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zoological Journal ofthe Linnean Society (1987), 91: 107-135. With 7 figures The eutherian stapedial artery: character analysis and implications for superordinal relationships JOHN R. WIBLE flepartment of Anatomy, Uniuersity of Chicago, Chicago, ~ l l ~ 60637, ~ ~ i s U S .A . Received May 1.986, accepted for publication Septelnber 1986 Evidence from outgroups, ontogeny, neontology, and fossils is used to distinguish primitive and derived rharacter states for the major components of the eutherian stapedial artery in I 7 modern orders. Derived states support the following higher-level phylogenetic hypotheses: ( 1) Microchiroptera and Mcgachiroptera are monophylrtir; and (2) within Ungulata, Tubulidentata is the outgroup to the remaining modern orders, followcd in succession by Artiodactyla and then Cetacca. Three branches of the stapedial artery, the a. diploetica magna, ramus temporalis, and ramus posterior, all but neglerted in previous syntheses, are shown to be primitive for Eutheria and Amniota. KEY WORDS:-Stapedial rclationships rrania. artery - Eutheria - mammals - character analysis superordinal - ~ CONTENTS Introduction . , . . . . . , , Material and methods . , , . . . , Ramus superior and outgroup comparisons. Character analysis . . . . . . . . Proximal stapedial artery . . . . . Ramus posterior . . . . . . . Ramus superior/ramus inferior bifurcation . Ramus superior . . . . . . . Meningeal rami . . . . . . . Ramus temporalis. . . . . . . Arteria diploetira magna . . . . . Ramus inferior . . . . . . . Maxillary artery . . . . . . . Ramus infraorbitalis . . . . . . Ramus orbitalis . . . . . . . Other anastomoses . . . . . . Discussion . . . . . . . . . . Lagomorpha, Rodentia, and Macroscelidea Microchiroptera and Megachiroptera . . Ungulata. . . . . . . . . Acknowledgements . . . . . . . References. . . . . . . . . . List of abbreviations . . . . . . . + 0024-4082/87/100107 29 $03.00/0 , . . , . , . . . , . . . . . . . . . . . . . . . . . . . . . , . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . . . . . . . . . . . . . . . . . . . . . . 108 . . . 109 110 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111 112 I15 1 16 116 1 17 118 120 I21 123 I24 125 125 I26 126 I28 129 130 I3 I 135 107 0 1987 T h e Linnean Society of London .I. K. WlHLE 108 1N'I'KOL) U C'I'ION The stapedial artery (also called thc orbital, temporal, or orbitoteniporal artery by some authors) can be traced within Vertebrata from selachians to mammals (de Beer, 1926; Goodrich, 1930). It is dcrived from the artery of the second branchial or hyoid arch (the second aortic arch) and arises from the internal carotid near the hyomaridibula in fish or the stapes (columella auris) in tetrapods (de Beer, 1926; Goodrich, 1930). Within Mammalia, the stapedial artery is the original supplicr of blood to the supraorbital, infraorbital, and mandibular regions in most embryos and also the major supplier to those regions in many adults (Wible, 1984). For students of mammalian systematics, the stapedial artery, its branches, arid associated grooves, canals, and foramina are widely recognized as important sources of traits for rcconstruc.ting phylogenetic relationships (e.g. Bugge, 1974; Wahlert, 1974; MacPhee & Cartmill, 1986). Despite the importance of the stapedial artery in mammalian oritogeriy arid phylogeny, knowledge of this vessel is in many regards rather limited. Ontogeny of the stapedial artery has been studied in detail in only 13 forms, representing nine of the 20 modern orders (Tablc 1). Although the stapedial artery and its branchcs have been described in a wide assortment of adult mammals, the homologies of some segments are uncertain. For instance, in most mammals thc branch of the stapedial artery that supplies the infraorbital region (the ramus infraorbitalis) runs through the orhitotemporal region ventral to the skull base (Wible, 1984); however, in dipodoid rodents the supposedly homologous vessel lies dorsal to the alisphenoid and leaves the cranial cavity with the maxillary nerve (Bugge, 1971). A number of models, or morphotypes, of the cranial arteries in ancestral cuthcrians have appeared in recent years (Szalay, 1972, 1975; Bugge, 1974; Archibald, 1977), but these generally have been based on Table 1. References on Stapedial Artery Ontogeny in Mammals Marsupialia D f l $ y U T U S quo// Carnivora canis ,familiaris Lagomorpha O~yrtolaguscunicu1u.c. Rodentia RauuJ Erethizon dorsnlum Chiroptera Rhinolophus hipposideroj Vespertilio murinus Primates Gnla,<o s~nigalensis Tarsius spectrum Homo sapiens Insec tivora Talpa europaea Artiodactyla .?US Sl'T!fa Hyraroidea Procauia capensis Wiblc (1984) Wible (1984) Fuchs (1905) Tandlrr (1902) Struthers (1930) Grosser ( I90 I ) Grosser (1901) H. Butler (1983) Hafferl (1916) Tandler (1902), Padget (1948) Sicher (1913) von Hofrnann (1914) Lindahl & Lundberg (1946) EU 1 HERIAN STAPEDIAL ARTERY 109 analyses of only a few eutherian orders and have not included data from relevant outgroups (marsupials, monotremes, and sauropsids, i.e. reptiles, plus birds). Absence of a broad comparative approach has handicapped these reconstructions. For example, the ramus temporalis, a branch of the stapedial artery that supplies the temporalis muscle in some modern eutherians (e.g. microchiropterans, Grosser, 1901; Buchanan & Arata, 1969; xenarthrans, Bugge, 1979), has not been included in these morphotypes, yet the antiquity of this vessel is supported by the occurrence of apparently homologous vessels in living reptiles ( Cartmill & MacPhee, 1980; Wible, 1984). This paper synthesizes current ontogenetic, neontological, and palaeontological evidence concerning the eutherian stapedial system with consideration of the pattern in non-eutherian amniotes. A detailed character analysis of the stapedial artery, its branches, and associated grooves, canals, and foramina is presented for 17 of the 18 modern eutherian orders (detailed descriptions are not currently available for Sirenia). This character analysis is the basis for a reconstruction of the stapedial system in ancestral eutherians and a discussion of superordinal relationships of certain eutherian groups. MATERIAL AND ME'I'HODS T h e method of phylogenetic analysis employed here is a two-step process: ( 1 ) distinguishing homologous and homoplastic features and (2) arranging the character states of homologous features in a transformation series (morphocline) to show the direction of evolutionary change (see Bock, 1977). Positional relationship is used as the major criterion for determining homology in the amniote stapedial system. However, analyses of positional relationships are not confined to the adult. Ontogenetic data are included wherever possiblc, because the process of development provides a level of resolution to analyses of similarities and differences that is unattainable in the study of a single stage such as the adult. Embryonic origin is a second criterion of homology only for the most proximal portion of the stapedial artery, because of its derivation from the second aortic arch. The remaining portions of tha stapedial system are secondary outgrowths unrelated to the embryonic aortic arches, and the timing of their ontogenetic formation varies considerably between species. Criteria commonly used for identifying the most primitive (plesiomorphous) character state in a transformation series include: "( 1) commonality or frequency of distribution of character states; (2) outgroup comparisons; ( 3 ) analysis of character covariance in relation to a 'form-function complex'; (4) study of ontogenetic transformations; and (5) reference to the relative geochronologic age of taxa with certain character states" (Novacek, 1980: 37). While debate concerning the validity of certain criteria continues (e.g. Bishop, 1982; Alberch, 1985), I advocate multiple testing with as many relevant criteria as is possible. Of the five criteria cited above, I rely most on outgroup comparison, ontogeny, and commonality. Evidence from the fossil record is of value, but only for those portions of the stapedial system that leave imprints in bone (grooves, canals, or foramina). Although several factors, including body size and auditory specializations, are thought to account for changes in the distributional pattern 110 -1 R WlBLE of the stapedial system in mammals (Fleischer, 1978; Packer, 1983), current understanding of causation (and resultant predictive power) is very limited. Therefore, I avoid discussion of 'form function complexes' here. Most of the data for the character analysis are taken from a comprehensive study of the ontogeny and phylogeny of the cranial arterial pattern in ten modern mammalian orders (Monotremata, Marsupialia, Xenarthra, Pholidota, Carnivora, Lagomorpha, Rodentia, Chiroptera, Artiodactyla, and Cetacea) and in several reptiles and birds (Wible, 1984). Data for