A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales

Extant baleen whales (Cetacea, Mysticeti) are all large filter-feeding marine mammals that lack teeth as adults, instead possessing baleen, and feed on small marine animals in bulk. The early evolution of these superlative mammals, and their unique feeding method, has hitherto remained enigmatic. Here, I report a new toothed mysticete from the Late Oligocene of Australia that is more archaic than any previously described. Unlike all other mysticetes, this new whale was small, had enormous eyes and lacked derived adaptations for bulk filter-feeding. Several morphological features suggest that this mysticete was a macrophagous predator, being convergent on some Mesozoic marine reptiles and the extant leopard seal (Hydrurga leptonyx). It thus refutes the notions that all stem mysticetes were filter-feeders, and that the origins and initial radiation of mysticetes was linked to the evolution of filter-feeding. Mysticetes evidently radiated into a variety of disparate forms and feeding ecologies before the evolution of baleen or filter-feeding. The phylogenetic context of the new whale indicates that basal mysticetes were macrophagous predators that did not employ filter-feeding or echolocation, and that the evolution of characters associated with bulk filter-feeding was gradual.     

Morphological specializations of baleen whales associated with hydrodynamic performance and ecological niche

Feeding behavior, prey type, and habitat appear to be associated with the morphological design of body, fluke, and flippers in baleen whales. Morphometric data from whaling records and recent stranding events were compiled, and morphometric parameters describing the body length, and fluke and flipper dimensions for an "average" blue whale Balaenoptera musculus, humpback whale Megaptera novaeangliae, gray whale Eschrichtius robustus, and right whale Eubalaena glacialis were determined. Body mass, body volume, body surface area, and fluke and flipper surface areas were estimated. The resultant morphological configurations lent themselves to the following classifications based on hydrodynamic principles: fast cruiser, slow cruiser, fast maneuverer, and slow maneuverer. Blue whales have highly streamlined bodies with small, high aspect ratio flippers and flukes for fast efficient cruising in the open ocean. On the other hand, the rotund right whale has large, high aspect ratio flukes for efficient slow speed cruising that is optimal for their continuous filter feeding technique. Humpbacks have large, high aspect ratio flippers and a large, low aspect ratio tail for quick acceleration and high-speed maneuvering which would help them catch their elusive prey, while gray whales have large, low aspect ratio flippers and flukes for enhanced low-speed maneuvering in complex coastal water habitats.     

Selection-delayed population dynamics in baleen whales and beyond

While it is known that population cycles are driven by delayed density-dependent feedbacks, the search for a common feedback mechanism in natural populations with cyclic dynamics has remained unresolved for almost a century. To identify the existence and cause of delayed feedbacks I apply six age- and sex-structured population dynamics models to seven species of baleen whales (suborder Mysticeti) that were heavily depleted by past commercial whaling. The six models include a predator–prey model with killer whale (Orcinus orca) as the predator, and five singe-species models based on (1) exponential growth, (2) density-regulated growth, (3) density-regulated growth with depensation, (4) delayed density-regulated growth and (5) selection-delayed dynamics. The latter model has a density-regulated growth rate that is accelerated and decelerated by the intra-specific natural selection that arises from the density-dependent competitive interactions between the individuals in the population. Essential parameters are estimated by a Bayesian statistical framework, and it is shown that baleen whales have a delayed recovery relative to density-regulated growth. The time-lag is not explained by depensation, or by interactions with prey or predators. It is instead resolved by a selection-delayed acceleration of the intrinsic growth rate. The results are discussed in relation to the literature on cyclic dynamics, and it is noted (1) that selection-delayed dynamics is both theoretically and empirically sufficient for cyclic population dynamics, (2) that it is widespread in natural populations owing to the widespread occurrence of otherwise unexplained phenotypic cycles in populations with cyclic dynamics, and (3) that there is a lack of empirical evidence showing that predator–prey interactions is a sufficient cause for the cyclic dynamics of natural populations. The conclusion stresses the importance of intra-specific delays in cyclic dynamics, and suggests that it is the acceleration of the growth rate, and not the growth rate itself, that is determined by the density-dependent environment.     

