Evolutionary novelties underlie sound production in baleen whales.

Baleen whales (mysticetes) use vocalizations to mediate their complex social and reproductive behaviours in vast, opaque marine environments1. Adapting to an obligate aquatic lifestyle demanded fundamental physiological changes to efficiently produce sound, including laryngeal specializations2-4. Whereas toothed whales (odontocetes) evolved a nasal vocal organ5, mysticetes have been thought to use the larynx for sound production1,6-8. However, there has been no direct demonstration that the mysticete larynx can phonate, or if it does, how it produces the great diversity of mysticete sounds9. Here we combine experiments on the excised larynx of three mysticete species with detailed anatomy and computational models to show that mysticetes evolved unique laryngeal structures for sound production. These structures allow some of the largest animals that ever lived to efficiently produce frequency-modulated, low-frequency calls. Furthermore, we show that this phonation mechanism is likely to be ancestral to all mysticetes and shares its fundamental physical basis with most terrestrial mammals, including humans10, birds11, and their closest relatives, odontocetes5. However, these laryngeal structures set insurmountable physiological limits to the frequency range and depth of their vocalizations, preventing them from escaping anthropogenic vessel noise12,13 and communicating at great depths14, thereby greatly reducing their active communication range.

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.

Baleen whale prey consumption based on high-resolution foraging measurements.

Baleen whales influence their ecosystems through immense prey consumption and nutrient recycling1-3. It is difficult to accurately gauge the magnitude of their current or historic ecosystem role without measuring feeding rates and prey consumed. To date, prey consumption of the largest species has been estimated using metabolic models3-9 based on extrapolations that lack empirical validation. Here, we used tags deployed on seven baleen whale (Mysticeti) species (n = 321 tag deployments) in conjunction with acoustic measurements of prey density to calculate prey consumption at daily to annual scales from the Atlantic, Pacific, and Southern Oceans. Our results suggest that previous studies3-9 have underestimated baleen whale prey consumption by threefold or more in some ecosystems. In the Southern Ocean alone, we calculate that pre-whaling populations of mysticetes annually consumed 430 million tonnes of Antarctic krill (Euphausia superba), twice the current estimated total biomass of E. superba10, and more than twice the global catch of marine fisheries today11. Larger whale populations may have supported higher productivity in large marine regions through enhanced nutrient recycling: our findings suggest mysticetes recycled 1.2 × 104 tonnes iron yr-1 in the Southern Ocean before whaling compared to 1.2 × 103 tonnes iron yr-1 recycled by whales today. The recovery of baleen whales and their nutrient recycling services2,3,7 could augment productivity and restore ecosystem function lost during 20th century whaling12,13.

Why are whales big? Genes behind ocean giants.

Gigantism is prevalent in animals, but it has never reached more extreme levels than in aquatic mammals such as whales, dolphins, and porpoises. A new study by Silva et al. has uncovered five genes underlying this gigantism, a phenotype with important connections to aging and cancer suppression in long-lived animals.

Convergence in hearing-related genes between echolocating birds and mammals.

Echolocation, the detection of objects by means of sound waves, has evolved independently in diverse animals. Echolocators include not only mammals such as toothed whales and yangochiropteran and rhinolophoid bats but also Rousettus fruit bats, as well as two bird lineages, oilbirds and swiftlets. In whales and yangochiropteran and rhinolophoid bats, positive selection and molecular convergence has been documented in key hearing-related genes, such as prestin (SLC26A5), but few studies have examined these loci in other echolocators. Here, we examine patterns of selection and convergence in echolocation-related genes in echolocating birds and Rousettus bats. Fewer of these loci were under selection in Rousettus or birds compared with classically recognized echolocators, and elevated convergence (compared to outgroups) was not evident across this gene set. In certain genes, however, we detected convergent substitutions with potential functional relevance, including convergence between Rousettus and classic echolocators in prestin at a site known to affect hair cell electromotility. We also detected convergence between Yangochiroptera, Rhinolophidea, and oilbirds in TMC1, an important mechanosensory transduction channel in vertebrate hair cells, and observed an amino acid change at the same site within the pore domain. Our results suggest that although most proteins implicated in echolocation in specialized mammals may not have been recruited in birds or Rousettus fruit bats, certain hearing-related loci may have undergone convergent functional changes. Investigating adaptations in diverse echolocators will deepen our understanding of this unusual sensory modality.

Ancient whale rhodopsin reconstructs dim-light vision over a major evolutionary transition: Implications for ancestral diving behavior.

