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Chapter 4 the Antiquity of Rhizomys and Independent Acquisition of Fossorial Traits in Subterranean Muroids

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Chapter 4 the Antiquity of Rhizomys and Independent Acquisition of Fossorial Traits in Subterranean Muroids Chapter 4 The Antiquity of Rhizomys and Independent Acquisition of Fossorial Traits in Subterranean Muroids LAWRENCE J. FLYNN1 ABSTRACT In parallel with the growing body of molecular data bearing on the relationships of muroids, particularly subterranean lineages, the relevant fossil record has improved to the point that its data constrain scenarios of evolution about both the timing and mode of evolution of burrowing muroids, especially bamboo rats, blind mole rats, and zokors. Morphologists have considered these groups phylogenetically distinct from each other, but the three lineages appear to be related as a monophyletic Family Spalacidae, sister taxon to all other living muroids, based on both nuclear and mitochondrial genes. Although living genera are fully subterranean, the fossil record shows that the three groups evolved burrowing characteristics independently. Bamboo rats (Rhizomyinae) have the longest fossil record, extending into the Late Oligocene, but do not show fossorial traits until the Late Miocene. Blind mole rats (Spalacinae) have a fossil record nearly that long, and its early members also lack burrowing traits. Zokors (Myospalacinae) show characteristics considered derived relative to other groups, and have a shorter fossil record. The fossil record of the Tribe Rhizomyini, living Asian bamboo rats, extends to about 10 million years ago, with early species distinct at the generic level from living Rhizomys. The oldest well- known species assignable to an extant genus is Rhizomys (Brachyrhizomys) shansius from the early Pliocene of Yushe Basin, China, north of the geographic range of modern Rhizomys.A hypothesis of close relationship of bamboo rats, blind mole rats, and zokors leads to a reevaluation of affinities of certain Asian fossil taxa and reevaluation of polarity of some features, but molecular data are not yet robust enough to clarify interrelationships of the groups. Morphological and fossil data suggest that myospalacines are more closely related to rhizomyines than to spalacines, and that known Early Miocene rhizomyines are close to the stem zokor morphotype. INTRODUCTION like North American gophers and even ‘‘The panoply of adaptations necessary for superficially like lipotyphlan moles. Nevo living underground in tubular burrows has (1999) explored this very subject in his book dramatically defined the blind mole rat on subterranean mammals. Since phenotypic phenotype, which facilitates their diagnosis resemblance of rodent burrowers is not an but obscures phylogenetic connections to especially strong argument for close relation- other muroid rodents.’’ This wonderful state- ship, fossorial lineages have been classified ment from Musser and Carleton (2005) could separately, often at the family level. Ironical- be applied as readily to bamboo rats as to ly, recent molecular work suggests that Spalax, the blind mole rat. Truly subterra- several different burrowers constitute, in fact, nean small mammals are obliged to spend at a monophyletic group. least 95% of the time underground. Given My personal fascination with bamboo rats this condition, adaptive constraints are fo- and relatives began with research on the cused such that phylogenetically remote taxa Siwalik fossil record of the Indian subconti- converge in body form, limb proportions, nent, which contains the lion’s share of what and skull structure. Old World burrowers is known of the history of the group. The like bamboo rats and blind mole rats look Late Tertiary basins of China, in which I 1 Peabody Museum of Archaeology and Ethnology, Harvard University, Cambridge, MA 02138 ([email protected]). 128 2009 FLYNN: ANTIQUITY OF RHIZOMYS 129 have had the pleasure to work with col- the family-level category to recognize these leagues in the field, also produce bamboo subdivisions, others, including Carleton and rats, as well as the endemic fossorial muroids Musser (1984) and McKenna and Bell (1997), known as zokors. It is the fossil record of have elected to give them lower rank China that provides knowledge delimiting the (subfamily), pending more data to clarify origin of the bamboo rat Rhizomys, and interrelationships. Such data are emerging includes remains of other enigmatic muroid from molecular as well as anatomical studies. precursors. These tend to endorse the higher categories This study begins with description of the that are evidenced by morphology (15 oldest fossil skull and postcrania of the genus subfamilies according to Carleton and Mus- Rhizomys, which derives from Pliocene Ep- ser, 1984), and to define clusters of them, och rocks of Yushe Basin, Shanxi Province, which correspond