The evolution of menopause in toothed whales.

Understanding how and why menopause has evolved is a long-standing challenge across disciplines. Females can typically maximize their reproductive success by reproducing for the whole of their adult life. In humans, however, women cease reproduction several decades before the end of their natural lifespan1,2. Although progress has been made in understanding the adaptive value of menopause in humans3,4, the generality of these findings remains unclear. Toothed whales are the only mammal taxon in which menopause has evolved several times5, providing a unique opportunity to test the theories of how and why menopause evolves in a comparative context. Here, we assemble and analyse a comparative database to test competing evolutionary hypotheses. We find that menopause evolved in toothed whales by females extending their lifespan without increasing their reproductive lifespan, as predicted by the 'live-long' hypotheses. We further show that menopause results in females increasing their opportunity for intergenerational help by increasing their lifespan overlap with their grandoffspring and offspring without increasing their reproductive overlap with their daughters. Our results provide an informative comparison for the evolution of human life history and demonstrate that the same pathway that led to menopause in humans can also explain the evolution of menopause in toothed whales.

A heavyweight early whale pushes the boundaries of vertebrate morphology.

The fossil record of cetaceans documents how terrestrial animals acquired extreme adaptations and transitioned to a fully aquatic lifestyle1,2. In whales, this is associated with a substantial increase in maximum body size. Although an elongate body was acquired early in cetacean evolution3, the maximum body mass of baleen whales reflects a recent diversification that culminated in the blue whale4. More generally, hitherto known gigantism among aquatic tetrapods evolved within pelagic, active swimmers. Here we describe Perucetus colossus-a basilosaurid whale from the middle Eocene epoch of Peru. It displays, to our knowledge, the highest degree of bone mass increase known to date, an adaptation associated with shallow diving5. The estimated skeletal mass of P. colossus exceeds that of any known mammal or aquatic vertebrate. We show that the bone structure specializations of aquatic mammals are reflected in the scaling of skeletal fraction (skeletal mass versus whole-body mass) across the entire disparity of amniotes. We use the skeletal fraction to estimate the body mass of P. colossus, which proves to be a contender for the title of heaviest animal on record. Cetacean peak body mass had already been reached around 30 million years before previously assumed, in a coastal context in which primary productivity was particularly high.

New heterodont odontocetes from the Oligocene Pysht Formation in Washington State, U.S.A., and a reevaluation of Simocetidae (Cetacea, Odontoceti).

Odontocetes first appeared in the fossil record by the early Oligocene, and their early evolutionary history can provide clues as to how some of their unique adaptations, such as echolocation, evolved. Here, three new specimens from the early to late Oligocene Pysht Formation are described further increasing our understanding of the richness and diversity of early odontocetes, particularly for the North Pacific. Phylogenetic analysis shows that the new specimens are part of a more inclusive, redefined Simocetidae, which now includes Simocetus rayi, Olympicetus sp. 1, Olympicetus avitus, O. thalassodon sp. nov., and a large unnamed taxon (Simocetidae gen. et sp. A), all part of a North Pacific clade that represents one of the earliest diverging groups of odontocetes. Amongst these, Olympicetus thalassodon sp. nov. represents one of the best known simocetids, offering new information on the cranial and dental morphology of early odontocetes. Furthermore, the inclusion of CCNHM 1000, here considered to represent a neonate of Olympicetus sp., as part of the Simocetidae, suggests that members of this group may not have had the capability of ultrasonic hearing, at least during their early ontogenetic stages. Based on the new specimens, the dentition of simocetids is interpreted as being plesiomorphic, with a tooth count more akin to that of basilosaurids and early toothed mysticetes, while other features of the skull and hyoid suggest various forms of prey acquisition, including raptorial or combined feeding in Olympicetus spp., and suction feeding in Simocetus. Finally, body size estimates show that small to moderately large taxa are present in Simocetidae, with the largest taxon represented by Simocetidae gen. et sp. A with an estimated body length of 3 m, which places it as the largest known simocetid, and amongst the largest Oligocene odontocetes. The new specimens described here add to a growing list of Oligocene marine tetrapods from the North Pacific, further promoting faunistic comparisons across other contemporaneous and younger assemblages, that will allow for an improved understanding of the evolution of marine faunas in the region.

Determinants of lungworm specificity in five cetacean species in the western Mediterranean.

