Olfaction written in bone: cribriform plate size parallels olfactory receptor gene repertoires in Mammalia.

The evolution of mammalian olfaction is manifested in a remarkable diversity of gene repertoires, neuroanatomy and skull morphology across living species. Olfactory receptor genes (ORGs), which initiate the conversion of odorant molecules into odour perceptions and help an animal resolve the olfactory world, range in number from a mere handful to several thousand genes across species. Within the snout, each of these ORGs is exclusively expressed by a discrete population of olfactory sensory neurons (OSNs), suggesting that newly evolved ORGs may be coupled with new OSN populations in the nasal epithelium. Because OSN axon bundles leave high-fidelity perforations (foramina) in the bone as they traverse the cribriform plate (CP) to reach the brain, we predicted that taxa with larger ORG repertoires would have proportionately expanded footprints in the CP foramina. Previous work found a correlation between ORG number and absolute CP size that disappeared after accounting for body size. Using updated, digital measurement data from high-resolution CT scans and re-examining the relationship between CP and body size, we report a striking linear correlation between relative CP area and number of functional ORGs across species from all mammalian superorders. This correlation suggests strong developmental links in the olfactory pathway between genes, neurons and skull morphology. Furthermore, because ORG number is linked to olfactory discriminatory function, this correlation supports relative CP size as a viable metric for inferring olfactory capacity across modern and extinct species. By quantifying CP area from a fossil sabertooth cat (Smilodon fatalis), we predicted a likely ORG repertoire for this extinct felid.

Domesticating olfaction: Dog breeds, including scent hounds, have reduced cribriform plate morphology relative to wolves.

The domestic dog is assumed by nearly everyone to be the consummate smeller. Within the species Canis familiaris individual breeds, such as the bloodhound or beagle, are known as olfactory stars. These are "scent breeds," a grouping variably defined as a genetic clade or breed class commonly used for scent detection tasks. Previous work suggests that the dog has a more robust olfactory anatomy than many mammal species. Now we undertake a closer investigation of the dog's olfactory system, both in relationship to its closest wild relatives, the wolf and coyote, and across individual breeds. First, we seek to resolve whether the dog has lost olfactory capacity through its domestication from the wolf lineage. Second, we test the inertial lore that among dogs, "scent breeds," have a superior olfactory facility. As a measure of relative olfactory capacity, we look to the cribriform plate (CP), a bony cup in the posterior nasal cavity perforated by passageways for all olfactory nerve bundles streaming from the periphery to the brain. Using high-resolution computed tomography (CT) scans and digital quantification, we compare relative CP size in 46 dog breeds, the coyote and gray wolf. Results show the dog has a reduced CP surface area relative to the wolf and coyote. Moreover, we found no significant differences between CP size of "scent" and "non-scent" breeds. Our study suggests that the dog lost olfactory capacity as a result of domestication and this loss was not recovered in particular breed groupings through directed artificial selection for increased olfactory facility.

Olfaction at depth: Cribriform plate size declines with dive depth and duration in aquatic arctoid carnivorans.

It is widely accepted that obligate aquatic mammals, specifically toothed whales, rely relatively little on olfaction. There is less agreement about the importance of smell among aquatic mammals with residual ties to land, such as pinnipeds and sea otters. Field observations of marine carnivorans stress their keen use of smell while on land or pack ice. Yet, one dimension of olfactory ecology is often overlooked: while underwater, aquatic carnivorans forage "noseblind," diving with nares closed, removed from airborne chemical cues. For this reason, we predicted marine carnivorans would have reduced olfactory anatomy relative to closely related terrestrial carnivorans. Moreover, because species that dive deeper and longer forage farther removed from surface scent cues, we predicted further reductions in their olfactory anatomy. To test these hypotheses, we looked to the cribriform plate (CP), a perforated bone in the posterior nasal chamber of mammals that serves as the only passageway for olfactory nerves crossing from the periphery to the olfactory bulb and thus covaries in size with relative olfactory innervation. Using CT scans and digital quantification, we compared CP morphology across Arctoidea, a clade at the interface of terrestrial and aquatic ecologies. We found that aquatic carnivoran species from two lineages that independently reinvaded marine environments (Pinnipedia and Mustelidae), have significantly reduced relative CP than terrestrial species. Furthermore, within these aquatic lineages, diving depth and duration were strongly correlated with CP loss, and the most extreme divers, elephant seals, displayed the greatest reductions. These observations suggest that CP reduction in carnivorans is an adaptive response to shifting selection pressures during secondary invasion of marine environments, particularly to foraging at great depths. Because the CP is fairly well preserved in the fossil record, using methods presented here to quantify CP morphology in extinct species could further clarify evolutionary patterns of olfactory loss across aquatic mammal lineages that have independently committed to life in water.

Quantifying the cribriform plate: influences of allometry, function, and phylogeny in Carnivora.

The small, perforated bony cup of the anterior cranial fossa called the cribriform plate (CP) is perhaps the best-preserved remnant of olfactory anatomy in fossil mammal skulls. The CP and its myriad foramina record the passage of peripheral olfactory nerves from nasal cavity to olfactory bulb. Previous work has suggested that CP surface area reflects aspects of olfactory capacity (as inferred from habitat and observed behavior) in mammals. To further explore the utility of CP as a proxy for olfactory function, we designed novel, nondestructive digital methods to quantify CP morphology from dry skulls. Using CT scans and 3-D imaging software, we quantified CP features from 42 species of Carnivora, a group that represents a wide spectrum of ecologies and sensory demands. Two metrics, CP surface area (CPSA) and cumulative CP foramina area (FXSA), scaled to skull length with negative allometry, and differed between aquatic and terrestrial species, with the former having reduced areas. Number of foramina (NF) was not correlated with skull length but tended to be greater in caniforms than feliforms. Both CPSA and FXSA are well correlated with ethmoturbinal surface area, a known osteological correlate of olfactory function. This suggests that CPSA and FXSA are useful proxies for olfactory ability, especially when studying fossils or skulls in which turbinals are not preserved. Total area of CP foramina (FXSA), an exacting measure of olfactory nerve endocasts, is tightly correlated with CPSA. Because of this, it may be desirable to use CPSA alone as a proxy given that it is easier to measure than FXSA.