title: How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites.
abstract: 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 multifunctional genes. To distinguish between these two hypotheses, we investigated how secondary loss of the worker phenotype in workerless ant social parasites impacted genome evolution across two independent origins of social parasitism in the ant genera Pogonomyrmex and Vollenhovia. 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. Virtually all annotated genes were expressed to some degree in both castes of the host, with most shifting in queen-worker bias across developmental stages. As a result, despite >1 My of divergence from the last common ancestor that had workers, 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 multifunctional genome, rather than sequence differences, have played a predominant role in the evolution of social parasitism, and perhaps also in the many gains and losses of phenotypes in the social insects.
authors.affiliation: Department of Biology, Earlham College crsmith.ant@gmail.com alexander.mikheyev@oist.jp.
authors.forename: Chris R
authors.initials: CR
authors.lastname: Smith
authors.affiliation: Department of Biology, University of Vermont.
authors.forename: Sara
authors.initials: S
authors.lastname: Helms Cahan
authors.affiliation: Institute for Evolution and Biodiversity, Westfälische Wilhems-Universität Münster, Münster, Germany.
authors.forename: Carsten
authors.initials: C
authors.lastname: Kemena
authors.affiliation: Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington DC.
authors.forename: Seán G
authors.initials: SG
authors.lastname: Brady
authors.affiliation: Department of Computer Science, University of Illinois Urbana-Champaign.
authors.forename: Wei
authors.initials: W
authors.lastname: Yang
authors.affiliation: Institute for Evolution and Biodiversity, Westfälische Wilhems-Universität Münster, Münster, Germany.
authors.forename: Erich
authors.initials: E
authors.lastname: Bornberg-Bauer
authors.affiliation: School of Life Sciences, Arizona State University.
authors.forename: Ti
authors.initials: T
authors.lastname: Eriksson
authors.affiliation: School of Life Sciences, Arizona State University.
authors.forename: Juergen
authors.initials: J
authors.lastname: Gadau
authors.affiliation: School of Life Sciences, Arizona State University.
authors.forename: Martin
authors.initials: M
authors.lastname: Helmkampf
authors.affiliation: Department of Entomology, University of Georgia Department of Animal Biology, University of Illinois Urbana-Champaign.
authors.forename: Dietrich
authors.initials: D
authors.lastname: Gotzek
authors.affiliation: Ecology and Evolution Unit, Okinawa Institute of Science and Technology, Onna, Okinawa, Japan.
authors.forename: Misato
authors.initials: M
authors.lastname: Okamoto Miyakawa
authors.affiliation: Department of Animal Biology, University of Illinois Urbana-Champaign Department of Entomology, University of Illinois Urbana-Champaign.
authors.forename: Andrew V
authors.initials: AV
authors.lastname: Suarez
authors.affiliation: Ecology and Evolution Unit, Okinawa Institute of Science and Technology, Onna, Okinawa, Japan crsmith.ant@gmail.com alexander.mikheyev@oist.jp.
authors.forename: Alexander
authors.initials: A
authors.lastname: Mikheyev
mesh_terms: D000818:Animals; D001000:Ants / Q000145:classification* / Q000235:genetics*; D001522:Behavior, Animal / Q000502:physiology*; D005075:Biological Evolution; D005260:Female; D020869:Gene Expression Profiling; D017344:Genes, Insect; D056726:Genetic Association Studies; D040481:Genome Components; D008297:Male; D012098:Reproduction / Q000235:genetics; D012641:Selection, Genetic; D012919:Social Behavior; D059467:Transcriptome
keywords: ant; caste; genome; phenotypic plasticity; social parasite