J Ornithol (2007) 148 (Suppl 2):S455–S458 DOI 10.1007/s10336-007-0159-8 REVIEW The renaissance of avian paleontology and its bearing on the higher-level phylogeny of birds Gerald Mayr Received: 12 February 2007 / Revised: 24 May 2007 / Accepted: 24 May 2007 / Published online: 20 June 2007 Ó Dt. Ornithologen-Gesellschaft e.V. 2007 Abstract Recent phylogenetic analyses provide strong by only a few specialists and, unlike the situation in evidence for some previously undetected clades of mor- mammalogy (e.g., Novacek 1992; Asher et al. 2003; phologically very divergent avian groups. Also, within the Boisserie et al. 2005), fossil taxa are usually not considered past decades, palaeornithology has experienced a renais- in analyses of and discussions on the phylogeny of extant sance and the Paleogene fossil record of birds is avian taxa, other than calibrations of molecular clocks approaching that of mammals in the number of recorded (e.g., Cracraft et al. 2004; Livezey and Zusi 2007). Livezey higher-level taxa. However, there is still little mutual ex- and Zusi (2007, p. 4) even went as far as to note that fossil change between students of these different data, as birds ‘‘typically provide only substandard anatomical molecular systematists are often unfamiliar with the fossil material or incomplete specimens’’. Certainly, this is not record of birds, whereas palaeornithologists only recently true. Many Paleogene taxa are known from complete started to interpret their fossils in the light of modern skeletons which are often complemented by three-dimen- phylogenetic analyses. Here, this deficiency is remedied in sionally preserved isolated bones, and sometimes even a brief overview of some fossil ‘‘missing links’’ between exhibit remarkable soft-tissue preservation (e.g., Mayr extant higher avian groups, which combine derived char- 2005a, 2006). acters of a certain taxon and plesiomorphic characters of its The significance of fossils as ‘‘missing links’’ (transi- sister group. tional forms) between morphologically disparate clades of extant birds has been vilified as the ‘‘most prevalent idio- Keywords Fossil birds Á Missing links Á syncracy [sic] of paleontological perspectives’’ by Livezey Palaeornithology Á Phylogeny and Zusi (2007, p. 49). Indeed, fossils are not mandatory for a reconstruction of the phylogeny of extant organisms. However, stem group representatives of a certain clade Introduction may support existing phylogenetic hypotheses on widely divergent taxa, if they exhibit old bauplan characteristics In the past few decades, the Paleogene (pre-Miocene) fossil which were reduced or transformed in the crown group. In record of birds has approached that of mammals, at least in the following, three examples of such ‘‘missing links’’ are terms of the recognized higher-level taxa (e.g., Mayr given, which provide independent evidence for recently 2005a). However, the avian fossil record is still overseen established phylogenetic hypotheses. Communicated by F. Bairlein. Flamingos (Phoenicopteriformes) and grebes (Podicipediformes) G. Mayr (&) Forschungsinstitut Senckenberg, Sister group relationship between flamingos (Phoenicop- Sektion Ornithologie, Senckenberganlage 25, 60325 Frankfurt am Main, Germany teriformes) and grebes (Podicipediformes) was first pro- e-mail: [email protected] posed in a molecular study of van Tuinen et al. (2001), who 123 S456 J Ornithol (2007) 148 (Suppl 2):S455–S458 analyzed mitochondrial and nuclear DNA sequences as extremitas sternalis of the coracoid which forms three well as DNA–DNA hybridization data, and also resulted pointed projections, the absence of pneumatic foramina in from sequence analyses of the nuclear ZENK gene (Chubb the fossa pneumotricipitalis of the humerus, the presence of 2004), the RAG-2 exon (Cracraft et al. 2004), RAG-1 gene a tuberculum on the os carpi ulnare at the insertion area of (Ericson et al. 2006: Fig. ESM 2), the myoglobin intron 2 the ligamentum humerocarpale, and the fact that the fourth (Ericson et al. 2006: Fig. ESM 3), and combined sequences phalanx of the fourth toe is shorter than the third phalanx of ADH5, GPD3–5, FGB7, 12S rDNA, 16S rDNA, and (Mayr and Knopf 2007). Charadriiform affinities of the tRNA Valine (Fain and Houde 2007). Derived morpho- Turnicidae are further supported by the osteology of the logical characters shared by flamingos and grebes were first early Oligocene fossil taxon Turnipax, which is known identified by Mayr (2004) and augmented by Manegold from skeletons from Ce´reste in France and Frauenweiler in (2006). Germany. The two species of Turnipax are small birds and A flamingo–grebe clade is strongly supported by the combine derived characteristics of crown group Turnicidae fossil Palaelodidae, which have an abundant