“Condylarth” Carsioptychus Coarctatus: Implications for Early Placental Mammal Neurosensory Biology and Behavior
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THE ANATOMICAL RECORD (2018) The Brain and Inner Ear of the Early Paleocene “Condylarth” Carsioptychus coarctatus: Implications for Early Placental Mammal Neurosensory Biology and Behavior 1 1 2 JOE CAMERON, SARAH L. SHELLEY, THOMAS E. WILLIAMSON, AND STEPHEN L. BRUSATTE 1,2* 1School of GeoSciences, University of Edinburgh, Grant Institute, Edinburgh, Scotland, UK 2New Mexico Museum of Natural History and Science, Albuquerque, New Mexico ABSTRACT Mammals underwent a profound diversification after the end-Cretaceous mass extinction, with placentals rapidly expanding in body size and diver- sity to fill new niches vacated by dinosaurs. Little is known, however, about the brains and senses of these earliest placentals, and how neurosensory features may have promoted their survival and diversification. We here use computed tomography (CT) to describe the brain, inner ear, sinuses, and endocranial nerves and vessels of Carsioptychus coarctatus, a peripty- chid “condylarth” that was among the first placentals to blossom during the few million years after the extinction, in the Paleocene. Carsioptychus has a generally primitive brain and inner ear that is similar to the inferred ancestral eutherian/placental condition. Notable “primitive” features include the large, anteriorly expanded, and conjoined olfactory bulbs, pro- portionally small neocortex, lissencephalic cerebrum, and large hindbrain compared to the cerebrum. An encephalization quotient (EQ) cannot be confidently calculated because of specimen crushing but was likely very small, and comparisons with other extinct placentals reveal that many Paleocene “archaic” mammals had EQ values below the hallmark threshold of modern placentals but within the zone of nonmammalian cynodonts, indicative of small brains and low intelligence. Carsioptychus did, however, have a “conventional” hearing range for a placental, but was not particu- larly agile, with semicircular canal dimensions similar to modern pigs. This information fleshes out the biology of a keystone Paleocene “archaic” pla- cental, but more comparative work is needed to test hypotheses of how neu- rosensory evolution was related to the placental radiation. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Grant sponsor: Bureau of Land Management; Grant sponsor: *Correspondence to: Stephen L. Brusatte, School of GeoS- Natural Environment Research Council; Grant sponsor: Univer- ciences, University of Edinburgh, Grant Institute, James Hutton sity of Edinburgh School of GeoSciences, National Science Foun- Road, Edinburgh EH9 3FE, Scotland, UK. E-mail: stephen. dation; Grant numbers: DEB 1654952, EAR-1325544; Grant [email protected] sponsor: European Research Council (ERC) under the European Received 6 December 2017; Revised 4 April 2018; Accepted 16 Union’s Horizon 2020 Research and Innovation Programme; April 2018. Grant number: 756226; Grant sponsor: Marie Curie Career Inte- DOI: 10.1002/ar.23903 gration Grant; Grant number: 630652; Grant sponsor: Royal Published online 00 Month 2018 in Wiley Online Library Society Research Grant; Grant number: RG130018. (wileyonlinelibrary.com). © 2018 WILEY PERIODICALS, INC. 2 CAMERON ET AL. Key words: mammal; placental; sensory evolution; neuroanat- omy; CT scanning; end-Cretaceous extinction The end-Cretaceous extinction, 66 million years ago, ancestors of modern perissodactyls and artiodactyls was a pivotal event in mammalian history. The first (Prothero et al., 1988; Rose, 2006). placentals—species, like humans, that give live-birth to “Condylarths” are therefore pivotal for understanding well-developed young—probably originated during the the evolution of the earliest placentals after the dino- Late Cretaceous, but then rapidly diversified to fill new saur extinction. But, although they are represented by a niches in the ensuing Paleocene, after the nonavian dino- rich fossil record, there has been scant work on their saurs went extinct (Murphy et al., 2001; Meredith et al., neurosensory biology. Over the last few years, some 2011; dos Reis et al., 2012, 2014; Liu et al., 2017). Studies studies have used computed tomography (CT) to recon- have shown that mammalian taxonomic diversity, body struct the brains and sense organs of the “condylarth” size, morphological disparity, and evolutionary rates Hyopsodus (Orliac et al., 2012a; Ravel and Orliac, increased after the extinction of the nonavian dinosaurs 2015), and other Paleocene “archaic” mammals (Muizon (Alroy, 1999; Slater, 2013; Grossnickle and Newham, et al., 2015; Orliac and O’Leary, 2016; Napoli et al., 2016; Halliday et al., 2016; Halliday and Goswami, 2018), which gives insight into their intelligence and 2016a, 2016b), but nonetheless, many