Phylogenetic and Transcriptomic Analysis of Chemosensory Receptors in a Pair of Divergent Ant Species Reveals Sex-Specific Signatures of Odor Coding

Abstract

Ants are a highly successful family of insects that thrive in a variety of habitats across the world. Perhaps their best-known features are complex social organization and strict division of labor, separating reproduction from the day-to-day maintenance and care of the colony, as well as strict discrimination against foreign individuals. Since these social characteristics in ants are thought to be mediated by semiochemicals, a thorough analysis of these signals, and the receptors that detect them, is critical in revealing mechanisms that lead to stereotypic behaviors. To address these questions, we have defined and characterized the major chemoreceptor families in a pair of behaviorally and evolutionarily distinct ant species, Camponotus floridanus and Harpegnathos saltator. Through comprehensive re-annotation, we show that these ant species harbor some of the largest yet known repertoires of odorant receptors (Ors) among insects, as well as a more modest number of gustatory receptors (Grs) and variant ionotropic glutamate receptors (Irs). Our phylogenetic analyses further demonstrate remarkably rapid gains and losses of ant Ors, while Grs and Irs have also experienced birth-and-death evolution to different degrees. In addition, comparisons of antennal transcriptomes between sexes identify many chemoreceptors that are differentially expressed between males and females and between species. We have also revealed an agonist for a worker-enriched OR from C. floridanus, representing the first case of a heterologously characterized ant tuning Or. Collectively, our analysis reveals a large number of ant chemoreceptors exhibiting patterns of differential expression and evolution consistent with sex/species-specific functions. These differentially expressed genes are likely associated with sex-based differences, as well as the radically different social lifestyles observed between C. floridanus and H. saltator, and thus are targets for further functional characterization. Our findings represent an important advance toward understanding the molecular basis of social interactions and the differential chemical ecologies among ant species.

Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

“…Overall, the elevated number of desaturase genes and their variability in sequence and expression might reflect increased demand for chemical signal diversity used in ant social communication. Consistent with this, gene families presumably involved in the perception of these signals (e.g., olfactory receptors) (Smith et al 2011b;Zhou et al 2012) exhibit similar expansions.…”

Molecular traces of alternative social organization in a termite genome

“…Tables 21-24) identified 336 genes in Z. nevadensis, of which 280 were potentially functional. While this number is much higher than is typically observed in insects, it is intermediate to that of bees and ants 7,27,28 , reflecting the central role of odorants in eusociality. While the total gene numbers are comparable, their distribution within gene families diverged greatly from what has been observed in Hymenoptera.…”

“…While the total gene numbers are comparable, their distribution within gene families diverged greatly from what has been observed in Hymenoptera. Odorant receptors (ORs), which confer most of the specificity and sensitivity of insect olfaction, are expanded in ants (344-400) 7,9,27 and honey bees (163) 28 , but only 69 (63 intact) were found in Z. nevadensis. While the gustatory receptor (GR) repertoire in Z. nevadensis of 87 genes (80 intact) is comparable to that of other social insects (range 10-97 copies), Z. nevadensis shows lineage-specific expansions in different gene subfamilies compared with eusocial Hymenoptera such as the carbon dioxide receptors 7,27,28 Ny2 FS2 FS3 MS1 MS2 MS3 FA FPI FNI1 FNI2 FNI3 FNR1 FNR2 MA MPI MNI1 MNI2 MNR1 MNR2 MNR3 FS1 E W1 W2 Ny1 Ny2 FS2 FS3 MS1 MS2 MS3 FA FPI FNI1 FNI2 FNI3 FNR1 FNR2 MA MPI MNI1 MNI2 MNR1 MNR2 MNR3 Relative expression of genes that showed upregulated gene expression in male reproductives and (a) that occurred within Z. nevadensis-specific subtrees in each gene tree family and that belonged to significantly expanded gene families and (b) that belonged to a gene family with the largest known copy number among insects, but that is not significantly expanded.…”

“…Hymenoptera species 7,27,28 . The termite IR repertoire includes 13 conserved members present throughout insects, and expansions in three subfamilies of 17, 48 and 66 genes, respectively (corresponding to two domain architectures in Table 1).…”

Dissecting ant recognition systems in the age of genomics

“…In part, these differences represent a loss of Or genes in A. mellifera and N. vitripennis, but birth-and-death analysis also suggests that each of these four ant lineages has also experienced net expansions in Or gene number [37]. Interestingly, one Or gene subfamily, characterized by a 9-exon gene structure, has undergone a remarkable diversification in ants, hinting that some of these genes may code for the colonymate recognition cue receptors [7,8,37]. In the Argentine ant, for example, this subfamily has expanded to 136 genes [8], and the red harvester ant (P. barbatus) genome harbours 169 9-exon Or genes [7].…”