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Phylogeny and Ecological Radiation of Tyrannidae (Aves, Passeriformes)

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Phylogeny and Ecological Radiation of Tyrannidae (Aves, Passeriformes) TyrantBlackwell Publishing Ltd flycatchers coming out in the open: phylogeny and ecological radiation of Tyrannidae (Aves, Passeriformes) JAN OHLSON, JON FJELDSÅ & PER G. P. ERICSON Submitted: 28 August 2007 Ohlson, J., Fjeldså J. & Ericson, P. G. P. (2008). Tyrant flycatchers coming out in the open: Accepted: 15 December 2007 phylogeny and ecological radiation of Tyrannidae (Aves, Passeriformes). — Zoologica Scripta, doi:10.1111/j.1463-6409.2008.00325.x 37, 315–335. Tyrant flycatchers constitute a substantial component of the land bird fauna in all South American habitats. Past interpretations of the morphological and ecological evolution in the group have been hampered by the lack of a well-resolved hypothesis of their phylogenetic interrelationships. Here, we present a well-resolved phylogeny based on DNA sequences from three nuclear introns for 128 taxa. Our results confirm much of the overall picture of Tyrannidae relationships, and also identify several novel relationships. The genera Onychorhynchus, Myiobius and Terenotriccus are placed outside Tyrannidae and may be more closely related to Tityridae. Tyrannidae consists of two main lineages. An expanded pipromorphine clade includes flatbills, tody-tyrants and antpipits, and also Phylloscartes and Pogonotriccus. The spadebills, Neopipo and Tachuris are their closest relatives. The remainder of the tyrant flycatchers forms a well-supported clade, subdivided in two large subclades, which differ consistently in foraging behaviour, the perch-gleaning elaeniines and the sallying myiarchines, tyrannines and fluvicolines. A third clade is formed by the genera Myiotriccus, Pyrrhomyias, Hirundinea and three species currently placed in Myiophobus. Ancestral habitat reconstruction and divergence date estimation suggest that early divergence events in Tyrannida took place in a humid forest environment during the Oligocene. Large-scale diversification in open habitats is confined to the clade consisting of the elaeniines, myiarchines, tyrannines and fluvicolines. This radiation correlates in time to the expansion of semi-open and open habitats from the mid-Miocene (c. 15 Mya) onwards. The pipromorphine, elaeniine and myiarchine–tyrannine–fluvicoline clades each employ distinct foraging strategies (upward striking, perch-gleaning and sallying, respectively), but the degree of diversity in morphology and microhabitat exploitation is markedly different between these clades. While the pipromorphines and elaeniines each are remarkably homogenous in morphology and exploit a restricted range of microhabitats, the myiarchine–tyrannine–fluvicoline clade is more diverse in these respects. This greater ecological diversity, especially as manifested in their success in colonizing a wider spectrum of open habitats, appears to be connected to a greater adaptive flexibility of the search-and-sally foraging behaviour. Corresponding author: Jan I. Ohlson, Department of Vertebrate Zoology and Molecular Systematics Laboratory, Swedish Museum of Natural History, P.O. Box 50007, SE-104 05 Stockholm, Sweden; Depart- ment of Zoology, University of Stockholm, SE-106 91 Stockholm, Sweden. E-mail: [email protected] Jon Fjeldså, Zoological Museum, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark. E-mail: [email protected] Per G. P. Ericson, Department of Vertebrate Zoology, Swedish Museum of Natural History, P.O. Box 50007, S-104 05 Stockholm, Sweden. E-mail: [email protected] Introduction suboscines (c. 400 species in c. 100 genera) belong in Tyrannidae The South American avifauna is characterized by a high degree (tyrant flycatchers), one of the largest and most diverse of all of continental endemism at high taxonomic levels. One of bird families. Some well-known genera (e.g. Myiarchus, these radiations, the New World suboscines (Furnariida: Tyrannus and Pitangus) include rather large and conspicuous ovenbirds, woodcreepers, antbirds, tapaculos and their allies; species, reputed for their aggressive behaviour, but most and Tyrannida: cotingas, manakins, tyrant flycatchers and members of the family are more anonymous, dull-coloured, their allies) makes up approximately two-thirds of the South small- to medium-sized insectivores. Tyrant flycatchers American passerines. More than a third of the New World typically forage by different search-and-sally techniques or © 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters • Zoologica Scripta, 37, 3, May 2008, pp 315–335 315 Phylogeny and ecological radiation of Tyrannidae • J. Ohlson et al. by gleaning the foliage of trees and bushes like warblers, but characters. W. E. Lanyon (1984–1988c) did not analyse his many species also