Genomics of social organisation in the ant, Leptothorax acervorum

Geographically isolated populations of L. acervorum are polymorphic for the number of reproductive queens in multi-queen colonies. Either all queens reproduce (polygyny) or worker aggression limits reproduction to one queen (functional monogyny). Previous work using pooled RAD-seq data suggests that a contiguous region of ~6 Mb is involved in determining social phenotype. I sequenced, assembled, and annotated the first draft assemblies of the L. acervorum genome. Two complementary analyses were employed to identify signatures of selection associated with social organisation using whole-genome resequencing data. An FST outlier analysis identified genomic regions differentiated between populations with alternative social organisation. Haplotype homozygosity statistics identified regions showing evidence of recent or ongoing selective sweeps driving divergence between populations with alternative social organisation.

These analyses confirm and expand on previous work by showing that a large (<= 16 Mb) and likely contiguous region of the L. acervorum genome is differentiated along lines of social organisation. This region shares homology with Solenopsis invicta chromosome 2 and contains genes with functions known to be important in regulating social behaviour. Two isolated peaks of differentiation were detected in scaffolds which bear no homology with S. invicta chromosome 2, one of which intersects with a homologue of Neuroligin-4, a gene associated with autism spectrum disorder in humans. This suggests that social organisation in L. acervorum is polygenic, and that one region involved may be the fourth social chromosome discovered in ants. Further, the mitochondrial genome of L. acervorum has been used to analyse of the phylogeography of the Formicoxenus genus-group, showing range expansion in the last 0.5 MA originated from within the Iberian peninsula.

By identifying and exploring the genomic architecture underpinning polymorphic social organisation in L. acervorum, this work highlights the power of genomic techniques to uncover the genetic basis of complex phenotypes in non-model organisms.