Among animals, insects are renowned for their extraordinary uses of olfactory signals in diverse behaviors. Furthermore, insects conservatively represent at least 50% of the known species on the planet, a fact suggesting their olfactory systems have become enormously divergent in complexity and application, while remaining similar in underlying mechanism. We can thus predict to find the homologues of olfactory genes throughout the insect group, and further predict that olfactory based behaviors have diverged in part through mutation or duplication and subsequent natural selection of olfactory genes. Since the natural selection agent in most cases relates to the behavior that olfaction is supporting, studying the evolution of olfactory related genes offers the opportunity to study the evolution of such olfactory based behaviors as food or host selection and sex.
We can consider three groups of olfactory specific genes, classified by their degree of duplication within a given species.
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Group 1 |
Genes expressing in association with all olfactory neurons. |
Example: transductory proteins such as olfactory specific G-proteins or ion channels. |
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Group 2 |
Genes expressing in association with large subsets of olfactory neurons. |
Example: Odorant Binding Proteins. |
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Group 3 |
Genes whose expression defines the phenotypes of individual olfactory neurons. |
Example: Odor Receptors. |
Group 3 olfactory genes... Of these three groups, genes encoding odor receptors (ORs) are clearly the most diverse, and are enormously interesting from functional and developmental / gene regulatory perspectives. However, while it is easy to employ phylogenetic analysis to group these genes in classes that may relate to function, their large numbers make it nearly impossible to distinguish between parologous (divergent) vs. orthologous (convergent) pairs when comparing two species. ORs are thus arguably awkward to use in an evolutionary analysis of behavior, since it is difficult to determine with any confidence which pairs derived from common gene duplication events. The exception to this would be class comparisons between OR genes encoding pheromone vs. general odorant receptors, and possibly between OR genes encoding receptors functioning in aquatic vs. terrestrial environments. Such genes are known for certain vertebrates, but are as yet unavailable for insects.
Group 1 olfactory genes... At the other extreme, olfactory specific transductory genes that are olfactory specific clearly permit the analysis of duplications which gave rise to olfactory tissues. However, the common distribution of these gene products among all classes of olfactory neurons and the interactions of their products with common cellular processes suggests that a phylogenetic analysis of such genes is not likely to shed much light on either the evolution or mechanisms of chemoreception as they relate to specific behaviors.
Group 2 olfactory genes... OBPs. In the middle, the group of genes encoding Odorant Binding Proteins (OBPs) are well suited to an evolutionary analysis of olfactory based behavior. OBPs are small water soluble proteins residing in olfactory sensilla within the fluid that baths the olfactory neurons. OBPs are the initial biochemical step in odor reception, transporting odor molecules to the receptor proteins residing in the neuronal membranes. Furthermore, OBPs are likely a terrestrial adaptation, originally recruited to help solubilize the relatively aqueous insoluble volatile molecules used as odorant signals in terrestrial environments.
First of all, the number of OBP genes per individual is a managable (<10). Different OBPs express in association with olfactory neurons having decidedly different behavioral roles, including mate (sex) and food selection. Second, members of the insect OBP family have been identified from several insect orders, indicating OBPs are wide spread olfactory markers within the insects. Third, OBP proteins are encoded by relatively small mRNAs (800-1600 bases) which comprise the most abundant mRNAs found in antennal tissue. It is thus easy to clone OBP sequences from a species of choice, and relatively easy to obtain a representational sampling of the OBPs present in a given species. Phylogenetic analysis indicates that many of these OBPs show clear monophyletic origins within their groupings, but indicate a clear need for more sequences from more species in order to better understand the parologous relationships of these proteins.
Our goal is to clarify different OBP lineages and relate these lineages to the specific behavioral function of the olfactory neurons with which a given lineage expresses in a given species of insect. For one thing, we would like to clarify whether diverse OBPs derived from a single duplication event establishing a broad but monophyletic family (homologous), or multiple independent duplications producing lineages that are converging due to related function (homoplasic). Furthermore, this phylogenetic approach allows us to predict physiological and behavioral functions, a prediction that can be experimentally tested or verified.
For example, we know that one lineage of lepidopteran OBPs known as Pheromone Binding Proteins (PBPs) associate with the sex-pheromone sensitive neurons of male antenna. PBPs are also observed expressing in subsets of olfactory sensilla in female antennae, permitting the hypothesis that these female sensilla respond to sex-pheromone or a component of the sex-pheromone. In another example (see Larry Zweibel's work), certain female Anopheles mosquito species prefer humans as source of blood meal, while females of other Anopheles species prefer non-human animals. Also, it is females and not males that are attracted to animals for blood meals. An analysis of OBPs between species might reveal the molecular basis between human and non-human preferences in host selection, and further provide molecular markers to identify exactly which olfactory sensilla are involved in host selection. An analysis between OBPs of male and female might similarly permit the identification of the olfactory pathways involved in host selection.