A new baleen whale from the Late Miocene of Denmark and early mysticete hearing

Abstract:  The extinct mysticete fauna of the North East Atlantic is primarily known from the abundant but fragmented Belgian specimens. Compared to the well-preserved contemporary mysticete fauna from deposits in North America, there are only few near complete European Miocene mysticete fossils. Presented here is a new, almost complete fossil baleen whale Uranocetus gramensis gen. et sp. nov. from the Upper Miocene Gram Formation in South West Denmark. It is the first stem-balaenopterid that has an initial stage of reduction in the mandibular cavity and a rostral configuration that is intermediate between that of other stem-balaenopterids and true balaenopterids. It is likely that Uranocetus used a gulp feeding technique that approaches that of balaenopterids. Details of the periotic and mandibular morphology place Uranocetus in the family Diorocetidae Steeman 2007. The large mandibular cavity in Uranocetus and most other extinct mysticetes, when compared to the reduced condition in recent mysticetes, is not an indication that early mysticetes used odontocete-like echolocation. In Uranocetus and a distantly related mysticete, high frequency sounds in the range odontocetes use for echolocation would suffer a significant volume loss across the lateral mandibular wall on the passage towards the inner ear. A reduction in the mandibular cavity in separate evolutionary lineages of mysticetes may be the result of a shift towards the use of low frequency sounds.     

Morphological variation among the inner ears of extinct and extant baleen whales (Cetacea: Mysticeti)

Living mysticetes (baleen whales) and odontocetes (toothed whales) differ significantly in auditory function in that toothed whales are sensitive to high‐frequency and ultrasonic sound vibrations and mysticetes to low‐frequency and infrasonic noises. Our knowledge of the evolution and phylogeny of cetaceans, and mysticetes in particular, is at a point at which we can explore morphological and physiological changes within the baleen whale inner ear. Traditional comparative anatomy and landmark‐based 3D‐geometric morphometric analyses were performed to investigate the anatomical diversity of the inner ears of extinct and extant mysticetes in comparison with other cetaceans. Principal component analyses (PCAs) show that the cochlear morphospace of odontocetes is tangential to that of mysticetes, but odontocetes are completely separated from mysticetes when semicircular canal landmarks are combined with the cochlear data. The cochlea of the archaeocete Zygorhiza kochii and early diverging extinct mysticetes plot within the morphospace of crown mysticetes, suggesting that mysticetes possess ancestral cochlear morphology and physiology. The PCA results indicate variation among mysticete species, although no major patterns are recovered to suggest separate hearing or locomotor regimes. Phylogenetic signal was detected for several clades, including crown Cetacea and crown Mysticeti, with the most clades expressing phylogenetic signal in the semicircular canal dataset. Brownian motion could not be excluded as an explanation for the signal, except for analyses combining cochlea and semicircular canal datasets for Balaenopteridae. J. Morphol. 277:1599–1615, 2016. © 2016 Wiley Periodicals, Inc.     

Molecular cloning of urea transporters from the kidneys of baleen and toothed whales

Urea transport in the kidney is important for the production of concentrated urine. This process is mediated by urea transporters (UTs) encoded by two genes, UT-A (Slc14a2) and UT-B (Slc14a1). Our previous study demonstrated that cetaceans produce highly concentrated urine than terrestrial mammals, and that baleen whales showed higher concentrations of urinary urea than sperm whales. Therefore, we hypothesized that cetaceans have unique actions of UTs to maintain fluid homeostasis in marine habitat. Kidney samples of common minke (Balaenoptera acutorostrata), sei (B. borealis), Bryde's (B. brydei) and sperm whales (Physeter macrocephalus) were obtained to determine the nucleotide sequences of mRNAs encoding UT. The sequences of 2.5-kb cDNAs encode 397-amino acid proteins, which are 90-94% identical to the mammalian UT-A2s. Two putative glycosylation sites are conserved between the whales and the terrestrial mammals, whereas consensus sites for protein kinases are not completely conserved; only a single protein kinase A consensus site was identified in the whale UT-A2s. Two protein kinase C consensus sites are present in the baleen whale UT-A2s, however, a single protein kinase C consensus site was identified in the sperm whale UT-A2. These different phosphorylation sites of whale UT-A2s may result in the high concentrations of urinary urea in whales, by reflecting their urea permeability.     

