Bird evolution in the Eocene: climate change in Europe and a Danish fossil fauna

The pattern of the evolutionary radiation of modern birds (Neornithes) has been debated for more than 10 years. However, the early fossil record of birds from the Paleogene, in particular, the Lower Eocene, has only recently begun to be used in a phylogenetic context to address the dynamics of this major vertebrate radiation. The Cretaceous-Paleogene (K-P) extinction event dominates our understanding of early modern bird evolution, but climate change throughout the Eocene is known to have also played a major role. The Paleocene and Lower Eocene was a time of avian diversification as a result of favourable global climatic conditions. Deteriorations in climate beginning in the Middle Eocene appear to be responsible for the demise of previously widespread avian lineages like Lithornithiformes and Gastornithidae. Other groups, such as Galliformes display replacement of some lineages by others, probably related to adaptations to a drier climate. Finally, the combination of slowly deteriorating climatic conditions from the Middle Eocene onwards, appears to have slowed the evolutionary rate in Europe, as avian faunas did not differentiate markedly until the Oligocene. Taking biotic factors in tandem with the known Paleogene fossil record of Neornithes has recently begun to illuminate this evolutionary event. Well-preserved fossil taxa are required in combination with ever-improving phylogenetic hypotheses for the inter-relationships of modern birds founded on morphological characters. One key avifauna of this age, synthesised for the first time herein, is the Lower Eocene Fur Formation of Denmark. The Fur birds represent some of the best preserved (often in three dimensions and with soft tissues) known fossil records for major clades of modern birds. Clear phylogenetic assessment of these fossils will prove critical for future calibration of the neornithine evolutionary timescale. Some early diverging clades were clearly present in the Paleocene as evidenced directly by new fossil material alongside the phylogenetically constrained Lower Eocene taxa. A later Oligocene radiation of clades other than Passeriformes is not supported by available fossil data.     

Rates of dinosaur limb evolution provide evidence for exceptional radiation in Mesozoic birds

Birds are the most diverse living tetrapod group and are a model of large-scale adaptive radiation. Neontological studies suggest a radiation within the avian crown group, long after the origin of flight. However, deep time patterns of bird evolution remain obscure because only limited fossil data have been considered. We analyse cladogenesis and limb evolution on the entire tree of Mesozoic theropods, documenting the dinosaur–bird transition and immediate origins of powered flight. Mesozoic birds inherited constraints on forelimb evolution from non-flying ancestors, and species diversification rates did not accelerate in the earliest flying taxa. However, Early Cretaceous short-tailed birds exhibit both phenotypic release of the hindlimb and increased diversification rates, unparalleled in magnitude at any other time in the first 155 Myr of theropod evolution. Thus, a Cretaceous adaptive radiation of stem-group birds was enabled by restructuring of the terrestrial locomotor module, which represents a key innovation. Our results suggest two phases of radiation in Avialae: with the Cretaceous diversification overwritten by extinctions of stem-group birds at the Cretaceous–Palaeogene boundary, and subsequent diversification of the crown group. Our findings illustrate the importance of fossil data for understanding the macroevolutionary processes generating modern biodiversity.     

A new assemblage of Cenozoic lungfishes (Dipnoi: Lepidosirenidae) from the late Oligocene Nsungwe Formation,Rukwa Rift Basin,southwestern Tanzania

Lungfish (Dipnoi) date back to the Devonian, and some fossil taxa as well as extant African lungfishes are known for their ability to aestivate, tolerating low-oxygen environments associated with seasonal drying. Extant lungfishes are separated into two families: Lepidosirenidae (Protopterus in Africa and Lepidosiren in South America) and Neoceratodontidae (Neocerotadus in Australia). African lungfishes were more geographically and phylogenetically diverse on the continent in the past than they are today, with only 5% of extinct taxa recorded from the sub-Saharan fossil record. Given the sparse record of Lepidosirenidae fossils from continental Africa, any new materials are important for understanding diversification of the clade. Here we describe new lungfish fossils cautiously referable to Protopterus annectens and Protopterus aethiopicus, which are strongly supported sister taxa based on the molecular phylogeny. Specimens were collected from the late Oligocene Nsungwe Formation in the Rukwa Rift Basin (RRB) of southwestern Tanzania. The late Oligocene Nsungwe Formation represents a sequence of continental rift-fill deposits of the Songwe sub-basin of the RRB and is subdivided into the lower Utengule and upper Songwe members. Recovery of such material from the Paleogene of Africa below the equator addresses a sizable gap in the lungfish fossil record. It also expands the Nsungwe Formation fauna that includes invertebrates, alestid fishes, ptychadenid anurans, snakes, and several clades of mammals, deepening paleoecological insights into the late Oligocene record of the continental African interior. At present, P. aethiopicus and P. dolloi have an extensive modern eastern African distribution associated with the rift lakes and a region where extant members of P. annectens are not presently known. Fossil specimens described herein document presence of the clade during Paleogene volcanic activity in the western branch of the Eastern African Rift System.     