fossil record (including a highly peculiar morphology of the coracoid) in the Paleogene and Neogene of Europe (Mayr 2004, with a plesiomorphic ‘‘charadriiform’’ overall morphology 2005a; note that Livezey and Zusi 2007, p. 50, misquoted (Mayr 2000, Mayr and Knopf 2007). Before any molecular Mayr (2005a) in stating that the ‘‘intermediacy of two evidence for charadriiform affinities of the Turnicidae was skeletal features between Juncitarsus […] and the Pal- available, the striking character mosaic of this fossil taxon aelodidae […] provides a morphological link between raised the question whether ‘‘buttonquails are highly Phoenicopteriformes and Podicipediformes’’; the com- modified Charadriiformes which evolved from a Turnipax- ments in that study pertained to Palaelodus only). Pal- like ancestor’’ (Mayr 2000, p. 629). aelodids are unanimously considered stem lineage representatives of the Phoenicopteriformes and possess a deep lower jaw which suggests the existence of a Owlet-nightjars (Aegothelidae) and apodiform birds ‘‘primitive filter-feeding apparatus’’ (Cheneval and Escuillie´ 1992, p. 209). However, they have much shorter It has recently also been suggested that the ‘‘Caprimulgi- hindlimbs than crown group Phoenicopteriformes and the formes’’ (nightjars and allies) are not monophyletic, and tarsometatarsi in particular ‘‘show many similarities with that owlet-nightjars (Aegothelidae) are the sister group of those of a foot-propelled diving bird such as Podiceps swifts and hummingbirds (Apodiformes). The owlet- [Podicipedidae]’’ (Cheneval and Escuillie´ 1992). In the nightjar–apodiform clade was first proposed from an light of the new phylogenetic hypotheses, it is reasonable analysis of morphological characters, and apomorphies of to consider the similarities between Palaelodidae and this clade include a derived morphology of the quadrate Podicipedidae to be plesiomorphic. Because grebes and and the splenius capitis muscle (Mayr 2002a). A clade palaelodids are aquatic birds which use their hindlimbs (Aegothelidae + Apodiformes) is supported by an indel in for propulsion, it is thus most parsimonious to assume the c-myc gene (Mayr et al. 2003) and resulted from all that the stem species of the Phoenicopteriformes was also subsequent molecular analyses (Cracraft et al. 2004; Eric- an aquatic bird which used its hind limbs for propulsion son et al. 2006; Barrowclough et al. 2006). in the water (Mayr 2004; contra Storer 2006). Species on Nevertheless, the extant representatives of this clade are the stem lineage of the Phoenicopteridae then entered a morphologically very different, and owlet-nightjars, for new ecological zone, as filter feeders in shallow waters example, differ markedly from apodiform birds in their (see Mayr 2007a). feathering. In the light of the novel phylogenetic hypothesis, it is thus notable that the Middle Eocene Parargornis messel- Buttonquails (Turnicidae) and shorebirds ensis, a stem group representative of the Trochilidae, (Charadriiformes) exhibits an owlet-nightjar-like feathering with short and rounded wings and a long tail (Mayr 2005b). Parargornis Molecular analyses provide strong evidence that button- messelensis further has an owlet-nightjar or swift-like beak quails (Turnicidae), traditionally most often considered and certainly was an insectivorous bird. It is most parsi- aberrant ‘‘gruiform birds’’, are representatives of the monious to assume that the feathering of Parargornis is Charadriiformes (shorebirds and allies) (Paton et al. 2003; plesiomorphic for the total group of Trochilidae (stem Cracraft et al. 2004; Fain and Houde 2004, 2007; Paton and group + crown group); the narrow wings of the crown Baker 2006; Ericson et al. 2006). Derived morphological group representatives are functionally correlated with the features which are shared by crown group Turnicidae and highly specialized hovering flight of the nectarivorous other charadriiform birds include a derived shape of the crown group representatives. 123 J Ornithol (2007) 148 (Suppl 2):S455–S458 S457 Discussion Gruppen vorgestellt, die als ,,missing links’’ (morpholo- gische Zwischenformen) zwischen heutigen ho¨herrangigen All of the clades discussed above: (1) can be established Vogeltaxa betrachtet werden ko¨nnen, und abgeleitete with morphological apomorphies found in the crown group Merkmale eines Taxons mit plesiomorphen Merkmale representatives; (2) result from independent analyses of a seiner Schwestergruppe kombinieren. fair number of different gene sequences; and (3) are further supported by the mosaic character distribution of fossil Acknowledgments I thank two anonymous referees for comments avian taxa. Remarkably, however, none is recovered in the which improved the manuscript. analysis of Livezey and Zusi