Phylogeny and evolution of the Australo-Papuan honeyeaters (Passeriformes, Meliphagidae)

Abstract

We analyzed nucleotide variation at four loci for 75 species to produce a phylogenetic hypothesis for the Meliphagidae, and to examine the evolution and biogeographic history of the Meliphagidae. Both maximum parsimony and Bayesian methods of phylogenetic analysis were employed. The family was found to be monophyletic, though the genera Certhionyx, Anthochaera, and Phylidonyris were not. Four major clades were recovered and the spinebills (Acanthorhynchus) formed the sister clade to the remainder of the family in most analyses. The Australian endemic arid-adapted chats (Epthianura, Ashbyia) were found to be nested deeply within the family Meliphagidae. No evidence was found to support the hypothesis of separate New Guinean and Australian endemic radiations, nor of a close phylogenetic relationship between taxa from the New Guinea highlands and those from Australian northern rainforests.

Introduction

One of the dominant groups of birds in Australia and New Guinea, both numerically and ecologically, is the passerine family Meliphagidae, the honeyeaters. In certain habitats more than 12 species of honeyeater can co-occur seasonally (Keast, 1985). Although the family has its centers of diversity in Australia and New Guinea, meliphagids are also important endemic elements of the biota of many of the islands in the south Pacific.

Honeyeaters are diverse in size, morphology, and diet. They can be either nectarivorous, insectivorous, frugivorous, or more commonly, a combination of nectar- and insect-eating. Although many species have long, narrow, decurved bills, presumably adapted for nectar-feeding, these species are often insectivorous during certain seasons of the year (Lea and Gray, 1935; Rand and Gilliard, 1968). In Australia, honeyeaters are major pollinators of many endemic plant groups, including Banksia, Dryandra, Melaleuca, Hakea, and Eucalyptus (Paton and Ford, 1977; Recher, 1981). The Meliphagidae are an ecologically and evolutionarily significant element of the Australo-Papuan fauna and yet phylogenetic relationships within this large family are almost entirely unknown.

Traditionally the Meliphagidae were linked with the Nectariinidae (sunbirds) and other nectarivorous birds (Cracraft, 1981; Wetmore, 1960). DNA–DNA hybridization studies (Sibley and Ahlquist, 1985, Sibley and Ahlquist, 1990) and allozyme evidence (Christidis, 1991; Christidis and Schodde, 1991) demonstrated that the honeyeaters belong to a clade originating in the Australo-Papuan region and composed of the Meliphagidae, the Pardalotidae–Acanthizidae (Australasian warblers and allies), and Maluridae (Australasian fairy-wrens and grasswrens). Mitochondrial and nuclear sequence data (Barker et al., 2002; Cracraft and Feinstein, 2000; Ericson et al., 2002a, Ericson et al., 2002b) confirm close affinities between the Meliphagidae, Pardalotidae–Acanthizidae, and Maluridae.

Relationships within the Meliphagidae are poorly understood. There have been no phylogenetic studies of the entire family, but a few studies have examined relationships among some genera (Christidis and Schodde, 1993; Christidis et al., 1993). Published taxonomies for the Meliphagidae lack classification levels between family and genus: no subfamilies or tribes have been proposed (Christidis and Boles, 1994; Schodde, 1975; Schodde and Mason, 1999; Sibley and Monroe, 1990). The number of monotypic genera and the morphological distinctness of most genera have been cited as impediments to determining interrelationships within the family (Schodde, 1975; Schodde and Mason, 1999).

In the last decade, molecular and biochemical studies have modified the traditional composition of the family Meliphagidae. Sibley and Ahlquist (1990) demonstrated that the South African sugarbirds Promerops and New Guinean longbills Oedistoma and Toxorhamphus were not honeyeaters but more closely related to the Nectariniidae (Promerops) and Melanocharitidae (Oedistoma and Toxorhamphus). Sibley and Ahlquist also showed that the Australian chats, Epthianura and Ashbyia (formerly the Epthianuridae), were honeyeaters, a result which was supported by allozyme data (Christidis et al., 1993). In addition, DNA–DNA hybridization (Sibley and Ahlquist, 1990) and DNA sequence (Slikas et al., 2000) studies established that south Pacific Cleptornis was not a honeyeater but instead was closely related to the white-eyes (Zosteropidae). The genus Apalopteron from Bonin Island has likewise been shown to be a white-eye rather than a honeyeater, based on DNA sequence data (Springer et al., 1995). Another genus, Macgregoria, traditionally classified as a bird-of-paradise, was shown to be a honeyeater based on combined analyses of DNA sequence and morphological data (Cracraft and Feinstein, 2000).

Modifying the taxonomic review of the Meliphagidae by Sibley and Monroe (1990) with the recent changes described above, the family now comprises 182 species in 42 genera. Two of these genera (Moho and Chaetoptila) are extinct on Hawaii (Pratt et al., 1987). Australia has over 70 species of honeyeaters (Christidis and Boles, 1994), and New Guinea over 60 species (Beehler et al., 1986). A few genera are distributed across the Lesser Sunda Islands, the Moluccas and Sulawesi. One species of honeyeater, Lichmera limbata, crosses Wallace’s line, but occurs only as far west as Bali (Coates and Bishop, 1997). In the south Pacific, honeyeaters are distributed northwards from New Guinea to the Mariana Islands, as far south as New Zealand, and east to Hawaii (Pratt et al., 1987).

The main goal of this paper is to introduce a phylogenetic hypothesis for the family Meliphagidae. More specific goals are to: (1) examine systematic relationships of some taxonomically unstable genera (e.g., Certhionyx, Phylidonyris, and Meliphaga sensu lato); (2) determine the phylogenetic relationship of the Australian chats (Epthianura, Ashbyia), which are remarkable among the Meliphagidae for their adaptation to arid habitats; and (3) examine the biogeographical history of the family, especially the relationships among the New Guinean and Australian honeyeater faunas. In addition, we wanted to explore the utility of three different categories of genetic loci (mitochondrial protein-coding genes, mitochondrial ribosomal DNA, and a nuclear intron) for reconstructing phylogenetic relationships in such a large, divergent, and relatively old family of passerines.