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

Abstract

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.

Keywords: cribriform plate; olfactory receptor gene; olfactory sensory neuron; pseudogene; sabertooth cat; skull morphology.

Figure 1.

CP size varies markedly across mammal species. (a,b) Lateral views: (a) nine-banded armadillo (Dasypus novemcinctus) skull and (b) gorilla (Gorilla gorilla). (c–f) Dorsoposterior views: (c) armadillo, (d) dog (Canis familiaris, saluki breed), (e) little brown bat (Myotis lucifugus), and (f) gorilla. Red: CP. Green: turbinal bones (ethmoid, frontal and nasal) and partial nasal septum are only clearly viewable in lateral views.

Figure 2.

Linear correlation between relative CP size and ORG repertoire size was established and used to estimate likely ORG repertoire for the extinct sabertooth cat (S. fatalis). (a) Log–log regression plot of absolute CP surface area against body mass for 26 species (r² = 0.82, p < 0.001). Residuals from regression constitute relative CP size (RelCP) for each species and are used in all subsequent analyses. (b) Strong positive linear correlation between RelCP and the number of functional ORG (log₁₀) is shown in the RMA regression plot (r² = 0.76, p < 0.001, n = 26). (c) Linear correlation between RelCP and total ORG number (functional, pseudogenes) (log₁₀) (r² = 0.68, p < 0.001). (d) Axes from figure 2b plot are inverted and the RelCP value (green vertical line) for the sabertooth cat is applied to the regression equation. This predicts Smilodon to have had approximately 600 (581 685) functional ORG. Dotted lines: 95% CI around regression line (see Material and methods for details; see electronic supplementary material S12d for species labels).

Figure 3.

Nonlinear relationship between RelCP and OR pseudogene repertoires. (a) Dual trends are evident in the relationship between RelCP and the absolute number of OR pseudogenes, as delineated here by the vertical line: in species with the largest pseudogene counts (approx. greater than 750), the correlation is robust (r² = 0.74, p = 0.026, PGLS-r² = 0.72, p = 0.005); in the group of species with low pseudogene counts (approx. less than 500), there is no correlation. See electronic supplementary material, S11 for linear regressions on partitioned as well as non-partitioned data. (b) No linear relationship was found between RelCP and the percentage of pseudogenes present in ORG subgenomes. A high percentage of pseudogenes, a traditional measure of olfactory loss, is found here in taxa with the largest as well as smallest RelCPs (vertical line) and thus shown to be a poor indicator of relative olfactory ability. (Online version in colour.)

Figure 4.

Morphological disparity in CP seen in elephant, tarsier, platypus and dog skull models. Yellow top centre: CP of the African elephant (L. africana), viewed here from brain case, has the largest absolute and relative surface area and approximately 1000 foramina for passage of olfactory nerves to the brain. Extreme reduction in complexity is evident in CPs of the tarsier (T. syrichta) (green, lower left) and platypus (Ornithorhynchus anatinus) (orange, bottom centre) CPs. Dog (C. familiaris) CP (blue, lower right). The inset superimposed over elephant model shows tarsier, platypus and dog CPs to scale with the elephant's CP.