the remaining manimalian orders are from the following sources: Macroscelidea (Bugge, 1972, 1971; MacPhee, 1977, 1981), Dermoptera (Cartmill & MacPhee, 1980; pers. obs.), Scandentia (Spatz, 1964; Steuerwald, 1969; Bugge, 1972, 1974; MacPhee, 1977, 1981; Cartmill & MacPhee, 1980), Primates (Bugge, 1972, 1974; MacPhee & Cartmill, 1986), Insectivora (Bugge, 1972, 1974; MacPhee, 1977, 1981), 'l'ubulidentata (Patterson, 1975; Thewissen, 1985), Perissodactyla (Tandler, 1899; Sisson, 1914; Radinsky, 1965; Savage, Russell & Louis, 1965; Cifelli, 1982), Hyracoidea (Lindahl & Lundberg, 1946), and Proboscidea (M. Watson, 1875; Tassy, 1981). ~ Ramus superior and outgroup comparisons Determining the homologies of one component of the eutherian stapedial system, the ramus superior, has proven somewhat difficult. This vessel, one of the two ma.jor end-branches of the stapedial artery, accompanies the ophthalmic nerve into the supraorbital region; the ramus inferior, the other end-branch, bifurcates and gives off arteries that accompany the maxillary and mandibular nerves into the infraorbital and mandibular regions respectively (Fig. 1). This distributional pattern - proximal stapedial artery and superior and inferior rami - is very constant within Eutheria and is known to appear during ontogeny in some representatives of all orders except Tubulidentata, Cetacea, Perissodactyla, Proboscidea, and Sirenia. A similar distributional pattern develops and is retained in the adults of most reptiles and birds (Hafferl, 1933). T h e only significant difference concerns the course of the artery accompanying the ophthalmic nerve. I n reptiles and birds, this vessel follows a wholly extracranial course, lateral to the processus ascendens of the epipterygoid. I n contrast, the eutherian ramus superior pierces the tympanic roof and runs forward along the intracranial surface of the alisphenoid (which either wholly or i n part is the homologue of the processus ascendens of the epipterygoid). Either: ( I ) the eutherian ramus superior has a homologue in the sauropsid stapedial system and somehow has been incorporated into the cranial cavity or (2) the eutherian ramus superior is a neomorphic structure. The evidence from the cranial arteries in the remaining relevant outgroups (monotremes and marsupials) is equivocal. 'The stapedial system is greatly reduced and its end-branches are annexed to the external carotid system in the adults of all forms except the platypus Ornithorhynchus (Fig. 2). No rnonotreme or marsupial has a vessel wholly equivalent to the eutherian ramus superior at any point during ontogeny, supporting no. 2 above. (Ornithorhynchus has a somewhat similar vessel, but it is wholly extracranial (Fig. 2A).) Yet, some of the endbranches of the stapedial systems in monotremes and marsupials pass through the cranial cavity and correspond to portions of the eutherian rarnus superior, EUTHERIAN STAPEDIAL ARTERY r. sup. mr n 1 / 1.-0. oph. n. max. n. ic’a r.\mand. Figure 1. Reconstruction of the internal carotid and stapedial arteries in a hypothetical ancestral eutherian. A, Ventral view of left basicranium. B, Lateral view of right braincase. The auditory bulla (the protective shell composed of membrane, cartilage, and bone in varying proportions that covers the tympanic cavity ventrally) and two of the middle-ear ossicles, the malleus and incus, have been excluded to expose the arteries. Dashed arteries run within the cranial cavity, and the stippled portion of the a. diplortica magna lies in a canal between the squamosal and pars canalicularis of the auditory capsule. which could be taken as support for no. 1. Because the homologies of the ramus superior outside Eutheria are unresolved at present, outgroup comparison is not used as a criterion of morphocline polarity for that vessel. CHARACTER ANALYSIS Character state distributions for the various components of the stapedial system in 17 modern eutherian orders are presented in Table 2, and a reconstruction of the stapedial system in a hypothetical ancestral eutherian appears in Fig. 1. Several derived (apomorphous) anastomotic linkages to the plesiomorphous stapedial system are shown in Fig. 3. Character states are identified and morphocline polarities are assessed below. J. R. WIBLE A r. -r. prox. stap. a. s.-0. orb. u r. i.-0. ica 1 CCh max. a. \ r . mand. r. s.-o r. \\ ko. L- postgl. a.- max. a. cca Figure 2. 'l'he major cranial arteries in monotrrmes and marsupials. A, 'Ihc monotrcme Ornilhor/ynchu.c (after 'l'andlcr, 1899, 1901; D. M. S. Watson, 1916; Wible, 1984). B, The marsupial Diddphis (after 'l'andler, 1899; Wible, 1984). Tnchy,&ssuJ differs from Orniihorhiynchzts in that: thc proximal stapedial, ramus superior (?), and ramus inferior are lacking; the occipital artery originatcs from the rxterrial carotid (arid not the proximal stapedial); and the meningeal ramus of thc a. diploetica magna reaches forward to the orbit to supply the ramus supraorbitalis ('l'andler, 1899, 1901; LVible, 1984). Other marsupials that have been studied resemble Didelphis (Tandler, 1899; Archer, 1976; Wible, 1984); the most significant difference is the occurrence of an a. diploetica magna in some forms. Striped vessels are neomorphic anastomoses (thc stripcd portion of the ramus supraorbitalis of the opossum represents its origin from the ophthalmic branch of the intcrual carotid artery). I n the platypus, the stippled portions of the a. diploetica tnagna and ramus infraorbitalis lie within the posttemporal and alispherioid canals respectively, arid portions of the proximal stapedial and ramus superior (?) are covered by the expanded mastoid. In the opossum, the postglenoid artery enters thc cranial cavity via the postglenoid foramen (not visible here) and divides into a mcriirigcal rarrius arid a temporal ramus that passes through the subsquamosal foramen. Proximal stapedial artery The proximal stapedial artery, the stem of the stapedial, extends from the internal carotid beyond the stapes to the bifurcation of the superior and inferior rami. Character states of the proximal stapedial a. concern its site of origin from the internal carotid and its relationships to the stapes and the surface of the petrosal bone. I w o distinct patterns of origin for the proximal stapedial a. occur among r 7 (3) absent absent absent absent absent INTRATY MP. ?INTRATYMP. INTRATYMP. ?INTRATYMP. absent absent absent intrarran. intracran. * intracran. intrarran. intracran. absent r.sup. origin no no ?YES* sof YES* YES* YES* ?YES* YES* ?YES* YES* COF* COF* COF* COF COF* COF* COF COF* COF COF COF* COF* COF* no no YES* no ?YES* ?YES* YES* no YES* YES YES* no no YES ?YES* no no YES YES* YES YES* YES* YES* YES YES YES solsolsof COF (6) a.d. mag. (5) r. temp. (4) r.sup. orb.for. yes yes2 yes' yes ' Yes: Yes absent absent absent absent INTRATYMP. * INTRATYMP.* NO INTRATYMP.; yes 1 . yes' INTRATYMP. * yes', INTRATYMP. * yes ' ?INTRATYMP.* yes' 3' 2s 3 yes"5 NO yes', 2' yes2 yes'.' ves INTRATYMP. * INTRATYMP.* INTRATYMP.* INTRACRAN. intracran. intracran. intracran.* intracran. (8) max a. (7) r.inf. course (9) as canal as canal as canal EXTRACRAN. EXTRACRAN. EXTRACRAN. EXTRACRAN. EXTRACRAN. as canal EXTRACRAN. as canal as canal as canal intracran. intracran. EXTRACRAN. EXTRACRAN. EXTRACRAN. r.i.-o. course yes Yes Yes NO** NO Yes Yes NO NO?** NO NO NO NO** NO NO** NO NO NO (11) r. anast. yes NO NO NO Yes NO NO NO NO NO** NO** NO** NO** NO NO** NO NO NO Table 2. Character analysis of the adult stapedial artery in the modern euthrian orders (except Sirenia). Micro- and Megachiroptera are listed separately to address the issue of bat monophyly or diphyly (see Discussion). Character states that are plesiomorphous for Eutheria are in upper case; apomorphous states are in lower case. The superscripts on the maxillary artery refer to the different sorts of maxillary arteries described in the text. * Denotes the loss of that component of the stapedial artery in some representatives of ar, order; ** denotes the secondary addition of that anastomosis in some representatives of an order no no no no no no YES* no no no no YES* no YES* no no no no no XENARTHRA no PHOLIDOTA CARNIVORA YES* no LAGOMORPHA YES* RODENTIA MACROSCELIDEA YES MICROCHIROPTERA YES MEGACHIROPTERA YES* no DERMOPTERA YES SCANDENTIA YES* PRIMATES INSECTIVORA YES TUBULIDENTATA YES YES* ARTIODACTYLA CETACEA no PERISSODACTYLA no no HYRACOIDEA PROBOSCIDEA no (2) r. post (1) prox. stap.a. Table 2. Character Analysis of the Eutherian Stapedial Artery I14 J . R. WIBLE r. anast. r. orb. Figure 3. ‘l‘he major cranial arteries in a hypothetical ancestral ruthcrian showing four of the anastomoses (striped vessels) that occnr among modern forms. (‘l‘hc connection between the a. diploctica m q n a and orcipital artery is considered plesiomorphous for Eutheria.) modern mammals. In nearly all euthcrians in which this vessel appears (and in reptiles, birds, and