A phylogeny for the Cisticolidae (Aves: Passeriformes) based on nuclear and mitochondrial DNA sequence data, and a re-interpretation of an unique nest-building specialization

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Abstract

Based on some general similarities in feeding adaptations, a large number of Old World passerine birds were in the past lumped in one broad family, the Sylviidae. Recent molecular studies, starting with the DNA–DNA hybridization work by Sibley et al. [Sibley, C.G., Ahlquist, J.E., 1990. Phylogeny and Classification of Birds: A Study in Molecular Evolution, Yale University Press, New Haven, CT], have revealed that this group is in fact a paraphyletic assemblage, mainly in the superfamily Sylvioidea, and within this assemblage a distinct group (the Cisticolidae) can be identified around the genus Cisticola. In this study we try to define natural lineages within it, based on DNA sequence data from 35 ingroup taxa representing 12 putative genera. Both nuclear myoglobin intron II (630 bp in our study) and mitochondrial ND2 (1041 bp) genes were sequenced, and 1671 bp were aligned and subjected to parsimony, maximum likelihood and Bayesian analyses. The results strongly support the monophyly of a cisticolid clade, with the Malagasy warblers Neomixis constituting the deepest branch within the clade. Three major clades receive statistical support, but not all relationships between and within these are well resolved. All species of the genus Bathmocercus belong to the Cisticolidae but in two different clades. The tailorbirds appear also polyphyletic with most species of the genus Orthotomus (but O. cucullatus falling in the outgroup) and the African metopias being in two different clades. Also the genus Apalis is polyphyletic, but all other included genera seem to be confirmed as natural units. Based on these findings we resurrect the genera Scepomycter and Artisornis. Calamonastes is confirmed to be in the Cisticolidae and grouped with Camaroptera. Main basic nest types do not follow the phylogenetic branching, and notably the peculiar “tailorbird” technique of stitching leaves together around the nest is found in different parts of the phylogeny. The basic types of nests seem to be found in particular environments, and the sewing may therefore have evolved in some ancestor of the Cisticolidae and was later lost or modified in some genera or species following the spread of drier habitats from the mid-Miocene.

Introduction

Early classifications of oscine birds included in the family of Old World Warblers, the Sylviidae, a wide range of small foliage-gleaning oscine birds with slender bills, in some cases even including the Australo-Papuan malurid wrens and the Australasian acanthizids warblers (Sharpe, 1909). Over the years, some odd subgroups were removed from the family, but still after Beecher’s (1953) seminal analysis of oscine relationships based mainly on the jaw musculature, the Sylviidae was defined as a very broad group with 60–63 genera, nearly half of which were monotypic (Morony et al., 1975, Watson et al., 1986, Howard and Moore, 1991).

The old world warblers show a high percentage of species and genera of uncertain affinities, due to the lack of discrete character states defining lineages, and aggravated by the insufficient knowledge of their anatomy, natal and juvenile plumages, nests and eggs (Hall and Moreau, 1970, Urban et al., 1997). Several authors (Chapin, 1953, Hall and Moreau, 1970, Watson et al., 1986) had limited success with establishing relationships among old world warblers based on morphology, the ecological and behavioural characters such as vocalizations and shapes and structures of nests. Molecular studies would certainly give completely new insights concerning evolutionary units in the warbler assemblage (see Alström et al., 2005), and would thereby also allow new interpretations of ecological adaptations.

The DNA–DNA hybridization work by Sibley and Ahlquist (1990) represents the first major step in this direction, as it provided strong evidence for regarding the Old World Warblers as a paraphyletic complex, where groups of birds traditionally perceived as “warbler” formed several independent radiations, mainly within the superfamily Sylvioidea (Sibley and Monroe, 1990), and with the type genus Sylvia embedded in the radiation traditionally referred to as babblers (Timaliidae) (Cibois, 2003). Among the suggested independent warbler radiations was the “cisticolid” group, which included at that time the representatives of six genera of African “grass” and “tree warblers” (see Table 1). Sibley and Monroe (1990), in their attempted new avian classification, expanded the cisticolid group to all the species traditionally included in these six genera, as well as all the species of the genus Calamonastes and seven other monospecific genera (see Table 1).

