Synergistic innovations enabled the radiation of anglerfishes in the deep open ocean.

Major ecological transitions are thought to fuel diversification, but whether they are contingent on the evolution of certain traits called key innovations1 is unclear. Key innovations are routinely invoked to explain how lineages rapidly exploit new ecological opportunities.1,2,3 However, investigations of key innovations often focus on single traits rather than considering trait combinations that collectively produce effects of interest.4 Here, we investigate the evolution of synergistic trait interactions in anglerfishes, which include one of the most species-rich vertebrate clades in the bathypelagic, or "midnight," zone of the deep sea: Ceratioidea.5 Ceratioids are the only vertebrates that possess sexual parasitism, wherein males temporarily attach or permanently fuse to females to mate.6,7 We show that the rapid transition of ancestrally benthic anglerfishes into pelagic habitats occurred during a period of major global warming 50-35 million years ago.8,9 This transition coincided with the origins of sexual parasitism, which is thought to increase the probability of successful reproduction once a mate is found in the midnight zone, Earth's largest habitat.5,6,7 Our reconstruction of the evolutionary history of anglerfishes and the loss of immune genes support that permanently fusing clades have convergently degenerated their adaptive immunity. We find that degenerate adaptive immune genes and sexual body size dimorphism, both variably present in anglerfishes outside the ceratioid radiation, likely promoted their transition into the bathypelagic zone. These results show how traits from separate physiological, morphological, and reproductive systems can interact synergistically to drive major transitions and subsequent diversification in novel environments.

The genomic signatures of evolutionary stasis.

Evolutionary stasis characterizes lineages that seldom speciate and show little phenotypic change over long stretches of geological time. Although lineages that appear to exhibit evolutionary stasis are often called living fossils, no single mechanism is thought to be responsible for their slow rates of morphological evolution and low species diversity. Some analyses of molecular evolutionary rates in a handful of living fossil lineages have indicated that these clades exhibit slow rates of genomic change. Here, we investigate mechanisms of evolutionary stasis using a dataset of 1,105 exons for 481 vertebrate species. We demonstrate that two ancient clades of ray-finned fishes classically called living fossils, gars and sturgeons, exhibit the lowest rates of molecular substitution in protein-coding genes among all jawed vertebrates. Comparably low rates of evolution are observed at fourfold degenerate sites in gars and sturgeons, implying a mechanism of stasis decoupled from selection that we speculate is linked to a highly effective DNA repair apparatus. We show that two gar species last sharing common ancestry over 100 million years ago produce morphologically intermediate and fertile hybrids in the wild. This makes gars the oldest naturally hybridizing divergence among eukaryotes and supports a theoretical prediction that slow rates of nucleotide substitution across the genome slow the accumulation of genetic incompatibilities, enabling hybridization across deeply divergent lineages and slowing the rate of speciation over geological timescales. Our results help establish molecular stasis as a barrier to speciation and phenotypic innovation and provide a mechanism to explain the low species diversity in living fossil lineages.

A Morrison stem gekkotan reveals gecko evolution and Jurassic biogeography.

Geckos are a speciose and globally distributed clade of Squamata (lizards, including snakes and amphisbaenians) that are characterized by a host of modifications for nocturnal, scansorial and insectivorous ecologies. They are among the oldest divergences in the lizard crown, so understanding the origin of geckoes (Gekkota) is essential to understanding the origin of Squamata, the most species-rich extant tetrapod clade. However, the poor fossil record of gekkotans has obscured the sequence and timing of the assembly of their distinctive morphology. Here, we describe the first North American stem gekkotan based on a three-dimensionally preserved skull from the Morrison Formation of western North America. Despite its Late Jurassic age, the new species already possesses several key characteristics of the gekkotan skull along with retained ancestral features. We show that this new stem gekkotan, and several previously named species of uncertain phylogenetic relationships, comprise a widespread clade of early crown lizards, substantiating faunal homogeneity in Laurasia during the Late Jurassic that extended across disparate ecological, body-size and physiological classes.