embryonic marsupials), the proximal stapedial arises from the internal carotid within the tympanic cavity (middle-ear space) on the ventral surface of the promontorium of the petrosal bone (the cochlear housing). ‘ l h e only exceptions to this pattern within Mammalia (and Amniota) where the proximal stapedial artery occurs are found in the monotreme Ornithorhynchu.r and some muroid rodents. I n these forms, the proximal stapedial leaves the internal carotid posterior to the auditory bulla. As a consequence, the proximal stapedial has its own foramen of entrance into the tympanic cavity. This pattern results from a relative posteromedial movement in the internal carotid and proximal stapedial arteries during ontogeny in the muroid rodents (and possibly in the platypus) (Fig. 4) and is treated as an apomorphous character state in these forms. The proximal stapedial exhibits two character states in its relationship to the stapes among modern mammals. I n nearly all forms in which the artery is present, it passes through an opening (the obturator foramen) in the stapes, but in the monotreme Ornithorhynchus that opening is absent and the artcry runs behind the stapes. Some authors (e.g. Gregory, 1910; Segall, 1970) argue that an imperforate stapes is primitive for Mammalia (and Eutheria) and that an obturator foramen in the stapes is derived. Others (e.g. Goodrich, 1930; Archibald, 1979) claim the reverse. T h e latter view is followed here because: ( 1 ) an obturator foramen is found in the stapes of Mesozoic mammals where known (the Early Jurassic “triconodont” Morganucodon, Kermack, Mussett & Rigney, 1981; and a Late Cretaceous “unguiculate” eutherian, Archibald, 1979) and many advanced therapsids, including ictidosaurs, the probable sister-group of Mammalia (Hopson & Barghusen, 1986); and (2) an obturator foramen appears in the stapes in early ontogenetic stages of the monotreme Omithorhynchus, but is later lost (Goodrich, 1915, 1930). (See Novacek & Wyss, 1986b, for a different view of character transformation of the eutherian stapes.) - EU'IHERIAN STAPEDIAL AKTERY Early r. I I5 Late stages int. aud. bulla Figure 4. Schematic representation of the development of the internal carotid and stapedial arteries in muroid rodents. In early embryonic stages, the internal carotid runs ventral to the cochlear capsule (the cartilaginous precursor of the promontorium of the petrosal), and the proximal stapedial originates in front of the fenestra cochleae. In later stages, the internal carotid and proximal stapedial shift somewhat posteromedially relative to their prior positions. T h e presumptive auditory bulla (composed of connctive-tissue fihrrs and thr rctotympanic bone) is added in still later stages, excluding the origin of the proximal stapedial from the tympanic cavity and producing separate foramina for the internal carotid and stapedial arteries in the adult. As in other rodents, the proximal stapedial leaves the tympanic cavity through an opening in the tympanic roof and the ramus superior/rarnus inferior bifurcation is within the cranial cavity (not visible here). Ventrally open grooves or closed canals for the proximal stapedial appear in two places on the surface of the petrosal bone among many eutherians. The first is on the promontorium between the internal carotid artery and the fenestra vestibuli (the opening within which the footplate of the stapes sits). T h e second is on the roof of the tympanic cavity lateral to (or sometimes in common with) the facial sulcus or canal (the channel which accommodates the facial nerve in its course through the tympanic cavity). Facial sulci are widely distributed among monotremes, marsupials, and eutherians (van Kampen, 1905) and are surely plesiomorphous for Eutheria (and possibly for Mammalia because sulci appear in some triconodontids, Kermack, 1963; and multituberculates, Simpson, 1937; Kielan-Jaworowska, Presley & Poplin, 1986). However, the facial sulcus need not contain a proximal stapedial artery. Separate grooves and canals on the promontorium and tympanic roof specifically for the proximal stapedial are absent from non-therian mammals (except some multituberculates: Sloan, 1979; Kielan-Jaworowska, Presley & Poplin, 1986) and variably present among Late Cretaceous and Early Tertiary eutherians. Apparently, osseous channels for the proximal stapedial have been acquired independently numerous times within Eutheria. Those modern forms in which this vessel leaves no imprint on the petrosal bone (e.g. some insectivorans and microchiropterans) have retained the plesiomorphous state. Ramus posterior The ramus posterior is a small branch of the proximal stapedial that originates just before its parent vessel reaches the stapes (Fig. 1A). It runs posteriorly with the facial nerve to supply the stapedius muscle, the back of the tympanic cavity, and (sometimes) the mastoid region. I n most adult mammals, I16 -1. R . W1BI.E thc ramus posterior loses its connection to the proximal stapedial and anastomoses with a branch of the occipital or posterior auricular artery (forming what is termed a stylomastoid artery) (Fig. 3 ) . However, because a proximal stapedial origin for the ramus posterior is ontogenetically primary in Monotremata, Xenarthra, Lagomorpha, Kodentia, Microchiroptera, Artiodactyla, and Hyracoidea and a homologous vessel appears in a number of reptiles (Wible, 1984), I accept i t as plesiornorphous for Eutheria. The ramus posterior seldom leaves any impression on the petrosal bone among modern fbrms and has not yet been identified in any fossil skull. Ranius tuperiorlRamu.5 infirior biJurmtzon The bifurcation of the proximal stapedial artery into the ramus superior and ramus inferior exhibits two principal patterns among recent euthcrians. In some fbrms, thc bifiircation is ventral to the tympanic roof within the middle-ear cavity (Fig. 1A): the ramus inferior then runs forward into the orbitotemporal region vcntral to the tympanic roof and the ramus superior moves dorsally into the cranial cavity through the tympanic roof: In some others (lagoniorphs, rodents, elephant shrews, and bats), the proximal stapedial pierces the tympanic roof and the ramus superior/ranius inferior bifurcation is within the cranial cavity: the ramus inferior then reaches the orbitotemporal region via a course dorsal to the tympanic roof (Fig. 4). A variant on this latter state is found in the tree shrew Tufiaia: the ramus superior/ramus inferior bifurcation is within the cranial cavity, but thc ramus inferior then runs forward vcntral to the tympanic roof (MacPhee, 1977, 1981, personal communication). However, this pattern is not found i n all tree shrews; in Piitocercus the bifurcation is ventral to the tympanic roof (Zeller, 1986). The intratympanic bifurcation is accepted as pleisomorphous for Eutlieria chiefly because that is the pattern in the monotreme Ornithorhynchus, the only non-eutherian mammal in which a complcte ramus inferior appears in the adult (Fig. 2A). Also, the lesser petrosal nerve, a branch of the glossopharyngeal nerve that runs with (or near) the ramus inferior in the platypus and eutherians (whether the artery is ventral or dorsal to the tympanic roof), lies ventral to the tympanic roof in the monotreme Tachyglossur and in marsupials. ‘ l w o sorts of openings transmit the proximal stapedial or ramus superior through the tympanic roof in modern eutherians. Some forms have a discrete foramen in the osseous tympanic roof, while in others there is merely a gap (the piriform fenestra of McDowell, 1958) between the various bony elements contributing to thc tympanic roof. As MacPhee (1981) suggests, a small piriform fenestra may be the plesiomorphous state for Eutheria, but the incidence of the various tympanic-roof openings among fossil forms is not well known. Ramus superior The eutherian ramus superior irrigates a very large area with branches that supply structures on both the intra- and extracranial surfaces of the occipital, orbitotemporal, and ethmoidal regions. From its origin on the proximal stapedial a., the ramus superior stretches dorsally along the intracranial surface o f the squamosal. I t moves medial to the petrosquamous sinus (the dural sinus EV I HERIAN STAPEDIAL ARTERY 117 that drains into the external jugular vein via the postglenoid foramen) and sends a large branch off posteriorly. This posterior branch of the ramus superior in turn supplies meningeal rami, one or more temporal rami, and an arteria diploetica magna that are discussed separately below. The main (or anterior) portion of the ramus superior runs forward medial to the squamosal, parietal, and alisphenoid (or sometimes frontal), supplying additional meningeal rami en route. Entering the back of the orbit, the ramus superior (more correctly now, the ramus supraorbitalis) ends in vessels that travcl with the lacrimal, frontal, and ethmoidal branches of