2021•Brain Behavior and EvolutionOpen access

Exceptionally Steep Brain-Body Evolutionary Allometry Underlies the Unique Encephalization of Osteoglossiformes

Masahito Tsuboi

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Abstract

Brain-body static allometry, which is the relationship between brain size and body size within species, is thought to reflect developmental and genetic constraints. Existing evidence suggests that the evolution of large brain size without accompanying changes in body size (that is, encephalization) may occur when this constraint is relaxed. Teleost fish species are generally characterized by having close-fitting brain-body static allometries, leading to strong allometric constraints and small relative brain sizes. However, one order of teleost, Osteoglossiformes, underwent extreme encephalization, and its mechanistic bases are unknown. Here, I used a dataset and phylogeny encompassing 859 teleost species to demonstrate that the encephalization of Osteoglossiformes occurred through an increase in the slope of evolutionary (among-species) brain-body allometry. The slope is virtually isometric (1.03 ± 0.09 SE), making it one of the steepest evolutionary brain-body allometric slopes reported to date, and it deviates significantly from the evolutionary brain-body allometric slopes of other clades of teleost. Examination of the relationship between static allometric parameters (intercepts and slopes) and evolutionary allometry revealed that the dramatic steepening of the evolutionary allometric slope in Osteoglossiformes was a combined result of evolution in the slopes and intercepts of static allometry. These results suggest that the evolution of static allometry, which likely has been driven by evolutionary changes in the rate and timing of brain development, has facilitated the unique encephalization of Osteoglossiformes.

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Brain-body static allometry, which is the relationship between brain size and body size within species, is thought to reflect developmental and genetic constraints. Existing evidence suggests that the evolution of large brain size without accompanying changes in body size (that is, encephalization) may occur when this constraint is relaxed. Teleost fish species are generally characterized by having close-fitting brain-body static allometries, leading to strong allometric constraints and small relative brain sizes. However, one order of teleost, Osteoglossiformes, underwent extreme encephalization, and its mechanistic bases are unknown. Here, I used a dataset and phylogeny encompassing 859 teleost species to demonstrate that the encephalization of Osteoglossiformes occurred through an increase in the slope of evolutionary (among-species) brain-body allometry. The slope is virtually isometric (1.03 ± 0.09 SE), making it one of the steepest evolutionary brain-body allometric slopes reported to date, and it deviates significantly from the evolutionary brain-body allometric slopes of other clades of teleost. Examination of the relationship between static allometric parameters (intercepts and slopes) and evolutionary allometry revealed that the dramatic steepening of the evolutionary allometric slope in Osteoglossiformes was a combined result of evolution in the slopes and intercepts of static allometry. These results suggest that the evolution of static allometry, which likely has been driven by evolutionary changes in the rate and timing of brain development, has facilitated the unique encephalization of Osteoglossiformes.

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Available abstract

Brain-body static allometry, which is the relationship between brain size and body size within species, is thought to reflect developmental and genetic constraints. Existing evidence suggests that the evolution of large brain size without accompanying changes in body size (that is, encephalization) may occur when this constraint is relaxed. Teleost fish species are generally characterized by having close-fitting brain-body static allometries, leading to strong allometric constraints and small relative brain sizes. However, one order of teleost, Osteoglossiformes, underwent extreme encephalization, and its mechanistic bases are unknown. Here, I used a dataset and phylogeny encompassing 859 teleost species to demonstrate that the encephalization of Osteoglossiformes occurred through an increase in the slope of evolutionary (among-species) brain-body allometry. The slope is virtually isometric (1.03 ± 0.09 SE), making it one of the steepest evolutionary brain-body allometric slopes reported to date, and it deviates significantly from the evolutionary brain-body allometric slopes of other clades of teleost. Examination of the relationship between static allometric parameters (intercepts and slopes) and evolutionary allometry revealed that the dramatic steepening of the evolutionary allometric slope in Osteoglossiformes was a combined result of evolution in the slopes and intercepts of static allometry. These results suggest that the evolution of static allometry, which likely has been driven by evolutionary changes in the rate and timing of brain development, has facilitated the unique encephalization of Osteoglossiformes.

Key concepts: Allometry, Encephalization, Brain size, Biology, Evolutionary biology, Zoology, Phylogenetics, Ecology

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