Phylogenetic relationships of tyrant-flycatchers (Aves: Tyrannidae), with an emphasis on the elaeniine assemblage

Abstract

The tyrant-flycatchers (Tyrannidae) are arguably the largest avian family in the Western Hemisphere with approximately 100 genera and 430 species. Although the composition of the family is largely settled, intergeneric relationships are poorly understood. Morphological and behavior-based classifications are in disagreement with DNA–DNA hybridization data, and both have recently been contradicted by DNA-sequence studies. However, previous DNA-sequence sampling has mostly focused on two out of the six traditional tribes. In this study, we have sampled mitochondrial and nuclear sequences of additional tyrannid genera from across the Tyrannidae, with particularly dense coverage of a third tribe (Elaeniini). Our data corroborate previous DNA-sequence studies that demonstrate a basal division of Tyrannidae into a pipromorphine group (recruited from two morphological tribes) and the core Tyrannidae. Furthermore, we identify a new assemblage that includes Platyrinchus and the enigmatic Neopipo, although the position of this lineage within the Tyrannidae remains incertae sedis. Within the core Tyrannidae, we find strong support for a monophyletic elaeniine assemblage, and discuss a number of strongly supported sub-clades and species-level arrangements that display varying levels of agreement with previous classifications. The elaeniine assemblage may be the sister group to all other core Tyrannidae, and it is in virtually complete congruence with a previous classificatory scheme based on syringeal morphology.

Introduction

Comprising approximately 100 genera and 430 species, the tyrant flycatchers (Aves: Tyrannidae) are arguably the largest bird family in the Western Hemisphere (Fitzpatrick, 2004a). Confined to the New World, they constitute one of the four major bird radiations that make up the bulk of the Neotropics’ unparalleled passerine diversity (the other three being furnariids, thamnophilid antbirds and nine-primaried oscines). Despite their spectacular diversification across the Neotropics, the Tyrannidae have received relatively little attention by phylogeneticists, and can be considered one of the last big pieces of terra incognita in avian family-level systematics. However, an increased understanding of phylogenetic relationships within the Tyrannidae would help us uncover the mechanisms that have led to such a great wealth of morphological and behavioral adaptations associated with this large avian radiation.

Though not exempt from the presence of odd taxa of problematic placement, the genus-level taxonomy within Tyrannidae and—to a lesser extent—its delineation towards other families have been relatively stable over the years (Fitzpatrick, 2004a). In contrast, the classification of tyrannid genera into subfamilies and tribes has been a task of substantial and on-going difficulty. Traylor, 1977, Traylor, 1979 comprehensive revisions can be regarded as the first modern attempt at tyrannid classification. His treatment was expanded and improved upon by Lanyon, 1986, Lanyon, 1988a, Lanyon, 1988b, whose pioneering work synthesized previous morphological and behavioral data with skeletal traits, with a special emphasis on his own syringeal character data. Subsequently, Fitzpatrick (2004a) summarized these classifications in his family treatise (Fig. 1), but did not take into account information available from recent DNA-sequence studies.

In summary, Fitzpatrick’s (2004a) treatment divides the Tyrannidae into three core subfamilies (Elaeniinae, Fluvicolinae, Tyranninae) plus the anomalous Tityrinae, which are sometimes raised to family level and placed as sister to the Tyrannidae (Fig. 1). Each of the core subfamilies is divided into two tribes. One of them, the Contopini, was newly erected by Fitzpatrick (2004b) to accommodate a number of genera that had variously been known as the “restricted Empidonax assemblage” (Birdsley, 2002) or “Empidonax group” (Lanyon, 1986) and that are distinct from other Fluvicolinae. Similarly, Lanyon (1988b) delineated his “Elaenia assemblage”—which is largely congruent with Fitzpatrick’s (2004a) tribe Elaeniini—on the basis of an apomorphic configuration of the nasal septum, and he then offered a well-resolved morphology-based tree as a phylogenetic hypothesis for intergeneric relationships within this group (see different fonts in Fig. 1). As a result, Fitzpatrick (2004a) placed most of the remaining genera of the subfamily Elaeniinae in their own tribe Platyrinchini (Fig. 1), which is mainly made up of Lanyon’s (1988a) “tody-tyrant and flatbill assemblage”. The morphological studies of Traylor, 1977, Traylor, 1979 and Lanyon, 1986, Lanyon, 1988a, Lanyon, 1988b have been revisited using altered methodologies and aims (McKitrick, 1985, Birdsley, 2002); however, the resulting classifications were either not in great conflict with the previous works, or were poorly resolved.

