A new dolphin with tusk-like teeth from the late Oligocene of New Zealand indicates evolution of novel feeding strategies.

All extant toothed whales (Cetacea, Odontoceti) are aquatic mammals with homodont dentitions. Fossil evidence from the late Oligocene suggests a greater diversity of tooth forms among odontocetes, including heterodont species with a variety of tooth shapes and orientations. A new fossil dolphin from the late Oligocene of New Zealand, Nihohae matakoi gen. et sp. nov., consisting of a near complete skull, earbones, dentition and some postcranial material, represents this diverse dentition. Several preserved teeth are horizontally procumbent, including all incisors and canines. These tusk-like teeth suggest adaptive advantages for horizontally procumbent teeth in basal dolphins. Phylogenetic analysis places Nihohae among the poorly constrained basal waipatiid group, many with similarly procumbent teeth. Features of N. matakoi such as its dorsoventrally flattened and long rostrum, long mandibular symphysis, unfused cervical vertebrae, lack of attritional or occlusal wear on the teeth and thin enamel cover suggest the rostrum and horizontally procumbent teeth were used to injure and stun prey though swift lateral head movements, a feeding mode that did not persist in extant odontocetes.

Speciation in the deep: genomics and morphology reveal a new species of beaked whale Mesoplodon eueu.

The deep sea has been described as the last major ecological frontier, as much of its biodiversity is yet to be discovered and described. Beaked whales (ziphiids) are among the most visible inhabitants of the deep sea, due to their large size and worldwide distribution, and their taxonomic diversity and much about their natural history remain poorly understood. We combine genomic and morphometric analyses to reveal a new Southern Hemisphere ziphiid species, Ramari's beaked whale, Mesoplodon eueu, whose name is linked to the Indigenous peoples of the lands from which the species holotype and paratypes were recovered. Mitogenome and ddRAD-derived phylogenies demonstrate reciprocally monophyletic divergence between M. eueu and True's beaked whale (M. mirus) from the North Atlantic, with which it was previously subsumed. Morphometric analyses of skulls also distinguish the two species. A time-calibrated mitogenome phylogeny and analysis of two nuclear genomes indicate divergence began circa 2 million years ago (Ma), with geneflow ceasing 0.35-0.55 Ma. This is an example of how deep sea biodiversity can be unravelled through increasing international collaboration and genome sequencing of archival specimens. Our consultation and involvement with Indigenous peoples offers a model for broadening the cultural scope of the scientific naming process.

Extensively remodeled, fractured cetacean tympanic bullae show that whales can survive traumatic injury to the ears.

Underwater human activities and anthropogenic noise in our oceans may be a major source of habitat degradation for marine life. This issue was highlighted by the opening of the United States Eastern Seaboard for seismic oil and gas exploration in 2014, which generated massive media coverage and widespread concern that seismic surveys could kill or deafen whales. We discovered 11 new specimens of fractured and healed cetacean ear bones, out of a survey of 2127 specimens housed in museum collections. This rare condition has been previously reported only in two specimens of blue whales (Balaenoptera musculus) from the early 1900s, summarized by Fraser & Purves (1953). All of our new specimens are represented by species for which this condition had never been reported previously, including both baleen and toothed whales. The baleen whale specimens (Balaenoptera physalus, Balaenoptera borealis, Balaenoptera acutorostrata) were collected during Canadian commercial whaling operations in the Atlantic Ocean in the 1970s; the specimens include ear bones with well-healed fractures, demonstrating that baleen whales are capable of overcoming traumatic injury to the ears. The toothed whale specimens (Delphinus sp., Berardius bairdii) were found dead on beaches in 1972 and 2001, respectively, with less remodeled fractures. Thus, ear injuries may be more lethal to the echolocating toothed whales, which rely on hearing for navigation and foraging. We explore several hypotheses regarding how these injuries could have occurred, and conclude that the most parsimonious explanations appear to be both direct and indirect effects of lytic processes from disease or calcium depletion, or damage from external pressure waves. Although further research is required to confirm whether the fractures resulted from natural or human-induced events, this study underscores the importance of museum collections and the work of stranding networks in understanding the potential effects of modern human activities on marine mammal health.

