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Smith CR, Helms Cahan S, Kemena C, Brady SG, Yang W, Bornberg-­Bauer E, Eriksson T, Gadau J, Helmkampf M, Gotzek D, Miyakawa MO, Suarez A, and Mikheyev A
How do genomes create novel phenotypes? Insights from the loss of the worker caste in ant social parasites
Mol Biol Evol, 2015

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A central goal of biology is to uncover the genetic basis for the origin of new phenotypes. A particularly effective approach is to examine the genomic architecture of species that have secondarily lost a phenotype with respect to their close relatives. In the eusocial Hymenoptera, queens and workers have divergent phenotypes that may be produced via either expression of alternative sets of caste-specific genes and pathways, or differences in expression patterns of a shared set of multi-functional genes. To distinguish between these two hypotheses, we investigated how secondary loss of the worker phenotype in workerless ant social parasites independently evolved in the myrmicine genera Pogonomyrmex and Vollenhovia impacted parasite genome evolution. We sequenced the genomes of three social parasites and their most-closely related eusocial host species, and compared gene losses in social parasites with gene expression differences between host queens and workers. Our results indicate that when a worker caste was present, virtually all annotated genes were expressed to some degree in both castes, with many shifting in queen-worker bias across developmental stages. As a result, despite >1 million years of divergence from the host lineages, the social parasites showed strikingly little evidence of gene loss, damaging mutations or shifts in selection regime resulting from loss of the worker caste. This suggests that regulatory changes within a multi-functional genome, rather than sequence differences, have played a larger role in the evolution of social parasitism, and perhaps also in the many independent gains and losses of phenotypes in the social insects.