Multiphase progenetic development shaped the brain of flying archosaurs

Abstract

The growing availability of virtual cranial endocasts of extinct and extant vertebrates has fueled the quest for endocranial characters that discriminate between phylogenetic groups and resolve their neural significances. We used geometric morphometrics to compare a phylogenetically and ecologically comprehensive data set of archosaurian endocasts along the deep evolutionary history of modern birds and found that this lineage experienced progressive elevation of encephalisation through several chapters of increased endocranial doming that we demonstrate to result from progenetic developments. Elevated encephalisation associated with progressive size reduction within Maniraptoriformes was secondarily exapted for flight by stem avialans. Within Mesozoic Avialae, endocranial doming increased in at least some Ornithurae, yet remained relatively modest in early Neornithes. During the Paleogene, volant non-neoavian birds retained ancestral levels of endocast doming where a broad neoavian niche diversification experienced heterochronic brain shape radiation, as did non-volant Palaeognathae. We infer comparable developments underlying the establishment of pterosaurian brain shapes.

Beyond Endocasts: Using Predicted Brain-Structure Volumes of Extinct Birds to Assess Neuroanatomical and Behavioral Inferences

“…Thus, it is likely that our extinct sample does not capture the period in avian evolution during which the hyperpallium was expanding to the size seen in most birds today. The hyperpallium is also hypothesized to have been key to avian diversification and success after the K-Pg extinction [14,19], so there may be selective pressure to maintain a minimum size of this avian brain structure.…”

“…Walsh et al [48] argued that the lack of a Wulst in the Cretaceous bird Cerebravis and the weak development of the Wulsts present on the endocasts of some early Cenozoic birds [19,20] do not support the interpretation of a Wulst in Archaeopteryx. Recently, Beyrand et al [14] subjected the London specimen and another specimen of Archaeopteryx (the Munich specimen) to synchrotron propagation phase-contrast X-ray microtomography, revealing that the putative Wulst feature in the London specimen is in fact a fracture and that the corresponding but unbroken surface of the Munich specimen shows no evidence of the Wulst.…”

“…Given the correlations found with higher-order behavioral traits associated with intelligence and relative brain volume (summarized in [7]), encephalization (i.e., the size of the brain relative to the body) has been a major topic of interest in endocast studies [8][9][10]. The overall shape of the endocast and how that shape correlates with behavioral and life-history traits have become more available for analysis with the advent of 3D geometric morphometric techniques [11][12][13][14]. The most common approach in endocast studies has been to describe a fossil endocast in comparison with its living relatives, both in terms of general morphology and relative size of discrete structures [7,9,11,[15][16][17][18][19][20][21][22][23][24][25][26].…”

Endocast structures are reliable proxies for the sizes of corresponding regions of the brain in extant birds

“…The majority of the Wulst is hyperpallium, which is analogous, and potentially homologous, to the mammalian primary visual, somatosensory, and motor cortices (Funke, 1989; Deng and Wang, 1993; Wild, 1997; Medina and Reiner, 2000; Wild and Williams, 2000; Manger et al, 2002; Reiner et al, 2005). The hyperpallium is a strictly avian brain region that is not present in the forebrains of nonavian reptiles or other vertebrates (Jarvis, 2009), so the presence and expansion of the Wulst is considered to be a hallmark of avian brain evolution (Walsh and Milner, 2011a; Balanoff et al, 2013; Beyrand et al, 2019). Although the hyperpallium is multifunctional, based on both hodology (i.e., neural pathways) and neurophysiology (Funke, 1989; Deng and Wang, 1993; Wild, 1997; Medina and Reiner, 2000; Wild and Williams, 2000; Manger et al, 2002; Reiner et al, 2005), the majority of studies have focused on its functions in visual processing.…”

Volume Tensor Estimation Using a Virtual Line Grid: Study of a Developing Pheasant Brain

“…It can be used to efficiently measure the shapes of pheasant brain compartments and detect changes in shapes of the pheasant forebrain and hindbrain during development (Tables 3 & 4). The results may be of particular benefit for interpreting the fossilised braincases of extinct birds and dinosaurs (Beyrand, 2019).…”