Evidence for convergent evolution of ultrasonic hearing in toothed whales (Cetacea: Odontoceti).

Toothed whales (Cetacea: Odontoceti) are the most diverse group of modern cetaceans, originating during the Eocene/Oligocene transition approximately 38 Ma. All extant odontocetes echolocate; a single origin for this behaviour is supported by a unique facial source for ultrasonic vocalizations and a cochlea adapted for hearing the corresponding echoes. The craniofacial and inner ear morphology of Oligocene odontocetes support a rapid (less than 5 Myr) early evolution of echolocation. Although some cranial features in the stem odontocetes Simocetus and Olympicetus suggest an ability to generate ultrasonic sound, until now, the bony labyrinths of taxa of this grade have not been investigated. Here, we use µCT to examine a petrosal of a taxon with clear similarities to Olympicetus avitus. Measurements of the bony labyrinth, when added to an extensive dataset of cetartiodactyls, resulted in this specimen sharing a morphospace with stem whales, suggesting a transitional inner ear. This discovery implies that either the lineage leading to this Olympicetus--like taxon lost the ability to hear ultrasonic sound, or adaptations for ultrasonic hearing evolved twice, once in xenorophids and again on the stem of the odontocete crown group. We favour the latter interpretation as it matches a well-documented convergence of craniofacial morphology between xenorophids and extant odontocetes.

Neuroanatomy and inner ear labyrinths of the narwhal, Monodon monoceros, and beluga, Delphinapterus leucas (Cetacea: Monodontidae).

Narwhals (Monodon monoceros) and belugas (Delphinapterus leucas) are the only extant members of the Monodontidae, and are charismatic Arctic-endemic cetaceans that are at risk from global change. Investigating the anatomy and sensory apparatuses of these animals is essential to understanding their ecology and evolution, and informs efforts for their conservation. Here, we use X-ray CT scans to compare aspects of the endocranial and inner ear labyrinth anatomy of extant monodontids and use the overall morphology to draw larger inferences about the relationship between morphology and ecology. We show that differences in the shape of the brain, vasculature, and neural canals of both species may relate to differences in diving and other behaviors. The cochleae are similar in morphology in the two species, signifying similar hearing ranges and a close evolutionary relationship. Lastly, we compare two different methods for calculating 90var - a calculation independent of body size that is increasingly being used as a proxy for habitat preference. We show that a 'direct' angular measurement method shows significant differences between Arctic and other habitat preferences, but angle measurements based on planes through the semicircular canals do not, emphasizing the need for more detailed study and standardization of this measurement. This work represents the first comparative internal anatomical study of the endocranium and inner ear labyrinths of this small clade of toothed whales.

Inference of facultative mobility in the enigmatic Ediacaran organism Parvancorina.

Establishing how Ediacaran organisms moved and fed is critical to deciphering their ecological and evolutionary significance, but has long been confounded by their non-analogue body plans. Here, we use computational fluid dynamics to quantitatively analyse water flow around the Ediacaran taxon Parvancorina, thereby testing between competing models for feeding mode and mobility. The results show that flow was not distributed evenly across the organism, but was directed towards localized areas; this allows us to reject osmotrophy, and instead supports either suspension feeding or detritivory. Moreover, the patterns of recirculating flow differ substantially with orientation to the current, suggesting that if Parvancorina was a suspension feeder, it would have been most efficient if it was able to re-orient itself with respect to current direction, and thus ensure flow was directed towards feeding structures. Our simulations also demonstrate that the amount of drag varied with orientation, indicating that Parvancorina would have greatly benefited from adjusting its position to minimize drag. Inference of facultative mobility in Parvancorina suggests that Ediacaran benthic ecosystems might have possessed a higher proportion of mobile taxa than currently appreciated from trace fossil studies. Furthermore, this inference of movement suggests the presence of musculature or appendages that are not preserved in fossils, but which would noneltheless support a bilaterian affinity for Parvancorina.

The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record.