the ophthalmic nerve. ‘The only character states of the eutherian ramus superior considered here concern its foramen of entrance into the orbit. The ramus superior either passes through the superior orbital fissure between the alisphenoid and orbitosphenoid or through a separate, more dorsally situated foramen lying near the juncture of the alisphenoid, orbitosphenoid, parietal, and frontal. A separate foramen (generally called the cranio-orbital or sinus canal foramen) is accepted as plesiomorphous for Eutheria, because that opening is more widespread among the modern orders and also appears in many Late Cretaceous and Early Tertiary forms (e.g. kennalestids, Kielan-Jaworowska, 1981; leptictids, P. M. Butler, 1956; arctocyonids, Russell, 1964). T h e intracranial portions of the ramus superior generally occupy grooves on the medial surfaces of the bones in the side wall of the braincase. The most prominent of these vascular grooves, the one for the anterior portion of the ramus superior, has been called variously the sinus canal (Parker, 1885), the lateral cerebral sinus (P. M. Butler, 1948), and the cranio-orbital sinus (Cartmill & MacPhee, 1980). Each of these terms implies that the major occupant of this vascular groove is the venous channel connecting the orbital and petrosquamous sinuses. Veins accompany the anterior portion of the ramus superior in the eutherians (and monotremes) investigated here, but the major occupant of the vascular groove is the artery. Similar grooves appear in extinct non-therian mammals (e.g. Morganucodon, Kermack et al., 1981; multituberculates, Kielan-Jaworowska et al., 1986) and advanced therapsids (Fourie, 1974) and, as Kielan-Jaworowska et al. (1986) suggest, may have bcen chiefly arterial in nature in these forms. Meningeal rami One or more meningeal rami originating from the intracranial portions of the ramus superior have been reported in representatives of all extant mammalian orders (except Sirenia) and are surely plesiomorphous for Eutheria and Mammalia. These rami course dorsally along the intracranial surfaces of the squamosal and parietal within the dura mater. In general, these vessels have been termed collectively the ‘middle meningeal artery’, but this usage is avoided here for the following reason. ‘Middle meningeal artery’ is a term of human anatomy, and the vessel in Homo may not be wholly homologous with the meningeal rami of the ramus superior. MacPhee & Cartmill (1986) suggest from positional relationships that the middle meningeal artery of man and other catarrhine primates is actually a compound vessel: its intracranial meningeal rami derive from the ramus superior, and its extracranial stem is a neomorph (a ramus anastomoticus) that grows out from the ramus inferior to annex the I18 J. R. WIBLE meningeal rami (Fig. 3 ) (which thereafter loses any connection with stapedialartery remnants within the tympanic cavity). Until the homologies of the human middle meningeal artery are resolved through detailed reanalyses of relevant ontogenetic stages, I recommend the term ‘meningeal rami’ [or the meningeal branches of the eutherian ramus superior. Ramu.r temporalis The eutherian ramus temporalis arises from the posterior branch of the ramus superior along the intracranial surface of the squamosal. It leaves the cranial cavity via foramina within or between the squamosal and parietal (dorsal to the external acoustic meatus) and supplies the posterior portion of the temporalis muscle. (The remaining portions of the temporalis muscle are supplied through branches of the external carotid artery.) One or more rami temporales have been reported for representatives of nine modern orders, but may be even more widespread within Euthcria (including Late Cretaceous and Early Tertiary forms) judging from the frequent occurrence of foramina along or near the parietosquamous juncture (see Cope, 1880; Russell, 1964; Kielan-Jaworowska, 1981). Such foramina are generally thought (e.g. Savage el al., 1965; Tassy, 1981) to be entirely venous in fossil forms, but this view must be amended in light of the widespread distribution of temporal rami among modern eutherians. Temporal rami are absent in all recent Dermoptera, Tubulidentata, Cetacea, Hyracoidea, and Proboscidea investigated to date, and the temporalis muscle in these forms is supplied exclusively through branches of the external carotid artery. The loss of the temporal rami is presumably the result of the decreased importance of the stapedial system in these groups. A stapedial origin for the temporal supply is accepted as plesiomorphous for Eutheria in part because a similar pattern appears in other amniotes. However, there is a difference in the course of this vasculature between modern therians and non-therian amniotes. In the latter forms, the vascular supply to the adductor mandibulae externus (in monotremes, the temporalis muscle) follows a wholly extracranial course, arising outside the braincase and running directly into the temporal region (Fig. 2A). O n the other hand, in most therians, the ramus temporalis originates within the cranial cavity and must pierce the side wall of the braincase (squamosal and/or parietal bones) to reach the temporalis muscle. (The eutherian and marsupial temporal rami have different vessels of origin within the cranial cavity: the posterior branch of the ramus superior in eutherians and, in marsupials, a branch of the external carotid system that enters the cranial cavity via the postglenoid foramen with the petrosquamous sinus (Fig. 2B).) The intracranial origin of the therian ramus temporalis appears to result from the expansion of the squamosal bone medial to the temporalis muscle. In advanced therapsids (Barghusen, 1968), extinct non-therian mammals (KielanJaworowska, 1971; Kermack et al., 1981; Crompton & Sun, 1985), and modern monotremes, the adductor mandibulae externus (or temporalis muscle) originates in part on the extracranial surface of the auditory capsule (Fig. 5A). In contrast, in therians, a portion of the squamosal bone (the squama) is interposed between the temporalis muscle on the one hand and the auditory capsule and ramus superior (or the postglenoid artery, in marsupials) on the other (Fig. 5B). EUTHERIAN STAPEDIAL ARTERY A P a r s canallcularis 119 ,squamosal brain cochlear capsule \ r. temp. incus ica ectopterygoid I . “-----1 / t e n s o r t y m p a n i m. dorsal ectotympanlc t -lateral parietal p r o x . s t a p . a. B I brain r . sup./r. inf. bifurcation cochlear capsule t e n s o r tympani m: I entotympanic U ectotympanic Figure 5. Schematic cross sections through the middle portions of developing tympanic regions, showing the varying relationship between the ramus temporalis, temporalis muscle, and the side wall of the braincase. A, 92 mm crown-rump length pouch young of the monotreme 7uchyglossus aculeatus (Duke University Comparative Embryological Collection no. 8327: section 622). B, 93.5 mm crown-rump length foetus of the megachiropteran Pleropus (Duke University Comparative Embryological Collection no. 83 1: scrtiori 1451). Shading by open circles indicates elements prrformed in cartilage; cross hatching denotes dermal bone. Note in B that ( I ) the proximal stapedial and ramus superior/ramus inferior bifurcation are dorsal to the tympanic roof (tegmen tympani), an apomorphous state found in lagomorphs, rodents, elephant shrews, and bats and (2) the tegmen tympani has a process jutting ventrally into the middle ear that forms continuous with the cartilage of the auditory tube, a bat autapomorphy. 120 .J. R. WIBLE Consequently, the ramus temporalis pierces this neomorphic portion of the squamosal bone to reac,h the temporalis muscle. Arteria diploetica magna ‘l’iie arteria diploetica magna is a little-known branch of the mammalian stapedial system that connects the posterior branch of the ramus superior and the occipital (or posterior auricular) branch of the external carotid system. T h e a. diploetica magna was first described in an adult monotreme, the Tasmanian echidna 7~achyglossu.rsetosus (“Echidna setasus”), by Hyrtl in 1853. In that form, the artery originates from the posterior branch of the ramus superior on the intracranial surface of the parietal. It leaves the cranial cavity between the parietal and the canalicular part of the petrosal (the portion that houses the u triclc and semicircular canals) and runs posteriorly in an extracranial space between the petrosal and squamosal that also includes part of the temporalis m u d e (Fig. 5A; Kuhn, 1971). This space, the posttemporal canal, opens onto the occiput via the posttemporal foramen between the petrosal and squamosal, and there the a. diploetica magna joins the occipital artery. Hyrtl (1854) next described this vessel in several adult xenarthrans, Tamandua tetradacgla (“M-Yrmecophaga tamandua”) and Dag~pusnovemcinctus. The a. diploetica magna of these forms differs