Brain morphology predicts social intelligence in wild cleaner fish

Zegni Triki,Redouan Bshary,Yasmin Emery,Rui F Oliveira,Magda C Teles

doi:10.1038/s41467-020-20130-2

Abstract

It is generally agreed that variation in social and/or environmental complexity yields variation in selective pressures on brain anatomy, where more complex brains should yield increased intelligence. While these insights are based on many evolutionary studies, it remains unclear how ecology impacts brain plasticity and subsequently cognitive performance within a species. Here, we show that in wild cleaner fish (Labroides dimidiatus), forebrain size of high-performing individuals tested in an ephemeral reward task covaried positively with cleaner density, while cerebellum size covaried negatively with cleaner density. This unexpected relationship may be explained if we consider that performance in this task reflects the decision rules that individuals use in nature rather than learning abilities: cleaners with relatively larger forebrains used decision-rules that appeared to be locally optimal. Thus, social competence seems to be a suitable proxy of intelligence to understand individual differences under natural conditions.

Highlights

It is generally agreed that variation in social and/or environmental complexity yields variation in selective pressures on brain anatomy, where more complex brains should yield increased intelligence
We investigated whether variation in social complexity and brain morphology together can predict cognitive performance in a wild population of cleaner fish Labroides dimidiatus
We find that large forebrains enable individuals to show social competence by performing locally adaptive decision-rules, suggesting forebrain size is important for complex social decisionmaking

Summary

Introduction

It is generally agreed that variation in social and/or environmental complexity yields variation in selective pressures on brain anatomy, where more complex brains should yield increased intelligence While these insights are based on many evolutionary studies, it remains unclear how ecology impacts brain plasticity and subsequently cognitive performance within a species. We show that in wild cleaner fish (Labroides dimidiatus), forebrain size of highperforming individuals tested in an ephemeral reward task covaried positively with cleaner density, while cerebellum size covaried negatively with cleaner density This unexpected relationship may be explained if we consider that performance in this task reflects the decision rules that individuals use in nature rather than learning abilities: cleaners with relatively larger forebrains used decision-rules that appeared to be locally optimal. One relevant laboratory-based task that simulates the situation where a resident and a visitor client simultaneously seek cleaning services is called the biological market or ephemeral reward task

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