Major Hurdles for the Evolution of Sociality

Why do most animals live solitarily, while complex social life is restricted to a few cooperatively breeding vertebrates and social insects? Here, we synthesize concepts and theories in social evolution and discuss its underlying ecological causes. Social evolution can be partitioned into (a) formation of stable social groups, (b) evolution of helping, and (c) transition to a new evolutionary level. Stable social groups rarely evolve due to competition over food and/or reproduction. Food competition is overcome in social insects with central-place foraging or bonanza-type food resources, whereas competition over reproduction commonly occurs because staying individuals are rarely sterile. Hence, the evolution of helping is shaped by direct and indirect fitness options and helping is only altruism if it reduces the helper’s direct fitness. The helper’s capability to gain direct fitness also creates within-colony conflict. This prevents transition to a new evolutionary level. 297 Click here to view this article's online features: • Download figures as PPT slides • Navigate linked references • Download citations • Explore related articles • Search keywords ANNUAL REVIEWS Further A nn u. R ev . E nt om ol . 2 01 6. 61 :2 97 -3 16 . D ow nl oa de d fr om w w w . a nn ua lr ev ie w s. or g A cc es s pr ov id ed b y 20 7. 24 1. 23 2. 18 9 on 0 5/ 07 /2 0. F or p er so na l u se o nl y. EN61CH16-Korb ARI 1 February 2016 12:54 Cooperation: an interaction in which partners help each other and each partner thereby increases its own direct fitness Fraternal transition: an association between units that are genetically similar (e.g., cells of a multicellular organism) Egalitarian transition: an association between two disparate units in which both partners reproduce (although not necessarily equally) Altruism: an interaction in which the actor increases the fitness of the recipient at a cost to its own direct fitness INTRODUCTION The evolution of adaptations through natural selection has long been interpreted as being driven mainly by competition among individuals over reproduction or, more precisely, among alleles over transmission to the next generation. Cooperation among individuals, though already considered by Darwin (36) and Kropotkin (88), has been recognized as a factor driving evolution only during the past few decades (Table 1; see sidebar, Synopsis of Recent Concepts). Building on work by Buss (27) and Michod & Roze (99), Maynard Smith & Szathmáry (97) identified cooperation as underlying all major transitions in evolution: from autonomous replicators to chromosomes, from asexual to sexual organisms, from prokaryotes to eukaryotes, from protists to multicellular organisms, and from solitary to social animals. The origin of sociality is the latest of these transitions, and group-living animals are therefore prominent models to study social evolution and the balance between cooperation and competition. Major transitions involve cooperation either among related units with a common ancestry (e.g., cells in a multicellular body; fraternal transitions) (24, 112, 113) or among unrelated units (e.g., organelles in eukaryotic organisms, symbioses between species; egalitarian transitions) (24, 112, 113). Egalitarian transitions evolve only if all involved parties can increase their direct reproductive success through these interactions. In contrast, altruism can evolve in fraternal transitions, where some units may be at least partly excluded from direct reproduction. The evolution of social insects with sterile worker castes clearly is a fraternal transition (Figure 1). Altruism and fraternal transitions are best explained by Hamilton’s theory of inclusive fitness (49, 53). It posits that, from the viewpoint of a particular allele in a focal individual, it does not matter whether its copies are transmitted to the next generation via offspring of the focal individual or offspring of the focal individual’s relatives. Inclusive fitness thus has two components: classical direct fitness from the individual’s own offspring and indirect fitness from the individual’s impact on the survival and reproduction of relatives (inclusive fitness perspective) (Figure 2). Altruistic Table 1 Recent concepts with classifications of the steps in social evolution Monogamyhypothesisa Sociality syndromesb Principles of social evolutionc Organismalityd Driving evolutionary forcese