Morinay Jennifer, Woodward Beth K, Russell Andrew F, Sharp Stuart P, Hatchwell Ben J
Ecology & Evolutionary Biology, School of Biosciences, University of Sheffield, Sheffield, UK.
Science and Technology Facilities Council, UKRI, Swindon, UK.
J Anim Ecol. 2025 Apr;94(4):485-500. doi: 10.1111/1365-2656.14237. Epub 2025 Jan 28.
The evolution of sociality is one of the major evolutionary transitions in the history of life and a key step in this transition is the occurrence of kin associations. Yet, the question of what demographic processes and environmental factors generate kin-structured populations and drive kin-directed cooperation remains open. In this review, we synthesise 30 years of studies of the long-tailed tit Aegithalos caudatus, which has a kin-selected cooperative breeding system with redirected help: failed breeders may help to raise offspring of conspecifics, typically relatives, breeding nearby. We describe the use of ecological, demographic, genetic and behavioural approaches to reveal: (a) how kin-structured populations (here 'kin neighbourhoods') arise; (b) why the prevalence of cooperation varies among populations and individuals; and (c) how variation in dispersal and opportunities for cooperation influence individual fitness. The kin neighbourhoods of long-tailed tits arise from three processes. First, natal dispersal is limited and sex-biased so many individuals, especially males, recruit as breeders close to their natal site. Second, neither dispersal nor migration necessarily disrupts kin associations because long-tailed tits often move with close relatives. Third, a small effective population size driven by high nest predation rates enhances within-population relatedness. Together, these processes set the scene for kin-directed helping behaviour by causing spatial clustering of relatives. The prevalence of cooperation within kin neighbourhoods depends on several factors, both at the population-level (annual nest predation rate and length of the breeding season) and individual-level (relatedness, familiarity, sex and condition). However, limited information on prior social association and the reliability of kin discrimination cues hampers our current understanding of individual helping decisions. Finally, variation in dispersal within and between sexes affects the probability of interacting with kin, the likelihood of cooperation, and accrual of the direct and indirect components of inclusive fitness. We use this comprehensive understanding of the factors driving cooperative behaviour in long-tailed tits to highlight gaps in knowledge and suggest future avenues for research in this system, and to make general inferences about the role of dispersal, demography and kinship in social evolution.
社会性的演化是生命史上主要的演化转变之一，而这一转变的关键步骤是亲属关联的出现。然而，关于哪些人口统计学过程和环境因素会产生亲属结构的种群并推动亲属导向的合作这一问题仍然没有答案。在这篇综述中，我们综合了30年来对长尾山雀（Aegithalos caudatus）的研究，该物种具有亲属选择的合作繁殖系统，存在 redirected help（此处存疑，可能是指“转向式帮助”之类的特定行为，因未明确，故保留英文）：繁殖失败的个体可能会帮助抚养同种个体（通常是亲属）在附近繁殖的后代。我们描述了如何运用生态、人口统计学、遗传和行为学方法来揭示：（a）亲属结构的种群（这里指“亲属邻域”）是如何形成的；（b）为什么合作的普遍程度在种群和个体之间存在差异；以及（c）扩散和合作机会的变化如何影响个体的适合度。长尾山雀的亲属邻域由三个过程形成。首先，出生后的扩散是有限的且存在性别偏差，因此许多个体，尤其是雄性，会在靠近其出生地的地方作为繁殖者定居。其次，扩散和迁徙不一定会破坏亲属关联，因为长尾山雀经常与近亲一起移动。第三，高巢穴捕食率导致的有效种群规模较小，增强了种群内部的亲缘关系。这些过程共同作用，通过导致亲属的空间聚集，为亲属导向的帮助行为创造了条件。亲属邻域内合作的普遍程度取决于几个因素，包括种群层面（年度巢穴捕食率和繁殖季节长度）和个体层面（亲缘关系、熟悉程度、性别和状况）。然而，关于先前社会关联的信息有限以及亲属识别线索的可靠性阻碍了我们目前对个体帮助决策的理解。最后，性别内部和性别之间扩散的变化会影响与亲属互动的概率、合作的可能性以及广义适合度的直接和间接成分的积累。我们利用对驱动长尾山雀合作行为因素的这种全面理解，来突出知识上的差距，并提出该系统未来的研究途径，以及对扩散、人口统计学和亲属关系在社会演化中的作用做出一般性推断。