questions remain sensory abilities. However, similar studies on other key about the timing, pace, and drivers of the placental radia- “condylarths” are needed, particularly exemplars of the “ ” tion (Archibald and Deutschman, 2001; Goswami, 2012; major condylarth subgroups, to gauge variation among O’Leary et al., 2013). the earliest placentals and better test hypotheses of Certain biological attributes of placental mammals how their neurosensory biology was related to extinction may have aided their survival during the end-Cretaceous and survivorship. fi extinction and/or promoted their diversification in the Here, for the rst time, we use CT data to describe the aftermath (Wilson, 2013). Recent work has focused on life brain, inner ear, sinuses, and endocranial nerves and ves- history traits such as nocturnal versus diurnal activity sels of a periptychid. Periptychidae is one of the major “ ” patterns (Maor et al., 2017; Wu et al., 2017). Much less condylarth subclades, and is recognized by a distinctive dentition and generalized terrestrial body plan (Shelley, attention has focused on neurosensory systems. Modern fi mammals have the proportionally largest brains relative 2017). The group diversi ed into ~45 species of small-to- to body size of any vertebrates, and a novel elaboration of medium-sized taxa in the very earliest Paleocene of North America, during the first ~4 million years after the end- the forebrain called the neocortex, which imparts height- Cretaceous extinction (Shelley et al., 2018; Matthew, ened intelligence, memory, and senses (Jerison, 1973; 1937; Archibald, 1998; Rose, 2006; Shelley, 2017). Using Nieuwenhuys et al., 1998). It is now well understood that high-resolution X-ray CT scans, we digitally visualize and this basic neurosensory bauplan was established early in describe the internal endocranial morphology of one of mammalian history, in Triassic and Jurassic taxa on the the best preserved periptychid skulls, a specimen of Car- stem lineage toward crown mammals (Rowe, 1996; Rowe fi sioptychus coarctatus (AMNH 27601). We make compari- et al., 2011). Similarly, other studies have identi ed sons to other mammals, both modern and extinct, and major elaborations to this bauplan during the early evolu- use numerical methods to estimate the general intelli- tion of modern placental orders such as artiodactyls, gence, hearing range, and agility of Carsioptychus. This rodents, and primates, most notably increases in ence- gives important new insight into the brains, senses, and phalization and the size of the neocortex (Silcox et al., neurosensory capabilities of some of the very first placen- 2009b; Orliac and Gilissen, 2012; Bertrand et al., 2016). tals to flourish after the dinosaur extinction. However, comparatively little is known about the brains Institutional abbreviations—AMNH, American and senses of the oldest placentals. Museum of Natural History, New York, NY; YPM, Pea- This gap in our knowledge largely stems from our poor body Museum of Natural History, Yale University, New understanding of the mammals that prospered during the Haven, CT. first ca. 10 million years after the end-Cretaceous extinc- tion, in the Paleocene (Williamson, 1996; Rose, 2006). MATERIALS AND METHODS There is a great diversity of these mammals, many of which likely belong to early diverging placental sub- Fossil Specimen groups, but much about their anatomy, phylogenetic rela- This study is based on part of AMNH 27601, a moder- tionships, and biology remains mysterious. Many of them ately complete cranium of the periptychid “condylarth” are so-called “archaic” species, which were clearly larger mammal Carsioptychus coarctatus (Fig. 1). The specimen, and more diverse than their Cretaceous forebears, but which consists of a partial skull and associated hind limb, whose relationships to the modern placental orders are was collected by George Gaylord Simpson in 1929 from contentious (see review in Rose, 2006). Perhaps the most the Nacimineto Formation at Barrel Springs Arroyo in notorious of these “archaic” placentals are the what is now the Bisti/De-na-zin Wilderness area of the “condylarths,” a nebulous assemblage of hundreds of spe- San Juan Basin, NM (Simpson, 1936a). The specimen is cies that were prevalent during the Paleocene and from either the lower or the upper fossil horizon (fossil Eocene. They are often considered to be primitive zone A or B: Williamson, 1996, fig. 18) and so is either ungulate-like mammals, and probably include the middle or late Puercan (Pu2 or Pu3) in age (Lofgren NEUROSENSORY ANATOMY OF EARLY PLACENTAL MAMMAL 3 Fig. 1. The cranium of the periptychid “condylarth” mammal Carsioptychus coarctatus (AMNH 27601) in dorsal (A), ventral (B), right lateral (C), and left lateral (D) views. Abbreviations: al, alisphenoid; ar, auditory region (promontorium of petrosal); bo, basioccipital;