Anatomy of nasal complex in the southern right whale, Eubalaena australis (Cetacea, Mysticeti).

The nasal region of the skull has undergone dramatic changes during the course of cetacean evolution. In particular, mysticetes (baleen whales) conserve the nasal mammalian pattern associated with the secondary function of olfaction, and lack the sound-producing specializations present in odontocetes (toothed whales, dolphins and porpoises). To improve our understanding of the morphology of the nasal region of mysticetes, we investigate the nasal anatomy, osteology and myology of the southern right whale, Eubalaena australis, and make comparisons with other mysticetes. In E. australis external deflection surfaces around the blowholes appear to divert water off the head, and differ in appearance from those observed in balaenopterids, eschrichtiids and cetotherids. In E. australis the blowholes are placed above hypertrophied nasal soft tissues formed by fat and nasal muscles, a pattern also observed in balaenopterids (rorqual mysticetes) and a cetotherid (pygmy right whale, Caperea marginata). Blowhole movements are due to the action of five nasofacial muscles: dilator naris superficialis, dilator naris profundus, depressor alae nasi, constrictor naris, and retractor alae nasi. The dilator naris profundus found in E. australis has not been previously reported in balaenopterids. The other nasofacial muscles have a similar arrangement in balaenopterids, with minor differences. A novel structure, not reported previously in any mysticete, is the presence of a vascular tissue (rete mirabile) covering the lower nasal passage. This vascular tissue could play a role in warming inspired air, or may engorge to accommodate loss of respiratory space volume due to gas compression from increased pressure during diving.

Ancestor-descendant relationships in evolution: origin of the extant pygmy right whale, Caperea marginata.

Ancestor-descendant relationships (ADRs), involving descent with modification, are the fundamental concept in evolution, but are usually difficult to recognize. We examined the cladistic relationship between the only reported fossil pygmy right whale, †Miocaperea pulchra, and its sole living relative, the enigmatic pygmy right whale Caperea marginata, the latter represented by both adult and juvenile specimens. †Miocaperea is phylogenetically bracketed between juvenile and adult Caperea marginata in morphologically based analyses, thus suggesting a possible ADR-the first so far identified within baleen whales (Cetacea: Mysticeti). The †Miocaperea-Caperea lineage may show long-term morphological stasis and, in turn, punctuated equilibrium.

Elemental and chemical characterization of dolphin enamel and dentine using X-ray and Raman microanalyzes (Cetacea: Delphinoidea and Inioidea).

Dolphins show increased tooth number and simplified tooth shape compared to most mammals, together with a simpler ultrastructural organization and less demanding biomechanical function. However, it is unknown if these factors are also reflected in the chemical composition of their teeth. Here, the bulk chemical composition and elemental distribution in enamel and dentine of extant dolphins were characterized and interpreted using X-ray and spectroscopy techniques. Teeth of 10 species of Delphinida were analyzed by WDX, EDX and Raman spectroscopy. For most of the species sampled, the mineral content was higher in enamel than in dentine, increasing from inner towards outer enamel. The transition from dentine to enamel was marked by an increase in concentration of the major components Ca and P, but also in Na and Cl. Mg decreased from dentine to enamel. Concentrations of Sr and F were often low and below detection limits, but F peaked at the outer enamel region for some species. Raman spectroscopy analyzes showed characteristics similar to carbonated hydroxyapatite, with the strongest peak for the phosphate PO4(3-) stretching mode at 960-961cm(-1). Dentine samples revealed a higher diversity of peaks representative of organic components and proteins than enamel. The similar distribution pattern and small variation in average concentration of major and minor elements in dentine and enamel of dolphins suggest that they are subject to strong physiological control. A clear trend of the elemental variations for all dolphin species sampled suggests that the general pattern of tooth chemistry is conserved among the Mammalia.

