Unexpected larger distribution of paleogene stem-rollers (AVES, CORACII): new evidence from the Eocene of Patagonia, Argentina

Here we present the first record of a stem-Coracii outside the Holarctic region, found in the early Eocene of Patagonia at the Laguna del Hunco locality. Ueekenkcoracias tambussiae gen. et sp. nov. consists of an incomplete right hind limb that presents the following combination of characters, characteristic of Coracii: relatively short and stout tibiotarsus, poorly developed crista cnemialis cranialis, short and wide tarsometatarsus, with the tuberositas m. tibialis cranialis located medially on the shaft, and curved and stout ungual phalanges. Although the presence of a rounded and conspicuous foramen vasculare distale and the trochlea metatarsi II strongly deflected medially resemble Primobucconidae, a fossil group only found in the Eocene of Europe and North America, our phylogenetic analysis indicates the new taxon is the basalmost known Coracii. The unexpected presence of a stem-Coracii in the Eocene of South America indicates that this clade had a more widespread distribution than previously hypothesized, already extending into the Southern Hemisphere by the early Eocene. Ueekenkcoracias tambussiae represents new evidence of the increasing diversity of stem lineages of birds in the Eocene. The new material provides novel morphological data for understanding the evolutionary origin and radiation of rollers and important data for estimates of the divergence time of the group.

The foot of Ueekenkcoracias has an anisodactyl toe arrangement (Fig. 2c), contrary to Leptosomidae, which has a zygodactyl-like arrangement 27 . In contrast to Primobucconidae, the pedal phalanges are short and robust, contrary to the phalanges of Leptosomidae, Todidae, Momotidae and Coraciidae that are elongated. Also, the unguals of Ueekenkcoracias present a very well-marked furrow on the sides, as in Alcedinidae. As in Septencoracias and Todidae, and contrary to Paracoracias and Primobucco, the first phalanx of the hallux is elongated. Nevertheless, in Todidae the first phalanx is the longest of all 21 , which is not the case for Ueekenkcoracias. The ungual phalanx I is stout, apparently lacking sulci, but with a well-developed tuberculum flexorium that is ventrally directed (similar to Alcedinidae and Leptosomidae). The tuberculum extensorium is small, although . ccc crista cnemialis cranialis, ccl crista cnemialis lateralis, cf crista fibularis, cl condylus lateralis, cm (f) condylus medialis (femur), cm (t) condylus medialis (tibiotarsus), fam facies articularis medialis, fid fossa infracotylaris dorsalis, fp fossa poplitea, fvd foramen vasculare distale, fvp foramina vascularia proximalia, I? metatarsi I?, II-IV trochlea metatarsi II-IV, ps pons supratendineus, se sulcus extensorius, tf trochlea fibularis, ttc tuberositas m. tibialis cranialis. Scale = 1 cm. www.nature.com/scientificreports/ conspicuous (well-developed in Todidae). Regarding the second toe, the second phalanx is markedly more elongated than the first, as in Septencoracias. The first phalanx of the third toe is robust and longer than the first phalanx of the first toe. The ungual phalanx II is stout and poorly curved. The fourth toe has the first phalanx longer than the rest, which are subquadrangular in shape. The configuration of phalanges resembles more the condition observed in Paracoracias with relatively short phalanges than the condition of Septencoracias and Alcedinidae, which have more elongated and slender phalanges.
Phylogenetic relationships. The parsimony phylogenetic analysis resulted in two most parsimonious trees of 205 steps (see "Methods" and Supplementary Information), generating a well resolved strict consensus tree (Fig. 3). The results of alternative methods of analysis resulted are identical in terms of the phylogenetic position of Ueekenkcoracias (see Supplementary Information)

Discussion
The presence of a stem-Coracii in South America is surprising, but the phylogenetic results and the presence of unique derived features of this clade, such as a rounded and conspicuous foramen vasculare distale and the trochlea metatarsi II strongly deflected medially, suggests Ueekenkcoracias is related to stem-Coracii from the Eocene of Europe and North America (e.g., Primobucconidae, Eocoracias, Paracoracias). The new specimen is the oldest record of Coracii outside Europe and North America, indicating that this clade had a more widespread distribution than previously hypothesized and extending its geographical range into the Southern Hemisphere by the early Eocene.
The unexpected presence of Old World birds outside their extant distribution has been reported in other instances during the Paleogene. However, these records mainly consist of stem groups recorded in North America. Such is the case, among others, of Tsidiiyazhi abini, a stem-Coliiformes from the early Paleocene of New Mexico 29 , Sandcoleus copiosus, a stem-Coliiformes from the early Eocene of Wyoming 6 , Foro panarium, a stem-Musophagiformes, and Celericolius acriala a stem-Coliiformes from the early Eocene of Wyoming 30,31 .
