Accelerated Brain Shape Evolution Is Associated with Rapid Diversification in an Avian Radiation

Abstract

Niche expansion is a critical step in the speciation process. Large brains linked to improved cognitive ability may enable species to expand their niches and forage in new ways, thereby promoting speciation. Despite considerable work on ecological divergence in brain size and its importance in speciation, relatively little is known about how brain shape relates to behavioral, ecological, and taxonomic diversity at macroevolutionary scales. This is due, in part, to inherent challenges with quantifying brain shape across many species.Here, we present a novel, semiautomated approach for rapidly phenotyping brain shape using semilandmarks derived from X-ray computed micro-tomography (microCT) scans.We then test its utility by parsing evolutionary trends within a diverse radiation of birds, kingfishers (Aves: Alcedinidae). Multivariate comparative analyses reveal that rates of brain shape evolution, but not beak shape, are positively correlated with lineage diversification rates. Distinct brain shapes are further associated with changes in body size and foraging behavior, suggesting both allometric and ecological constraints on brain shape evolution. These results are in line with the idea of brains acting as a "master regulator" of critical processes governing speciation, such as dispersal, foraging behavior, and dietary niche.

A brain-wide analysis maps structural evolution to distinct anatomical modules

“…Previous studies examining variation in the brain have mostly focused on volume or shape, with few providing a comparison of how shape and volume vary brain-wide (1, 2, 6, 14, 31). We sought to examine whether shape variation follows similar patterns as volume, suggesting shared origins of variation, or whether shape and volume were unrelated.…”

“…The small size of the larval fish permits brain wide imaging, and thus all experiments were done in 6 dpf larvae (Fig 1a). To produce a segmented atlas for cave and surface Astyanax, we used a previously published neuroanatomical atlas from a related fish, the common zebrafish (Danio rerio) 1,2 , that is neuroanatomically homologous with A. mexicanus 3 . The zebrafish brain browser (zbb) brain atlas was constructed using 210 unique neuroanatomical markers, that culminated in the segmentation of 180 different brain regions [4][5][6] .…”

“…Brain anatomy is highly variable across the animal kingdom, yet little is known about the general evolutionary principles driving anatomical evolution of the brain (1-5). Comparative studies have provided insight into evolutionary and developmental mechanisms influencing anatomical change, but a lack of direct genetic and functional experiments across species have remained a major impediment.…”

An atlas of the developing Tribolium castaneum brain reveals conservation in anatomy and divergence in timing to Drosophila melanogaster

“…The evolutionary connection between shape differences and their functional consequences seems to be more difficult to understand. Despite efforts in vertebrate brain evolution to identify such links (Eliason et al., 2021; Sansalone et al., 2020), corresponding efforts in arthropod evolution are rare. We assume that selection acts firstly on dimensions such as cell number, proliferation rate, as well as changes, truncation, or multiplication of connections.…”

An atlas of the developing Tribolium castaneum brain reveals conserved anatomy and divergent timing to Drosophila melanogaster

“…The evolutionary connection between shape differences and their functional consequences seems to be more difficult to understand. Despite efforts in vertebrate brain evolution to identify such links (Eliason et al, 2021;Sansalone et al, 2020), corresponding efforts in arthropod evolution are rare. We assume that selection acts firstly on dimensions such as cell number, proliferation rate, as well as changes, truncation, or multiplication of connections.…”