Estimating morphometric attributes of baleen whales with photogrammetry from small UASs: A case study with blue and gray whales

Small unmanned aircraft systems (sUASs) are fostering novel approaches to marine mammal research, including baleen whale photogrammetry, by providing new observational perspectives. We collected vertical images of 89 gray and 6 blue whales using low cost sUASs to examine the accuracy of image based morphometry. Moreover, measurements from 192 images of a 1 m calibration object were used to examine four different scaling correction models. Results indicate that a linear mixed model including an error term for flight and date contained 0.17 m less error and 0.25 m less bias than no correction. We used the propagation uncertainty law to examine error contributions from scaling and image measurement (digitization) to determine that digitization accounted for 97% of total variance. Additionally, we present a new whale body size metric termed Body Area Index (BAI). BAI is scale invariant and is independent of body length (R² = 0.11), enabling comparisons of body size within and among populations, and over time. With this study we present a three program analysis suite that measures baleen whales and compensates for lens distortion and corrects scaling error to produce 11 morphometric attributes from sUAS imagery. The program is freely available and is expected to improve processing efficiency and analytical continuity.     

Age estimation in bowhead whales using tympanic bulla histology and baleen isotopes

Tympanic bullae and baleen plates from bowhead whales of the Western Arctic population were examined. Growth layer groups (GLGs) in the involucrum of the tympanic bone were used to estimate age of the whales, and compared to stable isotope signatures along transects of baleen plates and the involucrum. The involucrum of the tympanic bone consists of three regions that form in utero, during nursing in the first year, and during the first decades of life, respectively. Life history events, such as annual migration, are recorded in the bowhead tympanic bulla. It is likely that bone growth in the bowhead tympanic occurs during periods of high food intake, while slow or arrested growth occurs during periods of low food intake. Comparisons between numbers of GLGs in the tympanic, number of isotopic oscillations in a baleen plate, length of the baleen plate, and total whale length show correlation coefficients as high as 0.97. The tympanic GLG method is particularly useful for estimating the age of whales up to 20 yr old.     

Analysis of the C4 genes in baleen whales using a human cDNA probe

We have used a human C4 cDNA probe to investigate the complement component C4 gene in four members of the family Balaenopteridae: fin whale (Balaenoptera physalus), sei whale (B. borealis), minke whale (B. acutorostrata), and bryde's whale (B. edeni). Restriction mapping of genomic DNA from the first three species suggests the presence of only one locus in these species, and also shows that the C4 genes in the three species are very similar. We have used 14 restriction endonucleases to investigate the restriction fragment length polymorphism (RFLP) of fin whales, 13 enzymes for sei whales, and 8 enzymes for the minke whale. No polymorphism was seen in DNA from the five minke whale samples, but Rsa I and Taq I restriction enzymes gave polymorphism in fin and sei whales whereas Hind III and Msp I restriction enzymes showed polymorphism in sei whales only. Only one bryde's whale sample was available for investigation. The study of DNA available from mother-fetus pairs from the two polymorphic species demonstrated a simple, two-allele transmission of RFLP alleles.     

Feeding ecology of gray whales inferred from stable-carbon and nitrogen isotopic analysis of baleen plates

Stable-carbon and nitrogen isotopic compositions (δ¹³C, δ¹⁵N) of baleen plates of two juvenile and four adult gray whales (Eschrichtius robustus) were examined. High variance in isotopic composition of baleen plates was detected among individuals and, unlike other migratory species of baleen whales examined isotopically, δ¹³C and δ¹⁵N values of most whales showed no regular oscillations. Only one baleen plate reflected the assumed principal Arctic prey (ampeliscid amphipods) during growth on the summer grounds. The rate of baleen growth inferred for one of the juveniles in the last 5 months of life (4.7 mm/week) was similar to the rate calculated previously for a rehabilitating gray whale calf. Autumn corresponded to the timing of the formation of lowest δ¹⁵N values measured along plates. We estimate that the baleen length in all adult gray whales recorded around a year of information (1.3 ± 0.3; Mean ± SD). This short period of dietary integration precludes long time series analyses in this species and reflects the extensive wear on baleen plates due to benthic foraging. Handling editor: M. Power     

Morphological and molecular evidence for a new species of Rhodotus from tropical and subtropical Yunnan,China