Meanwhile, molecule-based methods applied to tyrannid systematics have yielded surprising results. Based on DNA–DNA hybridization, Sibley and Ahlquist, 1985, Sibley and Ahlquist, 1990 placed a number of genera into tyrannid clades that largely coincide with Fitzpatrick’s (2004a) scheme; however, they singled out certain genera (Fig. 1) into a new family Pipromorphidae (=Mionectidae) and placed it basal to all Tyranni, i.e., the group comprising the Tyrannidae and all their nearest neighbors, such as Tityridae, Cotingidae (cotingas) and Pipridae (manakins). This treatment renders the Tyrannidae polyphyletic. Although DNA-sequence studies have also identified a “pipromorphine” lineage, it was basal to other tyrannids, but not outside the family itself (Johansson et al., 2002, Ericson et al., 2003, Fjeldså et al., 2003, Chesser, 2004, Barker et al., 2004, Ericson et al., 2006, Ohlson et al., 2007, Tello and Bates, 2007). This newly emerging clade Pipromorphinae includes as its core genera Todirostrum, Hemitriccus, Mionectes, Leptopgon and Corythopis, which have repeatedly come out in a highly supported lineage sister to all other tyrannids under study. Tello and Bates (2007) have added nine more genera to the pipromorphine assemblage, most of which have traditionally been considered part of the “tody-tyrant and flatbill assemblage” (Lanyon, 1988a) equivalent to Fitzpatrick’s (2004a) Platyrinchini (Fig. 1).

Tello and Bates (2007) also uncovered an odd tyrannid clade consisting of three previously unsampled genera (Onychorhynchus, Terenotriccus, Myiobius) that came out at an even more basal position than the Pipromorphinae. Such a systematic treatment had never been suggested before, and indeed Tello and Bates’s (2007) analyses left it open whether the non-tyrannid family Pipridae (manakins) is really more basal than this newly-identified flycatcher lineage. The fact that the three members of this strongly supported group are recruited from two different tribes (sensu Fitzpatrick, 2004a) highlights the strong disagreement between traditional morphology-based classifications and modern DNA sequence data. Furthermore, both Ericson et al. (2006) and Tello and Bates (2007) could not resolve the phylogenetic position of Platyrinchus within the Tyrannidae.

Outside of the new Pipromorphinae, sampling of tyrannid genera in DNA sequence studies has been limited. Cicero and Johnson (2002) clarified relationships among seven genera within the Contopini, however, assuming a priori that they constitute a monophyletic group. Ericson et al. (2006) incorporated 10 genera that came out as core tyrannids in their family-level sampling regime: A strongly supported fluvicoline group consisting of three genera (Gubernetes, Knipolegus, Fluvicola) emerged as sister to a Myiarchus-Tyrannus clade. This assemblage was placed as the sister group of a clade including five elaeniine genera (Myiopagis, Serpophaga, Elaenia, Inezia, Stigmatura). In Tello and Bates’s (2007) work, the Myiarchus-Tyrannus clade was joined by Ramphotrigon, while two genera from the tribe Contopini (Colonia, Empidonax) and three elaeniines (Capsiempis; Elaenia; Phyllomyias uropygialis) grouped together as expected. The elaeniine Myiotriccus, however, variously emerged as sister to all core Tyrannidae.

Considering the large incongruences between the morphological and DNA-based classifications of the Tyrannidae, sequence data of more genera are required. To this end, we here provide DNA sequence data from 48 genera of Tyrannidae (Fig. 1; Appendix 1). We concentrated on, but did not limit ourselves to, the Elaeniini (sensu Fitzpatrick, 2004a; Fig. 1), bringing our genus coverage of that large tribe up to 67%. We also incorporate previously generated sequences (mainly Tello and Bates, 2007, and Cicero and Johnson, 2002; see Appendix 2) to cover 85% of the genera of Fitzpatrick’s (2004a) now-invalidated Platyrinchini (most of which are in fact Pipromorphinae) and 79% of the genera of Contopini.