Novel neuroanatomical integration and scaling define avian brain shape evolution and development.

Akinobu Watanabe,Mark A Norell,Paul M Gignac,M Eugenia L Gold,Amy M Balanoff

doi:10.7554/elife.68809

Abstract

How do large and unique brains evolve? Historically, comparative neuroanatomical studies have attributed the evolutionary genesis of highly encephalized brains to deviations along, as well as from, conserved scaling relationships among brain regions. However, the relative contributions of these concerted (integrated) and mosaic (modular) processes as drivers of brain evolution remain unclear, especially in non-mammalian groups. While proportional brain sizes have been the predominant metric used to characterize brain morphology to date, we perform a high-density geometric morphometric analysis on the encephalized brains of crown birds (Neornithes or Aves) compared to their stem taxa-the non-avialan coelurosaurian dinosaurs and Archaeopteryx. When analyzed together with developmental neuroanatomical data of model archosaurs (Gallus, Alligator), crown birds exhibit a distinct allometric relationship that dictates their brain evolution and development. Furthermore, analyses by neuroanatomical regions reveal that the acquisition of this derived shape-to-size scaling relationship occurred in a mosaic pattern, where the avian-grade optic lobe and cerebellum evolved first among non-avialan dinosaurs, followed by major changes to the evolutionary and developmental dynamics of cerebrum shape after the origin of Avialae. Notably, the brain of crown birds is a more integrated structure than non-avialan archosaurs, implying that diversification of brain morphologies within Neornithes proceeded in a more coordinated manner, perhaps due to spatial constraints and abbreviated growth period. Collectively, these patterns demonstrate a plurality in evolutionary processes that generate encephalized brains in archosaurs and across vertebrates.

Highlights

The human brain, with its inflated cerebrum, is often considered the zenith of brain evolution
When morphospaces are constructed for locally aligned shape data of individual brain regions, cerebrum and optic lobe shapes largely separate Alligator, non-avialan coelurosaurs, and crown birds (Figure 2b,c), whereas cerebellum and medulla shapes partially overlap between these major clades (Figure 2d,e)
Our results indicate that crown birds (i) follow a distinct brain shape-to-size scaling relationship and (ii) possess a more integrated brain structure compared to non-avialan archosaurs that (iii) uniquely characterizes their brain development and evolution

Summary

Introduction

The human brain, with its inflated cerebrum, is often considered the zenith of brain evolution. Crown birds offer an excellent comparative system to mammals, even primates, because they share neuroanatomical features that evolved independently, including a relatively large brain size (Jerison, 1973; Nieuwenhuys et al, 1998; Northcutt, 2002; Butler and Hodos, 2005; Iwaniuk et al, 2005; Gill, 2006), globular brains with expanded cerebra, specialized cytoarchitecture and neuron types (Reiner et al, 2004; Dugas-Ford et al, 2012; Shanahan et al, 2013; Pfenning et al, 2014; Karten, 2015; Stacho et al, 2020), and the capacity to perform higher cognitive behaviors (Lefebvre et al, 2002; Weir et al, 2002; Emery, 2006; Auersperg et al, 2012; Kabadayi et al, 2016; Bayern et al, 2018; Boeckle et al, 2020). They feature remarkable variation in brain morphology that is conducive to macroevolutionary studies (Iwaniuk and Hurd, 2005; Figure 1)

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Results

Conclusion