Social regulation of a rudimentary organ generates complex worker-caste systems in ants

Rajendhran Rajakumar, Sophie Koch, Mélanie Couture, Marie-Julie Favé, Angelica Lillico-Ouachour, Travis Chen, Giovanna Blasis, Arjuna Rajakumar, Dominic Ouellette and Ehab Abouheif ()
Additional contact information
Rajendhran Rajakumar: McGill University
Sophie Koch: McGill University
Mélanie Couture: McGill University
Marie-Julie Favé: McGill University
Angelica Lillico-Ouachour: McGill University
Travis Chen: McGill University
Giovanna Blasis: McGill University
Arjuna Rajakumar: McGill University
Dominic Ouellette: McGill University
Ehab Abouheif: McGill University

Nature, 2018, vol. 562, issue 7728, 574-577

Abstract: Abstract The origin of complex worker-caste systems in ants perplexed Darwin1 and has remained an enduring problem for evolutionary and developmental biology2–6. Ants originated approximately 150 million years ago, and produce colonies with winged queen and male castes as well as a wingless worker caste7. In the hyperdiverse genus Pheidole, the wingless worker caste has evolved into two morphologically distinct subcastes—small-headed minor workers and large-headed soldiers8. The wings of queens and males develop from populations of cells in larvae that are called wing imaginal discs7. Although minor workers and soldiers are wingless, vestiges or rudiments of wing imaginal discs appear transiently during soldier development7,9–11. Such rudimentary traits are phylogenetically widespread and are primarily used as evidence of common descent, yet their functional importance remains equivocal1,12–14. Here we show that the growth of rudimentary wing discs is necessary for regulating allometry—disproportionate scaling—between head and body size to generate large-headed soldiers in the genus Pheidole. We also show that Pheidole colonies have evolved the capacity to socially regulate the growth of rudimentary wing discs to control worker subcaste determination, which allows these colonies to maintain the ratio of minor workers to soldiers. Finally, we provide comparative and experimental evidence that suggests that rudimentary wing discs have facilitated the parallel evolution of complex worker-caste systems across the ants. More generally, rudimentary organs may unexpectedly acquire novel regulatory functions during development to facilitate adaptive evolution.

Keywords: Pheidole; Rudimentary Wings; Imaginal Discs; Wing Disc; TT Hya (search for similar items in EconPapers)
Date: 2018
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DOI: 10.1038/s41586-018-0613-1

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