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Copyright © 2005 The Royal Society African endemics span the tree of songbirds (Passeri): molecular systematics of several evolutionary ‘enigmas’ *Author for correspondence (Email: pberesfo/at/botzoo.uct.ac.za). Received August 25, 2004; Accepted October 25, 2004. | |||||||
Abstract The deep divergence between the African endemic passerines Picathartidae (rockfowl Picathartes and rockjumpers Chaetops, four species) and the Passerida (ca. 3500 species) suggests an older history of oscines on the African continent than has previously been assumed. In order to determine whether any additional, unexpectedly deep lineages occur in African endemic songbirds, 29 species—including 10 enigmatic focal taxa endemic to southern Africa—were added to a large nuclear sequence dataset gathered from oscine songbirds (Passeri). Phylogenetic analyses of these data resolve many long-standing questions about the affinities of these birds, not all of which were predicted by traditional approaches. The application of a molecular clock indicates that most basal divergences in Passerida occurred in the middle to late Eocene, with divergences between African and Australasian core corvoids occurring somewhat later in the early Miocene. Consistent with inferences for mammals, divergences between Malagasy endemic passerines and their mainland relatives suggests an asynchronous colonization history. This emerging phylogenetic picture reveals that relationships within Old World families are highly informative regarding the early dispersal and radiation of songbirds out of Gondwana. Future analyses will depend on improving resolution of higher-level phylogenetic relationships among these groups, and increasing the density of taxon sampling within them. Keywords: oscines, Africa, Madagascar, Picathartidae, Old-World warbler | |||||||
1. Introduction The application of molecular systematics to the phylogeny of perching birds (Aves: Passeriformes) is providing robust hypotheses of their early history and evolution. Studies using different taxon and character sampling (Barker et al. 2002; Ericson et al. 2002a,b; Ericson & Johansson 2003; Barker et al. 2004) have corroborated a Gondwanan origin for basal branches of suboscines and oscines (Cracraft 2001), and suggest that major revisions to the widely accepted classification of Sibley & Ahlquist (1990) are necessary. The changing topology has already had an effect on reconstructing the evolution of cooperative breeding (Cockburn 2003), and similar insights into other features of life history and behavioural ecology may be anticipated as the passerine tree is resolved. Resolution of the oscine songbird tree promises to provide clues to the phylogenetic and spatial history of its large and often rapid radiation. In this respect, some of the more intriguing results of the molecular systematics analyses are indications that many early divergences involve African endemics. For instance, the emerging molecular phylogeny suggests that the sub-Saharan African rockfowl (Picathartes) and rockjumpers (Chaetops)—placed incertae sedis between Corvida and Passerida by Sibley & Ahlquist (1990)—may be the most basal branch within or sister to the Passerida (Ericson & Johansson 2003; Barker et al. 2004), an extremely speciose clade (approximately 3500 species) of phenotypically diverse oscine passerines. Although the recent analyses have suggested new, previously unrecognized relationships, as well as increasing signal for some higher-level groups (families and superfamilies), many relationships remain unresolved. While elements of Sibley & Ahlquist's (1990) passeridan superfamilies Muscicapoidea, Sylvioidea and Passeroidea have been corroborated, novel nodes of equivalent rank have emerged, rendering families as well as superfamilies paraphyletic. Thus, wrens, nuthatches and creepers form an assemblage termed the Certhioidea (Cracraft et al. 2004). Another example is Sibley & Ahlquist's (1990) Muscicapoidea, which is suggested to exclude Bombycillidae (Barker et al. 2002; Ericson & Johansson 2003; Cibois & Cracraft 2004; but see Barker et al. 2004) and current studies conflict regarding the relationships among the remaining muscicapid families (Cibois & Cracraft 2004; Voelker & Spellman 2004). Intriguingly, monophyly of both the superfamily Muscicapoidea and the traditional family Monarchidae is violated by recovery of a group of insectivorous ‘flycatching’ taxa that include genera (the African Elminia and Asian Culicicapa) from both of these groups (Pasquet et al. 2002; Barker et al. 2004). The superfamily