Elaboration and Innervation of the Vibrissal System in the Rock Hyrax <b><i>(Procavia capensis)</i></b>

Abstract

Mammalian tactile hairs are commonly found on specific, restricted regions of the body, but Florida manatees represent a unique exception, exhibiting follicle-sinus complexes (FSCs, also known as vibrissae or tactile hairs) on their entire body. The orders Sirenia (including manatees and dugongs) and Hyracoidea (hyraxes) are thought to have diverged approximately 60 million years ago, yet hyraxes are among the closest relatives to sirenians. We investigated the possibility that hyraxes, like manatees, are tactile specialists with vibrissae that cover the entire postfacial body. Previous studies suggested that rock hyraxes possess postfacial vibrissae in addition to pelage hair, but this observation was not verified through histological examination. Using a detailed immunohistochemical analysis, we characterized the gross morphology, innervation and mechanoreceptors present in FSCs sampled from facial and postfacial vibrissae body regions to determine that the long postfacial hairs on the hyrax body are in fact true vibrissae. The types and relative densities of mechanoreceptors associated with each FSC also appeared to be relatively consistent between facial and postfacial FSCs. The presence of vibrissae covering the hyrax body presumably facilitates navigation in the dark caves and rocky crevices of the hyrax's environment where visual cues are limited, and may alert the animal to predatory or conspecific threats approaching the body. Furthermore, the presence of vibrissae on the postfacial body in both manatees and hyraxes indicates that this distribution may represent the ancestral condition for the supraorder Paenungulata.

Review of sensory modalities of sirenians and the other extant Paenungulata clade

“…The vibrissae of hyracoideans, similar to those of sirenians, have dense distributions of Merkel endings, assisting in detecting the direction the hair is deflected (Sarko et al, 2011). Hyracoidean vibrissae are true vibrissae as each vibrissae contains a FSC consisting of a follicle core, dense innervations, and connective tissue capsule with a surrounding blood supply (Sarko, Rice, & Reep, 2015). Unique to the rock hyrax are the Merkel endings, which innervate the FSCs as they include dermal bulges containing Merkel complex endings at the rete ridge collar level (Sarko et al, 2015).…”

“…Hyracoidean vibrissae are true vibrissae as each vibrissae contains a FSC consisting of a follicle core, dense innervations, and connective tissue capsule with a surrounding blood supply (Sarko, Rice, & Reep, 2015). Unique to the rock hyrax are the Merkel endings, which innervate the FSCs as they include dermal bulges containing Merkel complex endings at the rete ridge collar level (Sarko et al, 2015). Mystacial FSCs of the rock hyrax are unique in their morphology as they contain longitudinal ridges and grooves, which extend from the cavernous sinus to the lower ring sinus level and are packed with axons ascending from the deep vibrissal nerves; two deep vibrissal nerves are responsible for the innervations of the FSCs of all body regions in hyrax (Sarko et al, 2015).…”

“…Unique to the rock hyrax are the Merkel endings, which innervate the FSCs as they include dermal bulges containing Merkel complex endings at the rete ridge collar level (Sarko et al, 2015). Mystacial FSCs of the rock hyrax are unique in their morphology as they contain longitudinal ridges and grooves, which extend from the cavernous sinus to the lower ring sinus level and are packed with axons ascending from the deep vibrissal nerves; two deep vibrissal nerves are responsible for the innervations of the FSCs of all body regions in hyrax (Sarko et al, 2015). The rock hyrax possesses guard hairs located proximal to the vibrissae; however, guard hairs do not contain a blood‐filled ring sinus or a capsule of dense connective tissue, but are rather associated with sebaceous glands and lanceolate endings (Sarko et al, 2015).…”

“…Mystacial FSCs of the rock hyrax are unique in their morphology as they contain longitudinal ridges and grooves, which extend from the cavernous sinus to the lower ring sinus level and are packed with axons ascending from the deep vibrissal nerves; two deep vibrissal nerves are responsible for the innervations of the FSCs of all body regions in hyrax (Sarko et al, 2015). The rock hyrax possesses guard hairs located proximal to the vibrissae; however, guard hairs do not contain a blood‐filled ring sinus or a capsule of dense connective tissue, but are rather associated with sebaceous glands and lanceolate endings (Sarko et al, 2015). The vibrissae of the rock hyrax likely serve complementary functions given their unique structure, which include detecting large hair deflections by the Merkel endings of the rete ridge collar, and smaller disturbances at the ring sinus level.…”

Constraints on the deformation of the vibrissa within the follicle

“…Whisker and follicle systems are thought to be traits of very basal mammals [ 13 – 15 ], or even the mammal-like reptile cynodonts [ 16 – 18 ], and whisker anatomy is strikingly similar for multiple species across a broad swath of the mammalian family tree. A list of these species helps impart an appreciation for the remarkable range of animals that share similar follicle characteristics and for the importance of this sensing modality in mammals: the rakali (water rat; Hydromys chrysogaster ) [ 19 ], naked mole-rats ( Heterocephalus glaber ) [ 20 ], tree squirrels ( Sciurus vulgaris ) [ 21 ], shrews ( Sorex araneus ) [ 22 ], rock hyrax ( Procavia capensis ) [ 23 ], tammar wallaby ( Macropus eugenii ) [ 24 ], manatee ( Trichechus manatus ) [ 25 , 26 ], harbor seal ( Phoca vitulina ) [ 27 ], ringed seal ( Pusa hispida ) [ 28 ], California sea lion ( Zalophus californianus ) [ 29 ], sea otter ( Enhydra lutris ) [ 30 ], bearded seal ( Erignathus barbatus ) [ 31 ], Eurasian otter and pole cat ( Lutra lutra and Mustela putorius ) [ 32 ], rats and cats ( Rattus norvegicus and Felis catus ) [ 11 ].…”