Periodic Reporting for period 1 - ConvergeAnt (Uncovering the genomic underpinnings of the convergent evolution of a major social trait)
Reporting period: 2019-10-04 to 2021-10-03
Ant colonies consist of specialised individuals performing distinct tasks, such that queens and males reproduce, while the workers care for the queen’s offspring, forage and defend the colony. The ancestral ant colony most certainly comprised a single queen and highly related workers. Over time, however, the more than 20,000 described extant ant species have evolved a remarkable diversity of social lifestyles and today occupy most terrestrial habitats. The sophisticated social structures of ant colonies largely depend on a fundamental trait that varies broadly across species: the number of reproductive queens in a colony. Notably, socially polymorphic species such as the red imported fire ant Solenopsis invicta have evolved the capability of founding colonies with either one or multiple reproductive queens. Colony queen number correlates with several other traits. For example, multiple-queen colonies have longer lifespans and queens with smaller body size and decreased fecundity relative to single-queen colonies. Previous work revealed that a supergene – a set of tightly linked genes inherited as a unit – controls the stable polymorphism in queen number in S. invicta. Yet, it remains unclear how supergenes might have shaped the evolution of other socially polymorphic ant species.
The overall objectives of the project were to trace the evolutionary origin of genetic features underlying the polymorphism in queen number across ant species, evaluate changes in gene family size and content across such species and identify convergent patterns of selection on coding sequences. The prevalent understanding of social organisation in ants postulated that environmental factors control the number of queens in a colony. Limited genomic research, however, previously revealed that certain ant species independently evolved supergenes controlling the polymorphism in queen number. For example, colonies of S. invicta with a single queen include members carrying only the Social B (SB) supergene haplotype on the ‘social chromosome’ (chromosome 16). Colonies of S. invicta with multiple queens, however, contain the alternative Sb haplotype in heterozygous (SB/Sb) queens and workers. In this MSCA-IF project, we conducted a comparative genomic study to reveal the origin and evolution of the fire ant supergene. Specifically, we applied population genetics and phylogenetic methods to reveal the origin and subsequent evolution of a supergene across multiple species of Solenopsis fire ants, assess whether specific gene families consistently associate with supergene haplotypes and identify patterns of positive selection. Challenging previous studies, the findings of this study revealed that the supergene variant Sb originated in S. invicta and then introgressed into other Solenopsis species.
The overall objectives of the project were to trace the evolutionary origin of genetic features underlying the polymorphism in queen number across ant species, evaluate changes in gene family size and content across such species and identify convergent patterns of selection on coding sequences. The prevalent understanding of social organisation in ants postulated that environmental factors control the number of queens in a colony. Limited genomic research, however, previously revealed that certain ant species independently evolved supergenes controlling the polymorphism in queen number. For example, colonies of S. invicta with a single queen include members carrying only the Social B (SB) supergene haplotype on the ‘social chromosome’ (chromosome 16). Colonies of S. invicta with multiple queens, however, contain the alternative Sb haplotype in heterozygous (SB/Sb) queens and workers. In this MSCA-IF project, we conducted a comparative genomic study to reveal the origin and evolution of the fire ant supergene. Specifically, we applied population genetics and phylogenetic methods to reveal the origin and subsequent evolution of a supergene across multiple species of Solenopsis fire ants, assess whether specific gene families consistently associate with supergene haplotypes and identify patterns of positive selection. Challenging previous studies, the findings of this study revealed that the supergene variant Sb originated in S. invicta and then introgressed into other Solenopsis species.
We conducted a comparative genomic analysis of Solenopsis fire ants to reveal the evolutionary history of a supergene variant responsible for the social polymorphism in queen number. In Solenopsis ants, some species have the capability to establish colonies comprising either one or multiple queens. We analysed a large set of genome-wide variants from 368 Solenopsis samples, including primarily haploid males of S. invicta and S. richteri. We performed phylogenomic analyses of concatenated single-nucleotide polymorphisms from a core set of single-copy genes located either along the supergene or elsewhere in the genome. The resulting phylogenetic trees revealed conflicting evolutionary histories between the supergene and the rest of the genome. Notably, the supergene phylogeny indicated that the Sb haplotype originated in S. invicta and then spread into other Solenopsis species through repeated backcrossing of hybrids with the parental species. Moreover, we further examined this finding that the Sb haplotype introgressed between Solenopsis species by applying a phylogeny-based using branch lengths of triplet subtrees and found significant support for the exchange of the Sb haplotype between species. This MSCA-IF project delivered new knowledge regarding its general goal of discovering genomic features associated with a social polymorphism in colony queen number across ant species. The results of these analyses substantially contributed to the general conclusions published in a recent paper (Nature Communications 13: 1180). The Fellow attended and participated in the organizing of the IUSSI NWES Winter Meeting 2020.
Our project investigated the genomic features that underpin the evolution of socially polymorphic ant species. The fundamental understanding of social organisation in ants previously assumed that the environment determines the number of queens in a colony. However, genomic data indicated that some ant lineages independently evolved supergenes controlling the polymorphism in queen number. Colonies of S. invicta with a single queen include members carrying only the Social B (SB) supergene haplotype. In contrast, colonies of S. invicta with multiple queens contain queens and workers carrying the alternative Sb haplotype in heterozygous genotypes (SB/Sb). In this MSCA-IF project, we performed a comparative genomic study to uncover the origin and evolution of the fire ant supergene. Specifically, we applied population genetics and phylogenetic methods to trace the evolutionary routes of a supergene across multiple species of Solenopsis fire ants. Phylogenetic analyses of genetic variants indicated that the Sb haplotype originated in S. invicta and then introgressed into other Solenopsis species. We further examined this finding by analysing the branch lengths of triplet subtrees and found significant support for the exchange of the Sb haplotype between species. These findings challenge the established understanding of how the genomic architecture underlying the polymorphism in queen number evolved in Solenopsis fire ants.
In addition to a published scientific article, we have one more manuscript under development. In this ongoing study, we aim to reveal protein-coding sequence changes linked to supergene haplotypes controlling ant social organisation. For this purpose, we have produced a set of genetic variants based on a new chromosome-level genome assembly of S. invicta. We have also generated an original gene set for this genome assembly using computational methods to predict genes from known transcripts and proteins. Moreover, we have mapped the 368 Solenopsis samples to the new genome assembly to generate a comprehensive set of genetic variants. Our continuing work intends to integrate the new genetic variants and gene set to evaluate whether protein-coding sequences harbour genetic changes consistently associated with supergene haplotypes across focal Solenopsis species. The findings of this project indicate that a complex trait such as the polymorphism in queen number can originate through a supergene variant able to cross species boundaries.
In addition to a published scientific article, we have one more manuscript under development. In this ongoing study, we aim to reveal protein-coding sequence changes linked to supergene haplotypes controlling ant social organisation. For this purpose, we have produced a set of genetic variants based on a new chromosome-level genome assembly of S. invicta. We have also generated an original gene set for this genome assembly using computational methods to predict genes from known transcripts and proteins. Moreover, we have mapped the 368 Solenopsis samples to the new genome assembly to generate a comprehensive set of genetic variants. Our continuing work intends to integrate the new genetic variants and gene set to evaluate whether protein-coding sequences harbour genetic changes consistently associated with supergene haplotypes across focal Solenopsis species. The findings of this project indicate that a complex trait such as the polymorphism in queen number can originate through a supergene variant able to cross species boundaries.