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Late Cretaceous Neornithine from Europe Illuminates Crown Bird Origins

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Late Cretaceous Neornithine from Europe Illuminates Crown Bird Origins 1 Late Cretaceous neornithine from Europe illuminates crown bird 2 origins 3 4 Daniel J. Field1*, Juan Benito1,2, Albert Chen1,2, John W.M. Jagt3, Daniel T. Ksepka4 5 6 1Department of Earth Sciences, University of Cambridge, Cambridge, UK. 2Department of 7 Biology & Biochemistry, Milner Centre for Evolution, University of Bath, Bath, UK. 8 3Natuurhistorisch Museum Maastricht, Maastricht, The Netherlands. 4Bruce Museum, 9 Greenwich, CT, USA. *e-mail: [email protected] 10 11 Our understanding of the earliest stages of crown bird evolution is hindered by an 12 exceedingly sparse Mesozoic fossil record. The most ancient phylogenetic divergences 13 among crown birds are known to have occurred in the Cretaceous1-3, but stem lineage 14 representatives of the deepest crown bird subclades—Palaeognathae (ostriches and 15 kin), Galloanserae (landfowl and waterfowl), and Neoaves (all other extant birds)—are 16 entirely unknown from the Mesozoic. As a result, key questions related to ancestral 17 crown bird ecology4,5, biogeography3,6,7, and divergence times1,8-10 remain unanswered. 18 Here, we report a new Mesozoic fossil that occupies a position close to the last common 19 ancestor of Galloanserae, filling a key phylogenetic gap early in crown bird 20 evolutionary history10,11. Asteriornis maastrichtensis, gen. et sp. nov., from the 21 Maastrichtian of Belgium, is represented by a nearly complete, three-dimensionally 22 preserved skull and associated postcranial elements. The fossil represents one of the 23 only well-supported crown birds from the Mesozoic Era12, and is the first Mesozoic 24 crown bird with well represented cranial remains. A. maastrichtensis exhibits a 25 heretofore undocumented combination of galliform (landfowl)-like and anseriform 26 (waterfowl)-like features, and, along with a previously reported Ichthyornis-like taxon 27 from the same locality13, provides the first direct evidence of co-occurring crown birds 28 and avialan stem birds. Its occurrence in the northern hemisphere challenges 29 biogeographic hypotheses of a Gondwanan origin of crown birds3, and its relatively 30 small size and possible littoral ecology may corroborate recently proposed ecological 31 filters4,5,9 influencing crown bird persistence through the end-Cretaceous mass 32 extinction. 33 34 By any measure, crown birds (Neornithes) are among the most diverse and 35 conspicuous extant tetrapods, yet their early evolutionary history is scarcely understood. 36 Apart from birds, all major extant tetrapod groups—lissamphibians14, squamates15, turtles16, 37 mammals17, and crocodylians18—are well-known from pre-Cenozoic crown group fossils. By 38 contrast, the Mesozoic record of well-supported crown birds is restricted to a single latest 39 Maastrichtian taxon, Vegavis iaai12. Several fragmentary Mesozoic fossils have at times been 40 referred to Neornithes19, although justifications for such assignments are questionable and 41 these purported records have not unambiguously withstood re-evaluation20,21. 42 We report a remarkable new crown bird from the Late Cretaceous of Belgium. The 43 fossil is between 66.8 and 66.7 million years old—making it the oldest unambiguous crown 44 bird fossil yet discovered—and provides important insight into the extent of Mesozoic 45 neornithine diversification prior to the end-Cretaceous mass extinction event, 66.02 MYA22. 46 Uniquely among crown birds from the Mesozoic and earliest Paleocene, the new fossil 47 includes a nearly complete, three-dimensionally preserved skull, yielding the first direct 48 insights into the nature of the crown bird skull early in neornithine evolutionary history. The 49 specimen exhibits a previously unseen combination of features diagnostic of Galliformes and 50 Anseriformes, which together form the crown clade Galloanserae, one of the most deeply- 51 diverging clades of crown birds and the sister group to the hyperdiverse extant clade 52 Neoaves1-3. Our most parsimonious phylogenetic hypothesis suggests that the fossil sits on 53 the stem lineage of Galloanserae, which would make it the only stem galloanseran yet known 54 and fill one of the most conspicuous phylogenetic gaps in the neornithine fossil record. 55 56 Systematic Palaeontology 57 Avialae Gauthier, 1986 58 Neornithes Gadow, 1892 59 Neognathae Pycraft, 1900 60 Pangalloanserae Gauthier and de Queiroz, 2001 61 Asteriornis maastrichtensis gen. et sp. nov. 62 63 Remarks. We use Avialae to refer to theropods crownward of Dromaeosauridae and 64 Troodontidae. Neornithes is equivalent to the bird crown group (Aves sensu23). 