The Loss of the Classic Nasolacrimal System in the Florida Manatee and Other Selected Paenungulate Species
Members representing the three paenungulate ("near-ungulate") orders, Hyracoidea, Proboscidea, and Sirenia, possess reinvented nasolacrimal systems not usually encountered among mammalian species. We have discovered that the Asian elephant (Elephas maximus), the rock hyrax (Procavia capensis), and the West Indian manatee (Trichecus manatus) lack lacrimal glands, lacrimal punctae, and nasolacrimal ducts as well as the tarsal glands and that the nasolacrimal systems of these species have been little understood. To that end, we have examined anatomically the nasolacrimal systems associated with their eyes.
Freshly collected formalin-preserved specimens from anterior adnexa of two or more individuals of each species (the Asian elephant, rock hyrax, and West Indian manatee) were examined stereomicroscopically and medial, central and lateral portions of each upper and lower palpebrae, as well as entire nictitating membranes (tertia palpebrae) and associated glandular tissue were embedded, sectioned and treated with a variety of stains that included: H&E, Massons trichrome, and PAS. In addition to the absence of lacrimal glands, there was a lack of tarsal (Meibomian) glands in either upper or lower eyelid of each species. However, the Asian elephant possessed highly developed sebaceous glands associated with each palpebral cilium (lash) and neighboring hair. The hyrax possessed uniquely developed sebum-forming compound glands within the anterior margin of the nictitating membrane at the region of the medial canthus. The upper and lower eyelids of both the Florida manatee and elephant contained extensive accessory glands, having been largely mucous in the manatee and serous in the elephant. All species had well developed tubuloalveolar glands of the nictitating membrane, which were mostly mucous in the manatee, serous in the elephant and seromucous in the hyrax. Lymphatic tissues were especially well developed in the Florida manatee.
The three orders that the present species represent are believed to be ancestrally linked through both morphological and molecular evidence.1,2 The lack of traditional nasolacrimal systems in these animals support their common evolutionary origin. The loss of both lacrimal and tarsal glands as well as those components for tear drainage suggest a shared aquatic past. The different ways that sebum-forming glands were reformed so that an oily layer is able to cover the seromucous portion of tears of the Asian elephant and the rock hyrax most likely are the result of the different ecological pressures encountered during their subsequent evolution.
1. Gheerbrant E, Domning DP, Tassy P. Paenungulata (Sirenia, Proboscidea, Hyracoidea, and Relatives). In "The Rise of Pacental Mammals", Eds. Rose, K.D. and Archibald, J.D., Johns Hopkins University Press, Baltimore, 2005.
2. Stanhope MJ, Madsen O, Waddell VG, Cleven GC, deJong WW, Springer, MS. Highly congruent molecular support for a diverse superordinal clade of endemic African mammals. Mol. Phylogen. Evol. 9:501-08, 1998.