Reciprocal genomic evolution in the ant-fungus agricultural symbiosis

Sanne Nygaard, Haofu Hu, Cai Li, Morten Schiøtt, Zhensheng Chen, Zhikai Yang, Qiaolin Xie, Chunyu Ma, Yuan Deng, Rebecca B. Dikow, Christian Rabeling, David R. Nash, William T. Wcislo, Sean G. Brady, Ted R. Schultz, Guojie Zhang, Jacobus J. Boomsma

Research output: Contribution to journalArticle

41 Citations (Scopus)

Abstract

The attine ant-fungus agricultural symbiosis evolved over tens of millions of years, producing complex societies with industrial-scale farming analogous to that of humans. Here we document reciprocal shifts in the genomes and transcriptomes of seven fungus-farming ant species and their fungal cultivars. We show that ant subsistence farming probably originated in the early Tertiary (55-60 MYA), followed by further transitions to the farming of fully domesticated cultivars and leaf-cutting, both arising earlier than previously estimated. Evolutionary modifications in the ants include unprecedented rates of genome-wide structural rearrangement, early loss of arginine biosynthesis and positive selection on chitinase pathways. Modifications of fungal cultivars include loss of a key ligninase domain, changes in chitin synthesis and a reduction in carbohydrate-degrading enzymes as the ants gradually transitioned to functional herbivory. In contrast to human farming, increasing dependence on a single cultivar lineage appears to have been essential to the origin of industrial-scale ant agriculture.

Original languageEnglish (US)
Article number12233
JournalNature Communications
Volume7
DOIs
StatePublished - Jul 20 2016
Externally publishedYes

Fingerprint

symbiosis
Symbiosis
Ants
fungi
genome
Fungi
Agriculture
Genes
chitin
Chitinases
biosynthesis
Chitin
agriculture
Biosynthesis
carbohydrates
leaves
Arginine
enzymes
Carbohydrates
shift

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

Cite this

Nygaard, S., Hu, H., Li, C., Schiøtt, M., Chen, Z., Yang, Z., ... Boomsma, J. J. (2016). Reciprocal genomic evolution in the ant-fungus agricultural symbiosis. Nature Communications, 7, [12233]. https://doi.org/10.1038/ncomms12233

Reciprocal genomic evolution in the ant-fungus agricultural symbiosis. / Nygaard, Sanne; Hu, Haofu; Li, Cai; Schiøtt, Morten; Chen, Zhensheng; Yang, Zhikai; Xie, Qiaolin; Ma, Chunyu; Deng, Yuan; Dikow, Rebecca B.; Rabeling, Christian; Nash, David R.; Wcislo, William T.; Brady, Sean G.; Schultz, Ted R.; Zhang, Guojie; Boomsma, Jacobus J.

In: Nature Communications, Vol. 7, 12233, 20.07.2016.

Research output: Contribution to journalArticle

Nygaard, S, Hu, H, Li, C, Schiøtt, M, Chen, Z, Yang, Z, Xie, Q, Ma, C, Deng, Y, Dikow, RB, Rabeling, C, Nash, DR, Wcislo, WT, Brady, SG, Schultz, TR, Zhang, G & Boomsma, JJ 2016, 'Reciprocal genomic evolution in the ant-fungus agricultural symbiosis', Nature Communications, vol. 7, 12233. https://doi.org/10.1038/ncomms12233
Nygaard, Sanne ; Hu, Haofu ; Li, Cai ; Schiøtt, Morten ; Chen, Zhensheng ; Yang, Zhikai ; Xie, Qiaolin ; Ma, Chunyu ; Deng, Yuan ; Dikow, Rebecca B. ; Rabeling, Christian ; Nash, David R. ; Wcislo, William T. ; Brady, Sean G. ; Schultz, Ted R. ; Zhang, Guojie ; Boomsma, Jacobus J. / Reciprocal genomic evolution in the ant-fungus agricultural symbiosis. In: Nature Communications. 2016 ; Vol. 7.
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