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Tracing the origin of a social chromosome in the red fire ant

Final Report Summary - SOCIAL CHROMOSOME (Tracing the origin of a social chromosome in the red fire ant)

This is a comprehensive summary overview of results, conclusions and the socio-economic impacts of the project. The publishable report shall be formatted to be printed as a stand alone paper document. This report should address a wide audience, including the general public.
• Is comprehensive, and describes the work carried out to achieve the project's objectives; the main results, conclusions and their potential impact and use and any socio-economic impact of the project. Please mention any target groups such as policy makers or civil society for whom the research could be relevant.

The project SOCIAL CHROMOSOME aimed to investigate the genomic underpinnings of a social polymorphism in fire ants. While it was recently uncovered, that in fire ants a complex phenotypic innovation and major transition in sociality, i.e. from single-queen colonies to multi-queen colonies with associated behavioural, physiological and morphological differences, was related to a large structural change of majority of a chromosome, the detailed genetic characteristics, the origin and the evolutionary patterns remain unclear. The structural change was determined to be an inversion which is associated with loss of recombination throughout the same region, thus forming a supergene. This lack of recombination is likely involved in the observed genomic characteristics in this region, such as increased content of repetitive elements, accumulation of deleterious mutations, differential expression of genes located in the supergene. In addition, recent analyses suggested dramatically reduced genetic diversity in the non-recombining variant of the supergene compared to the normally recombining variant. In addition, both variants are highly differentiated.
To uncover the origin and evolution of the social chromosome we combined structural with genetic and genomic analyses using the novel BioNano Irys optical mapping technology. The results from this part of the projects helped to improve the reference sequence assembly, but more importantly, it allowed the generation of highly contiguous optical chromosomes which then were used as a basis for direct comparisons of genome structures, therefore avoiding biases related to sequence assembly. The results showed that two large inversion are shared among the non-recombining supergene variant from 3 different socially polymorphic fire ant species, suggesting that the same inversions are present since a common ancestor. Furthermore the patterns of insertions and deletion, with an excess of the former and a growth in length within the non-recombining region, suggests, that in all three species, this region is not recombining. These patterns directly provided evidence for a hallmark of early stages of supergene evolution in which a degenerative expansion is happening. Similarity between species and supergene variants in terms of presence or absence of structural variants suggested again a common single ancestor for the social chromosome. Base on molecular dating, the divergence between both form was estimated to be about one million years, older than previously thought.
In the second major part of the project, we re-sequenced the genomes of about 160 haploid males from all sampled phylogenetic groups, including at least 4 outgroup species and all ingroup species and clades, thus we assume a complete taxon sampling. From this rich dataset we were able to generate phylogenetic tree for each target locus or gene. This analysis showed that the phylogenetic relationships across these fireants is complex and that hybrids occur. Interestingly we could show that for many studied loci and genes, the non-recombining variant show a single evolutionary origin within the recombining variants, consistent with our results from the optical mapping. Inconsistencies in the phylogenetic trees are currently being investigated still. Consistently, population structuring shows higher similarity by supergene variant than by species throughout the region of the social chromosome non-recombining part. Population genetic analyses revealed, that for specific populations , the non-recombining variants can exhibit very low genetic diversity and high differentiation to the recombining variant. This is consistent with general population genetic expectations for non-recombining supergenes. Surprisingly we found high differentiation and also a substantial genetic diversity between non-recombining variants of the supergene across different populations and between species. This surprising level of diversity and differentiation suggests high levels of gene conversion or hidden recombination to be present. This would be an unexpected finding if proven true. The complex analyses involved in this part of the project are currently finalized. Altogether, our project substantially advanced our knowledge about the fire ant social chromosome system and through direct comparisons of genomic structure provides one of the first direct evidences for a hallmark of early supergene evolution. The detailed results from our population genetic analyses will then shed light on potential functional aspects involved in the formation of the two types of colony organisation. This will be the first comprehensive study of this major transition in sociality and thus is expected to reach very high impact. Our comprehensive approach with direct comparisons of optical mapping furthermore will have profound impact on a wider research community studying structural variation. Our new approach has high power to detect thus far rarely studied large structural variants and avoids biases and problems related to fragmented reference sequence assemblies. This will be particularly interesting for researchers working on non-model organisms.