65 Pangalloanserae defines the most inclusive clade including Anser anser and Gallus gallus but 66 not Passer domesticus (i.e. the galloanseran total group). Further phylogenetic definitions are 67 presented in the Supplementary Information. 68 69 Etymology. Asteriornis from the name of the Titan goddess Asteria and the Greek ornis for 70 bird. In Greek mythology Asteria is the goddess of falling stars and transforms herself into a 71 quail, attributes reflected by both the impending K-Pg asteroid impact and the galloanseran 72 affinities of Asteriornis. The specific epithet maastrichtensis reflects the holotype’s 73 provenance from the Maastricht Formation (the type locality of the Late Cretaceous 74 Maastrichtian Stage). 75 76 Holotype. Natuurhistorisch Museum Maastricht (NHMM) 2013 008, a nearly complete, 77 articulated skull including mandibles and associated postcranial remains preserved in four 78 blocks (Fig. 1, Extended Data Figs. 1-7; see Supplementary Information for videos, character 79 information, measurements, and additional description and discussion). Preserved elements 80 include the premaxillae, maxillae, nasals, frontals, laterosphenoid, basisphenoid, mesethmoid, 81 left quadrate, left jugal, right palatine, and lower jaws. Associated postcranial elements 82 include incomplete femora, tibiotarsi, tarsometatarsus, and radius. 83 84 Locality and age. CBR-Romontbos Quarry, Eben Emael, Province of Liège, Belgium. 85 Valkenburg Member (66.8-66.7 Ma24), Maastricht Formation, Late Maastrichtian, 86 Cretaceous. Additional details regarding the locality and stratigraphic setting are presented in 87 the Supplementary Information. 88 89 Diagnosis. Asteriornis is unique among known taxa in exhibiting caudally pointed nasals 90 overlying the frontals and meeting at the skull’s midline, and a slightly rounded, unhooked 91 tip of the premaxilla. Additional unique character combinations from phylogenetic analyses 92 that differentiate Asteriornis are presented in the Supplementary Information. 93 94 Description 95 Asteriornis maastrichtensis is a small pan-galloanseran, with a mean body mass estimate of 96 394 g from hindlimb scaling regressions (~21st percentile among extant Galloanserae, 97 Extended Data Fig. 8)25. Complete measurements of NHMM 2013 008 are provided in the 98 Supplementary Information. 99 Most major cranial components are largely in their original anatomical positions. The 100 general appearance of the premaxillary beak resembles that of extant Galliformes, 101 particularly in its gently downcurved tip and delicate construction, lacking ossified joints 102 among the rostral components26. The contralateral frontal processes of the premaxillae are 103 unfused along their length, and the premaxillae and nasals are unfused at both their tomial 104 and narial contacts. The beak tip is unhooked, distinguishing Asteriornis from most 105 Galloanserae except certain Anatidae and Presbyornithidae. 106 The skull lacks a distinct nasofrontal hinge. As such, the architecture of this region 107 more closely resembles that of extant Galliformes than Anseriformes. At the midpoint of the 108 orbits the frontals are constricted, yielding an hourglass-shaped cranial roof with wider rostral 109 and caudal extremities. In dorsolateral view, the right postorbital process sweeps strongly 110 ventrally before deflecting rostrally to define part of the ventral margin of the orbit. 111 The left quadrate is well preserved in three dimensions and is generally similar to the 112 quadrate of the fossil pan-anseriform Presbyornis27 (Fig. 2, Extended Data Fig. 4). The 113 prootic and squamosal heads are divided by a well-developed incisure as in almost all 114 Neognathae, contrasting with the condition in crownward stem birds like Ichthyornis where 115 the division between these condyles is poorly marked, and Palaeognathae where the condyles 116 merge into a single head. Two pneumatic foramina pierce the quadrate: the foramen 117 pneumaticum rostromediale and the foramen pneumaticum basiorbitale. A tuberculum 118 subcapitulare is moderately developed on the lateral face of the otic process. This character 119 has been considered a derived feature of Galloanserae27; however, it is present in many 120 Neoaves, and given its absence in Palaeognathae and Ichthyornis may instead represent a 121 synapomorphy of Neognathae. The cotyla jugalis of the quadrate is fairly deep, with a 122 complete, un-notched rim. The pterygoid articulation is more widely separated dorsally from 123 the mandibular condyle than in most extant Galloanserae, and is very similar to that of 124 Presbyornis. 125 As in all known Galloanserae, the mandible of Asteriornis exhibits two cotylae for 126 articulation with the bicondylar quadrate and a blade-like retroarticular process. This process 127 is strongly hooked, and in its shape and proportions bears a strong resemblance to the 128 condition in the pan-anseriform Anatalavis oxfordi (Fig. 1d; Extended
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