The quality of the fossil record of Mesozoic birds

The Mesozoic fossil record has proved critical for understanding the early evolution and subsequent radiation of birds. Little is known, however, about its relative completeness: just how 'good' is the fossil record of birds from the Mesozoic? This question has come to prominence recently in the debate over differences in estimated dates of origin of major clades of birds from molecular and palaeontological data. Using a dataset comprising all known fossil taxa, we present analyses that go some way towards answering this question. Whereas avian diversity remains poorly represented in the Mesozoic, many relatively complete bird specimens have been discovered. New taxa have been added to the phylogenetic tree of basal birds, but its overall shape remains constant, suggesting that the broad outlines of early avian evolution are consistently represented: no stage in the Mesozoic is characterized by an overabundance of scrappy fossils compared with more complete specimens. Examples of Neornithes (modern orders) are known from later stages in the Cretaceous, but their fossils are rarer and scrappier than those of basal bird groups, which we suggest is a biological, rather than a geological, signal.     

Molecular and Paleontological Evidence for a Post-Cretaceous Origin of Rodents

The timing of the origin and diversification of rodents remains controversial, due to conflicting results from molecular clocks and paleontological data. The fossil record tends to support an early Cenozoic origin of crown-group rodents. In contrast, most molecular studies place the origin and initial diversification of crown-Rodentia deep in the Cretaceous, although some molecular analyses have recovered estimated divergence times that are more compatible with the fossil record. Here we attempt to resolve this conflict by carrying out a molecular clock investigation based on a nine-gene sequence dataset and a novel set of seven fossil constraints, including two new rodent records (the earliest known representatives of Cardiocraniinae and Dipodinae). Our results indicate that rodents originated around 61.7–62.4 Ma, shortly after the Cretaceous/Paleogene (K/Pg) boundary, and diversified at the intraordinal level around 57.7–58.9 Ma. These estimates are broadly consistent with the paleontological record, but challenge previous molecular studies that place the origin and early diversification of rodents in the Cretaceous. This study demonstrates that, with reliable fossil constraints, the incompatibility between paleontological and molecular estimates of rodent divergence times can be eliminated using currently available tools and genetic markers. Similar conflicts between molecular and paleontological evidence bedevil attempts to establish the origination times of other placental groups. The example of the present study suggests that more reliable fossil calibration points may represent the key to resolving these controversies.     

The oldest lamprophiid (Serpentes,Caenophidia) fossil from the late Oligocene Rukwa Rift Basin,Tanzania and the origins of African snake diversity

Extant snake faunas have their origins in the mid-Cenozoic, when colubroids replaced booid-grade snakes as the dominant species. The timing of this faunal changeover in North America and Europe based on fossils is thought to have occurred in the early Neogene, after a period of global cooling opened environments and made them suitable for more active predators. However, new fossils from the late Oligocene of Tanzania have revealed an early colubroid-dominated fauna in Africa suggesting a different pattern of faunal turnover there. Additionally, molecular divergence times suggest colubroid diversification began sometime in the Paleogene, although the exact timing and driving forces behind the diversification are not clear. Here we present the first fossil snake referred to the African clade Lamprophiinae, and the oldest fossil known of Lamprophiidae. As such, this specimen provides the only potential fossil calibration point for the African snake radiation represented by Lamprophiidae, and is the oldest snake referred to Elapoidea. A molecular clock analysis using this and other previously reported fossils as calibration points reveals colubroid diversification minimally occurred in the earliest Paleogene, although a Cretaceous origin cannot be excluded. The elapoid and colubrid lineages diverged during the period of global warming near the Paleocene-Eocene boundary, with both clades diversifying beginning in the early Eocene (proximate to the Early Eocene Climate Optimum) and continuing into the cooler Miocene. The majority of subclades diverge well before the appearance of colubroid dominance in the fossil record. These results suggest an earlier diversification of colubroids than generally previously thought, with hypothesized origins of these clades in Asia and Africa where the fossil record is relatively poorly known. Further work in these regions may provide new insights into the timing of, and environmental influences contributing to, the rise of colubroid snakes.     

