The Hydrodynamic Sensory System in the Skin of Cetaceans

Abstract

The skin’s sensory afferents have a myriad of varieties, tactile functions and specialized end‐organ receptors enabling species to exploit ecological niches. In typical vertebrate skin, from fish to humans, axons innervate relatively small discreet receptive fields, providing fine‐scale discrimination of texture or location of a pin prick.The cetacean suborders of Mysticeti (baleen) and Odontoceti (toothed) whales are fully‐aquatic glabrous‐skinned mammals, descendants of terrestrial hairy‐skinned arteriodactyls. Shaped by dynamic forces of the marine environment, nerves in the skin of cetaceans (whales, dolphins and porpoises) have adapted to assess critical aquatic information including current flow, swim turbulence, fish movement and boundary layers, as well as tactile touch, temperature and nociceptive stimuli. The anatomy of this highly‐derived sensory system was investigated in the flank skin of humpback whales (Megaptera novaeangliae, NMFS permits 14809, 15240) using antibodies against highly‐conserved molecules of physiologically‐distinct afferents identified in other mammalian species.Humpback whales inherited a genomically‐diverse suite of cutaneous axons, including low‐threshold mechanoreceptors that sense innocuous environmental signals, as well as high‐threshold thermoreceptors, chemoreceptors and nociceptors. However, during their transition from terrestrial artiodactyls into obligate marine mammals, axon morphology and organization diverged. Unlike other vertebrates, heterogenous axons in whale skin assemble into thread‐like bundles. These ensembles divide into smaller bundles, follow circuitous trajectories that form unpredictable shapes, and lack structural endings. Developmental research has shown that axonal growth in vertebrates is guided by the skin’s signaling molecules and external physical stimuli. As environmental forces are transmitted through the epidermis they convey stretch at the dermal‐epidermal junction, a mechanically unstable boundary where mechanoreceptors typically reside. While lacking these receptor endings, the whale’s polymodal axon bundles are anatomically positioned at the dermal‐epidermal junction to transduce signals. Similar axon bundles innervation is found in the odontocete Tursiops truncatus (bottlenose dolphins), evidence that this trait is a cetacean synapomorphy. The polymorphic nature of these sensory ensembles may be a tuning mechanism that targets maximal signal strength, detects functionally diverse information (hydrostatic or hydrodynamic forces) or compares attenuation of signal properties at different locations in the skin (frequency, angular velocity or amplitude).Hallmarks of a hydrodynamically‐tuned system include the capacity to detect and integrate multiple signal properties. In becoming secondarily aquatic mammals, cetaceans have reconstructed the vertebrate somatosensory plan.Support or Funding InformationNOAA Award #NA10SEC4810008.