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Systematics of Mustelid-Like Carnivores

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Systematics of Mustelid-Like Carnivores SYSTEMATICS OF MUSTELID-LIKE CARNIVORES JERRY W. DRAGOO AND RODNEY L. HONEYCUTT Departmentof Wildlifeand Fisheries Sciences, TexasA&M University,College Station, TX 77843 Present address of JWD: Museumof SouthwesternBiology, Departmentof Biology, Universityof New Mexico, Albuquerque,NM 87131 The phylogenetic relationships of the skunks to the Mustelidae and other caniform carni- vores were examined using mitochondrial-DNA (mtDNA) sequence data from portions of the 12S and 16S ribosomal RNA (rRNA) genes. Data were combined with partial sequences of the cytochrome b gene and morphological data obtained from the literature, and used in a total-evidence analysis. The Mustelidae represented a paraphyletic group, with the skunks (Conepatus, Mephitis, and Spilogale) and the Oriental stink badger (Mydaus) forming a monophyletic clade separate from a clade containing the rest of the Mustelidae and the monophyletic Procyonidae. Within the Mustelidae, minus the skunks and stink badger, only one currently recognized subfamily, the Lutrinae, represented a monophyletic group. The families Phocidae, Otariidae, and Odobenidae formed a monophyletic group that was the sister group to the clade composed of the skunks, procyonids, and mustelids. The families Ursidae and Canidae occurred at the base of the Caniformia clade. It is proposed that the skunks be elevated to the level of family and be referred to as the Mephitidae. The family Mephitidae includes the genera Mephitis (striped and hooded skunks), Conepatus (hog-nosed skunks), Spilogale (spotted skunks), and Mydaus (Oriental stink badgers). Key words: Mephitidae, Mustelidae, Carnivora, skunks, phylogeny, taxonomy In F. Gabriel Sagard-Theodat's "Histoire itinae (skunks), Melinae (badgers), Lu- du Canada," skunks were described as "les trinae (otters), and Mustelinae (the rest of enfants du diable," children of the devil the mustelids). Classically, the Mellivorinae (Coues, 1877; Seton, 1926), and their (honey badger) has been recognized as a unique method of defense and self- fifth subfamily (Anderson, 1989; Simp- preservation has sustained that reputation. son, 1945; Wozencraft, 1993). Wozencraft The enlarged anal scent glands of skunks (1989, 1993) placed the American badger have long been one of the characters that (Taxidea) as a separate subfamily, the Taxid- unites them with the weasel family, Musteli- iinae, and Anderson (1989) recognized the dae. However, this character alone does not South American genera Eira, Galictis, and define the relationship of skunks to any of Lyncodon as components of a distinct sub- the other mustelids. family, the Galictinae. Anderson (1989) also Extant members of the Mustelidae are di- mentioned the possibility of distinguishing agnosed as a monophyletic group on the the South American subgenus Grammogale basis of the loss of the carnassial notch on (genus Mustela) as a distinct subfamily. the upper fourth premolar, the loss of the Not only has the designation of subfami- upper second molar, as well as the enlarged lies in the Mustelidae been problematic, but scent glands (Bryant et al., 1993; Martin, the relationships among taxa within sub- 1989; Wozencraft, 1989). Four, to as many families and among many subfamilies have as seven, subfamilies are recognized cur- been difficult to decipher. The monophyly rently (Anderson, 1989; Eisenberg, 1989; of the North American skunks (Mephitinae) Wozencraft, 1989, 1993). The four sub- is well supported (Anderson, 1989; Dragoo families commonly accepted are the Meph- et al., 1993; Wozencraft, 1989, 1993), with Journal of Mammalogy, 78(2):426-443, 1997 426 May 1997 DRAGOO AND HONEYCUTT-SYSTEMATICS OF SKUNKS 427 three extant genera recognized, including (1993) based on a cladistic analysis of the Mephitis (hooded and striped skunks), Spi- Mustelidae using cranial, post-cranial, and logale (spotted skunks), and Conepatus soft anatomy suggested that Mydaus is a (hog-nosed skunks). Two Old World taxa, member of the Mephitinae. Ictonyx (African zorilla) and Mydaus (Ori- Recent morphological data (several fea- ental stink badger), among others, have tures of the cranium, dentition, and soft been included at various times in the sub- anatomy) have indicated a sister-group re- family Mephitinae. lationship between the Lutrinae and the Me- The inability to determine monophyletic phitinae (Hunt, 1974; Wozencraft, 1989; groups within the Mustelidae has contrib- Wyss and Flynn, 1993). These studies, how- uted to confusion regarding sister-group ever, were interested in higher-level rela- relations within the family. The African tionships and, thus, did not examine rela- zorilla (Ictonyx) has a color pattern that tionships below the familial