📄 evolutionary biology

Exploration and activity show contrasting familial resemblance

By decoupling locomotor behavior in newborn Trinidadian guppies, this study reveals that exploration and activity exhibit contrasting patterns of familial resemblance linked to fathers and mothers respectively, indicating that these traits are evolutionarily modular and can be independently targeted by natural selection to drive personality diversification.

Original authors: Morbiato, E., Glavaschi, A.

Published 2026-10-16

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CC BY 4.0

Original authors: Morbiato, E., Glavaschi, A.

Original paper licensed under CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/). ⚕️ This is an AI-generated explanation of a preprint that has not been peer-reviewed. It is not medical advice. Do not make health decisions based on this content. Read full disclaimer

Animals often seem to possess a unified personality, a single, consistent way of moving through the world. A bold fish might dart everywhere, while a shy one stays put. Scientists have long wondered if this consistency comes from a single, tightly woven system in the brain that controls all movement, or if different parts of behavior are actually separate modules that can change and evolve on their own. To understand this, researchers look at two fundamental choices an animal makes while moving: how much it moves, and where it chooses to go. The first is a measure of energy and speed, while the second is a measure of curiosity and risk-taking. If these two choices are locked together, an animal that moves a lot must also explore new places, and an animal that stays still must also avoid the unknown. This would limit the variety of personalities nature can create. However, if these two choices are independent, an animal could be very active but stay in a safe corner, or move very little but venture into dangerous, open spaces. This independence would allow for a much wider range of behavioral styles to develop over time.

A team of researchers set out to test whether these two aspects of movement are truly linked or if they operate as separate units. They chose to study newborn guppies, a small fish species known for its diverse behaviors. Because these fish are born ready to swim and do not rely on their parents for care, studying them immediately after birth allowed the scientists to see their natural tendencies before they learned anything from their environment. The researchers used a specific breeding method to separate the influence of the father from the mother. They mated one male with three different females, creating groups of half-siblings who shared the same father but had different mothers and grew up in different maternal environments. This setup allowed the team to see if the father's genes or the mother's influence were more important in shaping how much the fish moved versus where they chose to swim.

The scientists placed each newborn fish into a circular tank and filmed them for ten minutes. They measured two things: how much time the fish spent swimming, which represented activity, and how much time they spent in the open, exposed center of the tank, which represented exploration. The results showed that these two behaviors were not strongly linked at the individual level; a fish that swam a lot did not necessarily spend more time in the center. More importantly, the family patterns revealed a striking split. The tendency to explore the open center was strongly linked to the father. Fish that shared the same father tended to explore similarly, regardless of which mother they had. In contrast, the tendency to be active and move around was strongly linked to the mother. Fish that shared the same mother moved similarly, even if they had different fathers.

This finding suggests that the decision of how much to move and the decision of where to go are governed by different mechanisms. The study indicates that these two parts of a single swimming sequence are not controlled by one integrated system, but rather by distinct pathways that can be inherited differently. The researchers found that the father's influence on exploration was significantly stronger than the mother's, while the mother's influence on activity was significantly stronger than the father's. Because these traits are inherited through different channels, they can evolve separately. This means that natural selection could potentially make a population of fish that is very active but cautious, or very calm but adventurous, without being stuck in a rigid pattern where one trait forces the other. The study provides evidence that the building blocks of animal personality can be modular, allowing for a richer and more flexible diversity of behaviors to emerge in nature.

Technical Summary: Exploration and Activity Show Contrasting Familial Resemblance

Problem Statement
The paper addresses a fundamental question in behavioral ecology and evolutionary biology: whether complex behaviors that appear unitary are governed by a single integrated system or composed of distinct, semi-autonomous evolutionary modules. Specifically, the authors investigate the locomotor trajectory of animals, which is dictated by two distinct decisions: how much to move (activity) and where to go (exploration). While these components often covary phenotypically, it remains unclear if they share an underlying regulatory structure (phenotypic integration) or if they vary independently (modularity). Treating these dimensions as interchangeable or combining them into composite scores may obscure independent pathways of evolutionary potential. The study seeks to determine if activity and exploration are evolutionarily integrated or modular by examining how variation is transmitted across generations.