Cetaceans are fully aquatic mammals that descended from terrestrial ancestors, an iconic evolutionary transition characterized by adaptations for underwater foraging via breath-hold diving. Although the evolutionary history of this specialized behavior is challenging to reconstruct, coevolving sensory systems may offer valuable clues. The dim-light visual pigment, rhodopsin, which initiates phototransduction in the rod photoreceptors of the eye, has provided insight into the visual ecology of depth in several aquatic vertebrate lineages. Here, we use ancestral sequence reconstruction and protein resurrection experiments to quantify light-activation metrics in rhodopsin pigments from ancestors bracketing the cetacean terrestrial-to-aquatic transition. By comparing multiple reconstruction methods on a broadly sampled cetartiodactyl species tree, we generated highly robust ancestral sequence estimates. Our experimental results provide direct support for a blue-shift in spectral sensitivity along the branch separating cetaceans from terrestrial relatives. This blue-shift was 14 nm, resulting in a deep-sea signature (λmax = 486 nm) similar to many mesopelagic-dwelling fish. We also discovered that the decay rates of light-activated rhodopsin increased in ancestral cetaceans, which may indicate an accelerated dark adaptation response typical of deeper-diving mammals. Because slow decay rates are thought to help sequester cytotoxic photoproducts, this surprising result could reflect an ecological trade-off between rod photoprotection and dark adaptation. Taken together, these ancestral shifts in rhodopsin function suggest that some of the first fully aquatic cetaceans could dive into the mesopelagic zone (>200 m). Moreover, our reconstructions indicate that this behavior arose before the divergence of toothed and baleen whales.

Decadal migration phenology of a long-lived Arctic icon keeps pace with climate change.

Animals migrate in response to seasonal environments, to reproduce, to benefit from resource pulses, or to avoid fluctuating hazards. Although climate change is predicted to modify migration, only a few studies to date have demonstrated phenological shifts in marine mammals. In the Arctic, marine mammals are considered among the most sensitive to ongoing climate change due to their narrow habitat preferences and long life spans. Longevity may prove an obstacle for species to evolutionarily respond. For species that exhibit high site fidelity and strong associations with migration routes, adjusting the timing of migration is one of the few recourses available to respond to a changing climate. Here, we demonstrate evidence of significant delays in the timing of narwhal autumn migrations with satellite tracking data spanning 21 y from the Canadian Arctic. Measures of migration phenology varied annually and were explained by sex and climate drivers associated with ice conditions, suggesting that narwhals are adopting strategic migration tactics. Male narwhals were found to lead the migration out of the summering areas, while females, potentially with dependent young, departed later. Narwhals are remaining longer in their summer areas at a rate of 10 d per decade, a similar rate to that observed for climate-driven sea ice loss across the region. The consequences of altered space use and timing have yet to be evaluated but will expose individuals to increasing natural changes and anthropogenic activities on the summering areas.

Submesoscale coupling of krill and whales revealed by aggregative Lagrangian coherent structures.

In the marine environment, dynamic physical processes shape biological productivity and predator-prey interactions across multiple scales. Identifying pathways of physical-biological coupling is fundamental to understand the functioning of marine ecosystems yet it is challenging because the interactions are difficult to measure. We examined submesoscale (less than 100 km) surface current features using remote sensing techniques alongside ship-based surveys of krill and baleen whale distributions in the California Current System. We found that aggregative surface current features, represented by Lagrangian coherent structures (LCS) integrated over temporal scales between 2 and 10 days, were associated with increased (a) krill density (up to 2.6 times more dense), (b) baleen whale presence (up to 8.3 times more likely) and (c) subsurface seawater density (at depths up to 10 m). The link between physical oceanography, krill density and krill-predator distributions suggests that LCS are important features that drive the flux of energy and nutrients across trophic levels. Our results may help inform dynamic management strategies aimed at reducing large whales ship strikes and help assess the potential impacts of environmental change on this critical ecosystem.

Disentangling the influence of entanglement on recruitment in North Atlantic right whales.

North Atlantic right whales are Critically Endangered and declining, with entanglements in fishing gear a key contributor to their decline. Entanglement events can result in lethal and sub-lethal (i.e. increased energetic demands and reduced foraging ability) impacts, with the latter influencing critical life-history states, such as reproduction. Using a multi-event framework, we developed a Bayesian mark-recapture model to investigate the influence of entanglement severity on survival and recruitment for female right whales. We used information from 199 known-aged females sighted between 1977 and 2018, combined with known entanglements of varying severity that were classified as minor, moderate or severe. Severe entanglements resulted in an average decline in survival of 27% for experienced non-breeders, 9% for breeders and 26% for pre-breeding females compared with other entanglements and unentangled individuals. Surviving individuals with severe entanglements had low transitional probabilities to breeders, but surprisingly, individuals with minor entanglements had the lowest transitional probabilities, contrary to expectations underpinning current management actions. Management actions are needed to address the lethal and sub-lethal impacts of entanglements, regardless of severity classification.