level, except converges on that of the North American within the Mustelidae, which was analyzed spotted skunks (Spilogale). Many of the at the subfamilial level. early naturalists confused the two genera One of the primary difficulties in deter- (Nowak, 1991). Coues (1877) recognized mining the relationships among subfamilies the African Zorillinae as the Old World of mustelids is the diagnosis of monophy- representative nearest to the Mephitinae. letic groups on the basis of synapomorphies O'Brien et al. (1989), in a protein electro- as opposed to symplesiomorphies. The mor- phoresis study of black-footed ferrets and phological data uniting the skunks with any other weasels in the genus Mustela, used particular subfamily of the Mustelidae, or skunks, including Ictonyx (which was re- even to the family, have been based on ple- ferred to as the African striped skunk) as an siomorphic character states and convergent outgroup. They suggested an ancient split similarity. Recent examinations of non- between the skunks sensu lato and the ge- morphological characters have revealed a nus Mustela. somewhat different picture of relationships Traditionally, Mydaus has been placed of mustelids. For example, Wurster and Be- within the subfamily Melinae, yet some nirschke (1968:374) studied chromosomal consider the Melinae to be a polyphyletic data of various carnivores and indicated that group, primarily based on its inclusion the "skunks are remarkably different from (Bryant et al., 1993; Petter, 1971; Pocock, the rest of the family." These data suggest 1921; Radinsky, 1973; Simpson, 1945). that, karyologically, skunks are apomorphic Earlier researchers (Petter, 1971; Pocock, relative to other mustelids; however, these 1921; Simpson, 1945) suggested a sister- characters provide little information about group relationship between the skunks and the relationships of skunks to the mustelids. the badgers based on similar cranial char- Ledoux and Kenyon (1975) studied serum acters shared by the stink badger and the proteins and suggested that the Mustelinae, Mephitinae. Radinsky (1973) asked the Melinae, and Lutrinae shared a common an- question: Are stink badgers skunks? His an- cestry long after the lineage leading to the swer was inconclusive because the charac- modem Mephitinae diverged. ters he identified as being shared were Recent molecular studies of relationships symplesiomorphies. Although the shared of carnivores based on DNA hybridization characters were plesiomorphic, Radinsky (Arnason and Widegren, 1986; Wayne et al., (1973) argued that the fossil record pro- 1989) suggested that the family Musteli- vided support for the skunks and stink bad- dae is paraphyletic. Although nucleotide- gers being a monophyletic group, with fos- sequence data (Vrana et al., 1994) have pro- sil skunks dating from the Miocene and vided additional support for this observa- Pliocene in the Old World. Bryant et al. tion, these authors did suggest that data for 428 JOURNALOF MAMMALOGY Vol. 78, No. 2 more taxa of both skunks and mustelids vores by increasing the sampling of taxa, es- were needed. Finally, Ledje and Arnason pecially within the family Mustelidae, and (1996) examined sequence data for the en- in so far as possible, taxa were selected in tire cytochrome b gene and concluded that a manner that would allow for the consid- Mephitis and Spilogale were not part of the eration of both morphological and molecu- mustelid clade. lar data. Is the family Mustelidae monophyletic? Part of the answer to this question pertains MATERIALSAND METHODS to the of the placement subfamily Mephiti- Molecularcharacters were used to examinere- nae. The mustelids have been a difficult lationships among 26 species of carnivores to and the Mustelidae is in group classify, (Table 1). Representativesof the Feliformia(Fe- need of systematic revision. The objective lidae andHerpestidae) were used as the outgroup of this research was to address, using a mo- for analyses of the suborderCaniformia, which lecular approach, the phylogenetic relation- includes the skunks and the mustelids. The mo- ships among taxa of mustelids, especially lecular data consisted of mitochondrial-DNA those pertinent to the problem of mono- (mtDNA) sequences obtained during this study phyly of mustelids. Sequence data from two and, wheneverpossible, comparedto data in the GenBank databaseand recent mitochondrial genes (12S and 16S riboso- publications(Ar- nason and Johnsson, 1992; Janczewski et al., mal RNA) were used to assess the phylo- 1992; Vranaet al., 1994). genetic relationships among lineages of car- Total genomic DNA was isolated from frozen nivores, with a focus on primary diagnos- tissue, blood, and skin samples using the the clades within the Mustelidae ing major method of Hillis et al. (1990). Specific regions and examining the relationship of
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