Molecular phylogeny of the Herpestidae (Mammalia, Carnivora) with a special emphasis on the Asian Herpestes

Abstract

Until now, phylogenetic studies of the mongooses (Carnivora, Herpestidae) have not included an exhaustive sampling of the Asian members of this family. In this study, we used mitochondrial (Cytochrome b and ND2), nuclear (β-fibrinogen intron 7 and Transthyretin intron 1) sequences from almost all of the recognized mongoose species to produce a well-resolved phylogeny of the Herpestidae. We also performed molecular dating analyses to infer divergence dates of the different lineages within the Herpestidae. Our results confirmed the paraphyly of the Herpestes genus and other phylogenetic relationships, which previously had only been moderately supported. The Asian herpestid species were found to form a monophyletic group within the Herpestidae. Within the Asian species, a cyto-nuclear conflict was discovered between the small Indian mongoose (Herpestes auropunctatus), the Indian gray mongoose (Herpestes edwardsii) and the Javan mongoose (Herpestes javanicus), which may have occurred through interspecific hybridization. This study inferred an Early Miocene origin for the Herpestidae and a Middle Miocene origin for the Asian mongooses.

Introduction

The mongooses (Carnivora, Herpestidae) are small-bodied carnivores (total length ranging from 34 to 151 cm, and body weight from 200 g to 5 kg; Gilchrist et al., 2009). The majority are mainly carnivorous, feeding on invertebrates or small vertebrates, while some species are omnivorous (Gilchrist et al., 2009). They are terrestrial and mostly diurnal, although some species, such as the marsh mongoose (Atilax paludinosus), white-tailed mongoose (Ichneumia albicauda) and Meller’s mongoose (Rhynchogale melleri), are crepuscular or nocturnal (Ray, 1997, Kingdon, 1997, Gilchrist et al., 2009). Mongooses occupy a wide range of habitats, from deserts to tropical forests, across their natural range in Africa and Asia (Corbet and Hill, 1992, Kingdon, 1997). This distribution extends to the West Indies, Mauritius, Fiji, Okinawa and Adriatic Islands, where the small Indian mongoose (Herpestes auropunctatus) was introduced for biological control of rodents and snakes (Simberloff et al., 2000, Veron et al., 2007); this is now considered an invasive species in these islands (Morley, 2004, Yamada and Sugimura, 2004, Hays and Conant, 2007). The Egyptian mongoose (Herpestes ichneumon) is found in southern Europe (Wozencraft, 2005) and was also probably introduced in this area (Riquelme-Cantal et al., 2008).

The monophyly of the Herpestidae is supported by morphological (Pocock, 1919, Gregory and Hellman, 1939, Wozencraft, 1989), karyological (Fredga, 1972, Couturier and Dutrillaux, 1985) and molecular characters (Veron et al., 2004, Yu et al., 2004, Flynn et al., 2005, Perez et al., 2006). According to Wozencraft (2005), the Herpestidae comprises 33 species from 14 genera, with only one genus (Herpestes) occurring in Asia.

Previous molecular studies on the Herpestidae (Veron et al., 2004, Perez et al., 2006 and see also Flynn et al., 2005) revealed the existence of two main clades: (i) the true social mongooses (Crossarchus, Helogale, Liberiictis, Mungos, and Suricata), and (ii) the solitary mongooses (including the yellow mongoose Cynictis penicillata, which exhibits some social but not ‘true’ social behaviors; see Veron et al., 2004 for details). These results suggested a single origin for eusociality.

The preliminary results of these molecular studies also highlighted that Herpestes is not monophyletic as the two African species (H. ichneumon and Herpestes naso) are paraphyletic with regards to the Asian Herpestes species (Veron et al., 2004, Perez et al., 2006). This is also supported by karyological data as the Egyptian mongoose (H. ichneumon) displays important differences from the Asian Herpestes species (Fredga, 1972). This result was unexpected because the morphological literature consistently refers to Herpestes as a monophyletic unit (e.g., Taylor and Matheson, 1999). The marsh mongoose (A. paludinosus) and Galerella spp. were also often included in this genus (Fredga, 1972, Taylor, 1975, Wozencraft, 1989, Taylor and Goldman, 1993, Kingdon, 1997).

Veron et al. (2007) showed that the systematics of the Asian mongooses was unclear. This study, using mitochondrial DNA, revealed that the Javan mongoose (Herpestes javanicus) and small Indian mongoose (H. auropunctatus) are two distinct species, whereas previously, using morphological features, they were considered as one species (see Veron et al., 2007 for details). Moreover, the Javan mongoose was found to be the sister-taxon to the Indian gray mongoose (Herpestes edwardsii), rather than to the small Indian mongoose.

The Asian members of the herpestid family were not exhaustively sampled in these previous molecular studies, which only included the Javan mongoose (H. javanicus, sensu Veron et al., 2007), small Indian mongoose (H. auropunctatus, sensu Veron et al., 2007), Indian gray mongoose (H. edwardsii, Veron et al., 2004), and crab-eating mongoose (Herpestes urva, Perez et al., 2006). For this study we used samples from animals captured in the field and from museum specimens from almost all of the recognized mongoose species. For many of the Asian species, this is the first time they have been included in a molecular study of the Herpestidae. The main objective was to unravel the phylogeny of the Asian species and determine their systematic position within the mongoose family. We also aimed to estimate the divergence times within the Herpestidae. For this purpose, we used sequence data from mitochondrial DNA (mtDNA: Cytochrome b [Cytb] and NADH2 [ND2]) as well as nuclear DNA (nDNA: intron 7 of the β-fibrinogen [FGBi7]). Previously published sequences of a nuclear marker (Transthyretin intron 1 [TTRi1]) were also used to support the deepest nodes of the phylogeny.