Rhodotus has been regarded as a monotypic genus, consisting of only one species, R. palmatus, for a long time. Morphological and phylogenetic studies were carried out on collections of Rhodotus from temperate, subtropical and tropical China. Our phylogenetic analysis of DNA sequences of three loci (the internal transcribed spacer, the large subunit nuclear ribosomal RNA, and the translation elongation factor-1 alpha) revealed that there are two phylogenetic species in the northern hemisphere, which is in concordance with morphological traits, supporting the division of Rhodotus into two distinct species. Rhodotus asperior is described as a new species that differs phenotypically from R. palmatus in its broadly ellipsoid to subglobose, more roughened basidiospores, longer cheilocystidia with slightly thickened wall, and its occurrence in tropical and subtropical environments. The discovery of this new taxon indicates Rhodotus has a wider distribution than previously thought.     

Morphological and thermal properties of mammalian insulation: the evolutionary transition to blubber in pinnipeds

Carnivora includes three independent evolutionary transitions to the marine environment: pinnipeds (seals, sea lions, and walruses), sea otters, and polar bears. Among these, only the pinnipeds have retained two forms of insulation, an external fur layer and an internal blubber layer for keeping warm in water. In this study we investigated key factors associated with the transition to the use of blubber, by comparing blubber characteristics among the pinnipeds. Characteristics included gross morphology (blubber thickness), fat composition (fatty acid profiles, percentage lipid, and water), and thermal conductivity. Sea lions, phocids, and walrus, which have lower fur densities than fur seals, have thicker blubber layers than fur seals (P < 0.001). Comparisons of lipid content, water content, and fatty acid composition indicated significant differences in the composition of the inner and outer regions of the blubber between groups (P < 0.001), consistent with the hypothesis that phocids and sea lions utilize the outer layer of their blubber primarily for thermal insulation, and the inner layer for energy storage. Fur seals, by contrast, rely more on their fur for thermal insulation, and utilize their blubber layer primarily for energy storage. Comparing across carnivore species, differences in total insulation (fur and/or blubber) are influenced substantially by body size and habitat, and to a lesser extent by latitudinal climate. Overall, these results indicate consistent evolutionary trends in the transition to blubber and evidence for convergent evolution of thermal traits across lineages. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

Odontobius (Nematoda, Monhysteridae) from the baleen plates of whales and its relationship to Gammarinema living on crustaceans

Based on new material, the poorly known nematode species Odontobius ceti Roussel de Vauzème, 1834 is redescribed. It lives on the baleen plates of the baleen whales. It is argued that it belongs to the Monhysteridae sensu Lorenzen. Within this family, Odontobius appears to be most closely related to Gammarinema, species of which live externally on peracarid and decapod crustaceans. It is suggested that Odontobius ceti or its ancestor lived externally on crustaceans which were (or still are?) of nutritional importance to baleen whales and that in the course of feeding on these crustaceans the nematode became adapted to its current biotope.     

Spectroscopic and molecular dynamics evidence for a sequential mechanism for the A-to-B transition in DNA

The A-to-B form transition has been examined in three DNA duplexes, d(CGCGAATTCGCG)₂, d(CGCGAATTGCGC), and d(CGCAAATTTCGC), using circular dichroism spectroscopy, ultraviolet resonance Raman (UVRR) spectroscopy, and molecular dynamics (MD) simulation. Circular dichroism spectra confirm that these molecules adopt the A form under conditions of reduced water activity. UVRR results, obtained under similar conditions, suggest that the transition involves a series of intermediate forms between A and B. Cooperative and distinct transitions were observed for the bases and the sugars. Independent MD simulations on d(CGCGAATTCGCG)₂ show a spontaneous change from the A to B form in aqueous solution and describe a kinetic model that agrees well with UVRR results. Based on these observations, we predict that the mechanism of the transition involves a series of A/B hybrid forms and is sequential in nature, similar to previous crystallographic studies of derivatized duplexes. A simulation in which waters were restrained in the major groove of B DNA shows a rapid, spontaneous change from B to A at reduced water activity. These results indicate that a quasiergodic sampling of the solvent distribution may be a problem in going from B to A at reduced water activity in the course of an MD simulation.     

