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

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Beyond Endocasts: Using Predicted Brain-Structure Volumes of Extinct Birds to Assess Neuroanatomical and Behavioral Inferences diversity Article Beyond Endocasts: Using Predicted Brain-Structure Volumes of Extinct Birds to Assess Neuroanatomical and Behavioral Inferences 1, , 2 2 Catherine M. Early * y , Ryan C. Ridgely and Lawrence M. Witmer 1 Department of Biological Sciences, Ohio University, Athens, OH 45701, USA 2 Department of Biomedical Sciences, Heritage College of Osteopathic Medicine, Ohio University, Athens, OH 45701, USA; [email protected] (R.C.R.); [email protected] (L.M.W.) * Correspondence: [email protected] Current Address: Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA. y Received: 1 November 2019; Accepted: 30 December 2019; Published: 17 January 2020 Abstract: The shape of the brain influences skull morphology in birds, and both traits are driven by phylogenetic and functional constraints. Studies on avian cranial and neuroanatomical evolution are strengthened by data on extinct birds, but complete, 3D-preserved vertebrate brains are not known from the fossil record, so brain endocasts often serve as proxies. Recent work on extant birds shows that the Wulst and optic lobe faithfully represent the size of their underlying brain structures, both of which are involved in avian visual pathways. The endocasts of seven extinct birds were generated from microCT scans of their skulls to add to an existing sample of endocasts of extant birds, and the surface areas of their Wulsts and optic lobes were measured. A phylogenetic prediction method based on Bayesian inference was used to calculate the volumes of the brain structures of these extinct birds based on the surface areas of their overlying endocast structures. This analysis resulted in hyperpallium volumes of five of these extinct birds and optic tectum volumes of all seven extinct birds. Phylogenetic ANCOVA (phyANCOVA) were performed on regressions of the brain-structure volumes and endocast structure surface areas on various brain size metrics to determine if the relative sizes of these structures in any extinct birds were significantly different from those of the extant birds in the sample. Phylogenetic ANCOVA indicated that no extinct birds studied had relative hyperpallial volumes that were significantly different from the extant sample, nor were any of their optic tecta relatively hypertrophied. The optic tectum of Dinornis robustus was significantly smaller relative to brain size than any of the extant birds in our sample. This study provides an analytical framework for testing the hypotheses of potential functional behavioral capabilities of other extinct birds based on their endocasts. Keywords: endocast; neuroanatomy; brain; bird; evolution 1. Introduction Our deep fascination with extinct animals such as dinosaurs is driven not by their dry bones that remain with us today but by thinking of them as living and breathing animals, interacting with each other and their environments. These interactions are determined by the various behaviors in which organisms engage, which are in turn enabled by the functional capabilities of their brains. The brain-behavior connection in extant and extinct organisms has led to rapid growth of the field of comparative neuroanatomy [1–3]. In this field, correlations are drawn between the size of a brain structure in a species of extant animal and the relative emphasis on the behavior it mediates. Efforts to use these correlations to infer functional capabilities in extinct animals have been stymied by the fact that whole soft-tissue organs, including the brain, do not preserve in three dimensions in the fossil Diversity 2020, 12, 34; doi:10.3390/d12010034 www.mdpi.com/journal/diversity Diversity 2020, 12, 34 2 of 23 Diversity 2020, 12, x FOR PEER REVIEW 2 of 23 record.fact that The whole fossil soft record-tissue is organs, much betterincluding at preserving the brain, do hard not tissues preserve such in asthree bone, dimensions and fortunately, in the thefossil brain record. is surrounded The fossil record by bone is much to varying better at extents. preserving The hard space tissues within such these as bone, bones and constitutes fortunately, the endocranialthe brain is cavity, surrounded which canby bone then to serve varying as a mold extents. to generate The space a brain within endocast these bones (or simply constitutes “endocast” the forendocranial the remainder cavity, of which this article). can then These serve can as a be mold physical to generate endocasts a brain (e.g., endocast latex; [ 4(or]) or,simply more “endocast” commonly infor recent the remainder years, virtual of this endocasts article). These reconstructed can be physical from computed endocasts tomography (e.g., latex; [4 (CT),]) or, amore