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Anatomy of the Petrosal and Middle Ear of the Brown Rat, Rattus Norvegicus (Berkenhout, 1769) (Rodentia, Muridae)

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Anatomy of the Petrosal and Middle Ear of the Brown Rat, Rattus Norvegicus (Berkenhout, 1769) (Rodentia, Muridae) ANNALS OF CARNEGIE MUSEUM VOL. 86, NUMBER 1, PP. 1–35 31 MARCH 2020 ANATOMY OF THE PETROSAL AND MIDDLE EAR OF THE BROWN RAT, RATTUS NORVEGICUS (BERKENHOUT, 1769) (RODENTIA, MURIDAE) JOHN R. WIBLE Curator, Section of Mammals, Carnegie Museum of Natural History 5800 Baum Boulevard, Pittsburgh, Pennsylvania 15206 SARAH L. SHELLEY Postdoctoral Fellow, Section of Mammals, Carnegie Museum of Natural History 5800 Baum Boulevard, Pittsburgh, Pennsylvania 15206 ABSTRACT The anatomy of the petrosal and associated middle ear structures are described and illustrated for the brown rat, Rattus norvegicus (Berkenhout, 1769). Although the middle ear in this iconic mammal has been treated by prior authors, there has not been a comprehensive, well-illustrated contribution using current anatomical terminology. Descriptions are based on specimens from the osteological collections of the Section of Mammals, Carnegie Museum of Natural History, and a CT scanned osteological specimen from the Texas Memorial Museum. The petrosal, ectotympanic, malleus, incus, stapes, and inner ear were segmented from the CT scans. The petrosal of the brown rat is only loosely attached to the cranium, primarily along its posterior border; it is separated from the basisphe- noid, alisphenoid, and squamosal by a large piriform fenestra that transmits various neurovascular structures including the postglenoid vein. The extent of the piriform fenestra broadly exposes the tegmen tympani of the petrosal in lateral view. The floor of the middle ear is formed by the expanded ectotympanic bulla, which is tightly held to the petrosal with five points of contact. The surfaces of the petrosal affording contact with the ectotympanic bulla are the rostral tympanic process, the epitympanic wing, the tegmen tympani, two of the three parts of the caudal tympanic process, and the tympanohyal, with the ectotympanic fused to the last. The ectotympanic in turn is fused to the elongate rostral process of the malleus, which is only discoverable through the study of juvenile specimens. In addition to osteology, the major nerves, arteries, and veins of the petrosal are described and illustrated based on the literature and osteological correlates. The petrosal of the brown rat is compared with those of several Eocene rodents to put the extant form in the context of early members of the rodent lineage. Comparisons benefitted from CT scans of the middle Eocene ischromyoid Paramys delicatus Leidy, 1871, from the western United States, affording the first description of the endocranial surface of the petrosal in an Eocene rodent. The petrosals in the Eocene fossils are more tightly held in the cranium, but the ectotympanic contacts the petrosal through the same five points, with some modifications. The most unexpected discovery in Paramys delicatus was the presence of a prominent tentorial process of the parietal in contact with the reduced crista petrosa. KEY WORDS: basicranium, brown rat, Eocene, middle ear anatomy, Paramys delicatus, petrosal INTRODUCTION Discoveries of Mesozoic fossils preserving the petrosal recognized by Burgin et al. (2018). Muridae, the family in- and/or auditory ossicles are occurring at a rapid pace, cluding R. norvegicus, is the most diverse within Rodentia, which has made the evolution of the middle ear apparatus with 834 species (Burgin et al. 2018). Sixty-six species of in the mammal lineage one of the best documented and oft Rattus Fischer, 1803, are recognized by Musser and Car- cited examples of a morphological transformation series leton (2005). From proposed origins in central Asia, R. in vertebrates (Luo 2011). In addition to informing evo- norvegicus has spread in company with humans to all con- lutionary models of transformational change, these bony tinents except Antarctica and is the stock from which the elements are important sources of characters for phyloge- common laboratory rat was derived (Lindsey and Baker netic analysis across Mammaliaformes, the broader clade 2006). Given its preeminent role in biomedical research, the of mammals and their extinct relatives. The study of on- brown rat has been the subject of numerous contributions togeny and adult morphology of extant mammals is critical regarding all aspects of its anatomy. The most comprehen- for providing the bases for transformational models and sive anatomical treatments are those of Greene (1935), Heb- for proposing hypotheses of homology across the compo- el and Stromberg (1976), Popesko et al. (1992), and May- nent parts. Toward that end, over the last few years, the nard and Downes (2019), although their treatments of the senior author has been reporting on the petrosal and osse- skull are not in much detail. A vast literature addressing rat ous middle ear elements in various extant mammals (e.g., middle ear anatomy already exists, including general over- Wible 2009, 2010, 2011, 2012). The current report follows views (e.g., Hellström et al. 1982; Judkins and Li 1997), on in this mode by describing these structures in an iconic ex- osteology (e.g., Parent 1980, 1983; Wysocki 2008), on vas- tant placental, the brown rat, Rattus norvegicus (Berken- culature (e.g., Tandler 1899; Nabeya 1923; Guthrie 1963; hout, 1769), also known as the common rat, domestic rat, Szabó 1990, 1995), on musculature (e.g., Berge and Wirtz fancy rat, lab rat, Norway rat, or sewer rat (Burgin 2017). 