BACKGROUND: The highly derived morphology and astounding diversity of snakes has long inspired debate regarding the ecological and evolutionary origin of both the snake total-group (Pan-Serpentes) and crown snakes (Serpentes). Although speculation abounds on the ecology, behavior, and provenance of the earliest snakes, a rigorous, clade-wide analysis of snake origins has yet to be attempted, in part due to a dearth of adequate paleontological data on early stem snakes. Here, we present the first comprehensive analytical reconstruction of the ancestor of crown snakes and the ancestor of the snake total-group, as inferred using multiple methods of ancestral state reconstruction. We use a combined-data approach that includes new information from the fossil record on extinct crown snakes, new data on the anatomy of the stem snakes Najash rionegrina, Dinilysia patagonica, and Coniophis precedens, and a deeper understanding of the distribution of phenotypic apomorphies among the major clades of fossil and Recent snakes. Additionally, we infer time-calibrated phylogenies using both new 'tip-dating' and traditional node-based approaches, providing new insights on temporal patterns in the early evolutionary history of snakes. RESULTS: Comprehensive ancestral state reconstructions reveal that both the ancestor of crown snakes and the ancestor of total-group snakes were nocturnal, widely foraging, non-constricting stealth hunters. They likely consumed soft-bodied vertebrate and invertebrate prey that was subequal to head size, and occupied terrestrial settings in warm, well-watered, and well-vegetated environments. The snake total-group - approximated by the Coniophis node - is inferred to have originated on land during the middle Early Cretaceous (~128.5 Ma), with the crown-group following about 20 million years later, during the Albian stage. Our inferred divergence dates provide strong evidence for a major radiation of henophidian snake diversity in the wake of the Cretaceous-Paleogene (K-Pg) mass extinction, clarifying the pattern and timing of the extant snake radiation. Although the snake crown-group most likely arose on the supercontinent of Gondwana, our results suggest the possibility that the snake total-group originated on Laurasia. CONCLUSIONS: Our study provides new insights into when, where, and how snakes originated, and presents the most complete picture of the early evolution of snakes to date. More broadly, we demonstrate the striking influence of including fossils and phenotypic data in combined analyses aimed at both phylogenetic topology inference and ancestral state reconstruction.

Biotic replacement and mass extinction of the Ediacara biota.

The latest Neoproterozoic extinction of the Ediacara biota has been variously attributed to catastrophic removal by perturbations to global geochemical cycles, 'biotic replacement' by Cambrian-type ecosystem engineers, and a taphonomic artefact. We perform the first critical test of the 'biotic replacement' hypothesis using combined palaeoecological and geochemical data collected from the youngest Ediacaran strata in southern Namibia. We find that, even after accounting for a variety of potential sampling and taphonomic biases, the Ediacaran assemblage preserved at Farm Swartpunt has significantly lower genus richness than older assemblages. Geochemical and sedimentological analyses confirm an oxygenated and non-restricted palaeoenvironment for fossil-bearing sediments, thus suggesting that oxygen stress and/or hypersalinity are unlikely to be responsible for the low diversity of communities preserved at Swartpunt. These combined analyses suggest depauperate communities characterized the latest Ediacaran and provide the first quantitative support for the biotic replacement model for the end of the Ediacara biota. Although more sites (especially those recording different palaeoenvironments) are undoubtedly needed, this study provides the first quantitative palaeoecological evidence to suggest that evolutionary innovation, ecosystem engineering and biological interactions may have ultimately caused the first mass extinction of complex life.

Anatomical evidence for low frequency sensitivity in an archaeocete whale: comparison of the inner ear of Zygorhiza kochii with that of crown Mysticeti.

The evolution of hearing in cetaceans is a matter of current interest given that odontocetes (toothed whales) are sensitive to high frequency sounds and mysticetes (baleen whales) are sensitive to low and potentially infrasonic noises. Earlier diverging stem cetaceans (archaeocetes) were hypothesized to have had either low or high frequency sensitivity. Through CT scanning, the morphology of the bony labyrinth of the basilosaurid archaeocete Zygorhiza kochii is described and compared to novel information from the inner ears of mysticetes, which are less known than the inner ears of odontocetes. Further comparisons are made with published information for other cetaceans. The anatomy of the cochlea of Zygorhiza is in line with mysticetes and supports the hypothesis that Zygorhiza was sensitive to low frequency noises. Morphological features that support the low frequency hypothesis and are shared by Zygorhiza and mysticetes include a long cochlear canal with a high number of turns, steeply graded curvature of the cochlear spiral in which the apical turn is coiled tighter than the basal turn, thin walls separating successive turns that overlap in vestibular view, and reduction of the secondary bony lamina. Additional morphology of the vestibular system indicates that Zygorhiza was more sensitive to head rotations than extant mysticetes are, which likely indicates higher agility in the ancestral taxon.

Ediacaran marine animal forests and the ventilation of the oceans.

The rise of animals across the Ediacaran-Cambrian transition marked a step-change in the history of life, from a microbially dominated world to the complex macroscopic biosphere we see today.1,2,3 While the importance of bioturbation and swimming in altering the structure and function of Earth systems is well established,4,5,6 the influence of epifaunal animals on the hydrodynamics of marine environments is not well understood. Of particular interest are the oldest "marine animal forests,"7 which comprise a diversity of sessile soft-bodied organisms dominated by the fractally branching rangeomorphs.8,9 Typified by fossil assemblages from the Ediacaran of Mistaken Point, Newfoundland,8,10,11 these ancient communities might have played a pivotal role in structuring marine environments, similar to modern ecosystems,7,12,13 but our understanding of how they impacted fluid flow in the water column is limited. Here, we use ecological modeling and computational flow simulations to explore how Ediacaran marine animal forests influenced their surrounding environment. Our results reveal how organism morphology and community structure and composition combined to impact vertical mixing of the surrounding water. We find that Mistaken Point communities were capable of generating high-mixing conditions, thereby likely promoting gas and nutrient transport within the "canopy." This mixing could have served to enhance local-scale oxygen concentrations and redistribute resources like dissolved organic carbon. Our work suggests that Ediacaran marine animal forests may have contributed to the ventilation of the oceans over 560 million years ago, well before the Cambrian explosion of animals.

