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Origin of Malagasy Carnivora

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Origin of Malagasy Carnivora In: The Natural History of Madagascar (S. M. Goodman and J. Benstead, eds.) University of Chicago Press (in press) Origin of Malagasy Carnivora Anne D. Yoder1,2 and John J. Flynn3 1Department of Cell and Molecular Biology Northwestern University Medical School Ward Building 303 E. Chicago Ave. Chicago, IL 60611 2Department of Zoology Field Museum of Natural History Roosevelt Road at Lake Shore Drive Chicago, IL 60605 3Department of Geology Field Museum of Natural History Roosevelt Road at Lake Shore Drive Chicago, IL 60605 Address correspondence to: Anne D. Yoder Department of Cell and Molecular Biology 303 E. Chicago Ave., Ward Building Chicago, IL 60611-3008 e-mail: [email protected] phone: 312-503-0005 fax: 312-503-7912 Introduction As with the primates, the phylogenetic status of Malagasy Carnivora is of great significance for biogeographic theory generally, but most especially, for understanding the biogeographic history of Madagascar. Multiple phylogenetic origins, and thus multiple biogeographic invasions of Madagascar, have been proposed for the Carnivora. This proposal is almost certainly due to the morphological and ecological diversity apparent among these animals with at least three distinguishable morphological and ecological types among the seven recognized genera of Malagasy Carnivora. Four of the genera (Galidia, Galidictis, Mungotictus, and Salanoia) are described as "mongoose-like" and their common names reflect this distinction (e.g., Galidia is known as the "Malagasy ring-tailed mongoose"). All four genera weigh between 600 - 900 g, have agile, low-slung bodies, short legs, and long bushy tails. Crania are typically elongate and dorso-ventrally flattened with pointed muzzles; diet consists primarily of small vertebrates and insects (Albignac 1972; Albignac 1984) (see also pp. xx). The second morphological type, the Malagasy civets, comprises the two genera Fossa and Eupleres. Although these two taxa are considerably different from each other, both are considerably larger than the mongoose types and have longer legs relative to body length. Eupleres is remarkable for its unusual diet that consists chiefly of earthworms (Albignac 1984) and for the concomitant suite of craniodental specializations. Fossa and Eupleres both demonstrate physiological specializations that allow for fat storage in the tail during Madagascar's winter months. The third morphological type, represented by the monotypic genus Cryptoprocta, is unique. Commonly known as the "fosa" (not to be confused with the genus Fossa), Cryptoprocta weighs between 7-12 kg and is the largest member of Madagascar's extant Carnivora (see pp. xx). It is a powerful predator and excellent climber, known even to hunt and 2 capture lemurs. Like cats, Cryptoprocta has retractile claws, but like bears, its gait is plantigrade (Albignac 1972). Malagasy Carnivora diversity has been variously described by systematists. Gregory and Hellman's (1939) extensive analysis of the morphology, evolution, and classification of "civets" placed the Malagasy Carnivora in four taxa: Euplerinae (close to Asian hemigalines) and Fossinae within one lineage of Viverridae, Galidictinae as a basal lineage of Viverridae, and Cryptoproctinae within Felidae. Simpson (1945) placed them all in the family Viverridae and defined seven genera within three subfamilies: Galidiinae (the mongooses), Hemigalinae (including various Asian taxa with the Malagasy civets placed in the monotypic tribes Fossini and Euplerini, and Cryptoproctinae). Most recently, Wozencraft (1993) revised this arrangement by placing the Malagasy Hemigalinae into the Family Herpestidae (not recognized as a family by Simpson, 1945), raising the two monotypic tribes to subfamilies Euplerinae and Fossinae. Thus, at present, there are two families and four subfamilies that contain only seven genera. Furthermore, there is no consensus of opinion as to whether the various subfamilies are each more-closely related to continental Carnivora lineages (thus implying multiple colonizations of Madagascar) or whether they comprise a monophyletic lineage (various opinions can be found in Pocock 1916; Gregory and Hellman 1939; Albignac 1972; Hemmer 1978; Albignac 1984; Wozencraft 1989; Veron and Catzeflis 1993; Veron 1995). In particular, the position of Cryptoprocta has been controversial (Flower 1869; Pocock 1916; Gregory and Hellman 1939; Beaumont 1964; Hemmer 1978; Wozencraft 1989; Veron and Catzeflis 1993; Veron 1995). Thus, in addition to biogeographic and evolutionary implications, phylogenetic resolution can have significant consequences for Carnivora systematics as a whole. If, for example, the 3 Malagasy taxa are discovered to comprise a clade, then Wozencraft's (1993) designation of either Herpestidae or Viverridae (or both) becomes paraphyletic, profoundly affecting our understanding of higher-level Carnivora phylogeny and evolution. Cladistic and/or genetic investigations of Malagasy Carnivora phylogeny have been extremely limited. Early chromosome phenetic analyses concluded that the group is diphyletic or polyphyletic, representing two different invasions of Madagascar (Couturier et al. 1986; Razafimahatratra 1988), whereas a more recent DNA sequencing study (Slattery and O'Brien 1995) found that Fossa and Galidia comprise a clade. Taxon sampling in the second study was so limited, however, that the results do not bear significantly on the question of Malagasy Carnivora monophyly (i.e., Fossa was the only «viverrid» and Galidia the only «herpestid» included in the study). Other notable studies to have addressed the phylogeny of Malagasy Carnivora were focused on Cryptoprocta and included a DNA hybridization (Veron and Catzeflis 1993) and a cladistic analysis of morphological characters (Veron 1995). These two studies came to differing conclusions. The DNA hybridization study found that Cryptoprocta has affinities within the Herpestidae rather than the Viverridae (Fig. 1) whereas the morphological study grouped it with the Felidae, as did Gregory and Hellman (1939) (Fig. 2). The morphological study found the Malagasy mongooses to belong with other herpestids, although the two Malagasy civet genera were shown to occupy unresolved positions at the base of a combined herpestid/hyaenid clade. Flynn and Nedbal's (1998) cladistic analysis of nuclear transthyretin intron I sequence data strongly supported linking Galidia, the only Malagasy carnivoran included in the study, as sister taxon to other herpestids. Several observations can be made from a comparison of these studies: 1) an apparent conflict exists between morphological and molecular resolutions of 4 Cryptoprocta's position in the Carnivora phylogeny; 2) the placement of Malagasy mongooses within the Herpestidae may be well-justified on morphological grounds; and 3) the karyotypic and morphological data indicate that there may have been between two to four invasions of Carnivora lineages to Madagascar. To resolve these biogeographic and systematic issues, we have performed phylogenetic analysis on DNA sequences from three unlinked genetic markers: mitochondrial DNA (specifically, the cytochrome b and ND2 genes), the nuclear gene transthyretin (TR, intron I) and the nuclear interphotoreceptor retinoid-binding protein (IRBP, exon I). These markers were chosen because they are unlinked and should therefore provide independent estimates of Malagasy Carnivora history and also because they represent both coding (cytochrome b, ND2, and IRBP) and non-coding (TR) sequences, thereby providing both functional and neutral characters for phylogenetic analysis. Moreover, all four genes have been demonstrated to be informative for questions of both deep and recent mammalian interrelationships (Stanhope et al. 1996; Yoder et al. 1996; Zardoya and Meyer 1996; Flynn and Nedbal 1998; Yoder and Irwin 1999; Flynn et al. 2000). Materials and Methods DNA was extracted from either fresh or museum tissues for all Malagasy taxa; outgroup sequences were either extracted de novo or taken from GenBank (see Yoder et al., (in prep.) for voucher and accession numbers). All cytochrome b and IRBP DNA sequences were generated at Northwestern University while those for TR and ND2 were generated at the Molecular Systematics Laboratory at the Field Museum of Natural History. This separation of lab procedures and reagents further assures that the 5 phylogenies generated for each gene are independent. Extractions and sequencing followed methods detailed in Yoder et al. (1996) and Flynn and Nedbal (1998). PAUP* 4.0b2a (PPC) was employed for all phylogenetic analyses as well as for bootstrap tests of node support (Swofford 1998). Results and Discussion In Figure 3 we illustrate the results of the maximum parsimony analysis of the four genetic markers. For both of the mitochondrial data sets, a step matrix was imposed that weights transversions 10 times more heavily than transitions (i/v10 weighting). This follows the observation that transversions occur considerably more frequently than transitions in the evolution of mitochondrial DNA (Irwin et al. 1991; Wakeley 1996; Yang and Yoder 1999). For both of the nuclear data sets, all characters were equally weighted. A number of results are universal to the four maximum-parsimony gene trees. Most importantly for the focus of this contribution, Malagasy Carnivora are consistently shown to form a clade, and always with strong statistical support (bootstrap values between 71% and 99%). Within this clade, the mongoose "types" (Galidia, Galidictis, Mungotictis, and Salanoia,
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