Molecular phylogeny of Old World swifts (Aves: Apodiformes, Apodidae, Apus and Tachymarptis) based on mitochondrial and nuclear markers
Graphical abstract
Highlights
► The genera Apus and Tachymarptis are reciprocally monophyletic. ► The largely sympatric Palearctic Apus apus and A. pallidus were genetically not distinctive against each other. ► Asian A. pacificus and African A. caffer were paraphyletic with respect to closely related species. ► The superspecies concept cannot be properly applied within the genus Apus.
Introduction
According to the recent taxonomic classification by Chantler (1999; based on Brooke, 1970, Brooke, 1972) the swift family Apodidae is divided into two subfamilies, Cypseloidinae and Apodinae with the latter being distinctive by some anatomical traits such as a well-developed palatine process and only one carotid artery (Chantler, 1999). Cramp (1985) furthermore advocated the distinction of Chaeturinae as a third subfamily but this classification was refuted before by Brooke (1970). The subdivision of Apodinae into the three tribes Apodini, Collocaliini and Chaeturini (Chantler, 1999) received some recent support from molecular studies (Price et al., 2004, Price et al., 2005, Thomassen et al., 2005). However, there were some minor challenges to these traditional tribal classifications with respect to the position of Hirundapus not being included in the Chaeturini clade (Price et al., 2004, Price et al., 2005). Despite the first molecular evidence, taxon sampling in these previous studies was far from being complete with many genera still missing, and thus the higher-level phylogeny within Apodidae is yet to be fully resolved.
Within “typical swifts” of Apodini the systematics and taxonomy of the two Old World genera Apus and Tachymarptis have been under long-term debate. The erection of Tachymarptis Roberts, 1922 as a separate genus was not immediately adopted by the taxonomic authorities who continuously ranked the two species in question, the Alpine Swift and the Mottled Swift (T. melba and T. aequatorialis) under Apus (Cramp, 1985, Peters, 1940, Sangster et al., 1999, Vaurie, 1965). Nevertheless, with the advent of modern methods such as bioacoustics and molecular genetics Tachymarptis was more often accepted as a genus of its own (Chantler and Driessens, 2000, Clements, 2007, Dickinson, 2003, Eck, 1996, Sibley and Monroe, 1990, Wolters, 1982) and throughout this paper we follow the taxonomic approach by Chantler (1999; see Table 1).
Recent molecular studies shed first light on the within-tribe phylogenetic relationships of Apodini. Palm swifts of genus Cypsiurus turned out as the clear sister to a monophyletic group of three species: A. apus, A. affinis, T. melba (Price et al., 2004). Based on the supposed paraphyly of Apus demonstrated in two successive studies by Thomassen et al., 2003, Thomassen et al., 2005 the latter authors suggested to merge Tachymarptis in Apus, which was subsequently applied by some authorities (Wink, 2011). However, in all previous phylogenetic studies the same three out of seventeen currently accepted Apus and Tachymarptis species were included (Table 1). Thus, the absence of taxonomic controversy in Apus swifts might be due to the fact that comprehensive analyses of both comparative morphology and molecular data are still missing. Nevertheless, almost all taxonomic authorities having dealt with this group claimed that interspecific phylogenetic relationships in Apus are unclear. Based on the results from DNA–DNA hybridization studies Sibley and Monroe (1990) had already categorized five superspecies (Amadon, 1966) within Apus and three isospecies (taxonomically isolated taxa without any close phylogenetic relatives; Amadon and Short, 1992). This superspecies classification was later on largely adopted by Chantler (1999; see Table 1) who distinguished four superspecies only (compare Eck, 1996).
Here we provide a molecular phylogeny based on mitochondrial and nuclear sequence data for all 17 currently recognized swift species of genera Tachymarptis and Apus (including some doubtful subspecies) and discuss implications for systematics and current taxonomy.
Section snippets
Sampling and DNA extraction
We analyzed 86 samples of all currently recognized species of genera Apus and Tachymarptis (27 taxa belonging to 17 species, Table 1, Fig. 1; taxonomy according to Dickinson, 2003). Along with these, 23 samples from ten species of four other swift genera (Cypsiurus, Collocalia, Aerodramus, Chaetura) were sequenced. Further sequences of swift genera Aeronautes, Streptoprocne, Rhaphidura and Hirundapus were downloaded from GenBank and included in the analysis based on concatenated mtDNA data. As
Inter- and intrageneric phylogeny
The total evidence tree of Old World swifts based on 3601 bp of concatenated mitochondrial and nuclear sequences (cytb, 12S, fib7, GAPDH, 12884) is shown in Fig. 2. In the following, inter- and intrageneric phylogenetic relationships are described according to the multi-gene phylogeny and eventual differences to single- and two-gene reconstructions based on mitochondrial data alone are emphasized. Monophyly of each Apodidae tribe (Chaeturini, Collocaliini and Apodini) and of each swift genus (
Intergeneric relationships within Apodini
Our phylogenetic reconstructions largely confirm traditional groupings and molecular findings at the tribus level (Price et al., 2004, Price et al., 2005, Thomassen et al., 2005) though our taxon sampling was not exhaustive and further evidence is needed here. According to our phylogenetic reconstructions Apus and Tachymarptis are reciprocally monophyletic and these findings refute the hypothesized paraphyly of Apus on grounds of large intrageneric differences of karyotypes (Ribeiro et al., 2003
Acknowledgments
We are most grateful to a number of colleagues and institutions who provided sample loans for this study. These are: S. Frahnert, Museum für Naturkunde Berlin; R. van den Elzen, Zoologisches Forschungsmuseum Alexander Koenig Bonn; M. Unsöld, Zoologische Staatssammlung München; furthermore P. Becker, H.E. Lange, B. Nicolai, H.-H. Witt, all Germany; J. Barreiro, Museo Nacional de Ciencias Naturales Madrid, Spain; J. Cabot, Estación Biologica de Doñana, Sevilla, Spain; M. Louette, The Royal Museum
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