Passeroidea has received consistent support for the core members plus sunbirds (Nectariniidae) and fairy bluebirds and allies (Irenidae; Ericson & Johansson 2003; Barker et al. 2004), but a new clade not predicted by traditional taxonomy was recovered by Barker et al. (2004), including the southern African sugarbirds (Promerops), spot-throats (Arcanator) and dapple-throats (Modulatrix) as sister to the remaining Passeroidea. The emergence of these new clades, including deeply divergent African endemics, taken in consideration with the basal position of picathartids in Passerida, imply that other African birds traditionally considered ‘relict’ or ‘enigmatic’ (see Clancey 1986) might also provide information about deeper branches in the oscine songbird tree. Here, 29 new passerine taxa, including 10 purportedly ‘paleoendemic’ species selected for special attention, were added to the dataset of Barker et al. (2004). Ongoing revision of the oscine songbird tree promises to provide not only phylogenetic clues to the reconstruction of its large radiation, but also may yield critical data on its timing. Previous molecular analyses suggested that Passerida arrived in Africa following dispersal across Eurasia in the earliest Miocene, 25 Within the African biotic region, the temporal assembly and geographical origins of the Malagasy fauna remains an area of particular controversy. Madagascar rifted from continental Africa early in the break-up of Gondwana (approximately 160 | |||||||
(a) Taxon sampling Our taxon sampling was focused on passerine species and groups endemic to sub-Saharan Africa, with an emphasis on southern Africa (see table 1 for an overview of their taxonomic status). The species included in this study are listed in Electronic Appendix part A and include representatives of 41 families. In particular, we sampled both genera of Picathartidae (Picathartes and Chaetops), which have been placed incertae sedis by Sibley & Ahlquist (1990) between the oscine parvorders Corvida and Passerida, and which have received weak support as being part of the first branch within the Passerida (Ericson & Johansson 2003; Barker et al. 2004). We have included samples of the enigmatic Herero chat (Namibornis herero), white-tailed shrike or chatshrike (Lanioturdus torquatus), and nicators (Nicator chloris) in order to test their association with the Saxicolini, Malaconotini, and Pycnonotidae, respectively. We have included multiple representatives of the so-called African warblers (Cisticolidae), including the tailorbird (Orthotomus sutorius) which mitochondrial DNA (mtDNA) sequence data place with this group (Cibois et al. 2001), and the cinnamon-breasted warbler (Euryptila subcinnamomea), whose association with the group has not been tested. We have also sampled a wide variety of Old World warbler taxa with uncertain and controversial affinities, including Victorin's warbler (‘Bradypterus’ victorini), the Cape grass-warbler (Sphenoeacus afer), the fairy flycatcher (Stenostira scita), a crombec (Sylvietta), a longbill (Macrosphenus), the hylia (Hylia prasina), the fan-tailed grassbird (Schoenicola brevirostris) and the Damara rockjumper (Achaetops pycnopygius). The genera Sphenoeacus and Achaetops have been suggested to be part of a clade, including the genus Melocichla, owing to similarities in habit and morphological features (e.g. White 1960). By contrast, Olson (1998) determined A. pycnopygius to be so similar as to be congeneric with Chaetops, a taxonomic decision followed by a recent major treatment of African passerines (Fry et al. 2000). We have included data from two members of the endemic Malagasy ‘warbler’ radiation identified by Cibois et al. (1999, 2001); Xanthomixis (Phyllastrephus) zosterops (formerly Pycnonotidae) and Thamnornis chloropetoides (formerly Sylviidae). Finally, we have included data from the spot-throat and dapple-throat (Arcanator and Modulatrix), classified by Sibley and Ahlquist as babblers (tribe Timaliini), and the Cape sugarbird (Promerops cafer), classified with the flowerpeckers and sunbirds (Nectariniidae), all three of which appear to be part of a basal grouping within the Passerida (Barker et al. 2004). To provide a well-sampled framework to test hypotheses of relationship for these taxa, we have included representatives of all but one (Hypocoliidae) oscine passerine family as recognized by Sibley & Monroe (1990), including multiple representatives of most groups, with an emphasis on groups within the Passerida (Electronic Appendix part A). The passerine tree was rooted with sequences from Gallus and Coracias (Barker et al. 2004).