Since 1990, the number of genera currently assigned to this Cisticolidae family has grown from 14 (Sibley and Monroe, 1990), 19 (Dowsett and Forbes-Watson, 1993), 15 (Clements, 2000) to 21 recently (Dickinson et al., 2003), potentially extended to 25 with four uncertain genera (Table 1). The whole list given by Dickinson et al. (2003) represents about 130 species, very unevenly distributed between genera, (45 in Cisticola, 21 in Prinia, 21 in Apalis, but 16 monotypic genera). According to all these authors, the demarcation of the family remains problematic. Results of the first DNA sequence analyses (Cibois et al., 1999, Sefc et al., 2003) marginally covering the Cisticolidae proved the inclusion in this family of representatives of seven genera (including Cisticola), most of them integrated in the Cisticolidae by Dickinson et al. (2003) and adding Orthotomus (Asian Tailorbird) and the endemic genus Neomixis of Madagascar (three species, N. flavoviridis excluded, see Cibois et al., 2001). Recently, Beresford et al. (2005) added Euryptila subcinnamomea, and Alström et al. (2005), excluding Rhopophilus pekinensis, expanded the Cisticolidae with Bathmocercus cerviniventris, Heliolais erythropterus and Spiloptila clamans.

Most old world warblers build open-cup nests made of dry materials roughly interwoven with surrounding stems and grasses. Some others build domed nests or developed a deep bag-like nest with no roofed structure, bound together with the cobwed and hung from twig at the edge of a bush (Chapin, 1953, Urban et al., 1997). The Cisticolidae are remarkable in showing all these diverse nest types with various shapes. In addition, certain Cisticolidae have a noteworthy behaviour; they use cobwed, silk or fine vegetables fibres to bind and stitch together the margins of broad, usually green leaves, as a protective—and camouflaging—purse around the nest: they are called “tailorbirds”. As such this very special behaviour is unknown in other birds (Chapin, 1953, Urban et al., 1997).

The purpose of the present study, which is the most taxon-dense analysis of the Cisticolidae based on nuclear and mitochondrial DNA sequence data, is to provide a more detailed resolution of this family, and to define the phylogenetic relationships of some odd species and genera. We will in particular highlight the cases of tailorbirds, genera Orthotomus and Artisornis which form one genus in some classifications, and of Bathmocercus. Furthermore, we examine whether a well resolved phylogenetic hypothesis can throw new light on the adaptation of the basic nest types as well as on evolution of nest building technique within the Cisticolidae.

For this study, two genes have been used, one mitochondrial (ND2) and one nuclear (myoglobin intron II). These two genes, used by several studies to investigate phylogenies of passerines relationships, have given good results concerning relationships at the family and genus levels.

Section snippets

Taxon sampling

The biological material used for this study comprises tissue from fresh specimens as well as samples from skin of specimens. The fresh tissue, blood and flesh of birds preserved in alcohol or buffer solution, come from the tissue banks of the MNHN (Paris), of the Field Museum of Natural History (Chicago), and of the Zoological Museum (Copenhagen), while the skin of specimens was taken in the collections of the “Museum National d’Histoire Naturelle”.

The species taxonomy used in this study

DNA sequences

We were unable to obtain ND2 sequences for Calamonastes simplex, Cisticola brachypterus and C. juncidis as well as Sylvietta whytii; these species were therefore excluded from the separate ND2 and combined analyses. The obtained sequence data consisted of 630 bp for myoglobin intron II and 1041 bp for ND2, corresponding to the positions 5241–6281 of the chicken mitochondrial sequence (Desjardins and Morais, 1990). Sequence length in myoglobin intron II ranged from 573 bp (Camaroptera brevicaudata)

Discussion

Since the work of Sibley and Ahlquist (1990), which suggested the existence of a Cisticolidae family, five molecular studies have all recovered this lineage and have included additional genera (Cibois et al., 1999, Cibois et al., 2001, Sefc et al., 2003, Beresford et al., 2005, Alström et al., 2005). Our study also recovers this cisticolid clade, which regroups all the included genera from this study presented as Cisticolidae by Dickinson et al. (2003). This clade includes also part of the

Acknowledgments

We are grateful to the various researchers and institutions that provided several samples for our study, especially John Bates of the Field Museum of Chicago and also Michel Clouet who provided the sample of Incana incana. We thank Céline Bonillo and Josie Lambourdière for their technical assistance during laboratory work and Jérôme Fuchs for analytic expertise. This work was supported by the “Service de Systématique Moléculaire” of the “Museum National d’Histoire Naturelle” in Paris.

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