Modeling individual growth reveals decreasing gray whale body length and correlations with ocean climate indices at multiple scales.

Changes in body size have been documented across taxa in response to human activities and climate change. Body size influences many aspects of an individual's physiology, behavior, and ecology, ultimately affecting life history performance and resilience to stressors. In this study, we developed an analytical approach to model individual growth patterns using aerial imagery collected via drones, which can be used to investigate shifts in body size in a population and the associated drivers. We applied the method to a large morphological dataset of gray whales (Eschrichtius robustus) using a distinct foraging ground along the NE Pacific coast, and found that the asymptotic length of these whales has declined since around the year 2000 at an average rate of 0.05-0.12 m/y. The decline has been stronger in females, which are estimated to be now comparable in size to males, minimizing sexual dimorphism. We show that the decline in asymptotic length is correlated with two oceanographic metrics acting as proxies of habitat quality at different scales: the mean Pacific Decadal Oscillation index, and the mean ratio between upwelling intensity in a season and the number of relaxation events. These results suggest that the decline in gray whale body size may represent a plastic response to changing environmental conditions. Decreasing body size could have cascading effects on the population's demography, ability to adjust to environmental changes, and ecological influence on the structure of their community. This finding adds to the mounting evidence that body size is shrinking in several marine populations in association with climate change and other anthropogenic stressors. Our modeling approach is broadly applicable across multiple systems where morphological data on megafauna are collected using drones.

Morphology of nares associated with stereo-olfaction in baleen whales.

The sensory mechanisms used by baleen whales (Mysticeti) for locating ephemeral, dense prey patches in vast marine habitats are poorly understood. Baleen whales have a functional olfactory system with paired rather than single blowholes (nares), potentially enabling stereo-olfaction. Dimethyl sulfide (DMS) is an odorous gas emitted by phytoplankton in response to grazing by zooplankton. Some seabirds use DMS to locate prey, but this ability has not been demonstrated in whales. For 14 extant species of baleen whale, nares morphometrics (imagery from unoccupied aerial systems, UAS) was related to published trophic level indices using Bayesian phylogenetic mixed modelling. A significant negative relationship was found between nares width and whale trophic level (ß = -0.08, lower 95% CI = -0.13, upper 95% CI = -0.03), corresponding with a 39% increase in nares width from highest to lowest trophic level. Thus, species with nasal morphology best suited to stereo-olfaction are more zooplanktivorous. These findings provide evidence that some baleen whale species may be able to localize odorants e.g. DMS. Our results help direct future behavioural trials of olfaction in baleen whales, by highlighting the most appropriate species to study. This is a research priority, given the potential for DMS-mediated plastic ingestion by whales.

A longitudinal study of endocrinology and foraging ecology of subadult gray whales prior to death based on baleen analysis.

Individual-level assessments of wild animal health, vital rates, and foraging ecology are critical for understanding population-wide impacts of exposure to stressors. Large whales face multiple stressors, including, but not limited to, ocean noise, pollution, and ship strikes. Because baleen is a continuously growing keratinized structure, serial extraction, and quantification of hormones and stable isotopes along the length of baleen provide a historical record of whale physiology and foraging ecology. Furthermore, baleen analysis enables the investigation of dead specimens, even decades later, allowing comparisons between historic and modern populations. Here, we examined baleen of five sub-adult gray whales and observed distinct patterns of oscillations in δ15N values along the length of their baleen plates which enabled estimation of baleen growth rates and differentiation of isotopic niche widths of the whales during wintering and summer foraging. In contrast, no regular patterns were apparent in δ13C values. Prolonged elevation of cortisol in four individuals before death indicates that chronic stress may have impacted their health and survival. Triiodothyronine (T3) increased over months in the whales with unknown causes of death, simultaneous with elevations in cortisol, but both hormones remained stable in the one case of acute death attributed to killer whale predation. This parallel elevation of cortisol and T3 challenges the classic understanding of their interaction and might relate to increased energetic demands during exposure to stressors. Reproductive hormone profiles in subadults did not show cyclical trends, suggesting they had not yet reached sexual maturity. This study highlights the potential of baleen analysis to retrospectively assess gray whales' physiological status, exposure to stressors, reproductive status, and foraging ecology in the months or years leading up to their death, which can be a useful tool for conservation diagnostics to mitigate unusual mortality events.