1989; Berge and Wal 1990), and on aspects of development Rodents are the most diverse clade of extant mam- (e.g., Youssef 1966, 1969). Yet, there is not a well-illustrated mals accounting for 2,552 of 6,111 species of placentals comprehensive treatment on the petrosal osteology in the 2 ANNALS OF CARNEGIE MUSEUM VOL. 86 current comparative anatomical language. It is the goal of Paramys delicatus, American Museum of Natural His- this report to fill that void. However, it is not a goal here to tory (AMNH-FM) 12506, Black Fork Member, middle compare the middle ear of the brown rat broadly across Pla- Eocene, Bridger Formation, Bridger Basin, Wyoming, centalia, Euarchontoglires, or Rodentia. Our comparisons USA. Data were downloaded from morphosource.org are limited to some early and middle Eocene rodents in or- (https://www.morphosource.org/Detail/SpecimenDe- der to place the brown rat in context with the early members tail/Show/specimen_id/2381) with the permission of the of the rodent lineage. AMNH. Details on this scan are included in the supple- mental material to Bertrand et al. (2016). The left petrosal was segmented in Avizo 9.5.0 software (Visualization and MATERIALS AND METHODS Sciences Group, 1995–2018). Extant osteological specimens studied with a stereomicro- The anatomical terminology employed follows that in scope are from the Section of Mammals, Carnegie Mu- prior publications by the senior author (e.g., Wible 2008, seum of Natural History (CM). Adults are those with fully 2009, 2010, 2011, 2012). Usage of English equivalents of erupted M1–3. The primary specimens referred to in the the Nomina Anatomica Veterinaria (Fifth Edition, 2005), text are: abbreviated NAV here, is preferred when appropriate. Rattus norvegicus, CM 493, juvenile male, Pittsburgh, For certain anatomical systems, the NAV is not adequate Pennsylvania, U.S.A., October, 1898. M3 is in the process because its comparative base is not sufficiently broad. In of erupting. particular, this is the case for the vasculature and for the Rattus norvegicus, CM 10227, adult female, Butler ectotympanic and middle-ear ossicles. For the former, we County, Pennsylvania, U.S.A., October 25, 1934. employ the terminology in Wible (1984, 1987), and for the Rattus norvegicus, CM 17504, adult female, Pittsburgh, latter in Henson (1961). Allegheny County, Pennsylvania, U.S.A., July 14, 1939. Rattus norvegicus, CM 18604, young adult female, Institutional Abbreviations Andover, Essex County, Massachusetts, U.S.A., June 10, 1933. All molars are erupted but sutures between the com- AMNH—Department of Vertebrate Paleontology, Ameri- ponents of the occipital bone are retained (basi-, ex-, and can Museum of Natural History, New York, New York, supraoccipital). U.S.A. Rattus norvegicus, CM 21415, juvenile male, Dormont, CM—Section of Mammals, Carnegie Museum of Natural Allegheny County, Pennsylvania, U.S.A., April 29, 1943. History, Pittsburgh, Pennsylvania, U.S.A. M3 is in the process of erupting. TMM—Texas Memorial Museum, University of Texas, Rattus norvegicus, CM 29584, adult male, Somerset, Austin, Texas, U.S.A. Somerset County, Pennsylvania, U.S.A., August 8, 1949. USNM—National Museum of Natural History, Smithson- Rattus norvegicus, CM Teaching Collection, adult of ian Institution, Washington, D.C., U.S.A. unknown sex and geographic origin. Only the skull is known. There is no accompanying data, although its iden- DESCRIPTIONS tification to species was confirmed by the late Guy Musser, Curator Emeritus, American Museum of Natural History. Overview Because of the lack of data, we forcedly detached the audi- tory bulla from the petrosal and then the petrosal from the In ventral view in situ in the brown rat cranium, most of the cranium. petrosal is hidden by the auditory bulla, which is formed Rattus rattus, CM 101347, juvenile male, Exu, State of by the expanded ectotympanic bone (“e” in Fig. 1). Small Pernambuco, Brazil, April 15, 1977. M3 is fully formed portions of the petrosal are exposed ventrally posteromedi- and in a crypt. al and posterolateral to the bulla. The medial margin of the In addition, two micro-CT datasets were studied: petrosal approximates the occipital bone, here composed Rattus norvegicus, Texas Memorial Museum M-2272, of the fused basi- and exoccipital (“bo” and “eo,” respec- West Point, Hancock County, Illinois, U.S.A. Data were tively in Fig. 1). The petrosal and basioccipital (based on downloaded from DigiMorph.org (http://digimorph.org/ CM 18604, a juvenile preserving sutures within the occipi- specimens/Rattus_norvegicus/); University of Texas High- tal bone) contact in some specimens (e.g., CM 17504) but Resolution X-ray CT Facility Archive 2660, scanning in others (e.g., CM 10227) are separated by a gap, the ba- funded by Ms.
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