Evolution of olfaction in non-avian theropod dinosaurs and birds - PubMed (original) (raw)

Comparative Study

. 2011 Dec 22;278(1725):3625-34.

doi: 10.1098/rspb.2011.0238. Epub 2011 Apr 13.

Affiliations

Comparative Study

Evolution of olfaction in non-avian theropod dinosaurs and birds

Darla K Zelenitsky et al. Proc Biol Sci. 2011.

Abstract

Little is known about the olfactory capabilities of extinct basal (non-neornithine) birds or the evolutionary changes in olfaction that occurred from non-avian theropods through modern birds. Although modern birds are known to have diverse olfactory capabilities, olfaction is generally considered to have declined during avian evolution as visual and vestibular sensory enhancements occurred in association with flight. To test the hypothesis that olfaction diminished through avian evolution, we assessed relative olfactory bulb size, here used as a neuroanatomical proxy for olfactory capabilities, in 157 species of non-avian theropods, fossil birds and living birds. We show that relative olfactory bulb size increased during non-avian maniraptoriform evolution, remained stable across the non-avian theropod/bird transition, and increased during basal bird and early neornithine evolution. From early neornithines through a major part of neornithine evolution, the relative size of the olfactory bulbs remained stable before decreasing in derived neoavian clades. Our results show that, rather than decreasing, the importance of olfaction actually increased during early bird evolution, representing a previously unrecognized sensory enhancement. The relatively larger olfactory bulbs of earliest neornithines, compared with those of basal birds, may have endowed neornithines with improved olfaction for more effective foraging or navigation skills, which in turn may have been a factor allowing them to survive the end-Cretaceous mass extinction.

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Figures

Figure 1.

Figure 1.

Virtual brain endocast of Lithornis plebius, (a) in left lateral and (b) dorsal view, showing the location of the olfactory bulbs and cerebral hemispheres. The greatest linear dimension of the olfactory bulb and cerebral hemisphere, regardless of orientation, was used to calculate olfactory ratios (only rostrocaudal dimensions illustrated). Red features represent blood vessels, yellow features represent cranial nerves. Scale bar, 5 mm. Inset (not to scale) shows the position of the brain endocast within the skull of Lithornis promiscuus.

Figure 2.

Figure 2.

Plot of log-transformed olfactory ratio versus log-transformed body mass in avian and non-avian theropods. No significant correlation is observed between olfactory ratio and body mass among birds when phylogeny is considered (_r_2 = 0.009, p = 0.26). In contrast, a significant positive correlation is observed between olfactory ratio and body mass among non-avian theropods (_r_2 = 0.8, p < 1.27e − 7), indicating that olfactory ratios increase with body mass among non-avian theropods. The non-avian theropod regression (solid black line) and its extrapolation (black dashed line) bisect the distribution of olfactory ratios for birds. The majority of neornithine species basal to the common ancestor of Charadriiformes and Passeriformes have higher olfactory ratios than more derived taxa. Most basal birds fall near the non-avian theropod regression. The fossil diving bird Hesperornis plots near the extant divers Gavia immer (loon, G) and Pygoscelis adeliae (Adelie penguin, P). The error associated with Hesperornis reflects the uncertainty of its cerebral hemisphere length (see §3). The dromaeosaurid Bambiraptor (B) plots near Cathartes aura (turkey vulture, open circle) and Phoebastria nigripes (black-footed albatross, solid circle). The extinct palaeognath Lithornis (L) has high olfactory ratios. Green diamonds, dromaeosaurids; green squares, tyrannosaurids; green triangles, allosauroids; green stars, ceratosaurs; green circles, ornithomimosaurs; inverted green triangle, Citipati; green crosses, Dilong and Troodon; red circle, Archaeopteryx; red triangle, Confuciusornis; red cross, Ichthyornis; red diamond, Hesperornis; black circles, neornithines basal to charadriiform–passeriform common ancestor (based on molecular phylogeny); white circles, neornithines more derived than charadriiform–passeriform common ancestor (based on molecular phylogeny). Dashed grey lines represent the 95% confidence interval of the non-avian theropod regression.

Figure 3.

Figure 3.

Higher order phylogeny of Aves showing maximum-parsimony ancestral state reconstruction of olfactory ratios. (a) Molecular phylogeny based primarily on Hackett et al. [64]. (b) Morphological phylogeny based on Livezey & Zusi [65]. Major increases or decreases in olfactory ratio ancestral states are denoted with (+) and (−), respectively. Through avian evolution, major increases in olfactory ratios have occurred independently in many different lineages, primarily in clades basal to the common ancestor of Charadriiformes and Passeriformes. Significant decreases in olfactory ratios are prevalent in clades more derived than this common ancestor. Numbers between parentheses represent mean olfactory ratios for clades. See the electronic supplementary material for details.

Figure 4.

Figure 4.

Phylogeny of non-avian theropods and early birds showing maximum-parsimony ancestral state reconstruction of olfactory ratio residuals relative to the non-avian theropod regression. Residuals increase from the Maniraptoriformes common ancestor (node 1) to the Eumaniraptora common ancestor (node 2). Residuals then remain constant across the non-avian theropod/bird transition, between the Eumaniraptora common ancestor (node 2) and the Pygostylia common ancestor (node 3). Within Aves, residuals increase from negative values in basal birds to strongly positive values in neornithines, indicating that olfactory ratios increase and surpass values predicted by the regression for non-avian theropods. These results reveal that olfactory capabilities improved during the evolution from non-avian theropods to modern birds. Yellow box, Aves; blue box, Neornithes. Skulls with endocasts are, from top to bottom, Majungasaurus crenatissimus, Allosaurus fragilis, Tyrannosaurus rex, Struthiomimus altus, Bambiraptor feinbergi, Archaeopteryx lithographica, Ichthyornis dispar, Lithornis sp. and Presbyornis sp. Skulls are not to scale.

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