Degeneration of the Olfactory Guanylyl Cyclase D Gene during Primate Evolution

Janet M Young,Hang Waters,Emily R Liman,Hans-Jürgen Fülle,Cora Dong,Leslie Vosshall

doi:10.1371/journal.pone.0000884

Janet M Young, Hang Waters + Show 4 more

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https://doi.org/10.1371/journal.pone.0000884

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Abstract

BackgroundThe mammalian olfactory system consists of several subsystems that detect specific sets of chemical cues and underlie a variety of behavioral responses. Within the main olfactory epithelium at least three distinct types of chemosensory neurons can be defined by their expression of unique sets of signal transduction components. In rodents, one set of neurons expresses the olfactory-specific guanylyl cyclase (GC)-D gene (Gucy2d, guanylyl cyclase 2d) and other cell-type specific molecules. GC-D-positive neurons project their axons to a small group of atypical “necklace” glomeruli in the olfactory bulb, some of which are activated in response to suckling in neonatal rodents and to atmospheric CO2 in adult mice. Because GC-D is a pseudogene in humans, signaling through this system appears to have been lost at some point in primate evolution.Principal FindingsHere we used a combination of bioinformatic analysis of trace-archive and genome-assembly data and sequencing of PCR-amplified genomic DNA to determine when during primate evolution the functional gene was lost. Our analysis reveals that GC-D is a pseudogene in a large number of primate species, including apes, Old World and New World monkeys and tarsier. In contrast, the gene appears intact and has evolved under purifying selection in mouse, rat, dog, lemur and bushbaby.ConclusionsThese data suggest that signaling through GC-D-expressing cells was probably compromised more than 40 million years ago, prior to the divergence of New World monkeys from Old World monkeys and apes, and thus cannot be involved in chemosensation in most primates.

Highlights

The ability to detect chemicals in the environment is vital for many species to survive and reproduce, allowing individuals to locate food, establish a territory, find mates, and avoid predation or other dangers
Our findings reinforce a general theme emerging from previous studies that have shown that many components of olfactory and vomeronasal signaling have become pseudogenes over the course of primate evolution
Inspection of anatomical specimens reveals that the accessory olfactory bulb, the brain region to which vomeronasal organ (VNO) neurons project, is absent in Old World monkeys and apes and the VNO in these species, if present, contains only non-sensory cells [3,7]

Summary

Introduction

The ability to detect chemicals in the environment is vital for many species to survive and reproduce, allowing individuals to locate food, establish a territory, find mates, and avoid predation or other dangers. The main olfactory system contains a number of subsystems, some of which might be involved in pheromone detection or in the detection of other specific environmental signals [4,5,6]. In humans the vomeronasal organ appears to be vestigial: function was probably lost prior to the divergence of OW monkeys and apes [3,7,8,9]. Whether one or more of the main olfactory subsystems might function to detect pheromones or other specific environmental signals in humans is not known. These data suggest that signaling through GC-D-expressing cells was probably compromised more than 40 million years ago, prior to the divergence of New World monkeys from Old World monkeys and apes, and cannot be involved in chemosensation in most primates

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