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

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.

The costs and benefits of larger brains in fishes

“…This is of particular interest, because fish brains continue to show high levels of neurogenesis also in adulthood, in stark contrast to the very limited cellular development and regeneration of adult avian and mammalian brains (Zupanc & Horschke, 1995; Ganz & Brand, 2016). By extending the potential timeframe for brain growth, this may alter the costs and benefits of large brains in fishes (Tsuboi, 2021), despite the allometric relationships between body mass and brain mass in adults being similar for all vertebrate classes (Tsuboi et al, 2018). After initial examination of the data, we thus selected six ecological/phenotypic traits relevant to the above hypotheses, and devised three principal models to correlate these traits with brain weight, the most widely available measure of brain size, in a phylogenetically controlled way.…”

Convergent mosaic brain evolution is associated with the evolution of novel electrosensory systems in teleost fishes

“…A recent study found a steeper brain–body allometric relationship for osteoglossiforms compared to other actinopterygians, but not for seven other focal ray-finned fish orders, which may, in part, be driven by the highly speciose mormyroids ( Tsuboi, 2021 ). To determine if the evolution of an electrosensory system is associated with extreme encephalization or shifts in brain–body allometric relationships, we combined our data with published brain and body mass data across ray-finned fishes ( Tsuboi, 2021 ; Tsuboi et al, 2018 ), which resulted in a combined dataset of 870 species across 46 orders, with phylogenetic data from a previously assembled time-calibrated phylogeny ( Rabosky et al, 2018 ). We used Bayesian reversible-jump bivariate multiregime Ornstein–Uhlenbeck modeling (OUrjMCMC; Uyeda et al, 2017 ) to identify shifts in both y-intercept and slope of brain–body allometric relationships.…”

“…Indeed, when we allow only intercept to vary between grades while assuming parallel slopes, we no longer detect any reliable grade shifts within actinopterygians. Even when allowing slope to vary, two of our identified shifts were undetectable when assuming the brain–body allometry is constant within orders despite analyzing much of the same data ( Tsuboi, 2021 ).…”

“…To explicitly address whether shifts in the allometric relationship are associated with the evolution of electrosensory phenotypes, we ran OUrjMCMC models with fixed shifts for lineages that evolved ampullary electroreceptors, lineages that evolved tuberous electroreceptors, and lineages that evolved electrogenesis in addition to the following null hypotheses: a fixed shift at the branch leading to osteoglossiforms as found previously ( Tsuboi, 2021 ), only shifts in the allometric relationship for intercept but not slope, and a single allometric relationship across all taxa. We found that the model with eight shifts provided the best fit to the data (2ln(BF)>28; Figure 3—source data 4 ).…”

“…After constraint on total brain size was added in a bare-bones model of brain region evolutionary dynamics, the probability of mosaic evolution increased under most tested scenarios ( Avin et al, 2021 ). The decoupling of brain–body allometries has been reported in birds and mammals, whereas actinopterygians are consistently found to have more constrained allometric relationships, whether through explicit constraints or strong stabilizing selection ( Tsuboi, 2021 ; Tsuboi et al, 2018 ). Thus, it is entirely possible that the interactions of both region size and total brain size scaling may increase the likelihood of gross-scale mosaic brain evolution in fishes relative to birds and mammals.…”