Exploration and activity show contrasting familial resemblance

Abstract

Whether complex behaviours that appear unitary are governed by a single integrated system or composed of distinct evolutionary modules remains unclear. For instance, an animal's locomotion trajectory depends on two independent decisions: how much to move and where to go. Determining whether these behavioural dimensions are linked or vary independently is essential, as modular traits impact the evolutionary potential of complex phenotypes. We investigated this framework in newborn Trinidadian guppies (Poecilia reticulata ) by decoupling a single locomotor sequence into its exploratory and activity components and evaluating their structure of inclusive inheritance through a nested paternal half-sib breeding design. Our findings reveal that these behavioural dimensions exhibit contrasting patterns of familial resemblance, with exploration being structured with fathers, whereas activity with mothers. These findings indicate potential evolutionary decoupling between how much an animal moves and where it goes, supported by trait-specific structures of inclusive inheritance. Importantly, this modular architecture suggests that different components of a single locomotor sequence can be targeted independently by natural selection, providing a powerful mechanism to bypass rigid behavioural syndromes and drive the diversification of complex personality profiles.