Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator

Abstract

The organized societies of ants include short-lived worker castes displaying specialized behavior and morphology and long-lived queens dedicated to reproduction. We sequenced and compared the genomes of two socially divergent ant species: Camponotus floridanus and Harpegnathos saltator. Both genomes contained high amounts of CpG, despite the presence of DNA methylation, which in non-Hymenoptera correlates with CpG depletion. Comparison of gene expression in different castes identified up-regulation of telomerase and sirtuin deacetylases in longer-lived H. saltator reproductives, caste-specific expression of microRNAs and SMYD histone methyltransferases, and differential regulation of genes implicated in neuronal function and chemical communication. Our findings provide clues on the molecular differences between castes in these two ants and establish a new experimental model to study epigenetics in aging and behavior.

Figure 1

Ant proteome. Phylogenetic tree based on maximum likelihood analyses of a concatenated alignment of single-copy proteins (left), and orthology relationships in multiple insects (right), using H. sapiens as outgroup. The scale bar indicates 0.1 substitution/site.

Figure 2

Small RNA-seq and miRNA. (A) Classification of small RNA-seq reads from H. saltator gamergates (left) or workers (right). (B–D) Caste- and stage-specific expression of miRNAs in C. floridanus (B and D) and H. saltator (C). White bars represent qRT-PCR and indicate the mean + SEM, n=7. Black bars are scaled on the right y axis and indicate reads per million (RPM).

Figure 3

Aging pathways in H. saltator. (A) TERT transcript levels in egg, workers, and gamergates. RPKM, read per kilobase per million reads. (B) Transcript levels in gamergates vs. workers for SIRT1 and SIRT6 orthologues. White bars, qRT-PCR mean + SEM, n=7. Black bars, RNA-seq.

Figure 4

Potential epigenetic pathways in ants. (A) Ratio of 5-methyl-cytosine/total DNA in C. floridanus and H. saltator, as determined by dot blot densitometry. Bars show mean + SEM; p value is from repeated measurement ANOVA (Wilks’ lambda = 0.52), n=10. (B–C) Quantification of Hsal_14941 (B) and Hsal_08142 (C) expression in different developmental stages and castes. White bars, qRT-PCR mean + SEM, n=7. Black bars, RNA-seq.

Figure 5

Neurobiology and communication. (A) Quantification of 8 “GO:neurotransmitter binding” genes in head and thorax from major and minor workers in C. floridanus. White bars, qRT-PCR mean + SEM, n=9. Black bars, RNA-seq. (B) Quantification of fatty acid biosynthesis genes in H. saltator gamergates compared to non-reproductive workers. White bars, qRT-PCR mean + SEM, n=7. Black bars, RNA-seq.