Social complexity affects cognitive abilities but not brain structure in a Poecilid fish

Complex cognitive performance is suggested to be the out-turn of complex social life, allowing individuals to achieve higher fitness through sophisticated "Machiavellian" strategies. Although there is ample support for this concept, especially when comparing species, most of the evidence is correlative. Here we provide an experimental investigation of how group size and composition may affect brain and cognitive development in the guppy (Poecilia reticulata). For six months, we reared sexually mature female guppies in one of three different social treatments: (i) three female guppies; (ii) three female guppies mixed with three female splash tetras (Copella arnoldi), a species that co-occurs with the guppy in the wild; and (iii) six female guppies. We then tested the guppies performance in inhibitory control, associative learning and reversal learning tasks to evaluate their self-control, operant conditioning and cognitive flexibility capabilities. Afterwards, we estimated their brain size and the size of major brain regions using X-ray imaging technology. We found that individuals in larger groups of six individuals, in both same and mixed species treatments, outperformed individuals from the smaller groups of three guppies in reversal learning, with no apparent differences in the inhibitory control and associative learning tasks. This is rare evidence of how living in larger social groups improves cognitive flexibility, supporting that social pressures play an important role in shaping individual cognitive development. Interestingly, social manipulation had no apparent effect on brain morphology, but relatively larger telencephalons were associated with better individual performance in reversal learning. This suggests alternative mechanisms beyond brain region size enabled greater cognitive flexibility in individuals from larger groups.