The Evolution of Cooperation: Interacting Phenotypes among Social Partners

Abstract

Models of cooperation among nonkin suggest that social assortment is important for the evolution of cooperation. Theory predicts that interacting phenotypes, whereby an individual's behavior depends on the behavior of its social partners, can drive such social assortment. We measured repeated indirect genetic effects (IGEs) during cooperative predator inspection in eight populations of Trinidadian guppies (Poecilia reticulata) that vary in their evolutionary history of predation. Four broad patterns emerged that were dependent on river, predation history, and sex: (i) current partner behavior had the largest effect on focal behavior, with fish from low-predation habitats responding more to their social partners than fish from high-predation habitats; (ii) different focal/partner behavior combinations can generate cooperation; (iii) some high-predation fish exhibited carryover effects across social partners; and (iv) high-predation fish were more risk averse. These results provide the first large-scale comparison of interacting phenotypes during cooperation across wild animal populations, highlighting the potential importance of IGEs in maintaining cooperation. Intriguingly, while focal fish responded strongly to current social partners, carryover effects between social partners suggest generalized reciprocity (in which one helps anyone if helped by someone) may contribute to the evolution of cooperation in some, but not all, populations of guppies.

Correlated pay-offs are key to cooperation

“…However, there are many contexts in which generalized reciprocity rules may be employed in social groups, including mutual vigilance, cooperative hunting and territory defence, alternation between leading and following positions in group locomotion, mutual grooming or sharing of limited resources such as food and shelter. For example, in guppies, Poecilia reticulata, experimental subjects interacted more cooperatively with unfamiliar partners after receiving cooperative experience with others, depending on environmental conditions and sex [59], and in the field, guppy social networks are positively assorted by cooperative predator inspection behaviour [60]. So even if generalized reciprocity has not been unequivocally demonstrated in wild guppies, the crucial preconditions for this behaviour seem to occur in this species.…”

Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution?

“…From such studies, we know that variation in the social environment animals experience can generate evolutionary feedbacks mediated by IGEs if the social environment consists of genetically varying individuals; such feedbacks arise because the environment itself can evolve (Moore et al 1997;Bailey 2012). The strength and direction of IGEs can also evolve over time and across populations (Chenoweth et al 2010;Bailey and Zuk 2012;Kazancioğlu et al 2012;Edenbrow et al 2017), and associated social selection is predicted to vary accordingly (McGlothlin et al 2010). In recent years, IGEs have been incorporated into animal and plant breeding studies to more accurately predict evolutionary responses in agriculturally valuable traits, such as growth rate, thermal tolerance, and infection risk (Camerlink et al 2013(Camerlink et al , 2014(Camerlink et al , 2015Costa e Silva et al 2013;Anche et al 2014;Muñoz et al 2014;Alemu et al 2016;Baud et al 2017).…”

“…The timescale over which individual phenotypes change because of IGEs influences the outcome of evolutionary dynamics, depending on the number and frequency of social interactions (McGlothlin et al 2010;Saltz 2013;Schneider et al 2017;Anderson et al 2017;Edenbrow et al 2017). In addition, the phenotypic equilibrium for a trait affected by IGEs is determined partly by the whether the IGE is reciprocal or not (i.e., the same trait influences its own expression in focal and partner individuals, as in aggressive escalations, versus a focal trait that is affected by a different trait in an interacting partner, as in maternal care).…”

“…In Pogonomyrmex californicus, a harvester ant, variation in the social composition of founding groups of queens in cooperative colonies determines behavioral outcomes in aggression and brood care phenotypes (Clark and Fewell 2013). IGEs have been documented across a range of additional social traits, including paternal care (Head et al 2012), social dominance (Moore et al 2002;Wilson et al 2011), agonistic encounters (Wilson et al 2009;Santostefano et al 2016), group antipredator behavior (Bleakley et al 2009;Edenbrow et al 2017), and breeding date in birds (Germain et al 2016). In the mosquitofish Gambusia holbrooki, direct genetic effects (DGEs) influence the number of social partners that males of different color morphs encounter, illustrating how DGEs and IGEs can covary (Kraft et al 2016), a critical parameter influencing evolutionary dynamics (Bijma 2014).…”

Genetics and developmental biology of cooperation

“…However, this requires isogenic lines or large‐scale breeding designs with repeated measures of the same genotype with different social partners. Measuring individual‐level phenotypic proxies could provide a more feasible approach for vertebrates, assuming a close phenotype–genotype resemblance (Edenbrow et al., ). Those proxies could be estimates of the extent to which traits covary between interaction partners, for example, spatial proximity.…”