Jonathan H. Geisler

A phylogenetic blueprint for a modern whale

The emergence of Cetacea in the Paleogene represents one of the most profound macroevolutionary transitions within Mammalia. The move from a terrestrial habitat to a committed aquatic lifestyle engendered wholesale changes in anatomy, physiology, and behavior. The results of this remarkable transformation are extant whales that include the largest, biggest brained, fastest swimming, loudest, deepest diving mammals, some of which can detect prey with a sophisticated echolocation system (Odontoceti - toothed whales), and others that batch feed using racks of baleen (Mysticeti - baleen whales). A broad-scale reconstruction of the evolutionary remodeling that culminated in extant cetaceans has not yet been based on integration of genomic and paleontological information. Here, we first place Cetacea relative to extant mammalian diversity, and assess the distribution of support among molecular datasets for relationships within Artiodactyla (even-toed ungulates, including Cetacea). We then merge trees derived from three large concatenations of molecular and fossil data to yield a composite hypothesis that encompasses many critical events in the evolutionary history of Cetacea. By combining diverse evidence, we infer a phylogenetic blueprint that outlines the stepwise evolutionary development of modern whales. This hypothesis represents a starting point for more detailed, comprehensive phylogenetic reconstructions in the future, and also highlights the synergistic interaction between modern (genomic) and traditional (morphological+paleontological) approaches that ultimately must be exploited to provide a rich understanding of evolutionary history across the entire tree of Life.

Understanding phylogenetic incongruence: lessons from phyllostomid bats

All characters and trait systems in an organism share a common evolutionary history that can be estimated using phylogenetic methods. However, differential rates of change and the evolutionary mechanisms driving those rates result in pervasive phylogenetic conflict. These drivers need to be uncovered because mismatches between evolutionary processes and phylogenetic models can lead to high confidence in incorrect hypotheses. Incongruence between phylogenies derived from morphological versus molecular analyses, and between trees based on different subsets of molecular sequences has become pervasive as datasets have expanded rapidly in both characters and species. For more than a decade, evolutionary relationships among members of the New World bat family Phyllostomidae inferred from morphological and molecular data have been in conflict. Here, we develop and apply methods to minimize systematic biases, uncover the biological mechanisms underlying phylogenetic conflict, and outline data requirements for future phylogenomic and morphological data collection. We introduce new morphological data for phyllostomids and outgroups and expand previous molecular analyses to eliminate methodological sources of phylogenetic conflict such as taxonomic sampling, sparse character sampling, or use of different algorithms to estimate the phylogeny. We also evaluate the impact of biological sources of conflict: saturation in morphological changes and molecular substitutions, and other processes that result in incongruent trees, including convergent morphological and molecular evolution. Methodological sources of incongruence play some role in generating phylogenetic conflict, and are relatively easy to eliminate by matching taxa, collecting more characters, and applying the same algorithms to optimize phylogeny. The evolutionary patterns uncovered are consistent with multiple biological sources of conflict, including saturation in morphological and molecular changes, adaptive morphological convergence among nectar‐feeding lineages, and incongruent gene trees. Applying methods to account for nucleotide sequence saturation reduces, but does not completely eliminate, phylogenetic conflict. We ruled out paralogy, lateral gene transfer, and poor taxon sampling and outgroup choices among the processes leading to incongruent gene trees in phyllostomid bats. Uncovering and countering the possible effects of introgression and lineage sorting of ancestral polymorphism on gene trees will require great leaps in genomic and allelic sequencing in this species‐rich mammalian family. We also found evidence for adaptive molecular evolution leading to convergence in mitochondrial proteins among nectar‐feeding lineages. In conclusion, the biological processes that generate phylogenetic conflict are ubiquitous, and overcoming incongruence requires better models and more data than have been collected even in well‐studied organisms such as phyllostomid bats.

THE EVOLUTIONARY HISTORY OF CETACEAN BRAIN AND BODY SIZE

Cetaceans rival primates in brain size relative to body size and include species with the largest brains and biggest bodies to have ever evolved. Cetaceans are remarkably diverse, varying in both phenotypes by several orders of magnitude, with notable differences between the two extant suborders, Mysticeti and Odontoceti. We analyzed the evolutionary history of brain and body mass, and relative brain size measured by the encephalization quotient (EQ), using a data set of extinct and extant taxa to capture temporal variation in the mode and direction of evolution. Our results suggest that cetacean brain and body mass evolved under strong directional trends to increase through time, but decreases in EQ were widespread. Mysticetes have significantly lower EQs than odontocetes due to a shift in brain:body allometry following the divergence of the suborders, caused by rapid increases in body mass in Mysticeti and a period of body mass reduction in Odontoceti. The pattern in Cetacea contrasts with that in primates, which experienced strong trends to increase brain mass and relative brain size, but not body mass. We discuss what these analyses reveal about the convergent evolution of large brains, and highlight that until recently the most encephalized mammals were odontocetes, not primates.

A New Genus and Species of Late Miocene Inioid (Cetacea, Odontoceti) from the Meherrin River, North Carolina, U.S.A.