eat fruit and a few are specialized frugivores data within a cladistic framework, but a subsequent cladistic (Fitzpatrick 1980). They are distributed over the entire New analysis, extended with behavioural data from Fitzpatrick World, but are most diverse in the Neotropical region, with (1980), was performed by Birdsley (2002). He found support a steep decline in diversity northward through Central for a kingbird clade and for restricted myiarchine and America, with only five genera (Tyrannus, Myiarchus, Contopus, Empidonax clades, which agreed with the findings of W. E. Empidonax and Sayornis) reaching temperate North America. Lanyon, but found only weak support for his Elaenia and In South America, the tyrant flycatchers have undergone an flatbill and tody-tyrant assemblages. impressive morphological and ecological diversification. Several molecular studies have treated smaller groups of Here, they make up roughly one-third of the passerine bird tyrannids: Leptopogon (Bates & Zink 1994), Ochthoeca (García- communities in most habitats (Fitzpatrick et al. 2004) and, Moreno et al. 1998), Anairetes (Roy et al. 1999), Muscisaxicola together with the furnariids, they are the predominant avian (Chesser 2000), W. E. Lanyon’s Empidonax group (Cicero & predators on small- to medium-sized arthropod prey. There Johnson 2002), Myiarchus (Joseph et al. 2004) and the is further a general behavioural distinction between these kingbird assemblage (Mobley 2002). These studies focus on two groups: furnariids generally search for hidden prey in evolutionary and biogeographical issues within these groups, crevices and among debris and epiphytes, whereas tyrannids and do not address phylogenetic relationships at deeper search for exposed prey. levels. The only larger groups of tyrant flycatchers that have been While the phylogeny of Furnariida has been investigated the target of molecular studies are the flatbill and tody-tyrant in considerable detail (Irestedt et al. 2002; 2004a,b, 2006b), no (Tello & Bates 2007) and Elaenia assemblages (Rheindt et al. comprehensive molecular phylogeny exists for the Tyrannida. 2008) of Lanyon (1988a and 1988c, respectively). Much of the effort spent on tyrannid systematics have Due to the lack of a robust and well-resolved phylogenetic been concentrated on the deeper relationships in the group, hypothesis for the tyrant flycatchers, the factors behind their utilizing both morphology (e.g. McKitrick 1985; Prum & ecological success and adaptive diversity are largely obscure. Lanyon 1989; Prum 1990), allozymes (S. M. Lanyon 1985), Fitzpatrick (1980, 1985) found that differences in foraging DNA–DNA hybridization data (Sibley & Ahlquist 1985, behaviour, and the morphological adaptations connected to 1990) and DNA sequences (Irestedt et al. 2001; Johansson them, correspond remarkably well with the taxonomic groupings et al. 2002; Chesser 2004; Ericson et al. 2006). From these outlined by Traylor (1977, 1979). However, his hypothesis on the studies, it has emerged that Tyrannida consists of four main evolution of foraging behaviours and ecological adaptations lineages: (i) Cotingidae (cotingas); (ii) Pipridae (manakins); needs to be reinterpreted within a phylogenetic framework, (iii) Tyrannidae (tyrant flycatchers); and (iv) Tityridae (tityras, and this is one aim of this paper. We use DNA sequence data becards and mourners). Ericson et al. (2006) further demon- from three nuclear introns to investigate the relationships strated that Tyrannidae, Tityridae and the enigmatic Piprites between the majority of tyrant flycatcher genera. We use this (currently treated as incerta sedis; Remsen et al. 2007) form a phylogeny to investigate the evolution of the extant ecological monophyletic clade. diversity in Tyrannidae. We also calculate preliminary age Genus-level relationships among the tyrant flycatchers estimates of certain divergence events among the tyrant flycatchers have not yet been addressed with molecular data and Traylor’s and their allies, and relate these to the climatic and ecological (1977, 1979) classification has essentially been the basis for development in the Neotropics during the Tertiary. linear classifications used in standard works since (e.g. Sibley & Monroe 1990; Dickinson 2003; Fitzpatrick et al. 2004; Materials and methods Remsen et al. 2007). Several studies have used morphological Taxon sampling and data acquisition characters of the cranium and syrinx to clarify interrelation- One hundred and three species, representing 83% of the ships among tyrant flycatchers and their relatives (Warter genera in of Tyrannidae sensu Fitzpatrick et al. (2004) were 1965; Ames 1971; Traylor 1977, 1979; W. E. Lanyon 1984, sampled. Ten species of Tityridae (sensu Prum & Lanyon 1985, 1986, 1988a,b,c; Prum & Lanyon 1989; Mobley & 1989; Ericson et al. 2006) were included, representing
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