The rangeomorph Pectinifrons abyssalis: Hydrodynamic function at the dawn of animal life.

Rangeomorphs are among the oldest putative eumetazoans known from the fossil record. Establishing how they fed is thus key to understanding the structure and function of the earliest animal ecosystems. Here, we use computational fluid dynamics to test hypothesized feeding modes for the fence-like rangeomorph Pectinifrons abyssalis, comparing this to the morphologically similar extant carnivorous sponge Chondrocladia lyra. Our results reveal complex patterns of flow around P. abyssalis unlike those previously reconstructed for any other Ediacaran taxon. Comparisons with C. lyra reveal substantial differences between the two organisms, suggesting they converged on a similar fence-like morphology for different functions. We argue that the flow patterns recovered for P. abyssalis do not support either a suspension feeding or osmotrophic feeding habit. Instead, our results indicate that rangeomorph fronds may represent organs adapted for gas exchange. If correct, this interpretation could require a dramatic reinterpretation of the oldest macroscopic animals.

Gregarious suspension feeding in a modular Ediacaran organism.

Reconstructing Precambrian eukaryotic paleoecology is pivotal to understanding the origins of the modern, animal-dominated biosphere. Here, we combine new fossil data from southern Namibia with computational fluid dynamics (CFD) to test between competing feeding models for the Ediacaran taxon Ernietta. In addition, we perform simulations for multiple individuals, allowing us to analyze hydrodynamics of living communities. We show that Ernietta lived gregariously, forming shallow marine aggregations in the latest Ediacaran, 548 to 541 million years (Ma) ago. We demonstrate enhanced vertical mixing of the water column above aggregations and preferential redirection of current into body cavities of downstream individuals. These results support the reconstruction of Ernietta as a macroscopic suspension feeder and also provide a convincing paleoecological advantage to feeding in aggregations analogous to those recognized in many extant marine metazoans. These results provide some of the oldest evidence of commensal facilitation by macroscopic eukaryotes yet recognized in the fossil record.

Increase in metazoan ecosystem engineering prior to the Ediacaran-Cambrian boundary in the Nama Group, Namibia.

The disappearance of the soft-bodied Ediacara biota at the Ediacaran-Cambrian boundary potentially represents the earliest mass extinction of complex life, although the precise driver(s) of this extinction remain unresolved. The 'biotic replacement' model proposes that an evolutionary radiation of metazoan ecosystem engineers in the latest Ediacaran profoundly altered marine palaeoenvironments, resulting in the extinction of Ediacara biota and setting the stage for the subsequent Cambrian Explosion. However, metazoan ecosystem engineering across the Ediacaran-Cambrian transition has yet to be quantified. Here, we test this key tenet of the biotic replacement model by characterizing the intensity of metazoan bioturbation and ecosystem engineering in trace fossil assemblages throughout the latest Ediacaran Nama Group in southern Namibia. The results illustrate a dramatic increase in both bioturbation and ecosystem engineering intensity in the latest Ediacaran, prior to the Cambrian boundary. Moreover, our analyses demonstrate that the highest-impact ecosystem engineering behaviours were present well before the onset of the Cambrian. These data provide the first support for a fundamental prediction of the biotic replacement model, and evidence for a direct link between the early evolution of ecosystem engineering and the extinction of the Ediacara biota.

Suspension feeding in the enigmatic Ediacaran organism Tribrachidium demonstrates complexity of Neoproterozoic ecosystems.

The first diverse and morphologically complex macroscopic communities appear in the late Ediacaran period, 575 to 541 million years ago (Ma). The enigmatic organisms that make up these communities are thought to have formed simple ecosystems characterized by a narrow range of feeding modes, with most restricted to the passive absorption of organic particles (osmotrophy). We test between competing feeding models for the iconic Ediacaran organism Tribrachidium heraldicum using computational fluid dynamics. We show that the external morphology of Tribrachidium passively directs water flow toward the apex of the organism and generates low-velocity eddies above apical "pits." These patterns of fluid flow are inconsistent with osmotrophy and instead support the interpretation of Tribrachidium as a passive suspension feeder. This finding provides the oldest empirical evidence for suspension feeding at 555 to 550 Ma, ~10 million years before the Cambrian explosion, and demonstrates that Ediacaran organisms formed more complex ecosystems in the latest Precambrian, involving a larger number of ecological guilds, than currently appreciated.

