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A report on the results of phylogenetic analyses of the endemic African …


Biology Articles » Biogeography » Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily » Background

Background
- Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily

Rodents are the most speciose mammalian order and comprise almost half of all mammalian species diversity [1]. Within Rodentia, the most diverse assemblage is the superfamily Muroidea, with a global membership of 1300 living species and a natural distribution that includes all continents except Antarctica and all but the most remote islands. This remarkable group also includes the commensal rats and mice, long despised as human pests and agents of disease [2], but now highly valued as model organisms for research related to human health [3,4].

Not surprisingly, morphology-based classifications of muroid rodents were beset by problems of parallel evolution, with many common adaptations evolving independently on different landmasses. Molecular phylogenetic analyses are much less constrained by this problem and recent studies using slowly evolving nuclear genes have done much to clarify the membership and structure of Muroidea [5-7]. Recent classifications of this group recognize five or six family level lineages [7,8]. The speciose family Muridae Illiger, 1811 (150 genera and 730 species) is divided by Musser and Carleton [8] into five subfamilies, of which the Murinae Illiger, 1811 is the most diversified (126 genera, 561 species). Within the family Muridae, there is strong molecular support for three subfamilies (Deomyinae, Gerbillinae, Murinae) [subfamily Leimacomyinae of Musser and Carleton [8] has not yet been surveyed], and for a link between Deomyinae and Gerbillinae, with these as a sister clade to Murinae (this latter subfamily encompassing otomyines) [5-7].

The subfamily Murinae has a natural distribution that spans the Old World, including all of Africa and Eurasia, and extending to Australia, New Guinea and many islands of the western Pacific (we do not consider here the human-mediated distribution of a few commensal rodents of the genera Mus and Rattus in the Americas and throughout oceanic islands). More than 500 species are currently recognised [8], with centers of diversity and endemism in each of Tropical Africa, Southeast Asia, and the Australo-Papuan region [9,10]. Despite the obvious significance of this group for biogeographic studies, previous molecular studies have either had specific regional foci (e.g. Africa [11-13]; Philippines: [14]; Australia: [15,16] ; Eurasia: [17,18]) or employed immunological methods of uncertain reliability [10]. These studies have encouraged regionally-based classifications at tribal or subfamilial level, especially within the Australasian and Philippine regions where various higher level groupings are sometimes recognized (e.g. Anisomyini, Conilurini, Hydromyini, Phloeomyinae, Pseudomyinae, Rhynchomyinae). In Africa, Ducroz et al. [12] designated a tribe Arvicanthini for one well-supported monophyletic group. The most recent, global classification of Murinae [8] abandons the tribal level of classification in favour of a less formal arrangement of genera into divisions, following and improving a system already employed by Misonne [9]. Specifically, Musser and Carleton [8] (2005: pages 902 – 905) organize the 126 genera of the subfamily Murinae into 29 divisions, and consider the living taxa Myotomys, Otomys, and Parotomys as members of the subfamily Otomyinae.

Africa supports more than 25% of all living murine species including representatives of 32 endemic genera [8]. All African murines are endemic at species level and only two genera are shared between Africa and Eurasia. One of these is the genus Mus, which is widespread across Eurasia and is represented in Africa by an endemic subgenus, Nannomys, the African pigmy mice [19-21]. The second is the primarily African genus Myomyscus which has one species (M. yemeni) native to the Arabian Peninsula. A single origin for all African Murinae, except possibly Dasymys, was proposed by Watts and Baverstock [22] based on their analyses of albumin microcomplement fixation. In contrast, Chevret's [23] studies using the DNA/DNA hybridization method found a minimum of three ancient African lineages within Murinae, each associated with Eurasian taxa. Later studies using direct sequencing methods supported the notion of polyphyly for African Murinae, e.g. [12-14,16,24]. Jansa et al. [14] identified three distinct groups: the 'Arvicanthines' (sensu Ducroz et al. [12]), a 'Praomys group' (sensu Lecompte et al. [25]) and the genus Malacomys. The 'otomyines', a dentally distinctive African lineage with three genera (Myotomys, Otomys,Parotomys), are variously associated in molecular studies with either the Praomys group [10] or the arvicanthines [6,11,12,16,24]. Ducroz et al. [12] suggested recognition of this group at tribal rank, as Otomyini. However, Musser and Carleton [8] follow more traditional practice by recognizing a distinct subfamily Otomyinae within Muridae.

Numerous questions thus remain unresolved concerning the pattern and timing of African Murinae diversification. In particular, the relationships of the various African lineages with Asian genera are enigmatic, and the timing of most cladogenic events remains poorly resolved or understood. The latter issue is critical to understanding the history of faunal interchange via the Arabian plate following the collision of Africa with Asia around 16 and 20 Million years ago (Mya) [26,27]. Notably, the murine palaeontological record attests to the presence of some shared genera in Africa and Asia during the late Miocene and the Pliocene [28-30], but whether this is due to multiple faunal exchanges between Asia and Africa, to the presence of ancient shared lineages followed by vicariance, or else to convergent evolution, remains a matter of conjecture.

To more adequately assess the pattern and timing of faunal exchanges between Africa and Asia, it is necessary to first establish a more complete phylogenetic framework including all of the key African and Eurasian lineages, and then to derive reliable estimates of divergence times. The main objectives of our study are: (1) to provide a robust and comprehensive phylogeny of the extant African murines and to infer their relationships with the Asian Murinae using mitochondrial and nuclear gene sequences, (2) to provide a new systematic framework that accurately reflects the phylogeny of Murinae; (3) to estimate times of origin and diversification for the African murines lineages; and (4) to place this phylogeny in an historical and geographical context to gain insight into the origin and maintenance of African murine diversity.


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