The socio-genetics of a complex society: female gelada relatedness patterns mirror association patterns in a multi-level society.

Multilevel societies with fission–fusion dynamics—arguably the most complex animal societies—are defined by two or more nested levels of organization. The core of these societies are modular social units that regularly fission and fuse with one another. Despite convergent evolution in disparate taxa, we know strikingly little about how such societies form and how fitness benefits operate. Understanding the kinship structure of complex societies could inform us about the origins of the social structure as well as about the potential for individuals in these societies to accrue indirect fitness benefits. Here, we combined genetic and behavioural data on geladas (Theropithecus gelada), an Old World Monkey, to complete the most comprehensive socio-genetic analysis of a multilevel society to date. In geladas, individuals in the core social ‘units’, associate at different frequencies to form ‘teams’, ‘bands’ and, the largest aggregations, ‘communities’. Units were composed of closely related females, and females remained with their close kin during permanent fissions of units. Interestingly, female–female relatedness also significantly predicted between-unit, between-team and between-band association patterns, while male–male relatedness did not. Thus, it is likely that the socio-genetic structure of gelada society results from females maintaining associations with their female relatives during successive unit fissions—possibly in an attempt to balance the direct and indirect fitness benefits of group living. Overall, the persistence of associations among related females across generations appears to drive the formation of higher levels of gelada society, suggesting that females seek kin for inclusive fitness benefits at multiple levels of gelada society

具有裂变-融合动态（fission–fusion dynamics）的多层级社会——堪称最复杂的动物社会——以两层及以上的嵌套组织层级为定义特征。这类社会的核心为模块化社交单元，这些单元会定期彼此间发生裂变与融合。尽管在不同的分类群（taxa）中均出现了趋同演化（convergent evolution），但我们对这类社会的形成机制以及适合度收益（fitness benefits）的运作方式仍知之甚少。解析复杂社会的亲缘结构（kinship structure），有助于我们理解社会结构的起源，以及这类社会中的个体获取间接适合度收益的可能性。本研究结合了旧世界猴（Old World Monkey）狮尾狒（Theropithecus gelada）的遗传与行为数据，完成了迄今为止针对多层级社会最全面的社会遗传学（socio-genetic）分析。在狮尾狒群体中，核心社交「单元」内的个体会以不同的频率进行社交联结，进而形成「团队」、「群」以及规模最大的聚合体——「社群」。社交单元由亲缘关系紧密的雌性个体组成，且在单元发生永久性裂变时，雌性个体仍会与近亲保持结伴。值得注意的是，雌性间的亲缘关系同样能显著预测单元间、团队间以及群间的社交联结模式，而雄性间的亲缘关系则无此预测效果。因此，狮尾狒社会的社会遗传学结构，很可能源于雌性个体在接连不断的单元裂变过程中，始终与雌性亲属保持社交联结——这或许是为了平衡群体生活带来的直接与间接适合度收益。总体而言，跨世代的亲缘雌性个体间联结的持续性，似乎推动了狮尾狒社会更高层级结构的形成，这表明雌性个体为了获得广义适合度收益（inclusive fitness benefits），会在狮尾狒社会的多个层级中寻求亲缘伙伴。