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The cribriform plate: Evolution of mammalian olfaction written in bone

  • Author(s): Bird, Deborah Jean
  • Advisor(s): Van Valkenburgh, Blaire
  • et al.
Abstract

Deep inside the snout of nearly every mammal is a small, perforated bone that separates the nasal cavity from the brain case. It is called the cribriform plate (CP). Its holes, or foramina, usher olfactory nerve bundles on their path from nasal epithelium to the olfactory bulb of the brain. The imprint left in the CP bone by these nerves is the subject of this study. The size of the imprint describes the relative olfactory innervation in a given animal’s nose and varies under ecological and evolutionary pressures across all mammal species. As a well-preserved, quantifiable feature of skull morphology, the CP is a potentially informative tool for comparing olfactory capacity in extant as well as extinct species. However, in general, the CP is overlooked and understudied. This study developed novel digital methods to conduct a comprehensive comparative analysis of CP morphology across species from all mammalian superorders. I further analyzed relative CP size in the context of skull morphology, olfactory genomics, habitat, and behavior, to test the hypothesis that the CP is a valid proxy of olfactory function. I found a tight covariance between the surface area of the CP and the olfactory-related ethmoid and nasal turbinal bones. Results further revealed a strong positive relationship between relative CP size and the number of olfactory receptor genes in a species’ genome. I confirmed the near or total loss of the CP in the bottlenose dolphin (Tursiops truncatus) and reported an unsurpassed expansion in the relative CP size of the African elephant (Loxodonta africana), paralleling its highly expanded OR gene repertoire. Finally, this study discovered that within Carnivora, aquatic species, which are known to forage underwater without odor cues, have significantly smaller relative CPs than their terrestrial relatives. Within the aquatic carnivoran pinnipeds and sea otter, I found that relative CP size is inversely correlated with both diving depth and duration, suggesting that secondary adaptation to life underwater, especially at depth, favored the loss of olfactory function and morphology. In summary, the morphological, molecular and ecological coherence found in this study reinforces the CP as a stand-alone proxy of olfactory capacity that can be applied to living and extinct species, allowing us to document the evolution of olfactory function within mammals over geologic time.

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