BACKGROUND: Current data about Pseudaliidae show contrasting patterns of host specificity between congeneric species. We investigated how both contact and compatibility between hosts and parasites contributed to the patterns of lungworm infection observed in a community of five species of cetaceans in the western Mediterranean. METHODS: The lungs of 119 striped dolphins Stenella coeruleoalba, 18 bottlenose dolphins Tursiops truncatus, 7 Risso's dolphins Grampus griseus, 7 long-finned pilot whales Globicephala melas, and 6 common dolphins Delphinus delphis were analysed for lungworms. Parasites were identified by morphology and analysis of ITS2 sequences using both maximum likelihood and Bayesian inference methods. Body length was used as a proxy for lungworm species fitness in different hosts and compared with Kruskal-Wallis tests. Infection parameters were compared between cetacean species using Fisher's exact tests and Kruskal-Wallis tests. Phylogenetic specificity was explored by collating the overall lungworm species prevalence values in hosts from previous surveys in various localities. To explore the relative importance of vertical and horizontal transmission, Spearman's rank correlation was used to look for an association between host size and lungworm burden. A Mantel test was used to explore the association between lungworm species similarity and prey overlap using dietary data. RESULTS: Halocercus delphini had higher infection levels in striped dolphins and common dolphins; Stenurus ovatus had higher infection levels in bottlenose dolphins; and Stenurus globicephalae had higher infection levels in long-finned pilot whales. These results are congruent with findings on a global scale. Morphometric comparison showed that the larger nematodes were found in the same host species that had the highest parasite burden. Lungworms were found in neonatal striped dolphins and a Risso's dolphin, and there was a weak but significant correlation between host size and parasite burden in striped dolphins and bottlenose dolphins. There was also a weak but significant association between prey overlap and lungworm species similarity. CONCLUSIONS: Data indicate that phylogenetic specificity has an important role in governing host-parasite associations, as indicated by the higher infection levels and larger nematode size in certain hosts. However, diet can also influence infection patterns in these preferred hosts and contribute to less severe infections in other hosts.

First live sighting of Deraniyagala's beaked whale (Mesoplodon hotaula) or ginkgo-toothed beaked whale (Mesoplodon ginkgodens) in the western Pacific (South China Sea) with preliminary data on coloration, natural markings, and surfacing patterns.

Beaked whales represent around 25% of known extant cetacean species, yet they are the least known of all marine mammals. Identification of many Mesoplodon species has relied on examination of a few stranded individuals. Particularly, the ginkgo-toothed beaked whale (Mesoplodon ginkgodens) and Deraniyagala's beaked whale (Mesoplodon hotaula) are among the least-known of beaked whale species, without confirmed sightings of living individuals to date. We present a sighting of 3 free-ranging individuals of M. ginkgodens/hotaula whale from a dedicated marine mammal vessel survey carried out in the South China Sea in April and May 2019. Photographic data (301 photographs) from the sighting were compared to photos of fresh stranded ginkgo-toothed beaked whale and Deraniyagala's beaked whale from both historical and unpublished records. We found that free-ranging M. ginkgodens and M. hotaula individuals can be easily distinguished from other Mesoplodon species due to differences in melon and gape shapes and coloration patterns. However, accurate at-sea differentiation of M. ginkgodens and M. hotaula may not be possible due to high similarity in both coloration and scarring patterns. In addition to our photo-identification data, we collected what we believe to be the first preliminary descriptions of surfacing behavior and diving patterns of one of these species. Finally, the presence of scars possibly caused by fishing gear or marine litter raises concerns about anthropogenic impacts and conservation of these poorly known species.

The Karyotype of Blainville's Beaked Whale, Mesoplodon densirostris.

The karyotype of the Odontocete whale, Mesoplodon densirostris, has not been previously reported. The chromosome number is determined to be 2n = 42, and the karyotype is presented using G-, C-, and nucleolar organizer region (NOR) banding. The findings include NOR regions on 2 chromosomes, regions of heterochromatic variation, a large block of heterochromatin on the X chromosome, and a relatively large Y chromosome. The karyotype is compared to published karyograms of 2 other species of Mesoplodon.

Host phylogeny and life history stage shape the gut microbiome in dwarf (Kogia sima) and pygmy (Kogia breviceps) sperm whales.