A mitogenomic timescale for birds detects variable phylogenetic rates of molecular evolution and refutes the standard molecular clock

Current understanding of the diversification of birds is hindered by their incomplete fossil record and uncertainty in phylogenetic relationships and phylogenetic rates of molecular evolution. Here we performed the first comprehensive analysis of mitogenomic data of 48 vertebrates, including 35 birds, to derive a Bayesian timescale for avian evolution and to estimate rates of DNA evolution. Our approach used multiple fossil time constraints scattered throughout the phylogenetic tree and accounts for uncertainties in time constraints, branch lengths, and heterogeneity of rates of DNA evolution. We estimated that the major vertebrate lineages originated in the Permian; the 95% credible intervals of our estimated ages of the origin of archosaurs (258 MYA), the amniote-amphibian split (356 MYA), and the archosaur-lizard divergence (278 MYA) bracket estimates from the fossil record. The origin of modern orders of birds was estimated to have occurred throughout the Cretaceous beginning about 139 MYA, arguing against a cataclysmic extinction of lineages at the Cretaceous/Tertiary boundary. We identified fossils that are useful as time constraints within vertebrates. Our timescale reveals that rates of molecular evolution vary across genes and among taxa through time, thereby refuting the widely used mitogenomic or cytochrome b molecular clock in birds. Moreover, the 5-Myr divergence time assumed between 2 genera of geese (Branta and Anser) to originally calibrate the standard mitochondrial clock rate of 0.01 substitutions per site per lineage per Myr (s/s/l/Myr) in birds was shown to be underestimated by about 9.5 Myr. Phylogenetic rates in birds vary between 0.0009 and 0.012 s/s/l/Myr, indicating that many phylogenetic splits among avian taxa also have been underestimated and need to be revised. We found no support for the hypothesis that the molecular clock in birds "ticks" according to a constant rate of substitution per unit of mass-specific metabolic energy rather than per unit of time, as recently suggested. Our analysis advances knowledge of rates of DNA evolution across birds and other vertebrates and will, therefore, aid comparative biology studies that seek to infer the origin and timing of major adaptive shifts in vertebrates.     

Avian evolution, Gondwana biogeography and the Cretaceous-Tertiary mass extinction event

The fossil record has been used to support the origin and radiation of modern birds (Neornithes) in Laurasia after the Cretaceous-Tertiary mass extinction event, whereas molecular clocks have suggested a Cretaceous origin for most avian orders. These alternative views of neornithine evolution are examined using an independent set of evidence, namely phylogenetic relationships and historical biogeography. Pylogenetic relationships of basal lineages of neornithines, including ratite birds and their allies (Palaleocognathae), galliforms and anseriforms (Galloanserae), as well as lineages of the more advanced Neoves (Gruiformes, (Capimulgiformes, Passeriformes and others) demonstrate pervasive trans-Antarctic distribution patterns. The temporal history of the neornithines can be inferred from fossil taxa and the ages of vicariance events, and along with their biogeographical patterns, leads to the conclusion that neornithines arose in Gondwana prior to the Cretaceous Tertiary extinction event.     