Juvenile morphology in baleen whale phylogeny.

Phylogenetic reconstructions are sensitive to the influence of ontogeny on morphology. Here, we use foetal/neonatal specimens of known species of living baleen whales (Cetacea: Mysticeti) to show how juvenile morphology of extant species affects phylogenetic placement of the species. In one clade (sei whale, Balaenopteridae), the juvenile is distant from the usual phylogenetic position of adults, but in the other clade (pygmy right whale, Cetotheriidae), the juvenile is close to the adult. Different heterochronic processes at work in the studied species have different influences on juvenile morphology and on phylogenetic placement. This study helps to understand the relationship between evolutionary processes and phylogenetic patterns in baleen whale evolution and, more in general, between phylogeny and ontogeny; likewise, this study provides a proxy how to interpret the phylogeny when fossils that are immature individuals are included. Juvenile individuals in the peramorphic acceleration clades would produce misleading phylogenies, whereas juvenile individuals in the paedomorphic neoteny clades should still provide reliable phylogenetic signals.

The pygmy right whale Caperea marginata: the last of the cetotheres.

The pygmy right whale, Caperea marginata, is the most enigmatic of the living baleen whales (Mysticeti). Its highly disparate morphology and the virtual absence of a described fossil record have made it extremely difficult to place Caperea into a broader evolutionary context, and molecular and morphological studies have frequently contradicted each other as to the origins and phylogenetic relationships of the species. Our study of a wealth of material from New Zealand collections, representing a wide range of ontogenetic stages, has identified several new features previously unreported in Caperea, which suggest that the pygmy right whale may be the last survivor of the supposedly extinct family Cetotheriidae. This hypothesis is corroborated by both morphology-based and total evidence cladistic analyses, including 166 morphological characters and 23 taxa, representing all the living and extinct families of toothless baleen whales. Our results allow us to formally refer Caperea to Cetotheriidae, thus resurrecting the latter from extinction and helping to clarify the origins of a long-problematic living species.

Juvenile morphology: a clue to the origins of the most mysterious of mysticetes?

The origin of the pygmy right whale (Caperea marginata) has long been one of the most vexing conundrums of marine mammal evolution. The extremely disparate skeletal structure of Caperea and a patchy fossil record have left morphology and molecules at odds: whereas most morphological analyses ally Caperea with right whales (Balaenidae), most molecular studies instead suggest a close relationship with rorquals (Balaenopteridae) and grey whales (Eschrichtiidae). The morphological evidence supporting a Caperea-balaenid clade consists of several shared features of the skull and mandible, as traditionally observed in adult individuals. Here, we show that at least two of these features, the ascending process of the maxilla and the coronoid process, arise from substantially different precursors early during ontogeny and therefore likely do not represent genuine synapomorphies. Both of these juvenile morphologies have adult counterparts in the fossil record, thus indicating that the ontogenetic variation in the living species may be a genuine reflection of differing ancestral states. This new evidence contradicts previous morphological hypotheses on the origins of Caperea and may help to reconcile morphological and molecular evidence.

The better to eat you with: morphological disparity and enamel ultrastructure in odontocetes.

Variations in the shape and size of teeth have been associated with changes in enamel ultrastructure across odontocetes. Characterizing these features in extinct taxa can elucidate their functional morphology and feeding strategy, while also shedding light into macroevolutionary patterns during the evolutionary history of cetaceans. This study aimed to (1) describe the enamel and dentine ultrastructure of the Early Miocene odontocetes Notocetus vanbenedeni and Phoberodon arctirostris from Patagonia (Argentina) and (2) quantify tooth and enamel ultrastructure morphological disparity among odontocetes. Enamel was predominantly prismatic, thin in the anterior tooth of N. vanbenedeni and P. arctirostris; whilst thick on the posterior tooth of N. vanbenedeni. Together with skull morphology, data suggests a raptorial feeding strategy for P. arctirostris and a combination suction feeding method for N. vanbenedeni. Statistical analyses supported these inferences, indicating that enamel characters are useful for paleoecological research. Morphological disparity analyses showed that extant odontocetes occupy a larger morphospace and have more disparate morphologies, whilst extinct odontocetes were more similar among each other than with the extant group. There was no clear phylogenetic-based grouping, suggesting that tooth and enamel ultrastructure disparity were mainly driven by ecological pressures. These results highlight enamel ultrastructure as a source for broader-scale paleoecological studies in cetaceans.