from that of the echidna in that it no longer runs with the temporalis muscle in the posttemporal canal, but is separated from that muscle because of the expansion of the squama of the squamosal bone discussed above (Fig. 5B). Until recently, the a. diploetica magna has been thought (e.g. Tandler, 1899, 1901; Bugge, 1979) to be a peculiarity of these few forms. However, my studies (Wible, 1984) reveal that this vessel also appears in the monotreme Ornilhurhynchus (Fig. 2A) and in foetal and/or adult representatives of Marsupialia, Pholidota, Lagomorpha, Megachiroptera, Dermoptera, and Artiodactyla. In addition, an a. diploetica magna is figured (but not labelled) for a neonatal tree shrew Tupnia by Spatz (1964: figs 25, 26), and the caudal meningeal artery of the adult horse, which originates from the occipital artery and runs forward through a canal between the petrosal and squamosal (Sisson, 19 14), probably represents an a. diploetica magna. Finally, a probable homologue for the mammalian a. diploetica magna appears in a diverse lot of reptiles and birds. This branch of the stapedial system runs posteriorly along the auditory capsule through the region equivalent to the monotreme posttemporal canal - that is, medial to the adductor mandibulae externus and squamosal and ends in the occipital region. Such a vessel has been reported in crocodilians (Shiino, 1914), chelonians (Shindo, 1914; McDowell, 1961; Albrecht, 1976), lacertilians (Bhatia & Dayal, 1933; Oelrich, 1956), and birds (Wible, 1984). Given this wide distribution among reptiles, birds, and mammals, the a. diploetica magna is considered to be a plesiomorphous branch of the stapedial system in Amniota, Mammalia, and Eutheria. The a. diploetica magna has generally been overlooked by comparative anatomists and may be even more widespread within Amniota than is apparent from published sources. Large gaps (posttemporal foramina) connect the occipital and temporal regions in many non-therian amniotes, including advanced therapsids (e.g. Thrinaxodun, Fourie, 1974) and extinct nontherian EC'THERIAN STAPEDIAL AR r m y 121 niammals (e.g. Morganucodon, Kermack el al., 1981). These openings are thought by these and other authors to have transmitted only venous channels in these forms, similar to what has been reported for the colubrid snake Nalrix (Bruner, 1907) and the sand lizard Lacerta ngilis (Shindo, 1915). However, in light of the broad distribution of the a. diploetica magna among extant amniotes, the posttemporal foramen of advanced therapsids and extinct non-therian mammals probably contained an artery as well and, as Kielan-Jaworowska el al. (1986) have recently pointed out, may have been chiefly arterial in nature. T h e same holds for the smaller openings between the posterior border of the squamosal and canalicular part of the petrosal (postsquamosal foramina) that frequently appear in extinct and extant therian skulls (see Cope, 1880; Russell, 1964). Because the a . diploetica magna has received such little attention, its character states are not well understood. T h e therian vessel differs from that of monotremes in its relationships to the temporalis muscle and squamosal bone. The mammalian vessel is distinguished from that of other amniotes by the formation of an anastomosis to the external carotid system (Figs 2A, 3), and this pattern may be plesiomorphous for Mammalia and Eutheria. Within Mammalia, differences in the completeness of the anastomotic link between the stapedial and external carotid systems are as follows: ( 1 ) the a. diploetica magna forms a complete anastomotic link in the monotreme TnchygloJsus, dasypodid xenarthrans, and some marsupials; (2) it fails to reach the external carotid system in the marsupial Petrogale, the lagomorph O~c1olagus cuniculus, the megachiropteran Pteropuf, and the pholidotan Manis javanica; and (3) it loses its connection to the ramus superior in the monotreme Ornithorhynchus, bradypodid and myrmecophagid xenarthrans, dermopterans, the lagomorph Ochotona princeps, the artiodacty Tragulus, and the perissodactyl Equus. Rnmus inferior From its origin on the proximal stapedial artery, the ramus inferior runs forward into the temporal fossa and bifurcates into infraorbital and mandibular rami behind the mandibular nerve. In most eutherians and the monotreme Orni/horhynchus, the ramus inferior arises within the middle-ear cavity and travels ventral to the osseous tympanic roof next to the lesser petrosal nerve (or between the lesser petrosal and chorda tympani nerves). (As stated above, the tree shrew Tupaia exhibits a variant on this: the ramus inferior originates within the cranial cavity, but then exits that space and runs forward ventral to the tympanic roof.) T h e artery's passage beneath the tympanic roof is sometimes marked by a groove (e.g. some insectivorans) or canal (e.g. some scandentians), but these are certainly derived features because they are absent in extinct non-therian mammals (except some multituberculates; Kielan-Jaworowska el al., 1986) and most early eutherians. It is often said (e.g. van Kampen, 1905; van der Klaauw, 1931; MacPhee, 1981) that the ramus inferior sometimes runs in the petrotympanic (Glaserian) fissure, the groove in the tympanic roof for the chorda tympani nerve that is well developed among modern mammals only in insectivorans, tubulidentates, hyracoids, and some primates (Novacek, 1986). However, the only specific examples of a ramus inferior in the Glaserian fissure are in some primates (MacPhee & Cartmill, 1986), and the homologies of that vessel are controversial (see below). I n several eutherian orders (i.e. 122 J R WlBLE Xenarthra, Pholidota, Carnivora, Dermoptera, Artiodactyla, and Perissodactyla), the greatly reduced ramus inferior loses its attachment to the proximal stapedial and is annexed to the external carotid system as a tympanic branch of the maxillary artery (Fig. 3 ) . It is not certain whether this represents the plesiomorphous condition for the ramus inferior in these groups or whether the artery is secondarily reduced. The ramus inferior exhibits a unique pattern in Lagomorpha, Rodentia, Macroscelidea, and Chiroptera: it arises from the proximal stapedial within the cranial cavity and runs forward dorsal to the O S S ~ O U S tympanic roof (Fig. 4). After this intracranial course, the ramus inferior enters the temporal fossa eithcr through the piriform fenestra in lagomorphs, chiropterans, and most rodents or adjacent to the foramen ovale in macroscelideans. In dipodoid rodents, the ramus inferior continues forward within the cranial cavity and enters the orbit, as the ramus infraorbitalis, through the confluent superior orbital fissure/foramen rotundum. The ramus inferior in one extinct eutherian group, the Leptictidae, is thought by Novacek (1980, 1986) to have passed dorsal to the tympanic roof, but he remarks that the direct evidence for that pathway is somewhat ambiguous. The intracranial course of the ramus inferior can be interpreted in several ways: ( 1 ) The intracranial ramus inferior is not the homologue of the ramus inferior of other mammals, but a new anastomotic channel that forms dorsal to the tympanic roof. (2) It is the homologue of the ramus inferior of other mammals, and its course has been shifted dorsally relative to the tympanic roof. (3) It is the homologue of the ramus inferior of other mammals, but the tympanic roof has been shifted ventrally relative t o the artery. The first alternative is rejected, because the artery in question clearly is the homologue of the intratyrnpanic ramus inferior: both vessels run with the lesser petrosal nerve. If the true ramus inferior and lesser petrosal nerve have shifted dorsal to the tympanic roof in lagomorphs, rodents, macroscelideans, and chiropterans (no. 2), the developmental process involved may be similar to the relative posteromedial shift of the internal carotid and proximal stapedial arteries that occurs during ontogeny in some tnuroid rodents (Fig. 4).However, no apparent relative movement of the ramus inferior and lesser petrosal nerve during development has been found in the lagomorphs, rodents, and chiropterans studied by the author (Wible, 1984). At this time, the third alternative receives the most support, because there is some controversy about the homologies of one of the major tympanic-roof elements, the tegmcn tympani. This element, a mammalian neomorph (van der Klaauw, 1931; d e Brcr, 1937), forms in diverse ways in different groups of mammals. Based on these differences in ontogenetic formation, Kuhn (197 1 ) suggests that the tegmen tympani (or portions of it) may have been added to the tympanic roof independently numerous times within Mammalia. T h e variable relationship between the tegmen tympani and lesser petrosal nerve described above is strong support for Kuhn’s hypothesis, because nerve courses through the tympanic region have