Mitochondrial DNA phylogeny of babblers (Timaliidae)

The Auk 120(1):35-54, 2003

ABSTRACT.-The systematics of the babblers (Timaliidae) and related members of the Old World insectivorous passerines have been particularly difficult. To clarify our understanding of this group, phylogenetic relationships were constructed using sequences of three mitochondrial genes (cytochrome b, rRNA 12S and 16S). The results indicated that several species traditionally placed among babblers, the shrike babblers (Pteruthius) and the Gray-chested Thrush Babbler (Kakamega poliothorax), are not related to the Timaliidae, but belong to other passerine groups. Furthermore, the phylogenetic hypotheses inferred from molecular data suggest that the babblers assemblage includes two other oscine taxa traditionally considered to be distantly related, Sylvia (Sylviidae) and Zosterops (Zosteropidae). The polyphyly of several babbler genera is discussed, with particular attention to the laughingthrushes (genera Garrulax and Babax) for which the phylogeny is compared to previous hypotheses of relationships. Results from different tests under the maximum-parsimony and maximum-likelihood criteria indicate the rejection of the hypothesis of monophyly for the laughingthrushes group. Thus, the molecular phylogeny challenges the traditional classification of the Timaliidae. Received 26 February 2002, accepted 14 December 2002.

THE FAMILY TIMALIIDAE, the babblers, comprises more than 200 species, primarily forest birds, distributed for the most part in Indo Malayan Asia and Africa. Babblers have often been placed in the "Old World insectivorous" group, the Muscicapidae sensu lato, which includes various other passerines like the Turdidae (thrushes), Muscicapidae (flycatchers), and Sylviidae (warblers) (Hartert 1910, Mayr and Amadon 1951, Deignan 1964, Morony et al. 1975). Morphologically, babblers differ from thrushes and flycatchers by the lack of distinct juvenal plumage, and they differ from warblers by heavier size and shape, as well as being nonmigratory (McClure 1974). Babblers display great diversity in size, bill shape, and plumage coloration, and perhaps the most reliable character that unites babblers is their high sociability. They often gather in parties and flocks, and some species cooperate in nesting activities and communal defense (Lack 1968, Grimes 1976, Zahavi 1976, Gaston 1977). Most babbler species clump together when perched during the day and while roosting at night, and mutual preening is observed in many species (Simmons 1963).

Delacour (1946, 1950) conducted the main systematic review of the group. He defined 252 species in 47 genera, distributed into six tribes: Pellorneini, Pomatorhinini, Timaliini, Chamaeini, Turdoidini, and Picathartini (Table 1). Delacour's taxonomic list was proposed to follow a sequence from "primitive" (Pellorneini) to "derived" taxa (Picathartini), based mostly on his observation of plumage coloration (duller, more primitive) and bill shape. According to Delacour, the Old World warblers (Sylviidae) were the sister group of the Timaliidae. Since Delacour's work, the systematics of babblers has been the subject of limited revisions, dealing mostly with generic limits and definitions. The jungle babblers, genus Trichastoma and related genera, have been revised on the basis of phenetic analysis of morphological and ecological characters (Ripley and Beehler 1985). Other systematic works included considerations of morphological similarities, but no taxonomic decisions were based on discontinuous variation (Irwin 1983; Harrison 1986a, b; Van de Weghe 1988). Thus, the diagnosis and taxonomic sequence of the babblers given by Delacour has been largely followed by subsequent authors (including Peter's Checklist, Deignan 1964), until Sibley and Ahlquist's attempt to clarify the phylogeny of the Timaliidae using DNA hybridization (Sibley and Ahlquist 1982, 1990). They proposed important reevaluations of the systematics of several taxa traditionally placed among babblers. Firstly, they showed that the Australian and New Guinean genera (Garritornis and Pomatostomus) are in fact members of the Corvoidea, despite their morphological and ecological similarities with the Asian scimitar babblers (Pomatorhinus). Secondly, they suggested that the African rock-fowls (Picathartes), whose taxonomic position has long been debated (Lowe 1938, Webb 1949, Delacour 1950, Delacour and Amadon 1951, Mayr and Amadon 1951), are not closely related to the babblers, although their analysis failed in finding the sister group of that genus (Barker et al. [2002] confirmed with nuclear DNA sequence data that Picathartes does not belong to the core Sylvioidea). The phylogenetic tree obtained by Sibley and Ahlquist is presented in Figure 1. The main results are that (1) the laughingthrushes (Garrulax) are sister taxa to all other babblers; (2) the warbler genus Sylvia belongs to the babbler group, and is sister taxon to the Wrentit (Chamaea fasciata); and (3) all other African and Asian babblers studied are grouped together. However, those results should still be considered as provisional because of the low number of taxa studied (11 species for 9 genera), and methodological problems affecting their analysis of hybridization distances (Lanyon 1992, Mindell 1992). A previous cytochrome b study including a small number of babblers also placed Sylvia among babblers (Fjeldsa et al. 1999).