Conceptual and analytical worldviews shape differences about global avian biogeography

In a recent paper, we generated a new time tree of modern birds and integrated it with biogeographic and palaeontological information to formulate a model for their biogeographic history. We postulated that modern birds originated in West Gondwanan continents, from where they dispersed around the world. Mayr suggested that our selective use of the fossil record may have biased our ancestral area reconstructions. We argue that the use of the fossil record must be selective in order to avoid the influence of its severe geographic bias: rock formations with numerous high‐quality fossil birds are found only in North America and Europe. An indiscriminate use of the avian fossil record would bias any biogeographic analysis towards these two continents. Our biogeographic model is perfectly consistent with the existence of diverse fossil avifaunas in the Eocene of North America and Europe because dispersion out of South America occurred earlier, in the Palaeocene.     

First macrofossil record of Icacinaceae in East Asia (early Oligocene,Wenshan Basin) and its ecological implications

Icacinaceae are well represented in the modern tropical flora of East Asia, but this family has no confirmed macrofossils from this region. Most of the unambiguous fossils (e.g., endocarps) are from the Paleogene of North America and Europe, where the family is no longer present. Here we report a fossil endocarp of the liana genus Iodes from the Oligocene Wenshan flora, southwestern China. The fossil is relatively large (ca. 20 mm length, 11 mm width) and documents a vascular bundle inside the endocarp wall, a pattern of ridges enclosing few areoles, and an asymmetrical apex and rounded base. On the basis of these characteristics, we described a new species, Iodes elliptica, which represents the first Icacinaceae fruit fossil record from Asia. This fossil, consistent with recent reports of Iodes pollen from the Eocene of Hainan, indicates a long-standing presence of the genus in SE Asia, dating back to the Paleogene. Based on the climatic data of modern Iodes, and other fossil occurrences from Wenshan, we hypothesize that the climate in the region was subtropical during the Oligocene, supporting a rainforest, with an overall mixed regional flora of subtropical and tropical elements.     

Early penguin fossils, plus mitochondrial genomes, calibrate avian evolution

Testing models of macroevolution, and especially the sufficiency of microevolutionary processes, requires good collaboration between molecular biologists and paleontologists. We report such a test for events around the Late Cretaceous by describing the earliest penguin fossils, analyzing complete mitochondrial genomes from an albatross, a petrel, and a loon, and describe the gradual decline of pterosaurs at the same time modern birds radiate. The penguin fossils comprise four naturally associated skeletons from the New Zealand Waipara Greensand, a Paleocene (early Tertiary) formation just above a well-known Cretaceous/Tertiary boundary site. The fossils, in a new genus (Waimanu), provide a lower estimate of 61-62 Ma for the divergence between penguins and other birds and thus establish a reliable calibration point for avian evolution. Combining fossil calibration points, DNA sequences, maximum likelihood, and Bayesian analysis, the penguin calibrations imply a radiation of modern (crown group) birds in the Late Cretaceous. This includes a conservative estimate that modern sea and shorebird lineages diverged at least by the Late Cretaceous about 74 +/- 3 Ma (Campanian). It is clear that modern birds from at least the latest Cretaceous lived at the same time as archaic birds including Hesperornis, Ichthyornis, and the diverse Enantiornithiformes. Pterosaurs, which also coexisted with early crown birds, show notable changes through the Late Cretaceous. There was a decrease in taxonomic diversity, and small- to medium-sized species disappeared well before the end of the Cretaceous. A simple reading of the fossil record might suggest competitive interactions with birds, but much more needs to be understood about pterosaur life histories. Additional fossils and molecular data are still required to help understand the role of biotic interactions in the evolution of Late Cretaceous birds and thus to test that the mechanisms of microevolution are sufficient to explain macroevolution.     

Flight reconstruction of two European enantiornithines (Aves,Pygostylia) and the achievement of bounding flight in Early Cretaceous birds

Intermittent flight through flap‐gliding (alternating flapping phases and gliding phases with spread wings) or bounding (flapping and ballistic phases with wings folded against the body) are strategies to optimize aerial efficiency which are commonly used among small birds today. The broad morphological disparity of Mesozoic birds suggests that a range of aerial strategies could have evolved early in avian evolution. Based on biomechanics and aerodynamic theory, this study reconstructs the flight modes of two small enantiornithines from the Lower Cretaceous fossil site of Las Hoyas (Spain): Concornis lacustris and Eoalulavis hoyasi. Our results show that the short length of their wings in relation to their body masses were suitable for flying through strict flapping and intermittent bounds, but not through facultative glides. Aerodynamic models indicate that the power margins of these birds were sufficient to sustain bounding flight. Our results thus suggest that C. lacustris and E. hoyasi would have increased aerial efficiency through bounding flight, just as many small passerines and woodpeckers do today. Intermittent bounding appears to have evolved early in the evolutionary history of birds, at least 126 million years ago.     

