How do genomes create novel phenotypes Insights from the loss of the worker caste in ant social parasites

Chris R. Smith, Sara Helms Cahan, Carsten Kemena, Seán G. Brady, Wei Yang, Erich Bornberg-Bauer, Ti Eriksson, Juergen Gadau, Martin Helmkampf, Dietrich Gotzek, Misato Okamoto Miyakawa, Andrew V. Suarez, Alexander Mikheyev

Research output: Contribution to journalArticle

22 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)2919-2931
Number of pages13
JournalMolecular biology and evolution
Volume32
Issue number11
DOIs
StatePublished - Nov 2015

Keywords

  • ant
  • caste
  • genome
  • phenotypic plasticity
  • social parasite

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

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    Smith, C. R., Helms Cahan, S., Kemena, C., Brady, S. G., Yang, W., Bornberg-Bauer, E., Eriksson, T., Gadau, J., Helmkampf, M., Gotzek, D., Okamoto Miyakawa, M., Suarez, A. V., & Mikheyev, A. (2015). How do genomes create novel phenotypes Insights from the loss of the worker caste in ant social parasites. Molecular biology and evolution, 32(11), 2919-2931. https://doi.org/10.1093/molbev/msv165