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Molecular evolution in the double-clonal longhorn crazy ant

Periodic Reporting for period 1 - MELCA (Molecular evolution in the double-clonal longhorn crazy ant)

Reporting period: 2018-01-01 to 2019-12-31

"Sex is a ubiquitous phenomenon where the reshuffling and mixing of two genomes give rise to the genetic makeup of the next generation, a process that generates novel combinations of alleles and that is central to understanding evolution. Unusual genetic systems involving mating between partners from different lineages or species have evolved multiple times in the animal kingdom. Such systems have recently been reported in several ant genera. Ants, as other Hymenoptera, are haplo-diploid. Males are haploid and develop from unfertilized eggs, whereas queen and worker females are diploid and typically develop from fertilized eggs. ""Double-clonality"" represents a peculiar deviation from this canonical system. Under this system, all workers in the colony are hybrids but reproductive individuals are not. Workers are produced by sexual reproduction, while new reproductive queens are clones of their mother and males are clones of their father. The queen and male genomes therefore evolve as separate non-recombining entities, which only interbreed to produce sterile first-generation hybrid workers. Double-clonality has been reported in four invasive species to date, namely Wasmannia auropunctata, Vollenhovia emeryi, Paratrechina longicornis and Cardiocondyla kagutsuchi and may be discovered in many additional species in the future. No theory has been formulated on genome evolution in the context of these bizarre genetic systems and empirical data are still scarce. Beyond fundamental research, having genomic resources from different localities across the invasive ranges of this widespread species can help understand how this unique reproductive system could have facilitated the spread of these species.

The longhorn crazy ant Paratrechina longicornis is a common pest and one of the most broadly dispersed ants in the world. Recent research showed that colonies from Thailand display a double-clonal mating system. The objective of the H2020 MELCA action was to investigate the consequence of “double clonal” reproduction on genome evolution in Paratrechina longicornis. Our work provides genetic resources from several invasive populations and revealed further details on how the double-clonal reproductive system operates in this species, laying a solid foundation for understanding the interplay between molecular evolution of the genome and mode of sexual reproduction."
The stay of the postdoctoral fellow at the University of Lausanne realized all the expected impacts of the action in terms of training. The fellow became proficient in the field of genomics through workshops, hands-on experience, and guidance from the researchers of the University of Lausanne. He gained new laboratory and bioinformatics techniques to study genome evolution.

The action provided further details into the double-clonal mating system of the longhorn crazy ant Paratrechina longicornis from phylogeographic, behavioral and genetic aspects. We established P. longicornis as a laboratory model for studying genome evolution. We generated genetic resources to understand how the genomes of queens and males evolved under “double-clonality”. Our analyses revealed that “double-clonality” allows the maintenance of two highly divergent queen and male genomes in this P. longicornis. All populations surveyed were found to have a “double-clonal” genetic system. Queens and males sampled throughout the invasive range of the species belonged to two divergent lineages and all genotyped workers appeared hybrids of these two genetic lineages. These results suggest that gene mixing is not occurring anymore in this species.
The action contributed to the establishment of the longhorn crazy ant Paratrechina longicornis as a new model to study the impact of non-canonical reproductive systems on genome evolution. Under this system, males and females have independent genomes which come in a union in non-reproductive workers. Conflict and cooperation of genomic entities manifested in such systems would provide important and generalizable insight for the evolution of genomes in canonical systems. Furthermore, the potential link between the double clonal system and invasiveness of several ant species that have caused substantial economic and ecological damages makes our work especially valuable in providing guidelines to better control and manage such invasive species.
Paratrechina longicornis
"The ""double-clonal"" system of the longhorn crazy ant"