ABSTRACT A new genus and species of extinct inioid odontocete (Meherrinia isoni) is based on nine partial crania that probably originated from the late Miocene marine Eastover Formation in North Carolina, U.S.A. They were collected from the riverbed of the Meherrin River, a tributary of the Chowan River. Ossification of the mesethmoid and the tight inter-digitation of many sutures indicate that these specimens represent mature individuals. Key characteristics of the new inioid include maxillae that ‘squeeze’ the nasals into a slight hourglass shape and supraoccipital that is deeply wedged between the frontals and maxillae on the vertex. As compared to the extant iniid Inia geoffrensis (Amazon River dolphin) and the extant pontoporiid Pontoporia blainvillei (La Plata dolphin), Meherrinia is more plesiomorphic in having less elevated premaxillary eminences and supraorbital processes. In other respects Meherrinia is intermediate in morphology between the two extant genera of inioids. For example, the essentially symmetrical vertex is intermediate in height between the low and high vertices in Pontoporia blainvillei and Inia geoffrensis, respectively. A cladistic analysis of morphological and molecular data supports a sister-group relationship between Meherrinia and Inia; thus our new taxon is tentatively assigned to the Iniidae. If correct, this is the first iniid represented by diagnostic remains from marine deposits and just the second from North America.

The Origin of High-Frequency Hearing in Whales.

Odontocetes (toothed whales) rely upon echoes of their own vocalizations to navigate and find prey underwater [1]. This sensory adaptation, known as echolocation, operates most effectively when using high frequencies, and odontocetes are rivaled only by bats in their ability to perceive ultrasonic sound greater than 100 kHz [2]. Although features indicative of ultrasonic hearing are present in the oldest known odontocetes [3], the significance of this finding is limited by the methods employed and taxa sampled. In this report, we describe a new xenorophid whale (Echovenator sandersi, gen. et sp. nov.) from the Oligocene of South Carolina that, as a member of the most basal clade of odontocetes, sheds considerable light on the evolution of ultrasonic hearing. By placing high-resolution CT data from Echovenator sandersi, 2 hippos, and 23 fossil and extant whales in a phylogenetic context, we conclude that ultrasonic hearing, albeit in a less specialized form, evolved at the base of the odontocete radiation. Contrary to the hypothesis that odontocetes evolved from low-frequency specialists [4], we find evidence that stem cetaceans, the archaeocetes, were more sensitive to high-frequency sound than their terrestrial ancestors. This indicates that selection for high-frequency hearing predates the emergence of Odontoceti and the evolution of echolocation.

A New Basal Odontocete from the Upper Rupelian of South Carolina, U.S.A., with Contributions to the Systematics of Xenorophus and Mirocetus (Mammalia, Cetacea)

ABSTRACT We describe the odontocete, Ashleycetus planicapitis, gen. et sp. nov., based on a partial skull that was collected from the upper Rupelian (lower Oligocene) Ashley Formation near Charleston, South Carolina, and place it in the Ashleycetidae, fam. nov. Overall, the cranial morphology of this new species is plesiomorphic; it has an elongate, tabular intertemporal region, external nares well anterior to the antorbital notches, and anteromedially oriented lateral margins of the supraorbital processes. Xenorophus sloanii and Xenorophidae are rediagnosed, and the latter is also redefined as an apomorphy-based clade. This new definition should lead to greater stability because it excludes Archaeodelphis patrius, whose phylogenetic relationships have proven to be problematic. The holotype skull of the archaic odontocete Mirocetus riabinini, from probable upper Rupelian sediments of the lower Maikop beds of Azerbaijan, is redescribed, newly figured, and placed in the Mirocetidae, fam. nov. Previously regarded as an archaeocete, Mirocetus is here shown to be an odontocete. We added Ashleycetus, Albertocetus, and Mirocetus to a recently published supermatrix of morphological and molecular data. Although Ashleycetus, Archaeodelphis, and Mirocetus consistently occupy basal branch(es) within Odontoceti, their exact positions are sensitive to the value of a constant used in implied weighting for cladistics analysis. Three of the characters we find to be odontocete synapomorphies are closely associated with soft tissue structures implicated in the production and transmission of high-frequency sounds during echolocation. Detailed dissections of extant odontocetes are required to determine if these features can be considered evidence of echolocation in extinct taxa.

A toothless dwarf dolphin (Odontoceti: Xenorophidae) points to explosive feeding diversification of modern whales (Neoceti)

Toothed whales (Odontoceti) are adapted for catching prey underwater and possess some of the most derived feeding specializations of all mammals, including the loss of milk teeth (monophyodonty), high tooth count (polydonty), and the loss of discrete tooth classes (homodonty). Many extant odontocetes possess some combination of short, broad rostra, reduced tooth counts, fleshy lips, and enlarged hyoid bones—all adaptations for suction feeding upon fishes and squid. We report a new fossil odontocete from the Oligocene (approx. 30 Ma) of South Carolina (Inermorostrum xenops, gen. et sp. nov.) that possesses adaptations for suction feeding: toothlessness and a shortened rostrum (brevirostry). Enlarged foramina on the rostrum suggest the presence of enlarged lips or perhaps vibrissae. Phylogenetic analysis firmly places Inermorostrum within the Xenorophidae, an early diverging odontocete clade typified by long-snouted, heterodont dolphins. Inermorostrum is the earliest obligate suction feeder within the Odontoceti, a feeding mode that independently evolved several times within the clade. Analysis of macroevolutionary trends in rostral shape indicate stabilizing selection around an optimum rostral shape over the course of odontocete evolution, and a post-Eocene explosion in feeding morphology, heralding the diversity of feeding behaviour among modern Odontoceti.

