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An impression of a prominent dorsal supracondylar process is apparent proximal to the impression of the dorsal condyle. A narrow flexor process protrudes distal to the ventral condyle, and a portion of this structure is also visible in the first intermediate flake. Humerotricipital and scapulotricipital sulci are present. The left ulna is preserved as an impression on the main slab, with fragmentary remnants of the body on the counterpart.

The distal end and body of the right ulna are preserved on the main slab, with a small fragment of the proximal end preserved on the counterpart. Papillae remigales are not apparent, and the ulnar shaft is straight. The olecranon process is poorly preserved, with a moderate point, similar to Z. Left radius is preserved as a thin impression on the main slab and as fragments on counterpart, positioned slightly out of articulation with the left ulna.

Right radius is preserved as collapsed fragments in the main slab, fully disarticulated from the right ulna. The left ulnare is a poorly-exposed and crushed body on the main slab. The radiale is not visible. Phylogenetic context of Zygodactylus ochlurus n. Positions of variable taxa are indicated above the branches they occupy in the full tree set. Left and right pelvic elements are disarticulated from the sacrum and preserved on the main slab, with an additional impression of left pelvic elements on the second intermediate flake Fig.

The ilium is short and narrow with its preacetabular portion broadly recurved dorsally and longer than its postacetabular portion. The pubis is thin and angles away from the ischium rather than being subparallel to its ventral margin. The obturator foramen is continuous with the ischiopubic fenestra. The right femur is preserved as an impression on main slab, with the distal end passing ventral to sternal impression.

Left femur crosses under the impression of the left humerus on the same slab. The femora Fig. The trochanteric crests are not well projected proximally.

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The body and medial cnemial crest of the right tibiotarsus are preserved as an impression with collapsed fragments on the main slab. The large cranial cnemial crest, visible as an impression on the counterpart, is strongly projected cranially and dorsally. Distal end of the left tibiotarsus is visible on the main slab; body may continue beneath the sternum. Both tarsometatarsi are partially crushed. The right tarsometatarsus shows a prominent lateral plantar crest of the hypotarsus, as well as a slight convexity proximal to trochlea IV.

Left metatarsal I visible as a separate element alongside the left tarsometatarsus. Digit I:1 is proportionally more elongate in the new taxon than in Z. Capital and cervical tract feathers preserved as a darker halo of filamentous structures. Distal primary remiges IV-IX? Analysis with the complete set of 39 equally weighted characters resulted in 30 most parsimonious trees, from implicit enumeration in TNT v1.

IterPCR identified Zygodactylus ignotus , Primozygodactylus ballmanni , and Primozygodacylus quintus as unstable taxa. A reduced consensus of these 30 trees Fig. The overall size and limb proportions of Z. When compared using the geometric mean of major limb element lengths humerus, ulna, carpometacarpus, femur, tibiotarsus, and tarsometatarsus as a proxy for size, Z. When individual element lengths are scaled to this body size proxy, Z. Pedal phalanx proportions are another area where Z. The elongate proximal phalanx of the hallux that is diagnostic of Z.

The proportionally longer pedal digits seen in Z. While the morphology of the new species indicates it is a part of the same zygodactylid subclade, the proportions of the pedal phalanges relative to each other and the tarsometatarsus in Z. Taken together, the limb proportions of Z. This setting is a strong contrast from the tropical-subtropical lowland settings in which other Z ygodactylus species have been preserved [ 27 ], and suggests that zygodactylids were not restricted to relictual tropical habitats following Late Eocene global cooling.

Zygodactylid extinction may be expected to be explained by more complex factors. If their declining distribution tracked tropical-subtropical environments they may be expected to persist in parts of Africa and Asia [ 28 ]. Three major themes of passerine paleobiogeography have emerged from prior analyses. The first is the proposed persistence of the passeriform stem in the separated remnants of Gondwana in the Cenozoic [ 29 ]. Second is the vicariance and diversification of suboscines in South America, with subsequent radiation to Africa and Asia [ 30 , 31 ].

Third is the vicariance, diversification, and radiation of oscines from Australia [ 32 ]. The geographic distribution of stem passeriform fossils is largely incongruent with the hypothesis of a persistent Gondwanan stem [ 28 , 33 ]. The Eocene — Oligocene paleogeographic records of birds and mammals in Europe and North America show a consistent pattern. Early Eocene avian and mammalian faunas are similar between Europe and North America [ 34 , 35 ]. Late Eocene faunas show a combination of similarity and endemic radiations [ 34 , 36 ].

The disappearances of these taxa with widespread extant distributions have been proposed to track the retraction of key forested environments out of North America [ 40 ], similar to proposed patterns in primates [ 35 ]. The new species shows at least one subclade of zygodactylids, Zygodactylus , persists at least into the earliest Oligocene of North America. It is also this subclade that is known from the Oligocene and Miocene of Europe [ 2 , 7 , 11 ].

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The European zygodactylid Z. The latter date coincides with the uplift of Wallacea in the southwestern Pacific, which is thought to have facilitated the dispersal of oscines from Australia [ 32 ]. The early Oligocene may be characterized by Holarctic persistence of an increasingly diverse group of zygodactylids known from distinct environments including inferred arid, higher altitude sites in North America.

During this time oscine and suboscine crown Passeres are inferred to be dispersing into these environments [ 51 ]. Competitive interactions, documented among extant passeriform groups, have been suggested as factors in the ecological divergence of the crown passeriform radiation [ 30 ]. New records are needed to elucidate dynamics and potential drivers of survivorship and extinction during this key interval. With similar body sizes, stem passerines occupy a range of ecological settings in the face of rapidly changing environments in the early days of an late Paleogene icehouse world.

