NASBR 2015 (North American Society for Bat Research) conference in Monterey, CA. Olfaction is a primary sense used for food detection in plant-visiting bats. Olfactory receptors are diverse family of genes that code for odorant detectors in mammals. However, the relationship between dietary specialization and olfactory receptor repertoires remains unknown. New World Leaf-nosed bats (Phyllostomidae) have evolved adaptations to exploit plant resources, and many lineages are plant specialists. Recent analyses suggest the primarily frugivorous subfamily Stenodermatinae has a distinct olfactory receptor repertoire compared to insectivorous species, but there is no work to date examining whether species that specialize on particular plant genera also have more specialized olfactory receptors. We sequenced the olfactory receptor repertoires of three species of Carollia, a bat genus that varies in its dietary specialization to the soft fruits of Piper plants. We compared the olfactory receptor repertoires and the function of orthologous receptors among Carollia species that vary in their degree of specialization on Piper. The most dedicated Piper specialist, Carollia castanea, had a unique set of olfactory receptors not shared by the two more generalist species. These unique receptors potentially enable castanea to detect its primary resource to an extent that the other species cannot. This suggests relaxed selection on receptors in species with more specialized diets, and purifying selection in more generalist species that would maintain the ability to detect a wide range of odorant molecules.
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Wake up and smell the piper! Olfactory receptor repertoires reflect dietary specialization in bats
1. Wake up and smell the Piper!
Olfactory receptor repertoires
reflect diet specialization in bats
Carollia'perspicillata'
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Mutualisms are one of the most important ecological interactions among species. Fruit-frugivore interactions, such as is described with this Carollia and piper plant both contribute to the distribution and species richness of the plants because of the frugivores role in seed dispersal, and these interactions can determine the diversity of frugivores.
One of the most well-known examples of this diversity is within the New World Leaf-nosed bats, Phyllostomidae.
Remarkable number of bat-plant interactions within phyllostomids and their diversity allow us to compare sensory adaptations finding different food resources.
An important aspect of bat plant mutualism is that the bat has to find the fruit.
Most bats use echolocation and his is particularly useful for moving targets, such as insects, but the signals can get jammed and confusing in cluttered environments when a bat is looking for a stagnant fruit that may be buried under vegetation. Several behavioral assays such as the one here demonstrate bats supplementing echolocation with olfaction. The bat searches and explores the environment looking for food with its sense of smell and uses echolocation to correctly orient itself to grab the fruit.
The plants may evolve to attract their seed dispersers and pollinators by emitting strong-smelling odorants, but we also expect bats to have to machinery to find these odorant molecules of their resources.
The bat chemosensory system is composed of two systems, the vomeronasal and the main olfactory. Highlighted in red is where the main olfactory epithelium is distributed on the nasal turbinates. Within this tissue are thousands of receptors that will directly bind to speciifc odorant compounds and send to the signal to the brain to elicit a behavioral response.
The olfactory receptors are a great place to start when looking for adaptation, because they directly interact with the environmental ligand odors
However, in mammals, there are A LOT of them. They make up an average of 5% of the mammalian protein-coding genome.
Interestinly evolve in a birth-death manner, duplicating and pseudogenizing
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Today we will focus on the Carollia genus, that rely on plant resources for their food and in particular piper. Their weak bite force relative to the Stenodermatines show a specialization on soft fruits
We know carollia is distinct, but is there variation in carollia.
At the genus level, do species have comparative profiles?
Question 1: similar to niimura plot
Comparing numbers of functional and nonfunctional receptors has been a common approach to comparing olfactory repertoires, but we can further sort these receptors into different subfamilies based on there conserved membrane regions
This is a gene tree of mammalian olfactory receptors and a number of obvious divisions emerge.
Blue demonstrates Class I receptors that are receptors homologous vertebrates, while orange groups are mammalian specific. Through the birth-death process, the receptors have expanded and reduced across mammalian species.
With this classification, we can ask if certain subfamilies of receptors are more important in some species than in others.
Carollia sets up a nice system to ask if certain subfamilies reflect dietary specialization because of the continuum of piper specialization shown across the three species. Castanea almost exclusively feeds on piper while perspicillata shows a more generalist profile.
If the number of receptors relates to the number of different odorants one can detect and different subfamilies reflect different classes of ligands that receptors can bind, we might expect the number of receptors to be evenly distributed throughout the generalist species as it needs to detect a wide range of different resources, We expect a narrower diversity across families would be expected for the specialist, perhaps to better seek out piper ligands.
Does the specialist species have a unique set of receptors not shred with any other species?
To conclude, I want to summarize three points.
At the genus level, we see a large diversity in both number of receptors and receptor types.
The generalist had a more even distribution of olfactory subfamilies, but not necessarily the largest number of functional receptors.
Certain receptor subfamilies have expanded in the specialist species castanea, potentially fine-tuning its profile for targeting piper discriminating ripeness.
`Finally, I want to emphasize that we don’t know what each of these receptors bind to, but we now have a subset of potential receptors to look for adaptation within piper specialists. We can now form hypotheses about targeted receptors and their relationship with piper odorants, a goal for the future.