Cooperation and conflict during evolutionary transitions in individuality.

Cooperation received much less attention 30 years agothan other forms of ecological interaction, such ascompetition and predation. Workers generally viewedcooperation as being of limited interest, of specialrelevance to certain species (e.g. social insects, birds,humans and our primate relatives) but not of generalsigniﬁcance to life on earth. This view has changed, duein large part to the study of evolutionary transitions inindividuality (ETIs). What began as the study of animalsocial behaviour some 40 years ago has now embracedthe study of social interactions at all levels in thehierarchy of life. Instead of being seen as a specialcharacteristic clustered in certain lineages of socialanimals, cooperation is now seen as the primary creativeforce behind ever greater levels of complexity throughthe creation of new kinds of individuals. Cooperationplays this central role in ETIs because it exports ﬁtnessfrom the lower level (its costs) to the new higher level (itsbeneﬁts).How did this shift in understanding the importance ofcooperation come about? Darwin (1859), Wilson (1975)and Hamilton (1963, 1964a,b) all understood the import-ance of cooperation for social organisms. There waspioneering work done as early as 1902 on the importanceof cooperation in the struggle for existence (Kropotkin,1902), and there was the now widely accepted theory ofMargulis (1970, 1981) and others on the endosymbioticorigins of mitochondria and chloroplasts in the eukary-otic cell. However, cooperation was also viewed as adestabilizing force in ecological communities and likely oflimited signiﬁcance because of the positive feedbackloops it creates (May, 1973). Sociobiology had deﬁnedaltruism as its core problem (Wilson, 1975), but thealtruism problem was not viewed as general to life onearth until workers began applying cooperation thinkingto the evolution of interactions at other levels in thehierarchy of life in addition to social organisms, such asto the level of genes within gene groups (e.g. Eigen SPrice, 1970, 1972; e.g. Hamilton, 1975; Wade, 1978;Wilson, 1980). The evolutionary transitions problem(Maynard Smith, 1988, 1991; Maynard Smith & Szathm-a´ry, 1995) grew out of these two developments which, ineffect, extended the sociobiology revolution to all kindsof replicating units in the hierarchy of life.Lehmann & Keller (2006) propose a four-way classi-ﬁcation scheme for population models of the evolution ofcooperation, according to the issue of whether thebeneﬁts are direct (individual selection) or indirect (kinselection). Within the ﬁrst category of direct beneﬁts, adistinction is made according to whether the beneﬁts aremediated through the behaviour of another individual(as through learning in reciprocation) or not. Within thesecond category of kin-selected indirect effects, a distinc-tion is made as to whether there are many genesinvolved in the traits or a few (as in the ‘green-beard’effect).The distinction between direct and indirect effects iswidely used to describe social behaviour and the evolu-tionofﬁtnesseffects associated withinteractions betweenindividuals. This distinction seems less helpful, however,when one’s interest concerns the origin of the individualsthemselves, i.e. ETIs. Indeed the direct-indirect distinc-tion presumes that one knows what the individual is.Direct or indirect with regard to what? The individual,of course.Transforming our understanding of life is the realiza-tion that evolution occurs not only through evolutionwithin populations but also during ETIs – when groupsbecome so integrated they evolve into a new higher-levelindividual. The major landmarks in the diversiﬁcation oflife and the hierarchical organization of the living worldare consequences of a series of ETIs: from nonlife to life,from networks of cooperating genes to the ﬁrst prokary-otic-like cell, from prokaryotic to eukaryotic cells, fromunicellular to multicellular organisms, from asexual tosexual populations, and from solitary to social organisms.It is a major challenge to understand why (environmen-tal selective pressures) and how (underlying genetics,physiology and development) the basic features of anevolutionary individual, such as ﬁtness heritability,indivisibility, and evolvability, shift their reference fromthe old to the new level. Classifying the many factorsinvolved in the evolution of cooperation into a fewgeneral categories as Lehmann & Keller (2006) havedone will certainly help in meeting this challenge.Individuals often associate in groups, and under certainconditions these groups evolve into a new kind ofindividual. Cooperation is fundamental to this processbecause it transfers ﬁtness from the lower-level indivi-duals (in terms of its costs) up to the level of the group(the beneﬁts of cooperation), thereby serving to create anew level of ﬁtness and possibly, under certain condi-tions, a new higher-level individual (Michod, 1999).Indeed, as already mentioned, the major levels in thehierarchy of life (genes, gene networks, cells, eukaryoticcells, multicellular organisms) are thought to haveevolved from this process of individuation of groups(Maynard Smith & Szathma´ry, 1995; Michod, 1999).