(b) Molecular methods Nucleotide sequences of approximately 3![]() ![]() We estimated dates of divergences at several nodes based on the assumption that the New Zealand endemic Acanthisitta diverged from all other passeriforms at the same time that New Zealand rifted from Antarctica (Cracraft 2001; Barker et al. 2004), approximately 82 | |||||||
3. Results Sequences new to this study are indicated in Electronic Appendix part A along with their associated GenBank accession numbers. The equally weighted parsimony analysis of the RAG-1 and RAG-2 sequences in combination yielded 481 equally parsimonious trees, the consensus of which was well resolved, and which contained a large number of well-supported nodes (figure 1 and table 2). Bayesian analysis of the data yielded estimated nodal posterior probabilities that were completely consistent with the majority rule consensus of most-parsimonious trees (i.e. no node with greater then or equal to 0.95 estimated posterior probability conflicted with the parsimony consensus). The estimates presented are based on eight Metropolis-coupled Markov chain Monte Carlo (MC3) runs of 400
The relationships among higher taxa inferred here are largely congruent with those reported previously (Barker et al. 2002, 2004), given the differences in taxon and character sampling. Namely, we recover Acanthisitta as sister to all other passerines, and two major groups corresponding to the traditionally recognized suboscines and oscines. Further, within the oscine passerines, we recover a basal grade of Australasian groups, with Menura sister to all other oscines (figure 1, see also Electronic Appendix part B), rendering Sibley & Ahlquist's (1990) parvorder ‘Corvida’ a paraphyletic grade. Most corvoid lineages are comprised in a single, large, well supported group that has been termed the ‘core Corvoidea’ (Barker et al. 2002, 2004). A large group roughly corresponding to Sibley & Ahlquist's parvorder Passerida finds strong support, as do three groups roughly corresponding to their superfamilies Muscicapoidea, Passeroidea and Sylvioidea (figure 1, see also Electronic Appendix part B). As previously, this ‘Passerida’ clade forms an effective trichotomy with two other lineages, the Australasian Petroicidae, and the African Picathartidae, with optimal trees favouring a sister group relationship between the Passerida and the Petroicidae. In addition to this broad overview, we elaborate on the relationships of the focal enigmatic African taxa added in this study. Within the ‘core Corvoidea’ (figure 1), L. torquatus received strong support as the sister to Batis, but this lineage was not further resolved within a clade of corvidans that include Asian ioras and African bushshrikes. In the Passerida, the Herero chat (N. herero) appears to be more closely related to the saxicolines than to the turdines, although the composition of each of those groups is in flux (compare Cibois & Cracraft 2004; Voelker & Spellman 2004). Nicators (N. chloris) were not supported as bush shrikes (Malaconotidae) or bulbuls (Pycnonotidae), instead appearing in a basal grade with Alaudidae (larks) and many of Sibley & Ahlquist's (1990) Sylvioidea, which name we use for this group for brevity's sake. Given the basal position of Nicator, we suggest that the three species of nicators comprise a new family. Three different clades with ‘African warblers’ are well resolved in this monophyletic assemblage of Sylvioidea. The first includes the crombecs and a disparate array of southern African endemics, including the Damara rockjumper (A. pycnopygius), Cape grass-warbler (S. afer) and Victorin's warbler (Bradypterus/Cryptillas victorini); this novel clade is relatively basal within the Sylvioidea, sister to more than 1000 species. This clade probably also includes the African endemic Melocichla, which is grouped with Sphenoeacus and Sylvietta in Sibley & Ahlquist's (1990, pp. 798, Two additional clades are noteworthy in that they were not predicted by traditional classifications. The first includes Promerops, Arcanator and Modulatrix, all endemic to sub-Saharan Africa; we propose that the latter two taxa either be included in Promeropidae or be recognized with their own family name. This new clade is sister to an unresolved group that includes other Old World nectarivores (Nectariniidae, Irenidae and Dicaeidae) and core passeridans. Surprisingly, the African endemic fairy flycatcher (S. scita) is strongly supported as part of the previously recognized ‘sylvioid flycatcher’ clade, comprising the genera Elminia and Culicicapa. We suggest that these taxa, with Stenostira (Viellot 1818) having seniority, be recognized as the family Stenostiridae. The possible affinity of the African endemic Myioparus to Stenostira, suggested by Urban et al. (1997, p. 498), remains to be tested; other African or Asian species might conceivably fall into this novel clade. The taxonomic status of all these new higher-level groups will depend on further sampling within Passerida. | |||||||
