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

doi:10.1038/ncomms12233

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

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98 Scopus citations

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 language	English (US)
Article number	12233
Journal	Nature communications
Volume	7
DOIs	https://doi.org/10.1038/ncomms12233
State	Published - Jul 20 2016
Externally published	Yes

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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@article{83f3da2fe7f54c79bd0a82a7280ca56d,

title = "Reciprocal genomic evolution in the ant-fungus agricultural symbiosis",

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.",

author = "Sanne Nygaard and Haofu Hu and Cai Li and Morten Schi{\o}tt and Zhensheng Chen and Zhikai Yang and Qiaolin Xie and Chunyu Ma and Yuan Deng and Dikow, {Rebecca B.} and Christian Rabeling and Nash, {David R.} and Wcislo, {William T.} and Brady, {Sean G.} and Schultz, {Ted R.} and Guojie Zhang and Boomsma, {Jacobus J.}",

note = "Funding Information: This study was supported by grants from the Danish National Research Foundation (DNRF57) and the European Research Council (ERC Advanced grant 323085) (J.J.B.), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB13000000) (G.Z.), the Smithsonian Office of the Under Secretary for Science (T.R.S., S.G.B. and W.T.W.), the US National Science Foundation DEB-1456964 (C.R. and T.R.S.) and DEB-0949689 (T.R.S.), the US National Museum of Natural History (T.R.S.) and a University of Maryland-Smithsonian Institution Seed Grant (S.G.B. and T.R.S.). The Visitor's Office of the Smithsonian Tropical Research Institute provided logistic help and facilities to work in Gamboa and the Autoridad Nacional del Ambiente y el Mar (ANAM) gave permission to sample and export ants from Panama.",

year = "2016",

month = jul,

day = "20",

doi = "10.1038/ncomms12233",

language = "English (US)",

volume = "7",

journal = "Nature communications",

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T1 - Reciprocal genomic evolution in the ant-fungus agricultural symbiosis

AU - Nygaard, Sanne

AU - Hu, Haofu

AU - Li, Cai

AU - Schiøtt, Morten

AU - Chen, Zhensheng

AU - Yang, Zhikai

AU - Xie, Qiaolin

AU - Ma, Chunyu

AU - Deng, Yuan

AU - Dikow, Rebecca B.

AU - Rabeling, Christian

AU - Nash, David R.

AU - Wcislo, William T.

AU - Brady, Sean G.

AU - Schultz, Ted R.

AU - Zhang, Guojie

AU - Boomsma, Jacobus J.

N1 - Funding Information: This study was supported by grants from the Danish National Research Foundation (DNRF57) and the European Research Council (ERC Advanced grant 323085) (J.J.B.), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB13000000) (G.Z.), the Smithsonian Office of the Under Secretary for Science (T.R.S., S.G.B. and W.T.W.), the US National Science Foundation DEB-1456964 (C.R. and T.R.S.) and DEB-0949689 (T.R.S.), the US National Museum of Natural History (T.R.S.) and a University of Maryland-Smithsonian Institution Seed Grant (S.G.B. and T.R.S.). The Visitor's Office of the Smithsonian Tropical Research Institute provided logistic help and facilities to work in Gamboa and the Autoridad Nacional del Ambiente y el Mar (ANAM) gave permission to sample and export ants from Panama.

PY - 2016/7/20

Y1 - 2016/7/20

N2 - 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.

AB - 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.

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VL - 7

JO - Nature communications

JF - Nature communications

M1 - 12233

ER -

Reciprocal genomic evolution in the ant-fungus agricultural symbiosis

Abstract

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