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Auk, The, Jan 2003 by Mayr, Gerald
The Auk 120(1):145-151, 2003
ABSTRACT.-The phylogenetic relationships between early Tertiary and extant apodiform birds are only poorly understood, and this study is the first cladistic approach to this problem in which the Trochilidae are included.
The analysis supports monophyly of the Lower Oligocene Jungornis and extant Trochilidae, as well as monophyly of the Middle Eocene Scaniacypselus and extant Apodidae. The “Jungornithidae” sensu Karhu (1999) are shown to be paraphyletic with the Upper Eocene Argornis being the sister taxon of the taxon (Jungornis + extant Trochilidae). The osteology of Jungornis provides a transition between that of the highly derived extant Trochilidae and that of more generalized apodiform birds. An Argornis-like apodiform bird from the Middle Eocene of Messel shows a completely unexpected combination of a greatly abbreviated, apodiform humerus with a short and broad wing, and might indicate that the Trochilidae evolved from a short-winged ancestor. Received 8 April 2002, accepted 26 October 2002.
THERE IS INCREASING consensus that tree swifts (Hemiprocnidae), true swifts (Apodidae), and hummingbirds (Trochilidae) form a monophyletic clade that is supported by derived anatomical features and most biochemical and molecular analyses (see Johansson et al. 2001, Livezey and Zusi 2001, Mayr 2002). As shown by a recent phylogenetic analysis (Mayr 2002), owlet-nightjars (Aegothelidae) are the sister group of swifts and hummingbirds. Although Apodiformes have a comparatively extensive early Tertiary fossil record, phylogenetic relationships between the fossil and the extant taxa are only insufficiently understood.
One of the earliest swift-like birds described so far is Eocypselus vincenti Harrison 1984 from the lower Eocene of England. That species, which is known from a few isolated bones of only a single individual, was classified into a monotypic taxon, Eocypselidae, by Harrison (1984) but included in the Hemiprocnidae by Mourer-Chauvire (1988).
Much better represented by numerous isolated bones are the early Tertiary Aegialornithidae Lydekker 1891, which exhibit a rather generalized overall osteology resembling both extant Hemiprocnidae and-apart from the more abbreviated humerus and tarsometatarsus-extant Aegothelidae. The Aegialornithidae are either considered to be closely related to the Hemiprocnidae (e.g. Harrison 1984; Karhu 1988, 1992; Mlikovsky 2002) or “the last representatives of an old radiation directed toward the realization of the type ‘True Swifts'” (Mourer-Chauvire 1988:369).
A few isolated bones from the Upper Eocene to Lower Oligocene deposits of the Quercy were assigned to Cypselavus gallicus Gaillard 1908 (Mourer-Chauvire 1978) which is currently recognized as the earliest taxon of the Hemiprocnidae (Harrison 1984, Peters 1985, Mourer-Chauvire 1988). The earliest certain members of the Apodidae belong to Scaniacypselus Harrison 1984, which includes two species from the Middle Eocene of Denmark and Germany (Harrison 1984, Peters 1985, Mayr and Peters 1999).
Crown group Trochilidae have no early Tertiary fossil record. However, Karhu (1988) described a new apodiform taxon, Jungornis tesselatus, from the Lower Oligocene of the Northern Caucasus which agrees with extant Trochilidae in highly characteristic derived features of the humerus (Karhu 1988, 1992). Karhu (1988) classified J. tesselatus into a new taxon, Jungornithidae, to which he later (Karhu 1999) assigned the Upper Eocene species Argornis caucasicus Karhu 1999. Both Jungornis and Argornis are known from wing elements of a single individual only, and A. caucasicus clearly exhibits a less specialized wing morphology than J. tesselatus.
The only phylogenetic analysis of fossil apodiform birds in which the proposed relationships are depicted in some sort of phylogenetic tree is by Harrison (1984) who assumed a major split between a hemiprocnid and an apodid lineage (a recent cladistic analysis of apodiform birds by Dyke [2001] is based on a largely incorrect character matrix [see Mayr 2001] and is thus not discussed in the following). However, whereas Harrison (1984) listed some derived characters to support the apodid lineage, assignment of the taxa Eocypselus, Aegialornis, and Cypselavus to the hemiprocnid lineage was based on plesiomorphic characters (“more generalized humeral structure,” “long slender ulna” with “more generalized proximal end;” see Harrison 1984:172).
Except for Karhu (1988, 1992, 1999), most authors further omitted the Trochilidae from their comparisons, and the present study is the first cladistic approach to the phylogeny of early Tertiary Apodiformes in which hummingbirds are included.
MATERIAL AND METHODS
Anatomical terminology follows Baumel and Witmer (1993) and Vanden Berge and Zweers (1993), if not indicated otherwise. Comparisons with extant taxa are based on skeletons in the collection of Forschungsinstitut Senckenberg; concerning extant Apodiformes the following species were studied: Aegothelidae: Aegotheles cristatus; Hemiprocnidae: Hemiprocne comata; Apodidae: Chaetura vauxi, Apus apus, Collocalia vanikorensis, Co. salangana; Trochilidae: Phaethornis pretrei, Glaucis hirsuta, Amazilia versicolor, Archilochus colubris, Calypte anna, Anthracothorax sp., and Chrysolampis mosquitus. Information on osteology of the Cypseloidinae (Apodidae) is based on illustrations and descriptions in Cohn (1968), Ballmann (1976), and Collins (1976a).
