The genome of the leaf-cutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming

Abstract

We present a high-quality (>100× depth) Illumina genome sequence of the leaf-cutting ant Acromyrmex echinatior, a model species for symbiosis and reproductive conflict studies. We compare this genome with three previously sequenced genomes of ants from different subfamilies and focus our analyses on aspects of the genome likely to be associated with known evolutionary changes. The first is the specialized fungal diet of A. echinatior, where we find gene loss in the ant's arginine synthesis pathway, loss of detoxification genes, and expansion of a group of peptidase proteins. One of these is a unique ant-derived contribution to the fecal fluid, which otherwise consists of "garden manuring" fungal enzymes that are unaffected by ant digestion. The second is multiple mating of queens and ejaculate competition, which may be associated with a greatly expanded nardilysin-like peptidase gene family. The third is sex determination, where we could identify only a single homolog of the feminizer gene. As other ants and the honeybee have duplications of this gene, we hypothesize that this may partly explain the frequent production of diploid male larvae in A. echinatior. The fourth is the evolution of eusociality, where we find a highly conserved ant-specific profile of neuropeptide genes that may be related to caste determination. These first analyses of the A. echinatior genome indicate that considerable genetic changes are likely to have accompanied the transition from hunter-gathering to agricultural food production 50 million years ago, and the transition from single to multiple queen mating 10 million years ago.

Figure 1.

The leafcutter ant A. echinatior and annotation of its protein-coding genes. (A) A winged male of the Panamanian leaf-cutting ant A. echinatior in the fungus garden that is maintained by his major- and minor-worker sisters. (B) The total of 17,278 annotated protein-coding genes as obtained from de novo predictions, GLEAN acceptance, homology (to C. floridanus, H. saltator, A. mellifera, N. vitripennis, D. melanogaster, C. elegans, or H. sapiens) and transcriptome evidence. (Photo courtesy of David R. Nash © 2010.)

Figure 2.

Missing genes in the arginine biosynthesis pathway. The specific loss in A. echinatior of two genes that encode enzymes catalyzing two consecutive (final) steps in the biosynthesis of the amino acid arginine. Enzymes are denoted by purple boxes with the EC numbers inside. Pale purple boxes with dashed red borders indicate the two lost or pseudogenized genes.

Figure 3.

Peptidase expansions in the genome of A. echinatior. (A) Expansion of the M16 peptidase gene family with the insulin degrading enzyme, present in one or two copies in all investigated insect genomes (below dotted line), and nardilysin genes (above dotted line). The A. echinatior genes in each group are highlighted in yellow. Bootstrap support values >60% are given. (B) Expansion of the M14 peptidase gene family, with a dotted line separating two subfamilies. The A. echinatior genes are highlighted in yellow. Bootstrap support values >60% are given. Phum was included to increase resolution of this tree. Species (A. echinatior: Aech; H. saltator: Hsal; C. floridanus: Cflo; S. invicta: Sinv; A. mellifera: Amel; D. melanogaster: Dmel; N. vitripennis: Nvit; Pediculus humanus: Phum) and GenBank ID are given for each sequence.