A brief review of the fossil history of the family Rosaceae with a focus on the Eocene Okanogan Highlands of eastern Washington State, USA, and British Columbia, Canada

Many of the oldest definitive members of the Rosaceae are present in the Eocene upland floras of the Okanogan Highlands of northeastern Washington State and British Columbia, Canada. Over a dozen rosaceous taxa representing extant and extinct genera of all four traditionally recognized subfamilies are known from flowers, fruits, wood, pollen, and especially leaves. The complexity seen in Eocene Rosaceae suggests that hybridization and polyploidy may have played a pivotal role in the early evolution of the family. Increased species diversity and the first appearance of additional modern taxa occur during the Late Paleogene in North America and Europe. The Rosaceae become increasingly important components of fossil floras during the Neogene, with taxa adapted to many habitats.     

中国中生代的鸟类:介绍及综述

最近十来年 ,中国辽宁发现的早白垩世的鸟类化石超过了世界上其它任何一个地区。中国的中生代鸟类化石代表了始祖鸟化石之后鸟类历史上第一次显著的分异。它们不仅包括了带有明显恐龙祖先特征的长尾的鸟类 ,而且还包括了许多进步或特化的种类 ,如早白垩世最大的鸟类 ,最原始的反鸟类 ,以及保存最好的、飞行结构和现生鸟类几乎一样的今鸟类。这些早期鸟类在诸如飞行、大小和食性等所反映的演化、形态和生态学特征等方面出现了重大的分异。具有长尾骨骼的原始基干鸟类热河鸟和驰龙类具有的相似性 ,进一步支持了鸟类起源于恐龙的学说。中国发现的早白垩世的鸟类以及树栖的恐龙化石还为鸟类飞行的树栖起源假说提供了十分重要的证据。“恐龙下树”的假说结合了鸟类起源于恐龙的学说和鸟类飞行的树栖起源学说 ,因此也得到了化石证据的支持。由于多种恐龙带有羽毛 ,因此羽毛不一定代表了恒温。恒温的鸟类可能到了早白垩世的进步鸟类中才开始出现     

Exceptionally preserved North American Paleogene metatherians: adaptations and discovery of a major gap in the opossum fossil record

A major gap in our knowledge of the evolution of marsupial mammals concerns the Paleogene of the northern continents, a critical time and place to link the early history of metatherians in Asia and North America with the more recent diversification in South America and Australia. We studied new exceptionally well-preserved partial skeletons of the Early Oligocene fossil Herpetotherium from the White River Formation in Wyoming, which allowed us to test the relationships of this taxon and examine its adaptations. Herpetotheriidae, with a fossil record extending from the Cretaceous to the Miocene, has traditionally been allied with opossums (Didelphidae) based on fragmentary material, mainly dentitions. Analysis of the new material reveals that several aspects of the cranial and postcranial anatomy, some of which suggests a terrestrial lifestyle, distinguish Herpetotherium from opossums. We found that Herpetotherium is the sister group to the crown group Marsupialia and is not a stem didelphid. Combination of the new palaeontological data with molecular divergence estimates, suggests the presence of a long undocumented gap in the fossil record of opossums extending some 45Myr from the Early Miocene to the Cretaceous.     

Phylogenetic analysis of pelecaniformes (aves) based on osteological data: implications for waterbird phylogeny and fossil calibration studies

Background

Debate regarding the monophyly and relationships of the avian order Pelecaniformes represents a classic example of discord between morphological and molecular estimates of phylogeny. This lack of consensus hampers interpretation of the group''s fossil record, which has major implications for understanding patterns of character evolution (e.g., the evolution of wing-propelled diving) and temporal diversification (e.g., the origins of modern families). Relationships of the Pelecaniformes were inferred through parsimony analyses of an osteological dataset encompassing 59 taxa and 464 characters. The relationships of the Plotopteridae, an extinct family of wing-propelled divers, and several other fossil pelecaniforms (Limnofregata, Prophaethon, Lithoptila, ?Borvocarbo stoeffelensis) were also assessed. The antiquity of these taxa and their purported status as stem members of extant families makes them valuable for studies of higher-level avian diversification.