Gut microbiomes perform crucial roles in host health and development, but few studies have explored cetacean microbiomes especially deep divers. We characterized the gut microbiomes of stranded dwarf (Kogia sima) and pygmy (K. breviceps) sperm whales to examine the effects of phylogeny and life stage on microbiome composition and diversity. 16S rRNA gene sequence analysis revealed diverse gut communities (averaging 674 OTUs) dominated by a few symbiont taxa (25 OTUs accounted for 64% of total relative abundance). Both phylogeny and life stage shaped community composition and diversity, with species-specific microbiome differences present early in life. Further analysis showed evidence of microbiome convergence with host maturity, albeit through different processes: symbiont 'accumulation' in K. sima and 'winnowing' in K. breviceps, indicating different methods of community assembly during host development. Furthermore, culture-based analyses yielded 116 pure cultures matching 25 OTUs, including one isolate positive for chitin utilization. Our findings indicate that kogiid gut microbiomes are highly diverse and species-specific, undergo significant shifts with host development, and can be cultivated on specialized media under anaerobic conditions. These results enhance our understanding of the kogiid gut microbiome and may provide useful information for symbiont assessment in host health.

Wonky whales: the evolution of cranial asymmetry in cetaceans.

BACKGROUND: Unlike most mammals, toothed whale (Odontoceti) skulls lack symmetry in the nasal and facial (nasofacial) region. This asymmetry is hypothesised to relate to echolocation, which may have evolved in the earliest diverging odontocetes. Early cetaceans (whales, dolphins, and porpoises) such as archaeocetes, namely the protocetids and basilosaurids, have asymmetric rostra, but it is unclear when nasofacial asymmetry evolved during the transition from archaeocetes to modern whales. We used three-dimensional geometric morphometrics and phylogenetic comparative methods to reconstruct the evolution of asymmetry in the skulls of 162 living and extinct cetaceans over 50 million years. RESULTS: In archaeocetes, we found asymmetry is prevalent in the rostrum and also in the squamosal, jugal, and orbit, possibly reflecting preservational deformation. Asymmetry in odontocetes is predominant in the nasofacial region. Mysticetes (baleen whales) show symmetry similar to terrestrial artiodactyls such as bovines. The first significant shift in asymmetry occurred in the stem odontocete family Xenorophidae during the Early Oligocene. Further increases in asymmetry occur in the physeteroids in the Late Oligocene, Squalodelphinidae and Platanistidae in the Late Oligocene/Early Miocene, and in the Monodontidae in the Late Miocene/Early Pliocene. Additional episodes of rapid change in odontocete skull asymmetry were found in the Mid-Late Oligocene, a period of rapid evolution and diversification. No high-probability increases or jumps in asymmetry were found in mysticetes or archaeocetes. Unexpectedly, no increases in asymmetry were recovered within the highly asymmetric ziphiids, which may result from the extreme, asymmetric shape of premaxillary crests in these taxa not being captured by landmarks alone. CONCLUSIONS: Early ancestors of living whales had little cranial asymmetry and likely were not able to echolocate. Archaeocetes display high levels of asymmetry in the rostrum, potentially related to directional hearing, which is lost in early neocetes-the taxon including the most recent common ancestor of living cetaceans. Nasofacial asymmetry becomes a significant feature of Odontoceti skulls in the Early Oligocene, reaching its highest levels in extant taxa. Separate evolutionary regimes are reconstructed for odontocetes living in acoustically complex environments, suggesting that these niches impose strong selective pressure on echolocation ability and thus increased cranial asymmetry.

Energetic and physical limitations on the breaching performance of large whales.

The considerable power needed for large whales to leap out of the water may represent the single most expensive burst maneuver found in nature. However, the mechanics and energetic costs associated with the breaching behaviors of large whales remain poorly understood. In this study we deployed whale-borne tags to measure the kinematics of breaching to test the hypothesis that these spectacular aerial displays are metabolically expensive. We found that breaching whales use variable underwater trajectories, and that high-emergence breaches are faster and require more energy than predatory lunges. The most expensive breaches approach the upper limits of vertebrate muscle performance, and the energetic cost of breaching is high enough that repeated breaching events may serve as honest signaling of body condition. Furthermore, the confluence of muscle contractile properties, hydrodynamics, and the high speeds required likely impose an upper limit to the body size and effectiveness of breaching whales.

Description of a new species of beaked whale (Berardius) found in the North Pacific.

Two types of Berardius are recognised by local whalers in Hokkaido, Japan. The first is the ordinary Baird's beaked whale, B. bairdii, whereas the other is much smaller and entirely black. Previous molecular phylogenetic analyses revealed that the black type is one recognisable taxonomic unit within the Berardius clade but is distinct from the two known Berardius species. To determine the characteristics of the black type, we summarised external morphology and skull osteometric data obtained from four individuals, which included three individuals from Hokkaido and one additional individual from the United States National Museum of Natural History collection. The whales differed from all of their congeners by having the following unique characters: a substantially smaller body size of physically mature individuals, proportionately shorter beak, and darker body colour. Thus, we conclude that the whales are a third Berardius species.

