The genome of the fire ant Solenopsis invicta

Abstract

Ants have evolved very complex societies and are key ecosystem members. Some ants, such as the fire ant Solenopsis invicta, are also major pests. Here, we present a draft genome of S. invicta, assembled from Roche 454 and Illumina sequencing reads obtained from a focal haploid male and his brothers. We used comparative genomic methods to obtain insight into the unique features of the S. invicta genome. For example, we found that this genome harbors four adjacent copies of vitellogenin. A phylogenetic analysis revealed that an ancestral vitellogenin gene first underwent a duplication that was followed by possibly independent duplications of each of the daughter vitellogenins. The vitellogenin genes have undergone subfunctionalization with queen- and worker-specific expression, possibly reflecting differential selection acting on the queen and worker castes. Additionally, we identified more than 400 putative olfactory receptors of which at least 297 are intact. This represents the largest repertoire reported so far in insects. S. invicta also harbors an expansion of a specific family of lipid-processing genes, two putative orthologs to the transformer/feminizer sex differentiation gene, a functional DNA methylation system, and a single putative telomerase ortholog. EST data indicate that this S. invicta telomerase ortholog has at least four spliceforms that differ in their use of two sets of mutually exclusive exons. Some of these and other unique aspects of the fire ant genome are likely linked to the complex social behavior of this species.

Fig. 1.

(A) S. invicta males (larger, with wings) depart on mating flight while workers (smaller, wingless) patrol (photo by Yannick Wurm). (B) A fire ant researcher was stung by his study subject (photo by Daniel P. Wojcik, US Department of Agriculture Agricultural Research Service).

Fig. 2.

Taxonomic distribution of best blastp hits of S. invicta proteins to the nonredundant (nr) protein database (E < 10⁻⁵). Results were first plotted using MEGAN software (22) and then branches with fewer than 20 hits were removed, branch lengths were reduced for compactness, and tree topology was adjusted to reflect consensus phylogenies (23, 24).

Fig. 3.

S. invicta vitellogenins. (A) Four vitellogenins are located within a single 40,000-bp region of the S. invicta genome. (B) Parsimony tree of known hymenopteran vitellogenin protein sequences suggests that two rounds of vitellogenin duplication occurred after the split between ants and other hymenopterans including bees and wasps. (C) Quantitative RT-PCR of the four putative S. invicta vitellogenins on whole bodies of major workers (W) and mated queens (Q) (n = 10). The y axis indicates mRNA concentrations for the different vitellogenins. Values depicted by each bar are shown below the x-axis labels. Error bars represent SEs. Expression differences between queens and workers were significant (Bonferroni-corrected two-tailed t tests: *P < 0.05, ***P < 10⁻¹⁰).