Unique feeding morphology in a new prognathous extinct porpoise from the Pliocene of California.

Modern porpoises (Odontoceti: Phocoenidae) are some of the smallest cetaceans and usually feed near the seafloor on small fish and cephalopods [1-3]. Within both extinct and extant phocoenids, no evidence for specialized mandibular morphology has been documented [4-7]. Here we describe a new species of extinct porpoise, Semirostrum ceruttii, from the marine Pliocene San Diego (4.2-1.6 mega-annum, Ma) and Purisima (5-2.5 Ma) formations of California. The mandibles comprise a long, fused, and nearly edentulous prognathous symphysis, extending farther beyond the rostrum than in any known mammal. Phylogenetic analyses based on morphology reconstruct Semirostrum ceruttii as sister to extant (crown) porpoise species with moderate support. We describe the spectacularly preserved holotype specimen based on computed tomography (CT) scans, which allowed visualization of the elongate mental and accessory canals within the symphysis. The elongate canals are similar to those found in Rynchops birds [8] and were likely involved in sensory function. Oblique labial wear facets present on numerous small conical mandibular teeth posterior to the symphysis suggest regular contact with benthic substrate. The unique mandibular and dental characteristics, along with robust scapulae, sternum, and unfused cervical vertebrae, support the interpretation that this species employed a form of benthic skim feeding by using its mandible to probe for and obtain prey.

Comparative morphology of porpoise (Cetacea: Phocoenidae) pterygoid sinuses: phylogenetic and functional implications.

High-resolution X-ray computed tomographic scans were used to examine pterygoid sinus morphology within extant porpoise species and one delphinid (Tursiops truncatus), in order to consider: 1) intraspecific and interspecific variation among the studied species; 2) the most parsimonious sequence of character acquisition; and 3) the potential functional roles of the preorbital lobes of the sinuses in sound reflection. Scans revealed that the pterygoid/palatine regions are mediolaterally broader in the earliest diverging phocoenid (Neophocaena phocaenoides) and Tursiops truncatus than the dorsoventrally elongated sinuses observed in other species. Rostrocaudal lengths of the sphenoidal regions of the sinuses in all individuals studied are proportionally similar, indicating conservatism in this region across species. The neonate Phocoena phocoena has shorter preorbital lobes than adults, but they are still proportionally longer than Neophocaena phocaenoides and Phocoena spinipinnis. The preorbital lobes broaden mediolaterally to varying degrees across species; in particular, Phocoenoides dalli has the largest dorsal and lateral expansion of this region. Assuming the highest pulse frequency produced by porpoises is 150 kHz, all regions of the preorbital lobes are thick enough to reflect the wavelengths produced. In addition, the neonate preorbital lobes are not as elongated as they are in adults, and the dorsal third of this region may not reflect sound to the same extent. This study reinforces the importance of using nondestructive methods to quantify variation in endocranial anatomy and the value of CT data for recovering phylogenetically useful information, as well as functional roles sinuses play in concert with the soft tissue head anatomy for biosonar.

Morphology and variation in porpoise (Cetacea: Phocoenidae) cranial endocasts.

Evolution of endocranial anatomy in cetaceans is important from the perspective of echolocation ability, intelligence, social structure, and alternate pathways for circulation to the brain. Apart from the importance of studying brain shape and asymmetries as they relate to aspects of behavior and intelligence, cranial endocasts can show a close correspondence to the hydrostatic shape of the brain in life, and canals and grooves can preserve features of the circulatory system. Multiple samples are rarely available for studies of individual variation, especially in fossils, thus a first step in quantifying variation and making comparisons with fossils is made possible with CT scans of osteological specimens. This study presents a series of high-resolution X-ray CT-derived cranial endocasts of six extant species of Phocoenidae, a clade including some of the smallest and one of the rarest cetaceans. Degree of gyrification varies interspecifically and intraspecifically, possibly resulting from variation in preservation of the ossified meninges. Computed tomographic data show that visually assessed asymmetry in the cranial endocasts is not correlated with volumetric measurements, but nonetheless may reflect torsion in the skull's shape such that the right cerebral and cerebellar hemispheres extend rostrally and laterally more than the left. Vasculature and canals are similar to other described cetacean species, but the hypophyseal casts are unusual. Similarities between brain shape and volume measurements in the different species can be attributed to paedomorphism and concomitant variation in ecological preferences. This may explain similarities Neophocaena phocaenoides and Phocoena sinus share with the juvenile Phocoena phocoena specimen studied.