Speaker
Description
The cell-type specific pattern of odorant receptor (Or) expression, paired with their high rates of duplication, raises the question: How are the genetic origins of new Ors “coordinated” with the development of olfactory sensory neurons (OSN) so that they are uniquely expressed? To answer this question, we need to identify newly evolved Or genes and investigate how they have acquired their OSN-specific expression. We use the most duplicated/deleted Or subfamily in the D. melanogaster species group - the Or67a subfamily - as our experimental system. Our evolutionary analyses revealed that this subfamily is notable not only for its extensive copy number but also for containing jumping genes that have recurrently seeded new Or67a members over the flies’ main chromosomes. Several Or67a duplicates have experienced adaptive protein changes, with in vivo electrophysiological recordings substantiating their quick functional diversification. Contrary to the standard “one receptor-one neuron” expression pattern, we found that most Or67a duplicates are co-expressed with one or more Or67a copies in the same OSN population. However, despite co-expression being the dominant pattern, we also identified two instances of Or67a duplicates that have “escaped” co-expression and evolved distinct OSN expression. Using a combination of in situ hybridization and single nuclei RNA-seq experiments in D. suzukii and closely-related species, we discovered that these two Or67a copies have gained expression in preexisting neuron populations, having replaced their previous Ors. Our data suggest a model of Or-OSN evolution in which co-expression is often the first step of peripheral diversification. While co-expression may occasionally be adaptive, we suspect that it is frequently be transient, reflecting the contingent and opportunistic nature of evolutionary change. Our results also suggest that Or replacement outpaces the evolution of OSN, highlighting limitations in defining these cell-types based on their receptors alone.