non-destructive commonly samplingin recent techniqueyears, virtual [5]. endocasts The endocast reconstructed can be a very from accurate computed representation tomography of the(CT), size a non and-destructive shape of the externalsampling surface technique of the [5] brain. Thein endocast birds [6 ].can be a very accurate representation of the size and shape of the externalThe fidelity surface of the of avianthe brain endocasts in birds to [6] their. brains, and the fact that the endocast is the most direct evidenceThe of fidelity neuroanatomy of the avian available endocasts from to the their fossil brains, record, and has the ledfact many that the researchers endocast tois makethe most inferences direct aboutevidence behavior of neuroanatomy from the endocasts available of the from few the extinct fossil birds record, with three-dimensionallyhas led many researchers preserved to make skulls. Giveninferences thecorrelations about behavior found from with the higher-order endocasts of behavioral the few extinct traits associatedbirds with withthree intelligence-dimensionally and relativepreserved brain skulls. volume Given (summarized the correlations in [7 ]),found encephalization with higher- (i.e.,order the behavioral size of the traits brain associated relative towith the body)intelligence has been and a relative major topic brain of volume interest (summarized in endocaststudies in [7]), encephalization [8–10]. The overall (i.e., shape the size of theof the endocast brain andrelativ howe to that the shapebody) correlateshas been a with major behavioral topic of interest and life-history in endocast traits studies have [8– become10]. The more overall available shape forof analysisthe endocast with and the adventhow that of shape 3D geometric correlates morphometric with behavioral techniques and life- [history11–14]. traits The mosthave commonbecome approachmore available in endocast for analysis studies with has the been advent to describe of 3D geometric a fossil endocastmorphometric in comparison techniques with [11– its14] living. The relatives,most common both inapproach terms of in general endocast morphology studies has andbeen relative to describe size a of fossil discrete endocast structures in comparison [7,9,11,15 with–26 ]. Theseits living studies relatives, have allowed both in researchers terms of general to document morphology trends in and avian relative brain evolutionsize of discrete by using structures endocast morphology[7,9,11,15–26] as. These a proxy studies for neuroanatomy. have allowed Often,researchers they to link document the relative trends size in of avian an endocast brain evolution structure toby the using importance endocast of morphology the function as mediated a proxy for by neuroanatomy. its underlying brainOften, structure they link in the the relative extinct size species of an as comparedendocast structure to its extant to the relatives. importance of the function mediated by its underlying brain structure in the extinctOne species of the as endocast compared structures to its extant frequently relatives. used to infer behavior or functional capabilities is the sagittalOne eminence, of the endocast or Wulst structures (Figure1). frequently Its underlying used brainto infer structure, behavior the or hyperpallium,functional capabilities is the target is the of thesagittal thalamofugal eminence, visual or Wulst pathway, (Figure the 1). other Its underlying visual pathway brain in structure, birds. The the thalamofugal hyperpallium, visual is the pathway target hasof the been thalamofugal linked to perception visual pathway, of illusory the other contours visual [27 pathway], pattern in discrimination birds. The thalamofugal at a distance visual [28], higher-levelpathway has motion been linked integration to perception [29], spatial of illusory orientation contours [30 [27]], and, pattern visual discrimination magnetoreception at a distance [31,32 ]. Although[28], higher portions-level ofmotion the hyperpallium integration [29] are,also spatial involved orientation in somatosensation [30], and visual and magnetoreception motor control, it is still[31,32] thought. Although that the portions majority of of the this hyperpallium structure is devoted are also to involved integrating in somatosensation visual information and [33 motor]. Asa result,control, the it size is ofstill the thought Wulst on that an endocastthe majority is often of interpretedthis structure as correlating is devoted with to visualintegrating capabilities visual in extinctinformation birds. [33] Similar. As a to result, the optic the size lobe, of the the expansion Wulst on an of endocast the Wulst is (and often presumably, interpreted itsas correlating underlying brainwith structure)visual capabilities is a characteristic in extinct trait birds. of avian Similar brain to evolutionthe
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