Penguin heat-retention structures evolved in a greenhouse Earth.

Penguins (Sphenisciformes) inhabit some of the most extreme environments on Earth. The 60+ Myr fossil record of penguins spans an interval that witnessed dramatic shifts in Cenozoic ocean temperatures and currents, indicating a long interplay between penguin evolution and environmental change. Perhaps the most celebrated example is the successful Late Cenozoic invasion of glacial environments by crown clade penguins. A major adaptation that allows penguins to forage in cold water is the humeral arterial plexus, a vascular counter-current heat exchanger (CCHE) that limits heat loss through the flipper. Fossil evidence reveals that the humeral plexus arose at least 49 Ma during a 'Greenhouse Earth' interval. The evolution of the CCHE is therefore unrelated to global cooling or development of polar ice sheets, but probably represents an adaptation to foraging in subsurface waters at temperate latitudes. As global climate cooled, the CCHE was key to invasion of thermally more demanding environments associated with Antarctic ice sheets.

Radiation of extant cetaceans driven by restructuring of the oceans.

The remarkable fossil record of whales and dolphins (Cetacea) has made them an exemplar of macroevolution. Although their overall adaptive transition from terrestrial to fully aquatic organisms is well known, this is not true for the radiation of modern whales. Here, we explore the diversification of extant cetaceans by constructing a robust molecular phylogeny that includes 87 of 89 extant species. The phylogeny and divergence times are derived from nuclear and mitochondrial markers, calibrated with fossils. We find that the toothed whales are monophyletic, suggesting that echolocation evolved only once early in that lineage some 36-34 Ma. The rorqual family (Balaenopteridae) is restored with the exclusion of the gray whale, suggesting that gulp feeding evolved 18-16 Ma. Delphinida, comprising all living dolphins and porpoises other than the Ganges/Indus dolphins, originated about 26 Ma; it contains the taxonomically rich delphinids, which began diversifying less than 11 Ma. We tested 2 hypothesized drivers of the extant cetacean radiation by assessing the tempo of lineage accumulation through time. We find no support for a rapid burst of speciation early in the history of extant whales, contrasting with expectations of an adaptive radiation model. However, we do find support for increased diversification rates during periods of pronounced physical restructuring of the oceans. The results imply that paleogeographic and paleoceanographic changes, such as closure of major seaways, have influenced the dynamics of radiation in extant cetaceans.

A new archaic baleen whale Toipahautea waitaki (early Late Oligocene, New Zealand) and the origins of crown Mysticeti.

A new genus and species of extinct baleen whale †Toipahautea waitaki (Late Oligocene, New Zealand) is based on a skull and associated bones, from the lower Kokoamu Greensand, about 27.5 Ma (local upper Whaingaroan Stage, early Chattian). The upper jaw includes a thin, elongate and apparently toothless maxilla, with evidence of arterial supply for baleen. Open sutures with the premaxilla suggest a flexible (kinetic) upper jaw. The blowhole is well forward. The mandible is bowed laterally and slightly dorsally; unlike the Eomysticetidae, there are no mandibular alveoli, and the coronoid process is tapered and curved laterally. Jaw structure is consistent with baleen-assisted gulp-feeding. The age of early Chattian makes †Toipahautea a very early, if not the oldest named, toothless and baleen-bearing mysticete, suggesting that the full transition from toothed to baleen-bearing probably occurred in the Early Oligocene. Late Oligocene mysticetes vary considerably in jaw form and kinesis, tooth form and function, and development of baleen, implying a wide range of raptorial, suctorial and filter-feeding behaviour. More study may elucidate the function of jaws, teeth and baleen in terms of opportunist/generalist feeding, as in modern gray whales, versus specialized feeding. We here propose that early mysticetes, when transitioned from toothed to baleen-bearing, were generalists and opportunists instead of specializing in any forms of feeding strategies. In addition, two different phylogenetic analyses placed †Toipahautea either in a polytomy including crown Mysticeti, or immediately basal to the crown, and above †Eomysticetidae in both cases. Because the †Toipahautea waitaki holotype is an immature individual, it may plot more basally in phylogeny than its true position.