4. Discussion (a) Inferred dates of divergence We estimate the date of divergence of Picathartidae from Petroicidae and Passerida at 44.5![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() Certain focal enigmatic taxa did not appear to be particularly ‘old’, as indicated by, for example, the estimated age of the divergence between Lanioturdus and Batis at 14.3 Our data provide the first quantitative assessment of divergence times for all of the endemic passerine radiations in Madagascar, which suggests that as for mammals, dispersal of these lineages into Madagascar was asynchronous. The oldest of these is the suboscine Philepittidae (2 genera, 4 species), which we estimate dispersed into Madagascar between 42.0 and 31.8 (b) Biogeographic implications Our effort to clarify the enigmatic status of key taxa with molecular data has provided several novel hypotheses of relationship among oscine songbirds and suggested new biogoegraphic themes for research on passerine evolution. The unanticipated extent to which African endemics span the passeridan tree suggests a complicated role for Africa in the history of these oscine passerines. Interestingly, there is no readily available paleogeographic context for the estimated age of dispersal of Picathartidae (or the common ancestor of Picathartidae and Passerida) into Africa (44.5![]() ![]() ![]() Within Africa, our data suggest future avenues for exploring the geographical context of speciation. The deep node subtending the Picathartidae in our analysis supports the idea that lowland forest areas serve as a ‘museum’ of ancient diversity (Fjeldså 1994; Fjeldså & Lovett 1997). However, the existence of an apparently ancient montane clade, including Promerops, Modulatrix and Arcanator, underscores the spatio-temporal heterogeneity of montane areas. This suggests that African montane regions not only have an important role in recent diversification (Roy 1997; Roy et al. 1997), but also in harbouring ancient diversity. The existence of this clade suggests, on the one hand, that other southern and Eastern Arc relationships may be found, and on the other, that additional montane endemics may be informative about phylogenetic pattern. Thus, sampling other highland endemics such as the bush blackcap (Lioptilus), the grey-chested thrush-babbler (Kakamega; J. Fjeldså personal communication), and possibly the Abyssinian catbird (Parophasma) should also be considered in the near future. (c) Systematic implications The topology of Barker et al. (2004) considered along with these results make the challenge for resolving the deeper nodes in the oscine songbird tree clear; in addition, recent molecular studies of more distal taxa show that many traditional tribes and genera are not monophyletic (e.g. Beresford 2003; Voelker & Spellman 2004). Yet, in order to understand the assemblage of the African avifauna, monophyletic groups and their sister taxa must be delineated. Future studies designed to extract biogeographical signals should be designed carefully, since different higher-level groups will, by virtue of their affinity to other faunas, contain different kinds of signal. Thus, although it may be tempting to clarify area relationships with a large sample of African birds, these results indicate that excluding Australasian or New World exemplars from such a study may be ill-advised. In order to determine whether or not Old World warblers, or crown Sylvoidea, is ancestrally an African group, both the sister relationship of the clade (to larks or nicators) as well as the ancestral area of that sister clade will have to be known.The future analysis of other Old World enigmatic taxa might also resolve some of the basal passeridan nodes, such as the current polytomy between the rock-fowl, rockjumpers and Australo-Papuan robins. Olson (1979) has suggested a relationship between Picathartes and the southeast Asian ‘rail-babbler’ Eupetes. Inclusion of this enigmatic taxon in the phylogenetic analysis of passerines should be considered a priority. More broadly, increased sampling of all passerine groups distributed in Asia and southeast Asia should clarify the history of forest-mediated interchange with Africa. In particular, sampling of endemic Asian sylvioids will be informative with regard to the possible African origins of this group. Additionally, determining the relationships between endemic African groups and the Malagasy vangas, Oriental aegithinids (ioras), and the Australo-Paupuan boatbills (Dicrurinae: Monarchini; Monroe & Sibley 1993; Machaerirhynchidae; Dickinson 2003) should help clarify the history of corvoid dispersal. | |||||||