Methodology/Principal Findings

Pelecaniform monophyly is not recovered, with Phaethontidae recovered as distantly related to all other pelecaniforms, which are supported as a monophyletic Steganopodes. Some anatomical partitions of the dataset possess different phylogenetic signals, and partitioned analyses reveal that these discrepancies are localized outside of Steganopodes, and primarily due to a few labile taxa. The Plotopteridae are recovered as the sister taxon to Phalacrocoracoidea, and the relationships of other fossil pelecaniforms representing key calibration points are well supported, including Limnofregata (sister taxon to Fregatidae), Prophaethon and Lithoptila (successive sister taxa to Phaethontidae), and ?Borvocarbo stoeffelensis (sister taxon to Phalacrocoracidae). These relationships are invariant when ‘backbone’ constraints based on recent avian phylogenies are imposed.

Conclusions/Significance

Relationships of extant pelecaniforms inferred from morphology are more congruent with molecular phylogenies than previously assumed, though notable conflicts remain. The phylogenetic position of the Plotopteridae implies that wing-propelled diving evolved independently in plotopterids and penguins, representing a remarkable case of convergent evolution. Despite robust support for the placement of fossil taxa representing key calibration points, the successive outgroup relationships of several “stem fossil + crown family” clades are variable and poorly supported across recent studies of avian phylogeny. Thus, the impact these fossils have on inferred patterns of temporal diversification depends heavily on the resolution of deep nodes in avian phylogeny.     

The fossil record and limb disparity of enantiornithines, the dominant flying birds of the Cretaceous

Morphometric and stratigraphic analyses that encompass the known fossil record of enantiornithine birds (Enantiornithes) are presented. These predominantly flighted taxa were the dominant birds of the second half of the Mesozoic; the enantiornithine lineage is known to have lasted for at least 60 million years (Ma), up until the end of the Cretaceous. Analyses of fossil record dynamics show that enantiornithine 'collectorship' since the 1980s approaches an exponential distribution, indicating that an asymptote in proportion of specimens has yet to be achieved. Data demonstrate that the fossil record of enantiornithines is complete enough for the extraction of biological patterns. Comparison of the available fossil specimens with a large data set of modern bird (Neornithes) limb proportions also illustrates that the known forelimb proportions of enantiornithines fall within the range of extant taxa; thus these birds likely encompassed the range of flight styles of extant birds. In contrast, most enantiornithines had hindlimb proportions that differ from any extant taxa. To explore this, ternary diagrams are used to graph enantiornithine limb variation and to identify some morphological oddities ( Otogornis , Gobipteryx ); taxa not directly comparable to modern birds. These exceptions are interesting – although anatomically uniform, and similar to extant avians in their wing proportions, some fossil enantiornithines likely had flight styles not seen among their living counterparts.     

Comparative morphology of the radial carpal bone of neornithine birds and the phylogenetic significance of character variation

The morphology of the radial carpal bone (os carpi radiale) of neornithine birds is for the first time evaluated in a comparative context. An unexpected morphological variation of this bone is documented, and characteristic derived morphologies are identified. One of these characterizes a subclade of Accipitridae, which includes the taxa Harpiinae, Circinae, Melieraxinae, Accipitrinae, Milvinae, Haliaeetinae, Buteoninae, and Aquilinae. Another derived morphology of the radial carpal is found in the Picocoraciae, the clade including Coraciiformes sensu stricto, Alcediniformes, Bucerotes, and Piciformes. This latter morphology is absent in Leptosomidae and Trogonidae and constitutes the first morphological apomorphy of Picocoraciae. A distinctive morphology of the radial carpal is further present in passeriform birds. Character variation of the radial carpal provides new data for the evaluation of conflicting phylogenetic hypotheses, and it is detailed that the morphology of this bone further contributes to a phylogenetic placement of controversial avian taxa in the fossil record.