A complete multilocus species phylogeny of the tits and chickadees (Aves: Paridae)

Highlights

• The first complete species phylogeny of the family Paridae.

• Cephalopyrus is not a penduline tit, but belongs to the Paridae.

• Sombre Tits and Marsh Tits are non-monophyletic as currently circumscribed.

• Many unexpected relationships within the African tits.

• A new classification of Paridae.

Abstract

The avian family Paridae (tits and chickadees) contains c. 55 species distributed in the Palearctic, Nearctic, Afrotropics and Indomalaya. The group includes some of the most well-known and extensively studied avian species, and the evolutionary history, in particular the post-glacial colonization of the northern latitudes, has been comparably well-studied for several species. Yet a comprehensive phylogeny of the whole clade is lacking. Here, we present the first complete species phylogeny for the group based on sequence data from two nuclear introns and one mitochondrial gene for 67 taxa of parids. Our results strongly support the inclusion of the Fire-capped Tit (Cephalopyrus flammiceps), currently placed in the Remizidae, as the most basal member of the Paridae. The Yellow-browed Tit (Sylviparus modestus) and the Sultan Tit (Melanochlora sultanea) constitute the next two sequential branches whereas the remaining tits fall into two large clades, one of which contains the seed hoarding and nest excavating species. The indicated clades within these two groups are largely congruent with recent classifications, but with several unforeseen relationships, such as non-monophyly of the Sombre Tit (Poecile lugubris) and the Marsh Tit (Poecile palustris), as well as non-monophyly of both the African gray and the African black tits. Further, our results support a close relationship between the White-fronted Tit (Parus semilarvatus) and the varied Tit (Poecile varius) as well as a close relationship between the White-naped Tit (Parus nuchalis) and the Yellow-cheeked and Black-lored tits (Parus spilonotus and P. xanthogenys). Finally, Hume’s Ground-tit (Pseudopodoces humilis) is found to be closely related to the Green-backed Tit (Parus monticolus) and the Great Tit (Parus major). We propose a new classification that is in accordance with this phylogeny.

Introduction

The tits and chickadees (Paridae) constitute a morphologically homogenous avian family (Gosler and Clement, 2007, Harrap and Quinn, 1996). Of the c. 55 species traditionally assigned to the group, only two, the Sultan Tit (Melanochlora sultanea) and the Yellow-browed Tit (Sylviparus modestus) deviate from the typical “tit-like” appearance of the other taxa. This morphological homogeneity is also reflected in many classifications, with all but the Sultan and Yellow-browed tits often being placed in a single genus, Parus (Dickinson, 2003, Harrap and Quinn, 1996, Sibley and Monroe, 1990, Snow, 1967). More recently a third species with strikingly deviate appearance, Hume’s Ground-tit (Pseudopodoces humilis), previously considered the smallest of all corvids, was demonstrated to form part of the parid radiation (James et al., 2003). As the name implies Hume’s Ground-tit is primarily ground-living and distributed on the steppe landscape of the Tibetan Plateau. As with many other tit species it excavates its own nest hole, but in contrast to the other tits, the hole is dug in the ground. It has also been suggested that the Fire-capped Tit (Cephalopyrus flamiceps), which currently is placed in Remizidae (Penduline tits), may be a parid, “particularly in view of its habit of nesting in tree holes” (Gosler and Clement, 2007).

In more recent classifications of Paridae, three genera have typically been recognized (Melanochlora, Sylviparus and Parus). Yet it has also remained common practice to divide the largest of these genera, Parus, into several subgenera. For instance, Harrap and Quinn (1996) recognized 10 subgenera (Poecile, Periparus, Pardaliparus, Lophophanes, Melaniparus, Parus, Machlolophus, Cyanistes, Sittiparus, and Baeolophus), largely following Thielcke (1968). Some of these subgenera have in recent years been elevated to genera. For example, Gill et al. (2005) proposed the recognition of Poecile, Baeolophus, Lophophanes, Periparus, and Parus as distinct genera, in addition to Melanochlora, Sylviparus and Pseudopodoces. This arrangement was adopted by Gosler and Clement (2007) in their account of the Paridae for the Handbook of the Birds of the World. Although several aspects of this classification have been criticized (Päckert and Martens, 2008), we make use of this classification as a starting point for further discussion in this paper.

Although the number of taxa within the Paridae has remained relatively constant over time, the number of species recognized within the family has changed considerably over the years. Snow (1967) recognized 46 species of tits, but more recent checklists have recognized anywhere from 53 to 59 species (Clements, 2007, Dickinson, 2003, Gosler and Clement, 2007, Harrap and Quinn, 1996, Sibley and Monroe, 1990). These differences in species numbers are a reflection of the many uncertainties regarding the species status of several populations. In particular, the species status of some taxa presently lumped within the Great Tit, Parus major, which is widespread across the Palearctic, extending from Western Europe south to North Africa and east to China and Southeast Asia, continue to be debated. Within its range the Great Tit is divided into more than 30 subspecies (Gosler and Clement, 2007), which in turn are united in three groups (major, minor and cinereus) (Harrap and Quinn, 1996). Closely associated with these groups is the Turkestan Tit (Parus bokharensis), which in many recent classifications is treated as a distinct species (e.g. Dickinson, 2003, Gosler and Clement, 2007, Harrap and Quinn, 1996), but that earlier has been considered a subspecies of Parus major (Delacour and Vaurie, 1950, Vaurie, 1950); a view also supported by recent molecular data (Päckert et al., 2005). These studies suggest that major and bokharensis are conspecific whereas minor and cinereus constitute distinct species (Eck and Martens, 2006, Päckert et al., 2005).

Other taxa with uncertain species status include the Caspian Tit (Poecile lugubris hyrcanus) and the Songar Tit (Poecile montanus songarus), as well as other Central Asian forms of Poecile including the Black-bibbed Tit (Poecile palustris hypermelaenus) and the Spot-winged Tit (Periparus melanolophus). The first three taxa are sometimes considered distinct species (e.g. Harrap and Quinn, 1996) whereas the Spot-winged Tit appears to be nested within the Coal Tit (Parus ater) (Gill et al., 2005, Martens et al., 2006). The Canary Blue Tit (Cyanistes teneriffae) is a recently accepted split from the Eurasian Blue Tit (Cyanistes caeruleus) (Salzburger et al., 2002b).

The tits and chickadees are widely distributed, with 18 species in Palearctic, 15 in the Indomalayan and Afrotropical regions and 12 in the Nearctic. Collectively tits and chickadees occur in a wide range of habitats and can be found in virtually all wooded biomes (Gosler and Clement, 2007). However, with the exception of few species such as the Great Tit and the Black-capped Tit (Poecile atricapillus), most species are specialized in their choice of habitat (Gosler and Clement, 2007). Several groups of passerines have historically been associated with the tits, but recent molecular studies have demonstrated that the sister group is the Penduline tits (Remizidae; e.g. Barker et al., 2004, Johansson et al., 2008). However, the closest relative of this larger group in turn remains unresolved (Johansson et al., 2008), and the group falls outside the three main clades of Passerida (Sylvioidea, Muscicapoidea and Passeroidea).

In this paper we present a phylogeny of all 56 species of parids recognized by Gosler and Clement (2007). We also include several of the subspecies that some authors consider to be distinct species, including the Caspian and Black-capped Tits. In all, the phylogeny includes 67 ingroup taxa (Table 1).