First record of Ginkgo-toothed beaked whale (Mesoplodon ginkgodens) stranded in Korea.

Two stranded whales were found dead on the coast of Jeju, South Korea. Based on the outer appearance and autopsy findings, one was determined to be an adult and the other a calf. The carcasses were dissected for species identification and pathological examination. A genetic analysis was performed, and the morphological characteristics of the skull observed. Then, 448 bp of the 5' half of the mitochondrial (mt) DNA control region and 413 bp of the mtDNA cytochrome b gene were sequenced. A BLAST search revealed that the whales were ginkgo-toothed beaked whales (Mesoplodon ginkgodens). Morphological comparison of the adult skull with the holotype specimen confirmed the result. This is the first record of a stranded ginkgo-toothed beaked whale in Korea.

Contraction of the ROS Scavenging Enzyme Glutathione S-Transferase Gene Family in Cetaceans.

Cetaceans are a group of marine mammals whose ancestors were adaptated for life on land. Life in an aquatic environment poses many challenges for air-breathing mammals. Diving marine mammals have adapted to rapid reoxygenation and reactive oxygen species (ROS)-mediated reperfusion injury. Here, we considered the evolution of the glutathione transferase (GST) gene family which has important roles in the detoxification of endogenously-derived ROS and environmental pollutants. We characterized the cytosolic GST gene family in 21 mammalian species; cetaceans, sirenians, pinnipeds, and their terrestrial relatives. All seven GST classes were identified, showing that GSTs are ubiquitous in mammals. Some GST genes are the product of lineage-specific duplications and losses, in line with a birth-and-death evolutionary model. We detected sites with signatures of positive selection that possibly influence GST structure and function, suggesting that adaptive evolution of GST genes is important for defending mammals from various types of noxious environmental compounds. We also found evidence for loss of alpha and mu GST subclass genes in cetacean lineages. Notably, cetaceans have retained a homolog of at least one of the genes GSTA1, GSTA4, and GSTM1; GSTs that are present in both the cytosol and mitochondria. The observed variation in number and selection pressure on GST genes suggest that the gene family structure is dynamic within cetaceans.

Tooth Loss Precedes the Origin of Baleen in Whales.

Whales use baleen, a novel integumentary structure, to filter feed; filter feeding itself evolved at least five times in tetrapod history but demonstrably only once in mammals [1]. Living baleen whales (mysticetes) are born without teeth, but paleontological and embryological evidence demonstrate that they evolved from toothed ancestors that lacked baleen entirely [2]. The mechanisms driving the origin of filter feeding in tetrapods remain obscure. Here we report Maiabalaena nesbittae gen. et sp. nov., a new fossil whale from early Oligocene rocks of Washington State, USA, lacking evidence of both teeth and baleen. The holotype possesses a nearly complete skull with ear bones, both mandibles, and associated postcrania. Phylogenetic analysis shows Maiabalaena as crownward of all toothed mysticetes, demonstrating that tooth loss preceded the evolution of baleen. The functional transition from teeth to baleen in mysticetes has remained enigmatic because baleen decays rapidly and leaves osteological correlates with unclear homology; the oldest direct evidence for fossil baleen is ∼25 million years younger [3] than the oldest stem mysticetes (∼36 Ma). Previous hypotheses for the origin of baleen [4, 5] are inconsistent with the morphology and phylogenetic position of Maiabalaena. The absence of both teeth and baleen in Maiabalaena is consistent with recent evidence that the evolutionary loss of teeth and origin of baleen are decoupled evolutionary transformations, each with a separate morphological and genetic basis [2, 6]. Understanding these macroevolutionary patterns in baleen whales is akin to other macroevolutionary transformations in tetrapods such as scales to feathers in birds.

A description of echolocation clicks recorded in the presence of True's beaked whale (Mesoplodon mirus).