Close affinities of Ueekenkcoracias to these other stem-groups are unlikely based on its tarsometatarsus morphology. The tarsometatarsus of Coliiformes is markedly more elongated and slenderer, with the trochleae metatarsorum II and IV reaching almost the distal extension of trochlea metatarsi III 32 , and the trochlea metatarsi IV is more laterally disposed than in the fossil presented here. Moreover, the phalanges in Coliiformes are slenderer and, particularly, the first phalanx of the second toe is much shorter than in Ueekenkcoracias (e.g., Refs. 6,32 ); ungual phalanges are also slenderer in Coliiformes. In comparison with stem-Musophagiformes, the main differences include a shorter tibiotarsus and tarsometatarsus, a less developed crista cnemialis cranialis, and trochleae metatarsorum that are less spread than in Foro 30,33 .
A bird from the early Eocene of Europe and North America that has been related to Primobucconidae is Parvicuculus minor. However, the phylogenetic placement of that bird remains controversial 25,26 . Ueekenkcoracias shares with Parvicuculus a short and robust tarsometatarsus and the presence of a marked foramen vasculare distale, all features shared also with Primobucconidae. Moreover, Ueekenkcoracias has a shallower fossa infracotylaris dorsalis and a more medially located tuberositas m. tibialis cranialis. Also, the trochlea metatarsi IV in Parvicuculus is more proximally located than trochlea II (equally extended distally in Ueekenkcoracias) and more extended laterally (see Ref. 26 ).
Coracii is the clade that includes extant rollers (Coraciidae and Brachypteridae) and their fossil relatives, such as Primobucconidae, Eocoraciidae, Paracoracias and Geranopteridae 8,9 . Traditionally, Coracii was included within Coraciiformes. However, there is still debate about the monophyly of Coraciiformes, the clade that according to some authors (e.g., Refs. 10,24,34,35 ) includes other extant families such as Alcedinidae, Momotidae, Todidae, and Meropidae (Alcediniformes according to Ref. 36 ) together with Coracii. "Coraciiformes" have a relatively short tibiotarsus, with reduced cristae cnemiales, relatively short tarsometatarsus, widened in some groups (such as Alcedinidae), with the tuberositas m. tibialis cranialis medially located and a hypotarsus subtriangular or subrectangular with sulci and foramina. Among "Coraciiformes," a particular combination of characters of Ueekenkcoracias may suggest affinities with kingfishers (Alcedinidae), such as the presence of a femur with straight diaphysis, the condylus medialis of the tibiotarsus caudally projected, anisodactyl foot, short and wide tarsometatarsus with a widened proximal epiphysis (especially medially), foramina vascularia proximalia located at the same level proximally, tuberositas m. tibialis cranialis located medially on the diaphysis, trochlea metatarsi II strongly deflected medially, and presence of a large and rounded foramen vasculare distale. However, contrary to Alcedinidae, Ueekenkcoracias has a more developed eminentia intercotylaris, the first phalanx of the hallux is not medially expanded (an apomorphic condition of Alcedinidae according to Ref. 36 ), and the phalanges are shorter and stouter than those of the majority of the Alcedinidae (in which they are usually slender, although its length varies among genera: long in Dacelo, short in Megaceryle). If Ueekenkcoracias is a stem-kingfisher, this www.nature.com/scientificreports/ will imply a much earlier origin of the group, which has a scarce fossil record and an origination time estimated at ca. 37.5 Ma 35,37 , almost 15 Myr after the Ueekenkcoracias record. According to McCullough et al. 35 , Coraciiformes (i.e., Coracii + Alcediniformes) have a Palaeartic origin. They achieved this conclusion including some fossils of this large group in their analysis (e.g., Refs. 9,28 ). If Coraciiformes are monophyletic as proposed by those authors, then the clade seems to have conquered South America at least in four pulses: a lineage of stem-Coracii during the early Eocene and crown-Coraciiformes during the late Miocene-early Pleistocene (Alcedinidae twice in the late Miocene and Pleistocene, and Momotidae in the Pliocene 26,28 ). Otherwise, if Coraciiformes is paraphyletic, as most morphological-based analysis indicate 8 , Coraciiformes sensu stricto 36 reached South America before the Alcediniformes Alcedinidae, and Momotidae. From these groups, clearly, the lineage of stem-Coracii did not succeed, and the present distribution of Coraciiformes sensu lato in the world seems to be explained by the deterioration of warm climates at middle and high latitudes after the early Eocene climatic optimum, resulting in their extant pantropical distribution (e.g., Ref. 8 ).