been found to be very conservative among eutherians (MacPhee, 1977, 1981). EU’I’HERIAN STAPEDIAL ARTERY I23 The fate of the ramus inferior in adult humans (and in other primates) is a matter of some debate. According to most investigators (e.g. Tandler, 1902; Padget, 1948; Bugge, 1974), the ramus inferior is the extracranial stem of the human middle meningeal artery, which enters the cranial cavity immediately posterior to the mandibular nerve through the foramen ovale or its own foramen spinosum. MacPhee & Cartmill (1986) point out that this vessel, unlike the ramus inferior of other mammals, has no course along the tympanic roof. They suggest that the stem of the human middle meningeal artery is actually a ramus anastomoticus, a neomorphic vessel that enters the cranial cavity posterior to the mandibular nerve and anatomoses with the meningeal rami of the ramus superior (Fig. 3) in, for example, many carnivorans and ungulates. MacPhee & Cartmill further suggest that the ramus inferior is represented in adult humans by the anterior tympanic branch of the maxillary artery, a small vessel that runs with the chorda tympani nerve in the Glaserian fissure on the ventral surface of the tympanic roof. T h e controversy concerning the fate of the ramus inferior in adult humans (and in other primates) awaits detailed investigations of relevant ontogenetic stages. Maxillary artery In all recent mammals except some insectivorans and rodents, an anastomosis forms between the distal portions of the external carotid system and ramus inferior (or one of its major end-branches, the ramus infraorbitalis or ramus mandibularis) near the exit of the mandibular nerve from the cranial cavity (Fig. 3 ) . These anastomotic links, all of which are generally called maxillary arteries, exhibit a remarkable degree of variability in their origins, courses, and relationships to other structures. In addition, some forms have more than one type of anastomotic channel (e.g. dermopterans), I interpret this variability as evidence for the independent acquisition of anastomotic links between the stapedial and external carotid systems many times during mammalian phylogeny. Included under the category ‘maxillary artery’ are the following sorts of vessels: ( 1 ) An artery leaves the external carotid stem and moves forward medial to the mandible. It bends medially dorsal to Meckel’s cartilage and passes posterior to the lateral pterygoid muscle. After supplying the ramus mandibularis, it turns forward medial to the mandibular nerve beneath the foramen ovale. This sort of maxillary artery appears in the monotreme Omithorhynchus, megachiropterans, scandentians, perissodactyls, hyracoids, and some xenarthrans, carnivorans, rodents, microchiropterans, and insectivorans. It also appears in macroscelideans, but supplies only the ramus mandibularis in the adult (Bugge, 1972, 1974). Apparently, the connection between the infraorbital and mandibular rami is secondarily lost in elephant shrews. (2) An artery runs lateral to the mandibular nerve beneath the foramen ovale, but is otherwise similar to the first type (no. 1 above). This sort of maxillary artery appears in the monotreme Tachyglossus, pholidotans, artiodactyls, cetaceans, and some xenarthrans, carnivorans, and microchiropterans. ( 3 ) An artery sends channels both medial and lateral to the mandibular nerve beneath the foramen ovale. This sort of maxillary artery occurs in the 124 J. K. \.YIBLl< xenarthran Dasypus villosus (Tandler, 190 1) and the microchiropteran Artibeus l i t u r ~ ~ u(Buchanan s 8r Arata, 1969). (4) An artery runs forward between the mandible and Meckel’s cartilage, passing lateral to the mandibular nerve, but separated from i t by the lateral pterygoid muscle. It supplies a ramus mandibularis and turns dorsally in front of the lateral pterygoid muscle. This maxillary artery appears in marsupials, dermopterans, primates, and the xenarthran Tamandua letradacpla. (5) An artery leaves the external carotid stem and moves forward directly beneath the tympanic region. It then passes dorsally in front of the auditory bulla, well medial to Meckel’s cartilage. After supplying the ramus mandibularis, it turns forward medial to the mandibular nerve beneath the foramen ovale. This vessel, the pterygoorbital artery of some authors, appears in lagomorphs, dermopterans, and some rodents. The taxonomic significance of these various anastomoses is uncertain. Because the same anastomotic patterns are repeated within certain taxa, it would appear, at least in some cases, that these ‘maxillary arteries’ may be reliable indicators of phyletic relationship. I suspect that this is in particular relevant with regard to nos 4 arid 5 above, vessels which have a very restricted distribution within Eutheria. However, until more is known about intrataxon variation, I suggest caution. In the form that is known best, Homo .vapien.s, the maxillary artery varies considerably both in its relationship to the inferior head of the lateral pterygoid muscle and to some of the branches of the rnandibular nerve (Hollinshead, 1968). The only forms for which some sort of maxillary artery does not occur are in the orders Insectivora (chrysochlorids, soricids, and erinaccids) and Rodentia (dipodoids and some muroids and geomyoids). In each case in which the course of the ramus inferior has been described or figured (except the dipodoid rodents) , that vessel after supplying the ramus mandibularis continues forward medial to the mandibular nerve beneath the foramen ovale (Tandler, 1899; ROUX,1947; P. M. Butler, 1948; Wible, 1984). This course probably is the plesiomorphous one for the eutherian ramus inferior. ’The ramus inferior and ramus infraorbitalis in dipodoid rodents run dorsal to the skull base within the cranial cavity (Bugge, 1971). Ramus infraorbilalis From its origin on the ramus inferior (or maxillary artery), the ramus infraorbitalis runs forward through the orbitotcmporal region of the skull (Fig. 1B). In some forms (for example, the monotreme Tachyglossus, marsupials, and xenarthrans), the ramus infraorbitalis runs directly ventral to the skull base. In others (for example, the monotreme OrnilhorhynchuJ, lagomorphs, and scandentians), the ramus infraorbitalis passes through a canal (or opening) on the ventral surface of the skull base, generally termed an alisphenoid canal (Fig. 2A). Some authors (e.g. Novacek, 1980; Thewissen, 1985) support a n alisphenoid canal as plesiomorphous for Eutheria and its absence as an apomorphous state. However, because an alisphenoid canal is absent in extinct and extant non-eutherian mammals (except the platypus) and because i t exhibits a somewhat spotty distribution among extinct eutherians and some modern groups (e.g. insectivorans, carnivorans, and rodents), I and others (e.g. EU‘I’HERIAN S‘IAPEDIAL AK’I’ERY 125 Novacek, 1986) consider that this channel has been acquired independently numerous times within Mammalia. Also, alisphenoid canals do not develop in the same way in all forms. In some, these channels form within portions of the chondrocranium (for example, in the ala temporalis in the monotreme Ornithorhynchus; D. M. S. Watson, 1916; in the pterygoid process of the ala temporalis in the lagomorph Lepus, de Beer, 1937). In others (for example, the scandentian Tupaia; Spatz, 1964), the alisphenoid canal lies between the chondrocranial and dermal portions of the alisphenoid. Additional apomorphous states of the ramus infraorbitalis occur in dipodoid rodents and chiropterans. In these forms, the ramus infraorbitalis runs forward into the back of the orbit dorsal to the alisphenoid. ‘The chiropteran vessel enters and exits the cranial cavity through foramen ovale (or a separate opening in front of foramen ovale) and foramen rotundum respectively. I n dipodoid rodents, the ramus infraorbitalis originates from the ramus inferior within the cranial cavity and enters the back of the orbit through the confluent superior orbital fissure/foramen rotundum. Because these two variants exhibit different relationships to the skull base, they are probably not wholly homologous, nor are they homologous with the extracranial ramus infraorbitalis of other mammals. This is supported by the concurrent incidence of both intra- and extracranial infraorbital rami in the microchiropteran Artibeus lituratus (Buchanan & Arata, 1969). (The intracranial ramus infraorbitalis is absent in two microchiropterans, the rhinolophid Rhinolophus (Grosser, 1901 ; Kallen, 1977) and the phyllostomatid Desmodus (Kallen, 1977). I view these as derived conditions, because a separate foramen in front of the foramen ovale appears in other representatives of these families.) Ramus orbitalis Anastomoses frequently occur between the ramus infraorbitalis and the supraorbital branches of the ramus superior in extant mammals. T h e most frequent pattern for such anastomotic channels is a course