True's beaked whales (Mesoplodon mirus) were encountered on two separate shipboard surveys on 24 July 2016 and 16 September 2017 in the western North Atlantic Ocean. Recordings were made using a hydrophone array towed 300 m behind the ship. In 2016, three different groups were sighted within 1500 m of the ship; clicks were recorded for 26 min. In 2017, a single group of five whales was tracked over the course of five hours in which the ship maintained a distance <4000 m from the group. A total of 2938 frequency-modulated (FM) clicks and 7 buzzes were recorded from both encounters. Plausible inter-click-intervals (ICIs) were calculated from 2763 clicks, and frequency and duration measurements were calculated from 2150 good quality FM clicks. The median peak frequencies were 43.1 kHz (2016, n = 718) and 43.5 kHz (2017, n = 1432). Median ICIs were 0.17 s (2016) and 0.19 s (2017). The spectra and measurements of the recorded clicks closely resemble Gervais's beaked whale clicks (Mesoplodon europaeus) and distinguishing between the two species in acoustic data sets proves difficult. The acoustic behavior of True's beaked whales was previously unknown; this study provides a description of echolocation clicks produced by this species.

Analyses of ovarian activity reveal repeated evolution of post-reproductive lifespans in toothed whales.

In most species the reproductive system ages at the same rate as somatic tissue and individuals continue reproducing until death. However, females of three species - humans, killer whales and short-finned pilot whales - have been shown to display a markedly increased rate of reproductive senescence relative to somatic ageing. In these species, a significant proportion of females live beyond their reproductive lifespan: they have a post-reproductive lifespan. Research into this puzzling life-history strategy is hindered by the difficulties of quantifying the rate of reproductive senescence in wild populations. Here we present a method for measuring the relative rate of reproductive senescence in toothed whales using published physiological data. Of the sixteen species for which data are available (which does not include killer whales), we find that three have a significant post-reproductive lifespan: short-finned pilot whales, beluga whales and narwhals. Phylogenetic reconstruction suggests that female post-reproductive lifespans have evolved several times independently in toothed whales. Our study is the first evidence of a significant post-reproductive lifespan in beluga whales and narwhals which, when taken together with the evidence for post-reproductive lifespan in killer whales, doubles the number of non-human mammals known to exhibit post-reproductive lifespans in the wild.

The bony labyrinth of toothed whales reflects both phylogeny and habitat preferences.

The inner ear of toothed whales (odontocetes) is known to have evolved particular shapes related to their abilities to echolocate and move under water. While the origin of these capacities is now more and more examined, thanks to new imaging techniques, little is still known about how informative inner ear shape could be to tackle phylogenetic issues or questions pertaining to the habitat preferences of extinct species. Here we show that the shape of the bony labyrinth of toothed whales provides key information both about phylogeny and habitat preferences (freshwater versus coastal and fully marine habitats). Our investigation of more than 20 species of extinct and modern odontocetes shows that the semi-circular canals are not very informative, in contrast to baleen whales, while the cochlea alone bears a strong signal. Inner ear shape thus provides a novel source of information to distinguish between morphologically convergent lineages (e.g. river dolphins).

Unknown beaked whale echolocation signals recorded off eastern New Zealand.

The echolocation signals of most beaked whale species are still unknown. In fact, out of the 22 species comprising the family Ziphiidae, only the echolocation pulses for 7 species have been clearly described. This study describes two distinct beaked whale echolocation signals recorded in the Cook Strait region using passive acoustic technology. These signals differ from previously described Ziphiid species clicks. A description of the time-frequency characteristics of the two signals is provided. Understanding the characteristics of these signals is necessary to correctly identify species from their echolocation signals and enables future monitoring of beaked whales using passive acoustics techniques.

Evolution of cranial telescoping in echolocating whales (Cetacea: Odontoceti).

Odontocete (echolocating whale) skulls exhibit extreme posterior displacement and overlapping of facial bones, here referred to as retrograde cranial telescoping. To examine retrograde cranial telescoping across 40 million years of whale evolution, we collected 3D scans of whale skulls spanning odontocete evolution. We used a sliding semilandmark morphometric approach with Procrustes superimposition and PCA to capture and describe the morphological variation present in the facial region, followed by Ancestral Character State Reconstruction (ACSR) and evolutionary model fitting on significant components to determine how retrograde cranial telescoping evolved. The first PC score explains the majority of variation associated with telescoping and reflects the posterior migration of the external nares and premaxilla alongside expansion of the maxilla and frontal. The earliest diverging fossil odontocetes were found to exhibit a lesser degree of cranial telescoping than later diverging but contemporary whale taxa. Major shifts in PC scores and centroid size are identified at the base of Odontoceti, and early burst and punctuated equilibrium models best fit the evolution of retrograde telescoping. This indicates that the Oligocene was a period of unusually high diversity and evolution in whale skull morphology, with little subsequent evolution in telescoping.