The rich fossil plant assemblage at the Laguna del Hunco locality represents the environmental conditions in Patagonia during the early Eocene climatic optimum. Recent paleoenvironmental and floristic comparisons indicate that the closest modern analogs for the Laguna del Hunco flora are the Malesian lower-montane tropical, everwet rainforests 15 , where diverse extant "Coraciiformes" exist today. The Laguna del Hunco paleoenvironment resembles that reported for Holarctic stem-Coracii, such as Primobucconidae 7-9 in being a frost-free, warm lakeshore environment, although they differ in their seasonality (seasonally dry vs. everwet). In fact, the age of the Laguna del Hunco biota, ca. 52.2 Ma [13][14][15]19 , is very similar to that of the Fossil Butte Member of the Green River Formation (51.66 ± 0.09 Ma), the source of Primobucco mcgrewi 7,38 . Although Ueekenkcoracias is not the oldest stem-Coracii, due to the age of Septencoracias at ca. 54 Ma, the new taxon presented here provides important data for understanding the early biogeographic history of Coracii during the early Eocene.
According to Claramunt and Cracraft 34 , modern ornithofaunas are the result of recurrent dispersal events using two main routes: one connecting South America with the Old World via North America and another one connecting South America with Australia and New Zealand through Antarctica. Those authors 34 postulated that "Coraciiformes" (i.e., Coracii + Alcediniformes) colonized the Paleotropics from North American ancestors. Given the presence of many of these lineages in the early Paleogene of Europe, they inferred that "Coraciiformes" reached the western Palearctic through a North Atlantic corridor before ~ 52 Ma. Although the 'North American Gateway' hypothesis explains well the origins of Musophagiformes 30 and Coliiformes 29 , it does not explain the current fossil record of Coracii, due to the presence of Ueekenkcoracias as the basalmost stem-Coracii in the early Eocene of South America.
The arrival of a stem-Coracii lineage to South America may have occurred from North America if this clade has the biogeographic origin postulated by Ref. 34 , which would also open a second possible dispersal route from North America to Africa (in addition to the European route 34 ). Alternatively, the stem-Coracii may have arrived in South America from Africa if the latter continent is the biogeographic origin for the group, as postulated by the biogeographic analysis of Ericson 39 . Interestingly, this scenario is also compatible with the Afrotropical ancestral area reconstruction for several basal nodes of "Coraciiformes" + Piciformes in the analysis of Ref. 34 . This possibility is based on ancestral areas from biogeographic analyses, but unfortunately no records of stem-Coracii have been found yet in Africa.
In either scenario, a dispersal route for stem-Coracii across the South Atlantic between Africa and South America fits the biogeographic pattern 40,41 recognized for several vertebrate groups in the Eocene, including mammals (e.g., rodents 42 , primates 43 ), birds (e.g., Phorusrhacidae 44 , Opisthocomiformes 45 ), and reptiles 46,47 . Rafting events or even the possible presence of island chains 40 have been advocated as explanations for these faunal interchanges between Africa and South America during the Paleogene [40][41][42][43][44][45][46][47] . It is possible that small stem-Coracii also dispersed across the Southern Atlantic, either by flying, rafting, or island hopping while Africa was still relatively close to NE South America.

Conclusions
Ueekenkcoracias tambussiae provides evidence for the existence of a previously unrecognized group of birds in the early Eocene of South America and adds new information to the poorly known South American Paleogene ornithofaunas 11 . The new species is interpreted as a stem-Coracii, a clade that appears to have had a much wider distribution than previously thought. Ueekenkcoracias inhabited everwet rainforests during the Eocene in Patagonia. Moreover, Ueekenkcoracias provides new evidence that "Coraciiformes" (i.e., Coracii + Alcediniformes) have reached South America at least four times, once in the Paleogene and three times in the Neogene and early Pleistocene (see Refs. 35,37 ).
Ueekenkcoracias tambussiae adds to the increasing diversity of stem bird lineages recorded in the Eocene. Although Ueekenkcoracias is not the oldest record of Coracii, it represents the earliest divergent lineage of Coracii because it is positioned as the sister group of primobucconids and more derived taxa. Low branch support in our phylogenetic analysis is due to the incompleteness of the fossil, and additional fossil material will help to clarify the relationships of the fossil to other "Coraciiformes". The new discovery has a profound impact on the early biogeographical patterns of Coracii. The presence of the basalmost stem-roller Ueekenkcoracias in the Eocene of South America could be the result of dispersal events from North America or alternatively from Africa, resembling the biogeographic history proposed for other Paleogene vertebrates.  24,36 ). The phylogenetic position of the new taxon was evaluated using the character-taxon matrix of Ref. 9 , which includes 78 characters, an ingroup of 18 extant and extinct Picocoraciae, two Coliiformes, and Tyto (Strigiformes) as the outgroup. Following 9 , characters 13 and 17 were treated as ordered and an equally weighted parsimony analysis was performed using TNT (Tree analysis using New Technology) version 1.5 48 . An implicit enumeration tree search was conducted to provide an exact solution given the number of taxa in the matrix allowed this option. The strict consensus tree was generated from the most parsimonious trees obtained. Nodal support was evaluated using Bremer support and parsimony jackknifing in TNT. We additionally conducted a parsimony implied weight analysis in TNT 48 and a Bayesian analysis using Mr. Bayes using the Mkv model 49  www.nature.com/scientificreports/ Publisher's note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Methods
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/.