Re-evaluation of the Haarlem Archaeopteryx and the radiation of maniraptoran theropod dinosaurs

Abstract

Background: Archaeopteryx is an iconic fossil that has long been pivotal for our understanding of the origin of birds. Remains of this important taxon have only been found in the Late Jurassic lithographic limestones of Bavaria, Germany. Twelve skeletal specimens are reported so far. Archaeopteryx was long the only pre-Cretaceous paravian theropod known, but recent discoveries from the Tiaojishan Formation, China, yielded a remarkable diversity of this clade, including the possibly oldest and most basal known clade of avialan, here named Anchiornithidae. However, Archaeopteryx remains the only Jurassic paravian theropod based on diagnostic material reported outside China.

Results: Re-examination of the incomplete Haarlem Archaeopteryx specimen did not find any diagnostic features of this genus. In contrast, the specimen markedly differs in proportions from other Archaeopteryx specimens and shares two distinct characters with anchiornithids. Phylogenetic analysis confirms it as the first anchiornithid recorded outside the Tiaojushan Formation of China, for which the new generic name Ostromia is proposed here.

Conclusions: In combination with a biogeographic analysis of coelurosaurian theropods and palaeogeographic and stratigraphic data, our results indicate an explosive radiation of maniraptoran coelurosaurs probably in isolation in eastern Asia in the late Middle Jurassic and a rapid, at least Laurasian dispersal of the different subclades in the Late Jurassic. Small body size and, possibly, a multiple origin of flight capabilities enhanced dispersal capabilities of paravian theropods and might thus have been crucial for their evolutionary success.

Keywords: Anchiornithidae; Biogeography; Late Jurassic; Maniraptora; Radiation.

Fig. 1

Overview of the “Haarlem specimen”, holotype of Ostromia crassipes (Meyer, 1857). Counterslab, Teylers Museum TM 6929 (left) and main slab, TM 6928 (right). Rectangles indicate areas detailed in Fig. 3 (yellow) and Fig. 6 (white)

Fig. 2

Scatterplots for several proportions that can be established in Ostromia (red dots), comparing this taxon with specimens that can certainly be referred to Archaeopteryx (black dots). Red line shows the ordinary least squares regression fit and blue lines represent the 95% confidence intervals for the distribution of values of Archaeopteryx. a Ratio between metacarpal III and metacarpal I. b Ratio between phalanx I-1 and metacarpal I. c Ratio between phalanx I-1 and metacarpal III. d Ratio between ungual I and metacarpal I. e Ratio between ungual III and metacarpal III. f Ration between metatarsal III and tibia

Fig. 3

Anatomical details of the manus of Ostromia crassipes and Anchiornis huxleyi. a Detail of the preserved elements of the right manus on the main slab, showing longitudinal furrows (or their impressions) in metacarpal III and the manual phalanges (arrows). b Detail of the preserved elements of the right manus on the counterslab of the holotype of Ostromia crassipes (TM 6929), showing longitudinal furrows (or their impressions) in the manual phalanges (arrows). c, d Impression (c) and high-resolution cast (d) of the left manus of the holotype of Anchiornis huxleyi (Institute of Vertebrate Paleontology and Paleoanthropology IVPP V 14378), showing longitudinal furrows in the manual phalanges (arrows). All scale bars are 10 mm

Fig. 4

Details of manual phalanx I-1 of Ostromia crassipes, showing the regular development and non-collapsed margins of the longitudinal groove. a, stereophotograph. b, magnification of the shaft of the phalanx

Fig. 5

Manual phalanges of several other theropods preserved in highly compacted sediments, showing differences (a-d, f) and similarities (e) in preservation to the manual furrows in the Haarlem specimen. a Right manus of the Thermopolis specimen of Archaeopteryx, showing non-collapsed phalanges without furrows, as they are found in many specimens of this taxon (e.g. London, Berlin, Eichstätt, Munich, 11th specimen). b Right manus of the Solnhofen specimen of Archaeopteryx, showing partially collapsed and crushed phalanges with clearly broken margins. c Left manus of Sciurumimus albersdoerferi (BMMS BK 11) under UV light, showing partially compressed phalanges in this juvenile theropod. d Phalanx II-2 of Compsognathus longipes (SNSB-BSPG AS I 563), showing non-collapsed, but partially broken shaft. e Impression of phalanx I-1 of the holotype of Anchiornis huxleyi (IVPP V 14378), showing the impression of a regular longitudinal furrow, very similar to the impressions seen in the Haarlem specimen. f Phalanx I-1 of Caudipteryx (IVPP V 12430), showing collapse structure distally with clearly broken margins. Scale bars are in mm increments

Fig. 6

Pubic morphology of Ostromia. a Stereophotograph of the preserved pubis and impressions of the shaft, taken from a high quality cast at the BSPG. b outline reconstruction. Scale bar is 10 mm

Fig. 7

Comparison of pubic morphology of Ostromia (a) with Archaeopteryx (b-d) and Anchiornis (e, f). a Reconstructed pubis of Ostromia crassipes. b Pubis of the Berlin specimen of Archaeopteryx (photograph of high-quality cast at BSPG). c Pubes of the Munich specimen of Archaeopteryx. Note that the proximal shaft is of the left pubis, while the distal part is the right pubis, the proximal part of which is hidden by matrix. d Pubis of the 11th specimen of Archaeopteryx. Note that part of the shaft of the right pubis is visible distally, creating the impression of a flexed shaft. However, any impression of these structures would clearly show two pubic shafts, unlike the situation in the Haarlem specimen (see Fig. 5a). e Pubis of Anchiornis (BMNHC PH822; photo courtesy Rui Pei). f Pubis of Anchiornis (STM0-165; photo courtesy Wang Xiaoli)

Fig. 8

Occurrence of Ostromia within the “Solnhofen Archipelago” and distribution of theropod dinosaurs in the Jurassic of that area. Modified from Butzmann et al. [72]

Fig. 9

Time calibrated simplified phylogeny of maniraptoran theropods, indicating place of origin of the different clades. The relationships and stratigraphic and geographic distribution of maniraptorans indicate a rapid radiation in the late Middle to earliest Late Jurassic in eastern Asia. Node labels and abbreviations: 1, Coelurosauria; 2, Maniraptoriformes; 3, Maniraptora; 4, Pennaraptora; 5, Paraves; 6, Avialae; BAJ, Bajocian; BAT, Bathonian; BER, Berriasian; CAL, Callovian; KIM, Kimmeridgian; OXF, Oxfordian; TIT, Tithonian. Based on a phylogenetic analysis of 2 outgroups and 130 coelurosaurian ingroup taxa and 561 characters and the results of a S-DIVA analysis