5. Conclusion The paleogeological picture of the break-up of Gondwana enjoys ongoing clarification (e.g. Marks & Tikku 2001; Gelabert et al. 2002), even with respect to the African continental margin (Hofmann et al. 1997; Muelenkamp & Sissingh 2003). In addition to the possible role of drifting India (Cracraft 2001), the presence of Palaeocene dispersal routes west of drifting India, west of Madagascar, and east of Antarctica should be explored (in association with confidence limits around dates estimated both by molecular systematists and paleogeographers). The general problem might be mitigated if extinct lineages can be incorporated into this assessment, since the observation that the only sampled (extant) sister taxa to Passerida are narrowly distributed on the remnant of western Gondwana does not necessarily require that the common ancestor of Picathartidae and Passerida was so distributed. Thus, there are two aspects to reconstructing early passeridan history that should be explored: the available paleogeographic scenarios and alternative models of phylogenetic relationships (perhaps incorporating extinction probabilities). Fortunately, many more geographical signals for the biotic assemblage of the African passeridan fauna await clarification from well-sampled analyses of relationships at and below the family level. The proximity and ultimate contact of Africa to Eurasia, starting from approximately 40 The near future of passeridan systematics also promises to add new dimensions to other evolutionary hypotheses, such as independent origins of passerine flycatching (e.g. Monarchini, Muscicapini and Stenostiridae) and modes of passeridan speciation (Cockburn 2003; Ricklefs 2003). Having a resolved passeriform tree also provides an opportunity to explore the description and distribution of morphological characters, some of which have been rendered homoplasious by the emerging topology (e.g. the ‘corvoid’ humerus; Bock 1962). In terms of historical biogeography, the challenge for avian systematic biogeographers in reconstructing the African passeridan faunal assemblage is to detect Paleogene episodes of dispersal, and clarify the Neogene continuum of long-distance dispersal, species dispersion and isolating effects of migratory processes, and relate those to abiotic factors current or historical, as well as to patterns discerned from other groups. | |||||||
Acknowledgments PB was supported by a post-doctoral bursary from the University of Cape Town Research Foundation. FKB was supported in part by the Frank M. Chapman Memorial Fund at the American Museum of Natural History. TMC and PGR's research was supported by grants from the South African National Research Foundation and the University of Cape Town Research Committee. R. Bowie and C. Cohen generously provided assistance with sample collection. In addition to specimens provided by the Percy FitzPatrick Institute for African Ornithology (PFI), additional specimens were generously provided by the Burke Museum of Natural History and Culture (S. Edwards, S. Birks), the Field Museum (FMNH; S. Hackett, D. Willard), the Zoological Museum of the University of Copenhagen (ZMUC; J. Fjeldså, J.B. Kristensen) and the American Museum of Natural History (AMNH; P. Sweet). Analyses were performed using resources of the Computational Genetics Laboratory, University of Minnesota Supercomputing Institute. This research is part of the South African Department of Science and Technology's Centre of Excellence Programme led by the Percy FitzPatrick Institute. This paper is a contribution from the Monell Molecular Laboratory and the Cullman Research Facility in the Department of Ornithology, American Museum of Natural History, and has received generous support from the Lewis B. and Dorothy Cullman Program for Molecular Systematics Studies, a joint initiative of The New York Botanical Garden and The American Museum of Natural History. | |||||||
Footnotes As this paper exceeds the maximum length normally permitted, the authors have agreed to contribute to production costs. †Present address: The City College of New York, Convent Avenue at 138th Street, New York, NY 10031, USA. | |||||||
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