through the back of the orbit outside the periorbita (Fig. 3 ) . However, in dipodoid rodents, megachiropterans, and some microchiropterans, this vessel arises from the ramus infraorbitalis within the cranial cavity and enters the back of the orbit through the foramen rotundum (or the confluent superior orbital fissure/foramen rotundum). Also, in some forms (e.g. pholidotans, dermopterans) the supraorbital vessels originate directly from the ramus infraorbitalis and not from a separate anastomotic trunk. Because these vessels, which fall under the category ‘ramus orbitalis’, are absent from some extant forms and because they tend to be somewhat variable in their courses and relationships, I treat them as apomorphous states. (The term ‘ramus orbitalis’ is equivalent to the ‘external ophthalmic artery’ of the Nomzna anatomica ueterinaria, 1973, but is preferred here to avoid confusion with the ophthalmic branch of the internal carotid artery.) Other anastomoses Two other sorts of anastomotic channels join intracranial portions of the ramus superior. These vessels exhibit somewhat spotty distributions among modern mammals and apparently have arisen numerous times: 126 J . R. WIBLE ( 1 ) The ramus anastomoticus connects the maxillary artery to meningeal branches of the ramus superior through the foramen ovale (Fig. 3) in the Tachyglossus, dermoptcrans, tubulidentates, perissodactyls, monotrcmc hyracoids, proboscideans, and some carnivorans, rodents, artiodactyls, and cetaceans (and possibly some primates; MacPhee & Cartmill, 1986). (2) The arteria anastomotica, which joins intracranial portions of the ramus superior and internal carotid artery, appears in cetaceans, dermopterans, and some xenarthrans, pholidotans, carnivorans, rodents, and artiodactyls. D 1SC U SS10 N As is apparent in the foregoing character analysis (Table 2 ) , no modern eutherian retains all the primary components of the plesiomorphous stapedial system. The forms that most closely approximate the morphotypical pattern are certain insectivorans, which lack only an arteria diploetica magna. (This artery, in fact, may be present in some insectivorans, for instance, Eb1omy.r and Echinosorex, given the occurrence of well-developed postsquamosal foramina in macerated skulls.) In all modern eutherians studied to date, at least one major component of the stapedial system is lost or reduced and its end-branches are annexed to the external carotid system. Thc character analysis presented in Table 2 also reveals that many of the apomorphous states of the stapedial system are shared among the modern orders. These shared apomorphous states deserve further analysis, in particular because few synapomorphies of orders have been identified to date in syntheses of fossil and anatomical evidence on higher eutherian phylogeny (e.g. Novacek, 1980, 1982, 1986; MacPhee & Cartmill, 1986). T h e distribution of these apomorphous states of the stapedial system is such that some apparently have been acquired independently several times within Eutheria and are not reliable evidence of any superordinal affinity (for example, the loss of the ramus temporalis or the addition of an a. anastomotica). Other states, however, are consonant with superordinal groupings that have been proposed or supported by other researchers (e.g. McKenna, 1975; Szalay, 1977; Novacek, 1982, 1986). These groupings and apomorphous states are discussed below. Lagomorpha, Rodentia, and Macroscelidea There is a general consensus of late among paleontologists (e.g. McKenna, 1975; Szalay, 1977; Novacek, 1982, 1986) that the diverse assortment of extinct pseudictopids, zalambdalestids, eurymylids, and anagalids from the Late Cretaceous and Early Tertiary of Asia forms a closely knit group, which is in or near the ancestry of several modern eutherian orders in particular, Lagomorpha and Macroscelidea. Other groups that have been added to this grouping include the extinct palaeoryctines and leptictids (McKenna, 1975) and Rodentia (Novacek, 1982); i n fact, Novacek (1982) has revived Linnaeus’s original concept of Glires for lagomorphs and rodents and placed Macroscelidea as the sister group to Glires (Fig. 6). The grouping of these very diverse extinct and extant forms, which is equivalent to McKenna’s (1975) magnorder Ernotheria plus Rodentia, is supported by numerous cranioskeletal and dental features (discussed in the publications cited above and others cited therein), and ~ EUTHERIAN STAPEDIAL ARTERY 127 Figure 6. Phylogenetic relationships for the major groups of Recent and fossil (*) eutherians suggested by Novacek (1982: fig. I ) . Dashed linrs indicate highly tentative relationships. (Following Engelmann (l978), I use the term “Xenarthra” instead of “Edentata” for the monophyktir grouping of New World rdrntates.) the monophyly of Glires is supported by several derived features of foetalmembrane development and placental morphology (Luckett, 1977, 1985) and a wide assortment of cranioskeletal and dental features (Li & Ting, 1985; Luckett, 1985; Novacek, 1985). In the character analysis presented here, a derived pattern for the closure of the tympanic roof with the tegmen tympani ventral to the ramus superior/ramus inferior bifurcation and ramus inferior course is shared by Lagomorpha, Rodentia, and Macroscelidea and possibly by some of the extinct members of the ernothere-rodent clade (i.e. leptictids, Novacek, 1980; Pulueoryctes, pers. obs.). (Novacek’s (1986) proposal that leptictids are more closely related to insectivorans requires independent acquisition of the derived pattern of the ramus superiorlramus inferior bifurcation in these fossils.) The incidence of this feature among other extinct forms in this clade is not known, because the tympanic regions are either covered by a complete osseous bulla (e.g. Anugule; McKenna, 1963) or have rock matrix covering the tegmen tympani (e.g. Kennalestes and Asioryctes; pers. obs.). This apomorphous state is not unique to ernotheres and rodents, but appears in one other group, Chiroptera. Bats either have independently acquired this pattern of tympanic-roof closure or they may be the sister group of the ernothere-rodent clade. (The sub- and superordinal affinities of bats are discussed further below.) Another apomorphous feature that appears in many extinct and extant members of the ernothere-rodent clade (as well as in a number of other see Table 2) is the enclosure of the ramus infraorbitalis within a mammals canal in the alisphenoid bone. An alisphenoid canal is known for lagomorphs, ~ I28 J R WlBLE rodents, macroscelideans (Saban, 1956), leptictids (Novacek, 1980), anagalids (McKenna, 1963), and Pnlaeoryctes (Van Valen, 1966). It develops in a similar position within the cartilaginous ala temporalis in modern representatives of this clade, such as the lagomorph Lepus (de Beer, 1937), the rodents Rattus (Youssef, 1966) and Tntpra (Kadam, 1973), and the macroscelideari Elephunlulu~ ( ROUX, 1947), and may be a synapomorphy of the modern orders. Howcver, because an alisphenoid canal is absent in the earliest representatives of the ernothere-rodent clade, the kennalestids (Kielan-Jaworowska, 1981) and zalambdalestids (Kielan-Jaworowska & Trofimov, 1980), it is not a synapomorphy of this group. Microchiroptern and Megachiroptera Bats have traditionally becn thought to be monophyletic (Gregory, 1910; Simpson, 1945), but separate origins for micro- and megachiropterans within Eutheria recently have been supported by several investigatorq. Smith & Madkour (1980) use two features of the penis (absence of accessory cavernous tissue and presence of distally expanded, vascular corpus spongiosum) to suggest “a closer phylogenetic relationship between Megachiroptera, Dermoptera, and Primates than was previously supposed between Mega and Microchiroptera [ 1980: 3631.” Pettigrew (1986) and Pettigrew & Cooper (1986) report derived features of the visual pathways unique to Megachiroptera, Dermoptera, and Primates among vertebrates and suggest that megachiropterans and flying lemurs may be an early branch of the primate line (“aerial primates”). Pettigrew (1986) dismisses the 16 shared derived features employed by Novacek ( 1982) to link micro- and megachiropterans, because they are either associatcd with the adaptation to flight (possible convergences), not unique to bats within Eutheria, or possible plesiomorphies. Diphyletic origins for micro- and inegachiropterans are not supported by my character analysis of the eutherian stapedial artery. No shared derived features separately unite Micro- and Megachiroptera with any other modern order. In contrast, two unique apomorphous states strongly support the monophyly of bats. The first is the course of the ramus infraorhitalis. This artery enters the cranial cavity in front of the mandibular nerve, runs forward along the intracranial surface of the alisphenoid, and passes into the orbit with the