Methodology
The researchers investigated newborn Trinidadian guppies (Poecilia reticulata) using a nested paternal half-sib breeding design to decouple genetic and non-genetic parental effects.

Breeding Design: Adult males (sires) were sequentially paired with three virgin females (dams) to create paternal half-sib families. Offspring from the same sire but different dams share paternal genes but experience distinct maternal environments. This design allows for the separation of sire-associated variance (genetic and/or paternal effects) from dam-within-sire-associated variance (maternal genetic and/or non-genetic effects).
Subjects: Newborn offspring were tested within three days of birth to minimize the influence of divergent postnatal experiences.
Behavioral Assay: An open-field test was conducted in a circular arena. Two behavioral endpoints were quantified:
1. Activity: The proportion of time spent mobile (speed > 1 mm s⁻¹).
2. Exploration: The proportion of time spent in the central, exposed zone of the arena.
Statistical Analysis: A Bayesian bivariate hierarchical model was employed to partition variance into sire-associated, dam-within-sire-associated, and residual components. The model estimated correlations between activity and exploration at each variance level. The study focused on comparing the ordering of variance partition coefficients (VPC) between the two traits to test for modular versus integrated structures.

Key Results
The study found that activity and exploration exhibit contrasting patterns of familial resemblance, supporting the modular phenotype hypothesis:

Phenotypic Correlation: The two traits were weakly correlated at the phenotypic level (Spearman's $\rho$ = −0.09).
Exploration: Variance in exploration was primarily structured by the sire. The posterior median sire-associated VPC was 0.392, significantly larger than the dam-within-sire VPC (0.047).
Activity: Variance in activity showed the opposite pattern, being primarily structured by the dam. The posterior median dam-within-sire VPC was 0.389, significantly larger than the sire-associated VPC (0.024).
Contrast: The joint posterior probability that these opposing orderings occurred simultaneously was 0.943. Furthermore, the between-trait log variance-ratio contrast (comparing sire-to-dam ratios) was strongly positive (median 5.325), indicating a significantly greater sire-to-dam variance ratio for exploration than for activity.
Robustness: Sensitivity analyses confirmed that these results were not driven by prior specifications or specific paternal families, as the pattern persisted when restricting the analysis to sires with multiple dams or excluding individual sires.

Key Contributions

Decoupling Behavioral Dimensions: The study demonstrates that "activity" and "exploration," often treated as a single behavioral axis or personality trait, can be structurally decoupled.
Trait-Specific Inheritance: It provides empirical evidence that different components of a single locomotor sequence are governed by distinct structures of inclusive inheritance. Exploration appears linked to paternal factors, while activity is linked to maternal factors (which may include maternal genetic effects, prenatal environment, or early postnatal care).
Methodological Application: The paper successfully applies a Bayesian bivariate hierarchical model to partition familial variance in behavioral traits, offering a robust framework for distinguishing between integrated and modular behavioral architectures.

Significance and Claims
The authors claim that these findings indicate a potential evolutionary decoupling between how much an animal moves and where it goes. The modular architecture suggests that different components of a single locomotor sequence can be targeted independently by natural selection. This independence provides a mechanism to bypass rigid behavioral syndromes, thereby facilitating the diversification of complex personality profiles. By showing that these traits are not strictly integrated, the study suggests that the evolutionary potential of complex phenotypes is greater than previously assumed when behaviors are treated as monolithic units. The paper concludes that assessing the structure of familial resemblance is essential for understanding the evolutionary potential of complex behaviors.

Technical Summary: Exploration and Activity Show Contrasting Familial Resemblance

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