Molecular systematics and origin of sociality in mongooses (Herpestidae, Carnivora)

Abstract

The Herpestidae are small terrestrial carnivores comprising 18 African and Asian genera, currently split into two subfamilies, the Herpestinae and the Galidiinae. The aim of this work was to resolve intra-familial relationships and to test the origin of sociality in the group. For this purpose we analysed sequences of the complete cytochrome b gene for 18 species of Herpestidae. The results showed that the mongooses were split into three clades: (1) the Malagasy taxa (Galidiinae and Cryptoprocta), (2) the true social mongooses and (3) the solitary mongooses, each group being also supported by morphological and chromosomal data. Our results suggested unexpected phylogenetic relationships: (1) the genus Cynictis is included in the solitary mongoose clade, (2) the genera Liberiictis and Mungos are sister-group, and (3) the genus Herpestes is polyphyletic. We examined the evolution of the sociality in mongooses by combining behavioural traits with the cytochrome b data. Some of the behavioural traits provided good synapomorphies for characterizing the social species clade, showing the potential benefit of using such characters in phylogeny. The mapping of ecological and behavioural features resulted in hypothesizing solitary behavior and life in forest as the conditions at the base of the mongoose clade.

Introduction

The extant mongooses (Herpestidae) comprise 18 genera and 37 species of small terrestrial carnivores, found mainly in Africa, with 8 species of the genus Herpestes occurring in Asia. The recognition of the mongooses as a separate family by Gregory and Hellman (1939) has been confirmed by several studies (Bugge, 1978; Fredga, 1972; Hunt, 1987; Neff, 1983; Radinsky, 1975; Veron, 1995; Wozencraft, 1989; Wurster, 1969), although it was not followed by some authors who continued to include the mongooses in the Viverridae (Coetzee, 1977; Dargel, 1990; Ewer, 1973; Kingdon, 1977; Rosevear, 1974; Taylor, 1988; Simpson, 1945; Skinner and Smithers, 1990).

The phylogenetic relationships among the mongooses have been studied on the basis of morphological features (Baker, 1987; Gregory and Hellman, 1939; Hendey, 1974; Petter, 1969, Petter, 1974; Pocock, 1919; Stains, 1983; Veron, 1995; Wozencraft, 1989), karyological data (Couturier and Dutrillaux, 1985; Fredga, 1972) and allozymes (Taylor et al., 1991). Until the present study, the relationships within the Herpestidae have never been investigated using DNA sequencing data. Wozencraft (1989) considered three subfamilies, namely: (1) the Galidiinae, consisting of the Malagasy species, including the genera Galidia, Galidictis, Mungotictis, and Salanoia, (2) the Herpestinae, including the genera Atilax, Bdeogale, Herpestes, Ichneumia and Rhynchogale, and (3) the Mungotinae, with the genera Crossarchus, Cynictis, Dologale, Helogale, Liberiictis, Mungos, Paracynictis and Suricata. Wozencraft (1989) noted that the relationships within the Mungotinae were poorly understood and suggested two monophyletic groups within the Herpestinae: the Herpestes–Atilax clade and the Ichneumia–Bdeogale–Rhynchogale clade. Many authors (see Allen, 1924; Rosevear, 1974; Wozencraft, 1993) placed four small African species of Herpestes (flavescens, pulverulentus, sanguineus, and swalius) in a separate genus, Galerella, but this group was not recovered by the morphometric study of Taylor and Matheson (1999). The Liberian mongoose (Liberiictis kuhni), seen alive for the first time in 1989 (Taylor, 1992) has been live-trapped and studied for the first time in Ivory Coast by A. Dunham, providing new data on its behaviour. The phylogenetic relationships of this species are unknown but it has been suspected to be close to Crossarchus (Hayman, 1958; Honacki et al., 1982).

The family is currently split into two subfamilies, the Herpestinae (which includes the Mungotinae) and the Galidiinae (Wozencraft, 1993). Some recent studies (Veron, 1995; Veron and Catzeflis, 1993; Yoder et al., 2003) showed that the Malagasy carnivores currently placed in the Viverridae (Cryptoprocta, Eupleres, and Fossa) (Wozencraft, 1993) form a monophyletic group with the Malagasy mongooses (Galidiinae) which are the sistergroup of the other mongooses (Herpestinae).