to family-level taxa, fewer People’s Republic of China, and is housed in in number. Current molecular studies (Step- the American Museum of Natural History, pan et al., 2004; Jansa and Weksler, 2004) are New York. It demonstrates the generic beginning to survey Muroidea broadly, but identity of other less complete remains of individual efforts still sometimes miss key bamboo rats from the fossil record of China, taxa. The integrative analysis of Musser and and sheds light on the systematics of older Carleton (2005) draws on molecular and bamboo rats. This analysis leads to a morphological data and recognizes six fam- discussion of the phylogenetic relationships ilies within Muroidea: Platacanthomyidae of bamboo rats and the relevant fossil record, (usually not treated in molecular work), given that recent molecular work argues for Calomyscidae, Nesomyidae, Cricetidae, Mu- strong affiliation with Spalax and with the ridae, and Spalacidae. Steppan et al. (2004) diverse but local zokors of eastern Asia. and Jansa and Weksler (2004) show Spalaci- Previously, most systematists had con- dae to be the sister taxon to all other extant sidered the common origin of bamboo rats, Muroidea. Spalax, and zokors to be remote in time and The family-level taxon Spalacidae has likely not monophyletic. Finally, enigmatic come to be seen as a basal survivor of the elements in the fossil record of China are fabulous radiation leading to crown-group placed in the context of the evolutionary muroids. Spalacidae would be an ancient history of higher muroids, given a hypothesis branch of living Muroidea. Other more of close relationship of these burrowing primitive muroids, logically treated as inde- groups. pendent families, are all extinct. Hence the Eocene and early Oligocene radiations of muroids should be recognized at the family MUROID SYSTEMATICS rank (e.g., Eumyidae, Pseudocricetodontidae, Paracricetodontidae, Eucricetodontidae, Ta- Musser and Carleton (2005) give a thor- chyoryctoididae; see U¨ nay-Bayraktar, 1989), ough accounting of the history of muroid and not lumped in Cricetidae. Coming from classification. For the purposes of this paper, the molecular work, however, is the some- it is sufficient to note that the monophyly of what surprising linkage of Spalax and Muroidea is not a question, nor is (for the Rhizomys + Cannomys + Tachyoryctes with moment) the close relationship of South the fossorial zokor Myospalax. Musser and Asian bamboo rats (Rhizomys and Can- Carleton (2005) illustrate the colorful history nomys) and African mole rats (Tachyoryctes). of classification of these genera and show Relevant to the issues explored herein, that they have been associated in the past, however, is the family-level division of but not usually together to the exclusion of Muroidea and implied close relationships all other muroids. S¸en (1977) did suspect that within those families. these genera belonged together in Family Subdivisions of Muroidea have been evi- Spalacidae. This is an exciting and testable dent for many years, and these are treated hypothesis of relationship that makes review extensively by Musser and Carleton (2005). of the fossil record of these groups relevant. I While many authors have preferred to utilize begin with the bamboo rats. 130 BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY NO. 331 ABBREVIATIONS olingual reentrant on m3, reduced incisive foramina, and a host of fossorial features (chisel incisor, strong coronoid process on AMNH American Museum of Natural deepened mandible, modified humerus with History, New York broad epicondyles and strong deltoid crest, F:AM Frick mammal fossil collection broad skull with flaring zygoma and lamb- of the American Museum of doid crest). The genera Rhizomys and Can- Natural History nomys are distinguished from earlier taxa by Fm. formation the apomorphic high, round infraorbital GSP Geological Survey of Pakistan foramen lacking a ventral slit, and the latter MCZ Museum of Comparative Zoolo- is derived in its short M3 and m2, reduced gy, Harvard University, Cam- posterolophid on m2, and three crests on M2 bridge, MA and m2. Rhizomys has a deep dentary and its THP Tianjin Huang Pei, fossil collec- masseteric crest terminates below the front of tions of the Tianjin Museum of m1 or beyond, without an anterior extension, Natural History, P.R.C. four-crested M1–2 (strong mesoloph), meso- lophid indistinct on m3. The subgenus COMPARISONS: Among a large suite of Brachyrhizomys is characterized by features specimens in the collections of the Vertebrate that are likely primitive: lower crowned than Zoology Division of the AMNH and in the living Rhizomys, m2 longer than wide until MammalDepartmentofMCZ,usefulcompar- late wear, posterolophid on m3 incompletely isons were made among Rhizomys pruinosus isolated, masseteric crest not extending past pruinosus (AMNH 113477), Rhizomys pruino- anterior root of m1,
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