New records of the dolphin Albertocetus meffordorum (Odontoceti: Xenorophidae) from the lower Oligocene of South Carolina: Encephalization, sensory anatomy, postcranial morphology, and ontogeny of early odontocetes

We report five new specimens of xenorophid dolphins from North and South Carolina. Four of the specimens represent the xenorophid Albertocetus meffordorum, previously only known from the holotype skull. The other is a fragmentary petrosal from the upper Oligocene Belgrade Formation that we refer to Echovenator sp, indicating at least two xenorophids from that unit. Two of the Albertocetus meffordorum specimens are from the lower Oligocene Ashley Formation: 1) a partial skeleton with neurocranium, fragmentary mandible, ribs, vertebrae, and chevrons, and 2) an isolated braincase. The partial vertebral column indicates that Albertocetus retained the ancestral morphology and locomotory capabilities of basilosaurid archaeocetes, toothed mysticetes, and physeteroids, and caudal vertebrae that are as wide as tall suggest that the caudal peduncle, which occurs in all extant Cetacea, was either wide or lacking. CT data from the isolated braincase were used to generate a digital endocast of the cranial cavity. The estimated EQ of this specimen is relatively high for an Oligocene odontocete, and other aspects of the brain, such as its anteroposterior length and relative size of the temporal lobe, are intermediate in morphology between those of extant cetaceans and terrestrial artiodactyls. Ethmoturbinals are also preserved, and are similar in morphology and number to those described for the Miocene odontocete Squalodon. These fossils extend the temporal range of Albertocetus meffordorum into the early Oligocene, its geographic range into South Carolina, and expand our paleobiological understanding of the Xenorophidae.

New records of the archaic dolphin Agorophius (Mammalia: Cetacea) from the upper Oligocene Chandler Bridge Formation of South Carolina, USA

The stem odontocete Agorophius pygmaeus (Ashley Formation, lower Oligocene, South Carolina; 29.0–26.57 Ma) has been a critical point of comparison for studies of early neocete evolution owing to its early discovery as well as its transitional anatomy relative to archaeocete whales and modern odontocetes. Some time during the late nineteenth century the holotype skull went missing and has never been relocated; supplementary reference specimens have since been recently referred to the species from the Ashley Formation and the overlying Chandler Bridge Formation (upper Oligocene; 24.7–23.5). New crania referable to Agorophius sp. are identifiable to the genus based on several features of the intertemporal region. Furthermore, all published specimens from the Chandler Bridge Formation consistently share larger absolute size and a proportionally shorter exposure of the parietal in the skull roof than specimens from the Ashley Formation (including the holotype). Furthermore, these specimens include well-preserved ethmoid labyrinths and cribriform plates, indicating that Agorophius primitively retained a strong olfactory sense. These new crania suggest that at least two species of Agorophius are present in the Oligocene of South Carolina, revealing a somewhat more complicated taxonomic perspective.

An Unexpectedly Derived Odontocete from the Ashley Formation (Upper Rupelian) of South Carolina, U.S.A.

ABSTRACT Fossil whale material from the Oligocene-aged marine beds underlying the region around Charleston, South Carolina, has provided an unparalleled view of post-archaeocete cetacean evolution. Both the Chattian-aged Chandler Bridge Formation and the underlying Rupelian-aged Ashley Formation have yielded dozens of specimens, many yet-to-be described, that document an explosive evolutionary radiation at this time, particularly in odontocetes, but in early mysticetes as well. Specimens include early odontocetes, such as Ashleycetus planicapitis, Xenorophus sloanii, and Agorophius pygmaeus; the earliest baleen-bearing mysticetes, such as Eomysticetus whitmorei and E. carolinensis; and even multiple species of archaeocete-like toothed mysticetes, such as the recently described Coronodon havensteini. Herein, we describe yet another species of odontocete from the Ashley Formation, but one that is surprisingly derived relative to contemporary species noted above that maintain a pronounced intertemporal constriction, with broad exposure of the parietals across the skull roof. In contrast to those taxa, Ediscetus osbornei, gen. et sp. nov., shows an unexpectedly advanced degree of ‘telescoping’ whereby there is no exposure of the parietals across the vertex of the skull and only minimally exposed ‘parietal triangles’ at the lateral margins of the nearly lost intertemporal constriction. Phylogenetic analyses of a supermatrix of morphological and molecular data place E. osbornei slightly outside the odontocete crown group, with the presence of double-rooted teeth and a deep maxillary cleft, among other features, supporting this position. The holotype also has a well-developed articular ridge on the petrosal, typically considered a platanistoid synapomorphy, indicating that this character shows more homoplasy than generally realized.