Why Are Olfactory Systems of Different Animals So Similar?

Abstract

As we learn more about the neurobiology of olfaction, it is becoming increasingly clear that olfactory systems of animals in disparate phyla possess many striking features in common. Why? Do these features provide clues about the ways the nervous system processes olfactory information? This might be the case if these commonalities are convergent adaptations that serve similar functions, but similar features can be present in disparate animals for other reasons. For example, similar features may be present because of inheritance from a common ancestor (homology), may represent responses to similar constraints, or may be superficial or reflect strategies used by researchers studying the system. In this paper, I examine four examples of features of olfactory systems in members of different phyla: the presence of odorant binding proteins in the fluid overlying olfactory receptor neurons; the use of G protein-coupled receptors as odorant receptors; the use of a two-step pathway in the transduction of odorant signals; and the presence of glomerular neuropils in the first central target of the axons of olfactory receptor cells. I analyze data from nematodes, arthropods, molluscs, and vertebrates to investigate the phylogenetic distribution of these features, and to try to explain the presence of these features in disparate animals. Phylogenetic analyses indicate that these features are not homologous across phyla. Although these features are often interpreted as convergent adaptations, I find that alternative explanations are difficult to dismiss. In many cases, it seems that olfactory system features that are similar across phyla may reflect both responses to similar constraints and adaptations for similar tasks.

Morphology of the olfactory system in the predatory mite Phytoseiulus Persimilis

“…There is a striking similarity in several neuroanatomical and neurophysiological characters of olfactory systems in classes as diverse as Vertebrata, Insecta and Chelicerata (Hildebrand and Shepherd 1997;Strausfeld and Hildebrand 1999;Eisthen 2002;Davis 2004;Ache and Young 2005). In this study we investigate if the first olfactory neuropil of P. persimilis shares some of the characteristics that have been documented in so many species.…”

“…Each olfactory glomerulus is innervated by many olfactory receptor cells whereas the dendrites of only a few second-order neurons carry the information gathered in the glomerulus to higher centres of the brain; in Drosophila, for example,~1,300 olfactory receptor cells converge on~43 glomeruli (Lessing and Carlson 1999) and in the mouse several millions of olfactory receptor cells converge on~1,800 glomeruli (Mori et al 1999). The olfactory glomeruli are interconnected through a network of inhibitory GABAergic local interneurons that are innervated by the olfactory receptor cells and that also make recurrent connections with the second-order neurons (Hildebrand and Shepherd 1997;Strausfeld and Hildebrand 1999;Eisthen 2002;Davis 2004). The receptors act as molecular feature detectors and since an odorant may possess several molecular features it can be detected by several types of olfactory receptor cells (Wilson and Stevenson 2003).…”

From chemotaxis to the cognitive map: The function of olfaction

“…S1). Eisthen documents four convergences in the olfactory system in insects, crustaceans, nematodes, mollusks, and vertebrates: odorant binding proteins in the fluid overlying olfactory receptor (OR) neurons, G proteincoupled receptors as odorant receptors, a two-step pathway in the transduction of odorant signals, and the presence of glomerular neuropils in the first central target of the axons of OR cells (10).…”

Mas‐allatotropin in the developing antennal lobe of the sphinx moth Manduca sexta: Distribution, time course, developmental regulation, and colocalization with other neuropeptides

“…ALs of insects compare to olfactory bulbs of vertebrates by sharing their principal morphological organization into so-called olfactory glomeruli, but also by a number of basic physiological properties with respect to information processing (Hildebrand and Shepherd, 1997;Strausfeld and Hildebrand, 1999;Eisthen, 2002). Another characteristic of ALs and olfactory bulbs is the expression of a variety of neuropeptides (Smith et al, 1993;Caillol et al, 2003;Moody and Merali, 2004;Gutierrez-Mecinas et al, 2005;Schachtner et al, 2005).…”