Draft genome of the globally widespread and invasive Argentine ant ( Linepithema humile )

Abstract

Ants are some of the most abundant and familiar animals on Earth, and they play vital roles in most terrestrial ecosystems. Although all ants are eusocial, and display a variety of complex and fascinating behaviors, few genomic resources exist for them. Here, we report the draft genome sequence of a particularly widespread and well-studied species, the invasive Argentine ant ( Linepithema humile ), which was accomplished using a combination of 454 (Roche) and Illumina sequencing and community-based funding rather than federal grant support. Manual annotation of >1,000 genes from a variety of different gene families and functional classes reveals unique features of the Argentine ant's biology, as well as similarities to Apis mellifera and Nasonia vitripennis . Distinctive features of the Argentine ant genome include remarkable expansions of gustatory (116 genes) and odorant receptors (367 genes), an abundance of cytochrome P450 genes (>110), lineage-specific expansions of yellow/major royal jelly proteins and desaturases, and complete CpG DNA methylation and RNAi toolkits. The Argentine ant genome contains fewer immune genes than Drosophila and Tribolium , which may reflect the prominent role played by behavioral and chemical suppression of pathogens. Analysis of the ratio of observed to expected CpG nucleotides for genes in the reproductive development and apoptosis pathways suggests higher levels of methylation than in the genome overall. The resources provided by this genome sequence will offer an abundance of tools for researchers seeking to illuminate the fascinating biology of this emerging model organism.

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].…”

“…Although little is known about the role of specific desaturase genes in ant CHC production, in Drosophila, the desat1 gene is known to play a role in alkene biosynthesis [30,31]. In three of the sequenced ant genomes, annotation revealed 11-33 complete or fragmentary D9 desaturase genes [6][7][8]. Of these, one gene in both Atta cephalotes and Pogonomyrmex barbatus was identified as a clear orthologue of the Drosophila desat1 gene, and two such orthologues were discovered in Linepithema humile (the Argentine ant).…”

“…This is mostly clearly exemplified in the number of odourant receptor genes (Ors) that occur in the ant genomes: 399 in P. barbatus (55 of which are apparent pseudogenes) [7], 337 in L. humile (30 pseudogenes) [8], 377 (30 pseudogenes) in Harpegnathos saltator [37] and 407 (55 pseudogenes) in Camponotus floridanus [37]. For comparison, the genome of the honeybee, Apis mellifera, contains only 174 Or genes (11 pseudogenes) [38], and the jewel wasp, Nasonia vitripennis has 301 (76 pseudogenes) [39].…”

“…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]. Consistent with the use of these receptors for colonymate recognition, recent transcriptomic analysis of C. floridanus and H. saltator has revealed that the vast majority of these genes are expressed at higher levels in (female) workers, who display colonymate rsbl.royalsocietypublishing.org Biol Lett 9: 20130416 recognition behaviours, but not in males, who do not perform colonymate recognition [37].…”

“…Draft genome sequences have been published for a number of eusocial insects, including seven ant species [6][7][8][9][10][11], revealing myriad candidate genes for signal production and signal perception in colonymate recognition systems. At the same time, functional genetic tools offer powerful approaches to test hypotheses about the structure and function of recognition systems.…”