Gigantism Precedes Filter Feeding in Baleen Whale Evolution.

Baleen whales (Mysticeti) are the largest animals on Earth, thanks to their ability to filter huge volumes of small prey from seawater. Mysticetes appeared during the Late Eocene, but evidence of their early evolution remains both sparse and controversial [1, 2], with several models competing to explain the origin of baleen-based bulk feeding [3-6]. Here, we describe a virtually complete skull of Llanocetus denticrenatus, the second-oldest (ca. 34 Ma) mysticete known. The new material represents the same individual as the type and only specimen, a fragmentary mandible. Phylogenetic analysis groups Llanocetus with the oldest mysticete, Mystacodon selenensis [2], into the basal family Llanocetidae. Llanocetus is gigantic (body length ∼8 m) compared to other early mysticetes [7-9]. The broad rostrum has sharp, widely spaced teeth with marked dental abrasion and attrition, suggesting biting and occlusal shearing. As in extant mysticetes, the palate bears many sulci, commonly interpreted as osteological correlates of baleen [3]. Unexpectedly, these sulci converge on the upper alveoli, suggesting a peri-dental blood supply to well-developed gums, rather than to inter-alveolar racks of baleen. We interpret Llanocetus as a raptorial or suction feeder, revealing that whales evolved gigantism well before the emergence of filter feeding. Rather than driving the origin of mysticetes, baleen and filtering most likely only arose after an initial phase of suction-assisted raptorial feeding [2, 4, 5]. This scenario differs strikingly from that proposed for odontocetes, whose defining adaptation-echolocation-was present even in their earliest representatives [10].

A new tropical Oligocene dolphin from Montañita/Olón, Santa Elena, Ecuador.

A new small probable Oligocene dolphin from Ecuador represents a new genus and species, Urkudelphis chawpipacha. The new taxon is known from a single juvenile skull and earbones; it differs from other archaic dolphins in features including widely exposed frontals at the vertex, a dorsally wide open vomer at the mesorostral groove, and a strongly projected and pointed lateral tuberosity of the periotic. Phylogenetic analysis places it toward the base of the largely-extinct clade Platanistoidea. The fossil is one of a few records of tropical fossil dolphins.

A Link No Longer Missing: New Evidence for the Cetotheriid Affinities of Caperea.

The origins of the enigmatic pygmy right whale Caperea marginata, the only living member of its subfamily (Neobalaeninae), are an outstanding mystery of cetacean evolution. Its strikingly disparate morphology sets Caperea apart from all other whales, and has turned it into a wildcard taxon that holds the key to understanding modern baleen whale diversity. Morphological cladistics generally ally this species with right whales, whereas molecular analyses consistently cluster it with rorquals and grey whales (Balaenopteroidea). A recent study potentially resolved this conflict by proposing that Caperea belongs with the otherwise extinct Cetotheriidae, but has been strongly criticised on morphological grounds. Evidence from the neobalaenine fossil record could potentially give direct insights into morphological transitions, but is currently limited to just a single species: the Late Miocene Miocaperea pulchra, from Peru. We show that Miocaperea has a highly unusual morphology of the auditory region, resulting from a-presumably feeding-related-strengthening of the articulation of the hyoid apparatus with the skull. This distinctive arrangement is otherwise only found in the extinct Cetotheriidae, which makes Miocaperea a "missing link" that demonstrates the origin of pygmy right whales from cetotheriids, and confirms the latter's resurrection from the dead.