The affinities of the Late Triassic Cryptovaranoides and the age of crown squamates.

Most living reptile diversity is concentrated in Squamata (lizards, including snakes), which have poorly known origins in space and time. Recently, †Cryptovaranoides microlanius from the Late Triassic of the United Kingdom was described as the oldest crown squamate. If true, this result would push back the origin of all major lizard clades by 30-65 Myr and suggest that divergence times for reptile clades estimated using genomic and morphological data are grossly inaccurate. Here, we use computed tomography scans and expanded phylogenetic datasets to re-evaluate the phylogenetic affinities of †Cryptovaranoides and other putative early squamates. We robustly reject the crown squamate affinities of †Cryptovaranoides, and instead resolve †Cryptovaranoides as a potential member of the bird and crocodylian total clade, Archosauromorpha. Bayesian total evidence dating supports a Jurassic origin of crown squamates, not Triassic as recently suggested. We highlight how features traditionally linked to lepidosaurs are in fact widespread across Triassic reptiles. Our study reaffirms the importance of critically choosing and constructing morphological datasets and appropriate taxon sampling to test the phylogenetic affinities of problematic fossils and calibrate the Tree of Life.

Evolutionary origins of the prolonged extant squamate radiation.

Squamata is the most diverse clade of terrestrial vertebrates. Although the origin of pan-squamates lies in the Triassic, the oldest undisputed members of extant clades known from nearly complete, uncrushed material come from the Cretaceous. Here, we describe three-dimensionally preserved partial skulls of two new crown lizards from the Late Jurassic of North America. Both species are placed at the base of the skink, girdled, and night lizard clade Pan-Scincoidea, which consistently occupies a position deep inside the squamate crown in both morphological and molecular phylogenies. The new lizards show that several features uniting pan-scincoids with another major lizard clade, the pan-lacertoids, in trees using morphology were convergently acquired as predicted by molecular analyses. Further, the palate of one new lizard bears a handful of ancestral saurian characteristics lost in nearly all extant squamates, revealing an underappreciated degree of complex morphological evolution in the early squamate crown. We find strong evidence for close relationships between the two new species and Cretaceous taxa from Eurasia. Together, these results suggest that early crown squamates had a wide geographic distribution and experienced complicated morphological evolution even while the Rhynchocephalia, now solely represented by the tuatara, was the dominant clade of lepidosaurs.

Hidden species diversity in an iconic living fossil vertebrate.

Ancient, species-poor lineages persistently occur across the Tree of life. These lineages are likely to contain unrecognized species diversity masked by the low rates of morphological evolution that characterize living fossils. Halecomorphi is a lineage of ray-finned fishes that diverged from its closest relatives before 200 Ma and is represented by only one living species in eastern North America, the bowfin, Amia calva Linnaeus. Here, we use double digest restriction-site-associated DNA sequencing and morphology to illuminate recent speciation in bowfins. Our results support the delimitation of a second living species of Amia, with the timing of diversification dating to the Plio-Pleistocene. This delimitation expands the species diversity of an ancient lineage that is integral to studies of vertebrate genomics and development, yet is facing growing conservation threats driven by the caviar fishery.

Author Correction: Halszkaraptor escuilliei and the evolution of the paravian bauplan.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Halszkaraptor escuilliei and the evolution of the paravian bauplan.