maxillary nerve via the confluent superior orbital fissure/foramen rotundum. The second concerns the pattern of tympanic-roof closure. Along with lagomorphs, rodents, and macroscelideans, bats have the tegmen tympani ventral to the ramus superior/ramus inferior bifurcation and ramus inferior course. However, bats are distinguished from the other forms by the unique form of the tegmen tympani. In general, the mammalian tegmen tympani lies in a horizontal plane lateral to the promontorium of the petrosal arid forms a roof for the tympanic cavity. In chiropterans, however, the tegmen tympani is a slender, more vertically-orientated rod that projects ventrally into the tympanic cavity (Fig. 5B) and forms in continuity with the cartilage of the auditory tube (Wible, 1984). Bats have been placed in the superorder Archonta along with dermopterans, scandentians, and primates (McKenna, 1975; Szalay, 1977; Novacek & Wyss, 1986a). Novacek (1982) supports a grouping of Chiroptera and Dermoptera EU’I’HERIAN SlAPEDIAL ARTERY 129 (Fig. 6) with 12 synapomorphies. Only five bat-colugo synapomorphies are specializations of the flight apparatus (and therefore possible convergences, according to Pettigrew), and included in these five are the humeropatagialis and coracocutaneous muscles, unique elements not found in other gliding mammals. Because a bat-colugo clade seems reasonably well established (see also Novacek, 1986), the apomorphous pattern of the ramus superior/ramus inferior bifurcation and ramus inferior course that bats share with lagomorphs, rodents and macroscelideans apparently has been independently acquired. This is supported by the unique morphology of the chiropteran tegmeri tympani described above, which differs considerably from the horizontally-orientated element of lagomorphs, rodents, macroscelideans and most other mammals. Bats and colugos do not share any apomorphous features of the stapedial system or tympanic roof: in fact, the tegmen tympani is absent in colugos (Halbsguth, 1973) and the reduced ramus inferior and lesser petrosal nerve run ventral to the membranous tympanic roof (personal observation). Ungulata The ungulate radiation including the modern orders Tubulidentata, Artiodactyla, Cetacea, Perissodactyla, Hyracoidea, Proboscidea and Sirenia, is generally (e.g. Van Valen, 1971, 1978; and a number of extinct orders McKenna, 1975; Szalay, 1977; Novacek, 1982) held to be a monophyletic assemblage originating in or near the Arctocyonidae, one of several Late Cretaceous and Early Tertiary groups that are informally termed ‘condylarths’. Special relationships between certain condylarth families and modern orders have been demonstrated and generally accepted (for example, mesonychid condylarths and cetaceans; Van Valen, 1966, 1968), but the origins and interrelationships of most modern orders within Ungulata are the subject of considerable debate. Table 2 reveals that modern ungulates share a number of apomorphous states of the stapedial artery (losses and de nouo anastomotic linkages). T h e superordinal relationships suggested by this character distribution are depicted in Figure 7. Of particular interest to the interrelationships within Ungulata are the following: ~ ( 1 ) Tubulidentates are distinguished from the remaining modern orders by the retention of the stem of the ramus superior and a distinct foramen for that vessel in the suture between the petrosal (tegmen tympani) and squamosal. In fact, a foramen for the ramus superior distinguishes tubulidentates from all extinct ungulates except some Palaeocene condylarths (i.e. Arctogon, Arctocyonidev, and Pleuraspidotherium; Russell, 1964), and apparently in these forms the foramen is entirely within the tegmen tympani. (Thewissen (1985) reports that a fissure in the petrosquamous suture of two Middle Eocene artiodactyls may have transmitted a ramus superior, but such openings are absent from other Eocene artiodactyls, including the Early Eocene Diacodexis (Coombs & Coombs, 1982).) Tubulidentata either had a unique origin within Rrctocyonidae or, as has been suggested recently by Novacek (1982, 1986) and Thewissen (1985), an origin outside Ungulata. I30 J. R . WIBLE P Figure 7. Phylogenetic relationships of ungulate ordrrs modifird from Novacrk (1982: fig. 1 ) i n light of thr character analysis of the staprdial artcry. Nunibcrs r e h [(I thc following apomorphous charactri- states listed in ’I‘aldc 2: I , proximal stapcdial artery absent. 3, ramus superior ahsrnt. 9. ramus infraorbitalis enclosrd within an alisphrnoid canal. 1 1 ramus anastoinoticus pr(~scnt. ~ (2) Cetaceans, perissodactyls, hyracoids, and proboscideans are distinguished from artiodactyls by the loss of the proximal stapedial artery. Although this vessel is lacking in all modern representatives of these five orders, a distinct groove for the proximal stapedial appears on the promontorium of the petrosal in most condylarths (Russell, 1964; Cifelli, 1982) and in Eocene and Oligocene artiodactyls (Dechascaux, 1974; Webb & ‘Taylor, 1980; Coombs & Coombs, 1982). The absence of this groove in early cetaceans (Kellogg, 1936; Gingerich, Wells, Russell & Shah, 1983), perissodactyls (Radinsky, 1965; Savage et al., 1965; Cifelli, 1982), hyracoids (Whitworth, 1954), and proboscideans (Tassy, 1981) represents a derived state within Ungulata. ( 3 ) Perissodactyls, hyracoids, and proboscideans are distinguished from cetaceans by the addition of an alisphenoid canal for the infraorbital ramus and a ramus anastomoticus. The homologies of the alisphenoid canal of perissodactyls (Equus, Muggia, 1931) and hyracoids (Procavia, Lindahl, 1948) are supported by the ontogenetic formation of a canal within the cartilaginous ala temporalis; the development in proboscideans is not known. A grouping of pcrissodactyls, hyracoids, and proboscideans (along with Sirenia and two extinct groups, Desrnostylia and Embrithopoda) has been proposed elsewhere (Van Valcn, 1971, 1978), but the usefulness of the alisphenoid canal as a synapomorphy for this clade is uncertain. An alisphenoid canal appears in some condylarths including mesotiychids (Szalay & Gould, 1966), the probable sister group ol’Cetacea (Van Valen, 1966, 1968), and may have been added and lost several times within Ungulata. No other features of the stapedial system further distinguish relationships among perissodactyls, hyracoids, and proboscideans. ACKNOWLEDGEMENTS I thank the following individuals and institutions for access to seriallysectioned specimens: Prof. D. Starck and Prof. W. Maier (Goethe-Univcrsitat, Frankfurt am Main); Prof: H.-J. Kuhn (August-Universitat, G6ttingen); Prof. W. Reinbach (Karl-Universitat, Heidelberg); Dr H. E. Evans (Cornell EU'IHERIAN STAPEDIAL ARTERY 131 University, Ithaca); Drs M. Cartmill, R. D. E. MacPhee, E. L. Effmann, and K. L. Duke (Duke University, Durham); Dr R. Presley (University College, Cardiff); and Dr E. C. Boterenbrood (Hubrecht Laboratory, Utrecht). For access to skulls of extinct and extant mammals, I thank Drs R . H. Tedford, M. C. McKenna, and G. G. Musser (American Museum of Natural History, Ncw York); Drs B. D. Patterson and R . M. Timm (Field Museum of Natural History, Chicago); and Dr Z. Kielan-Jaworowska (Zaklad Paleobiologii, Warsaw). Numerous individuals at various institutions have contributed in significant ways towards the completion of this work. 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Folia prirnatologica, 47: 6 1-80. LIST OF ABBREVIATIONS A. anast. a. d. mag. acf >Is aud. bulla bO bs cc rca cof ct cca eo ex tracran. fi, fin lr 13.a hf ica intracran. i n t ratymp. I11 v lo mand. n. mas max. a . max. n. mr oa arteria anastomotica arteria diploetica magna anterior carotid foramen alisphenoid auditory hulla hasioccipi tal basisphcnoid cochlear capsule common carotid artery rranio-orhital foramen cavum tympani rxtrrnal carotid artrry exoccipital extracranial fenestra cochlear (round window) foramen magnum frontal foramen for stapedial artery hypoglossal foramen internal carotid artery intracranial intratympanic lateral head vein lamina obturans mandibular nerve mastoid portion of petrosal maxillary artery maxillary nerve meningeal ramus occipital artery of orb. for. oph. n. 0s par pcf Pf Pgf plf postgl. a. P' prox. stap. a. r. anast. r. I.-o. r. inf. r. mand. r. post. r. orb. r. s.-o. r. sup. r. temp rt sma sof sq temp. m. tt tYmP V VII optic foramen orbital foramen ophthalmic nerve orbitosphenoid parietal posterior carotid foramen piriform fenestra postglenoid foramen posterior lacerate foramen postglenoid artery promontorium of petrosal proximal stapedial artery ramus anastomoticus ramus infraorhitalis ramus inferior ramus mandibularis ramus posterior ramus orbitalis ramus supraorhitalis ramus superior ramus temporalis ramus temporalis stylomastoid artery superior orbital fissure squamosal temporalis muscle tegmen tympani tympanum trigeminal nerve facial nerve