In some species of mongooses, groups larger than a single family unit are found, and in some cases, individuals live in cohesive packs which forage and den together (Rood, 1983). Ecological and behavioural studies of the dwarf mongoose (Helogale parvula) (Creel and Waser, 1997; Rasa, 1973, Rasa, 1977, Rasa, 1987; Rood, 1978, Rood, 1980, Rood, 1983, Rood, 1987, Rood, 1990), the meerkat (Suricata suricatta) (Clutton-Brock et al., 1999; Ewer, 1963), the common cusimanse (Crossarchus obscurus) (Booth, 1960; Ewer, 1973; Goldman, 1987; Goldman and Dunham, in press; Rosevear, 1974) and the banded mongoose (Mungos mungo) (Cant, 2000; De Luca and Ginsberg, 2001; Hinton and Dunn, 1967; Neal, 1970; Rood, 1975) revealed that they live in cohesive social groups (packs) larger than a single family unit (Rood, 1975), breed cooperatively (lactation of multiple females, adult group members helping to guard and feed the young, coordination system of vigilance, see Clutton-Brock et al., 1999) and forage in packs. The yellow mongoose (Cynictis penicillata) lives in pairs or family groups in habitat similar to that of the meerkat (Cavallini, 1993b; Earle, 1981; Wenhold, 1990). The behavioural and ecological studies of the solitary mongooses have included the marsh mongoose (Atilax paludinosus) (Baker, 1988, Baker, 1989; Ray, 1997), the small Indian mongoose (Herpestes javanicus) (Cavallini and Serafini, 1995; Gorman, 1979), the Egyptian mongoose (Herpestes ichneumon) (Ben Yaacov and Yom-Tov, 1983; Delibes et al., 1984; Palomares and Delibes, 1992, Palomares and Delibes, 1993), the long-nosed mongoose (Herpestes naso) (Ray, 1997), the slender mongoose (Galerella sanguinea) (Baker, 1980; Jacobsen, 1982; Rood, 1989; Rood and Waser, 1978; Waser et al., 1994) and the Cape grey mongoose (Galerella pulverulenta) (Cavallini, 1992; Cavallini and Nel, 1990).

Some solitary mongooses have revealed more complex social systems and inter-individual contacts than expected (Palomares and Delibes, 1993, Palomares and Delibes, 2000) as well as a tendency to become gregarious in some conditions (see Cavallini and Nel, 1990 for Galerella pulverulenta; Rood, 1989; Rood and Waser, 1978; Waser et al., 1994 for Galerella sanguinea; Ben Yaacov and Yom-Tov, 1983; Palomares and Delibes, 1993 for Herpestes ichneumon; Waser and Waser, 1985 for Ichneumia albicauda).

Almost nothing is known about the social behaviour of the black-footed mongoose (Bdeogale nigripes) or of the bushy-tailed mongoose (Bdeogale crassicauda) (Kingdon, 1977), but the latter is believed to be nocturnal and solitary (Sale and Taylor, 1970; Skinner and Smithers, 1990; Taylor, 1987). The behaviour of Asian species (Herpestes brachyurus, H. edwardsii, H. javanicus, H. palustris, H. semitorquatus, H. smithii, H. urva, H. vitticollis) is also poorly known but these species are believed to be solitary (Gorman, 1979; Roberts, 1977) and diurnal (Santiapillai et al., 2000).

The social mongooses are generalized to have diurnal activity, live in open habitat and feed largely on invertebrates, whereas the solitary species are generalized to be nocturnal, live in forested habitats, feed on small vertebrates as well as invertebrates, and larger in size than the social mongooses (Gorman, 1979; Rood, 1986). Carnivores are believed to be primitively solitary, nocturnal forest-dwellers (Rood, 1983) and this is also thought to be the primitive condition for mongooses (Gorman, 1979; Gregory and Hellman, 1939; Savage, 1978).

The social mongooses were suspected to be close together (subfamily Mungotinae; Wozencraft, 1989) but the origin of sociality and of other life traits in the mongooses has never been tested in a phylogenetic framework. The aim of this study was to resolve intra-familial relationships among Herpestidae and to test if the social mongooses really form a monophyletic group, or if sociality has been acquired independently several times in this group (see Rood, 1986). This will also demonstrate if behavioural traits could be appropriate characters for phylogenetic investigations. Mitochondrial cytochrome b has been shown to be useful for elucidating intra-familial relationships within the Carnivora (Dragoo et al., 1993; Dragoo and Honeycutt, 1997; Gaubert et al., in press; Geffen et al., 1992; Koepfli and Wayne, 1998; Kurose et al., 2000; Ledje and Arnason, 1996; Masuda and Yoshida, 1994; Masuda et al., 1996; Veron and Heard, 2000). The present study provides a new data set of complete cytochrome b sequences for 18 species, belonging to 12 different genera of Herpestidae. Seven ecological and behavioural traits have been studied in order to test their evolution in a phylogenetic framework.