The evolution of birds from dinosaurs is a subject that has received great attention among vertebrate paleontologists. Nevertheless, the early evolution of the paravians, the group that contains birds and their closest non-avian dinosaur relatives, remains very poorly known. Even the most basal members of one paravian lineage, the Dromaeosauridae, already show a body plan that differs substantially from their closest non-paravian relatives. Recently, the dromaeosaurid Halszkaraptor escuilliei was described from the Cretaceous of Mongolia. Halszkaraptor possesses numerous unserrated premaxillary teeth, a platyrostral rostrum with a developed neurovascular system, an elongate neck, bizarrely-proportioned forearms, and a foreword-shifted center of mass, differing markedly from other paravians. A reevaluation of the anatomy, taphonomy, environmental setting, and phylogenetic position of H. escuilliei based on additional comparisons with other maniraptorans suggests that, rather than indicating it was a semiaquatic piscivore, the body plan of this dinosaur bears features widely distributed among maniraptorans and in some cases intermediate between the conditions in dromaeosaurids and related clades. I find no evidence for a semiaquatic lifestyle in Halszkaraptor. A phylogenetic reevaluation of Halszkaraptorinae places it as the sister clade to Unenlagiinae, indicating the bizarre features of unenlagiines previously interpreted as evidence of piscivory may also represent a mosaic of plesiomorphic, derived, and intermediate features. The anatomy of Halszkaraptor reveals that dromaeosaurids still possessed many features found in more basal maniraptoran and coelurosaur clades, including some that may have been tied to herbivory. Rather than being a semiaquatic piscavore, Halszkaraptor was a basal dromaeosaurid showing transitional features.

Trace fossils on dinosaur bones reveal ecosystem dynamics along the coast of eastern North America during the latest Cretaceous.

Direct evidence of paleoecological processes is often rare when the fossil record is poor, as in the case of the Cretaceous of eastern North America. Here, I describe a femur and partial tibia shaft assignable to theropods from two Late Cretaceous sites in New Jersey. The former, identifiable as the femur of a large ornithomimosaur, bears several scores interpreted as shark feeding traces. The tibia shaft has punctures and flaked bone from the bites of mid-sized crocodyliforms, the first documented occurrence of crocodyliform traces on dinosaur bone from the Maastrichtian of the Atlantic Coastal Plain. The surface of the partial tibia is also littered with indentations interpreted as the traces of invertebrates, revealing a microcosm of biological interaction on the coastal seafloor of the Cretaceous Atlantic Ocean. Massive crocodyliforms, such as Deinosuchus rugosus and the slightly smaller Deltasuchus motherali, maintained the role of terrestrial vertebrate taphonomic process drivers in eastern North America during the Cretaceous. The report of crocodyliform bite marks on the ornithomimosaur tibia shaft in this manuscript reinforces the importance of the role of crocodyliforms in the modification of terrestrial vertebrate remains during the Cretaceous in North America. The preserved invertebrate traces add to the sparse record of the presence of barnacles and other marine invertebrates on dinosaur bone, and the evidence of shark feeding on the ornithomimosaur femur support the "bloat-and-float" model of terrestrial vertebrate fossil deposition in marine deposits from the Cretaceous of eastern North America.

A tyrannosauroid metatarsus from the Merchantville Formation of Delaware increases the diversity of non-tyrannosaurid tyrannosauroids on Appalachia.

During the Late Cretaceous, the continent of North America was divided into two sections: Laramidia in the west and Appalachia in the east. Although the sediments of Appalachia recorded only a sparse fossil record of dinosaurs, the dinosaur faunas of this landmass were different in composition from those of Laramidia. Represented by at least two taxa (Appalachiosaurus montgomeriensis and Dryptosaurus aquilunguis), partial and fragmentary skeletons, and isolated bones, the non-tyrannosaurid tyrannosauroids of the landmass have attracted some attention. Unfortunately, these eastern tyrants are poorly known compared to their western contemporaries. Here, one specimen, the partial metatarsus of a tyrannosauroid from the Campanian Merchantville Formation of Delaware, is described in detail. The specimen can be distinguished from A. montgomeriensis and D. aquilunguis by several morphological features. As such, the specimen represents a potentially previously unrecognized taxon of tyrannosauroid from Appalachia, increasing the diversity of the clade on the landmass. Phylogenetic analysis and the morphology of the bones suggest the Merchantville specimen is a tyrannosauroid of "intermediate" grade, thus supporting the notion that Appalachia was a refugium for relict dinosaur clades.