Anatomy, feeding ecology, and ontogeny of a transitional baleen whale: a new genus and species of Eomysticetidae (Mammalia: Cetacea) from the Oligocene of New Zealand.

The Eocene history of cetacean evolution is now represented by the expansive fossil record of archaeocetes elucidating major morphofunctional shifts relating to the land to sea transition, but the change from archaeocetes to modern cetaceans is poorly established. New fossil material of the recently recognized family Eomysticetidae from the upper Oligocene Otekaike Limestone includes a new genus and species, Waharoa ruwhenua, represented by skulls and partial skeletons of an adult, juvenile, and a smaller juvenile. Ontogenetic status is confirmed by osteohistology of ribs. Waharoa ruwhenua is characterized by an elongate and narrow rostrum which retains vestigial alveoli and alveolar grooves. Palatal foramina and sulci are present only on the posterior half of the palate. The nasals are elongate, and the bony nares are positioned far anteriorly. Enormous temporal fossae are present adjacent to an elongate and narrow intertemporal region with a sharp sagittal crest. The earbones are characterized by retaining inner and outer posterior pedicles, lacking fused posterior processes, and retaining a separate accessory ossicle. Phylogenetic analysis supports inclusion of Waharoa ruwhenua within a monophyletic Eomysticetidae as the earliest diverging clade of toothless mysticetes. This eomysticetid clade also included Eomysticetus whitmorei, Micromysticetus rothauseni, Tohoraata raekohao, Tokarahia kauaeroa, Tokarahia lophocephalus, and Yamatocetus canaliculatus. Detailed study of ontogenetic change demonstrates postnatal elaboration of the sagittal and nuchal crests, elongation of the intertemporal region, inflation of the zygomatic processes, and an extreme proportional increase in rostral length. Tympanic bullae are nearly full sized during early postnatal ontogeny indicating precocial development of auditory structures, but do increase slightly in size. Positive allometry of the rostrum suggests an ontogenetic change in feeding ecology, from neonatal suckling to a more specialized adult feeding behaviour. Possible absence of baleen anteriorly, a delicate temporomandibular joint with probable synovial capsule, non-laterally deflected coronoid process, and anteroposteriorly expanded palate suggests skim feeding as likely mode of adult feeding for zooplankton. Isotopic data in concert with preservation of young juveniles suggests the continental shelf of Zealandia was an important calving ground for latitudinally migrating Oligocene baleen whales.

Baleen boom and bust: a synthesis of mysticete phylogeny, diversity and disparity.

A new, fully dated total-evidence phylogeny of baleen whales (Mysticeti) shows that evolutionary phases correlate strongly with Caenozoic modernization of the oceans and climates, implying a major role for bottom-up physical drivers. The phylogeny of 90 modern and dated fossil species suggests three major phases in baleen whale history: an early adaptive radiation (36-30 Ma), a shift towards bulk filter-feeding (30-23 Ma) and a climate-driven diversity loss around 3 Ma. Evolutionary rates and disparity were high following the origin of mysticetes around 38 Ma, coincident with global cooling, abrupt Southern Ocean eutrophication and the development of the Antarctic Circumpolar Current (ACC). Subsequently, evolutionary rates and disparity fell, becoming nearly constant after approximately 23 Ma as the ACC reached its full strength. By contrast, species diversity rose until 15 Ma and then remained stable, before dropping sharply with the onset of Northern Hemisphere glaciation. This decline coincided with the final establishment of modern mysticete gigantism and may be linked to glacially driven variability in the distribution of shallow habitats or an increased need for long-distance migration related to iron-mediated changes in glacial marine productivity.