The phylogenetic tree was constructed with the phylogenetic software PAUP (version 3.1; Swofford 1993), using a data set of 27 anatomical characters (see Appendix and Table 1 for character descriptions and data matrix). The only multistate character was coded as “ordered”. Unknown characters for particular taxa were coded as “missing”. The shortest tree was found with the exhaustive search option, and the analysis was run with the delayed transformation (DELTRAN) mode. The consistency index (CI), retention index (RI), and rescaled consistency index (RC) were calculated. Robustness of the tree was tested with a bootstrap analysis of 1,000 replicates. Extant Podargidae (Podargus strigoides) and Aegothelidae (Aegotheles cristatus) were used for outgroup comparisons.
RESULTS
The phylogenetic analysis of the character matrix (Table 1) resulted in 10 most-parsimonious trees, the consensus tree of which is shown in Figure 1.
The analysis supported monophyly of a clade including all apodiform taxa except Eocypselus and Aegialornis. Within that group, two lineages can be distinguished that include swifts and tree-swifts on the one hand, and hummingbirds on the other.
Monophyly of a clade including extant Hemiprocnidae, the fossil Scaniacypselus, and extant Apodidae is in concordance with previous phylogenetic hypotheses. Monophyly of the taxon (Scaniacypselus + extant Apodidae) received high bootstrap support; derived characters that support monophyly of extant Apodidae to the exclusion of Scaniacypselus are the greatly abbreviated proximal pedal phalanges (see figure 4 in Peters 1985 for absence of this feature in Scaniacypselus szarskii) and the absence of a well-marked fossa musculi brachialis (that fossa is visible in the type specimen of S. wardi).
The analysis further showed that the Jungornithidae sensu Karhu (1999) are paraphyletic and resulted in monophyly of the taxon (Argornis + [Jungornis + extant Trochilidae]). Sister group relationship between Argornis and the taxon (Jungornis + extant Trochilidae) is in concordance with the temporal occurrence of the fossil genera, with the Upper Eocene Argornis being geologically older than the Lower Oligocene Jungornis. Monophyly of Jungornis and extant Trochilidae is further supported by the fact that in Jungornis, as in extant hummingbirds, the M. biceps brachii has a single insertion on the ulna, whereas that muscle inserts on the radius only in extant Apodidae, and on both the ulna and the radius in extant Hemiprocnidae, the fossil Argornis, and most other birds (see Karhu 1999). Monophyly of extant Trochilidae to the exclusion of Jungornis is supported by numerous derived features including a peculiar morphology of the coracoid in which the processus procoracoideus is connected to the processus acrocoracoideus by an osseous bridge (Fig. 2).
DISCUSSION
As already noted by Karhu (1999), the fossil record of apodiform birds is in agreement with monophyly of swifts and hummingbirds. Monophyly of the taxon (Jungornis + Trochilidae) is supported by unique derived characters, and the osteology of Jungornis provides a transition between the highly derived morphology of extant Trochilidae and that of a more generalized apodiform bird (Figs. 2 and 3).The nectarivorous hummingbirds evolved a derived mode of hovering flight that allows them to remain virtually motionless in front of flowers. Probably as an adaptation to their unique way of locomotion, extant Trochilidae have unusually short wings (Rayner 1988) that differ from the long and pointed wings of swifts.
The feathering of either Argornis or Jungornis is unknown, but there is a specimen (Fig. 4) of an apodiform bird from the Middle Eocene of Messel, Germany, which is osteologically very similar to Argornis and in which the wing and tail feathers are excellently preserved (Mayr 2003). As in Argornis, the robust humerus is strongly abbreviated and bears a poorly developed processus musculi extensor metacarpi radialis which is much more protruding in other apodiform taxa with a similarly abbreviated humerus (i.e. Jungornis, extant Trochilidae, and the Apodidae; see Fig. 3). The Messel apodiform further exhibits the diagnostic characters that support monophyly of the taxon (Argornis + [Jungornis + extant Trochilidae]) (see Fig. 1). Most unusual and completely unexpected is the combination of a short and stout humerus with a short and broad wing, the tip of which is completely preserved in the specimen. If it is a stem group representative of the Trochilidae, the Messel apodiform might indicate that strongly elongated wings indeed are synapomorphic for the taxon (Hemiprocnidae + Apodidae) and that the Trochilidae evolved from a rather short-winged ancestor.
It has been assumed that hummingbirds evolved from insectivorous ancestors (e.g. Cohn 1968) and underlying the phylogeny in Figure 1, a “swift-like” or “aegothelid” beak almost certainly was present in the last common ancestor of the Apodiformes and is thus plesiomorphic for the taxon (Jungornis + Trochilidae). Hovering ability of hummingbirds might have primarily evolved as an adaptation for gleaning insects from the underside of leaves (Cohn 1968) or around flowers and was a preadaptation for the highly derived nectarivory of extant Trochilidae (Mayr and Manegold 2002).
ACKNOWLEDGMENTS
I thank S. Chapman (The Natural History Museum, London) for access to fossil specimens and R. Prum, K. Smith, R. Zusi, and two anonymous reviewers for comments on the manuscript. S. Trankner (Forschungsinstitut Senckenberg) took the photograph.
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Mayr, Gerald “Phylogeny of early tertiary swifts and hummingbirds (Aves: Apodiformes)”. Auk, The. Jan 2003. FindArticles.com. 17 Jan. 2014. http://findarticles.com/p/articles/mi_qa3793/is_200301/ai_n9214314