The morphology of the new taxon is convergent on crown Passeriformes in several respects. The new taxon has a smaller overall size than other zygodactylids. The limb proportions of the new taxon are also convergent on the ranges seen in crown Passeriformes, most notable in the length of proximal phalanx of the hallux.

Oligocene zygodactylids were not confined to relict tropical forests after Late Eocene global cooling. Paleoclimatic reconstructions place Z. The new taxon extends the temporal range of North American zygodactylids from the Early Eocene in to the Early Oligocene. Morphological characters of Zygodactylus luberonensis , Zygodactylus grandei , Zygodactylus ignotus , and Primozygodacylus spp. Character states for several outgroup taxa were included from published sources.

Extant Passeriformes were represented by two terminal taxa: the basal passeriform Acanthisitta chloris , and a supraspecific terminal SST taxon representing basal states for oscine and suboscine passeriforms, using states reported from published studies [ 6 ] derived from a composite of Tyrannus tyrannus , Thamnophilus caerulescens , Corvus brachrhynchos , and Menura novaehollandiae. The putative stem passeriform Jamna szybiaki [ 45 ] was also included.

Psittaciformes were represented by an SST containing Nestor meridionalis and Nestor notabilis [ 6 , 57 ], as well as a terminal for the fossil stem psittaciform Cyrilavis colburnorum [ 57 ]. Piciformes were represented by an SST derived from Dryocopus pileatus , Colaptes auratus , Galbula ruficauda , and Chelidoptera tenebrosa [ 6 ].

Phylogenetic analysis used equal weights and a maximum parsimony estimator in TNT 1. The piciform SST was selected as an outgroup to root the resulting trees. Iterative Reduced Positional Congruence iterPCR [ 60 ] was used to identify unstable taxa in the set of most parsimonious trees. Forschunginstitut Senckenberg, Frankfurt am Main, Germany. Daniel Brinkman at Yale Peabody Museum graciously provided access to the specimen for study. Beau Bradley granted access to confirm the coordinates of the type locality. Diego Pol, Gerald Mayr, and an anonymous reviewer provided insightful comments that improved the quality of the manuscript.

JC conceived of the study. TH and JC designed the study. All authors read and approved the final version of manuscript. Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Research article Open Access. A new zygodactylid species indicates the persistence of stem passerines into the early Oligocene in North America. Clarke 2. BMC Evolutionary Biology 19 Results Here we describe this fossil and identify it as a new species of Zygodactylus , a stem lineage passerine with a zygodactyl foot. Conclusions Eocene-Oligocene global cooling is known to have significantly remodeled both Palearctic and Nearctic mammal faunas but its impact on related avifaunas has remained poorly understood. Passeriformes Paleogene Paleobiogeography Zygodactylidae.

Holotype YPM VPPU , partially articulated skeleton preserved on main slab and counterpart, including two smaller flakes detached from the counterpart Fig.

Associated Data

Feather impressions surround the skeleton. Most elements are preserved as mouldic impressions and fragments of bone. Complete fusion of the synsacral vertebrae in YPM VPPU are taken here as an indicator of skeletal maturity, and thus adult size, for this specimen. Table 1 Selected measurements of Zygodactylus ochlurus n.

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Holotype Left carpometacarpus is preserved as a crushed body and impression on the main slab. Metacarpal I is broken off but the area of breakage on metacarpal II suggests it would have been quite short. The ulnocarpal trochlea is preserved as a faint impression and does not appear to be large or significantly projected caudoventrally.

A prominent intermetacarpal process is visible within the narrow intermetacarpal space Fig. A dentiform process is visible on the cranial margin of major metacarpal. Left major digit is preserved in articulation with carpometacarpus on the main slab. All digits are preserved as impressions in the main slab. Phalanx II:1 flares distally and is partially overlain by digit II As preserved, the impression of digit II:1 appears to possibly bear a distinct caudodistal processus not dissimilar to that seem in some Galbulae.

However, the impression shows a proximodistal furrow that is interpreted as more consistent with an underlying, separate, element such as a carpal or phalanx. Phylogenetic hypotheses Analysis with the complete set of 39 equally weighted characters resulted in 30 most parsimonious trees, from implicit enumeration in TNT v1. Morphological diversity within Zygodactylidae The overall size and limb proportions of Z.

Acknowledgements Daniel Brinkman at Yale Peabody Museum graciously provided access to the specimen for study. Availability of data and materials The datasets used during the current study are included as appendices. Ethics approval and consent to participate Not applicable. Consent for publication Not applicable. Competing interests The authors declare that they have no competing interests.

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References Brodkorb P. Catalogue of fossil birds: part 4 Columbiformes through Piciformes. Google Scholar Mayr G. Phylogenetic affinities of the enigmatic avian taxon Zygodactylus based on new material from the early Oligocene of France. J Syst Palaeontol. New specimens of zygodactylid birds from the middle Eocene of Messel, with description of a new species of Primozygodactylus. Acta Palaeontol Pol. Variations in the hypotarsus morphology of birds and their evolutionary significance. Acta Zool. New species of Primozygodactylus from Messel and the ecomorphology and evolutionary significance of early Eocene zygodactylid birds Aves, Zygodactylidae.

Hist Biol. Peer J. Cour Forsch Inst Senckenberg. Google Scholar Weidig I. Rec Aust Mus. Birds of the British lower Eocene. Tert Res Spec Paper. Google Scholar Ballmann P. A Phylogenomic study of birds reveals their evolutionary history. Phylogenomic analyses data of the avian phylogenomics project. A comprehensive phylogeny of birds Aves using targeted next-generation DNA sequencing. Jepsen G; Google Scholar Becker HF. Paleobotany at the New York botanical garden.