Morphological and molecular evidence for a new species of Perenniporia (Basidiomycota) from Tibet, southwestern China

A new polypore, Perenniporia tibetica, collected in Xizang (Tibet), southwestern China, is described and illustrated on the basis of morphological and molecular characters. Perenniporia tibetica is characterized by an annual growth habit, resupinate basidiocarps with a creambuff to pinkish-buff pore surface and white to cream-colored rhizomorphs, a dimitic hyphal system with slightly dextrinoid and distinctly cyanophilous skeletal hyphae, and basidiospores that are ellipsoid, truncate or not, strongly dextrinoid, and cyanophilous, 6.7–8.7 × 5.3–6.8 μm. Its preliminary phylogenetic relationships are inferred based on sequence data from the ribosomal ITS and LSU regions, both suggesting that P. tibetica forms a distinct lineage in the genus Perenniporia.     

Testing heterochrony: Connecting skull shape ontogeny and evolution of feeding adaptations in baleen whales

Ontogeny plays a key role in the evolution of organisms, as changes during the complex processes of development can allow for new traits to arise. Identifying changes in ontogenetic allometry—the relationship between skull shape and size during growth—can reveal the processes underlying major evolutionary transformations. Baleen whales (Mysticeti, Cetacea) underwent major morphological changes in transitioning from their ancestral raptorial feeding mode to the three specialized filter-feeding modes observed in extant taxa. Heterochronic processes have been implicated in the evolution of these feeding modes, and their associated specialized cranial morphologies, but their role has never been tested with quantitative data. Here, we quantified skull shapes ontogeny and reconstructed ancestral allometric trajectories using 3D geometric morphometrics and phylogenetic comparative methods on sample representing modern mysticetes diversity. Our results demonstrate that Mysticeti, while having a common developmental trajectory, present distinct cranial shapes from early in their ontogeny corresponding to their different feeding ecologies. Size is the main driver of shape disparity across mysticetes. Disparate heterochronic processes are evident in the evolution of the group: skim feeders present accelerated growth relative to the ancestral nodes, while Balaenopteridae have overall slower growth, or pedomorphosis. Gray whales are the only taxon with a relatively faster rate of growth in this group, which might be connected to its unique benthic feeding strategy. Reconstructed ancestral allometries and related skull shapes indicate that extinct taxa used less specialized filter-feeding modes, a finding broadly in line with the available fossil evidence.     

Morphological and molecular evidence for hybridization and introgression in a willow (Salix) hybrid zone

Hybrid zones provide biologists with the opportunity to examine genetic and ecological interactions between differentiated populations. Accurate identification of hybrid genealogies is considered a necessary prerequisite to understanding observed patterns of hybridization-related phenomena. We analysed molecular and morphological data from individuals in a hybrid zone between two species of willows (Salix sericea Marshall and S. eriocephala Michaux) and report the use of randomly amplified polymorphic DNA (RAPD), chloroplast DNA (cpDNA), and ribosomal DNA (rDNA) markers, as well as vegetative morphology and foliar chemistry data to identify individuals in terms of hybrid genealogy and to infer the direction and extent of backcrossing and introgression within the hybrid zone. A novel version of a maximum likelihood estimate approach (developed for this study) was used to calculate hybrid index scores from RAPD marker data; this method produced results similar to those obtained using traditional arithmetic methods. Distribution of rDNA, cpDNA, and chemistry data were examined within the graphical context of RAPD-based hybrid index score histograms and principal component analyses (PCA) on RAPD and morphology data. Seven of the 21 plants classified as S. eriocephala in the field were possible introgressants. Another plant presented an unequivocal example of backcrossed S. sericea chemistry and RAPD markers. Inter- and intraspecific chloroplast diversity found within the hybrid zone suggests both historic introgression (perhaps in a glacial refugium), and contemporary hybridization. Patterns of inheritance and expression within the hybrid zone suggest that morphological characters are often not expressed in a simple additive fashion, and problems associated with both morphological and molecular data are considered.     

Morphological evidence for a substance P projection from medial septum to hippocampus.

The medial septal nucleus provides one of the major afferents to the hippocampal formation. The two major types of neurons present in the medial septum are cholinergic and GABAergic, but other types of neurons are also present. A small population of substance P-containing neurons is present along the border between the medial and lateral septum, but it is unclear whether these project to the hippocampus. The present study, by employing both anterograde and retrograde tracing techniques, combined with immunocytochemistry for substance P, provides direct morphological evidence for a substance P projection from the lateral region of medial septum to a portion of CA2/3a, which is restricted to the mid-septotemporal portion of the hippocampus.