehensive understanding of the form and magnitude of the effects of these environmental changes on social interactions is currently lacking. Focusing on four major forms of rapid environmental change currently occurring, we review how these changing environmental gradients are expected to have immediate effects on social interactions such as communication, agonistic behaviours, and group formation, which will thereby induce changes in social organisation including mating systems, dominance hierarchies, and collective behaviour. Our review covers intraspecific variation in social interactions across environments, including studies in both the wild and in laboratory settings, and across a range of taxa. The expected responses of social behaviour to environmental change are diverse, but we identify several general themes. First, very dry, variable, fragmented, or polluted environments are likely to destabilise existing social systems. This occurs as these conditions limit the energy available for complex social interactions and affect dissimilar phenotypes differently. Second, a given environmental change can lead to opposite responses in social behaviour, and the direction of the response often hinges on the natural history of the organism in question. Third, our review highlights the fact that changes in environmental factors are not occurring in isolation: multiple factors are changing simultaneously, which may have antagonistic or synergistic effects, and more work should be done to understand these combined effects. We close by identifying methodological and analytical techniques that might help to study the response of social interactions to changing environments, highlight consistent patterns among taxa, and predict subsequent evolutionary change. We expect that the changes in social interactions that we document here will have consequences for individuals, groups, and for the ecology and evolution of populations, and therefore warrant a central place in the study of animal populations, particularly in an era of rapid environmental change.     

COOPERATIVE BREEDING FAVORS MATERNAL INVESTMENT IN SIZE OVER NUMBER OF EGGS IN SPIDERS

The transition to cooperative breeding may alter maternal investment strategies depending on density of breeders, extent of reproductive skew, and allo‐maternal care. Change in optimal investment from solitary to cooperative breeding can be investigated by comparing social species with nonsocial congeners. We tested two hypotheses in a mainly semelparous system: that social, cooperative breeders, compared to subsocial, solitarily breeding congeners, (1) lay fewer and larger eggs because larger offspring compete better for limited resources and become reproducers; (2) induce egg size variation within clutches as a bet‐hedging strategy to ensure that some offspring become reproducers. Within two spider genera, Anelosimus and Stegodyphus, we compared species from similar habitats and augmented the results with a mini‐meta‐analysis of egg numbers depicted in phylogenies. We found that social species indeed laid fewer, larger eggs than subsocials, while egg size variation was low overall, giving no support for bet‐hedging. We propose that the transition to cooperative breeding selects for producing few, large offspring because reproductive skew and high density of breeders and young create competition for resources and reproduction. Convergent evolution has shaped maternal strategies similarly in phylogenetically distant species and directed cooperatively breeding spiders to invest in quality rather than quantity of offspring.