The genomic organization of ant superorganisms

(Press-News.org) Aristotle praised the political organization of ant colonies while ancient Chinese Daoists appreciated ants as illustrative symbols showing how ephemeral human ambitions and power are. Throughout historical and pre-historic times, ant-workers are likely to be the first insects that toddlers relate to when they crawl around on all four.

Similar to so much else in biology, the first scientific understanding of ants goes back to Darwin, who spent many pages of the Origin of Species (1859) on these conspicuous social insects. Their very existence seemed to fly in the face of his theory of naturally selected adaptation -- how could ant workers have become so different from ant queens and ant males, he wondered, when workers are sterile and ‘cannot propagate their kind’?

Darwin hypothetically solved the enigma by assuming that natural selection had produced ant workers by increasing the reproductive success of their lifetime committed monogamous parents. Reproductive division of labor then becomes a logical corollary: ant males only provide sperm, the queens store that sperm for life allowing them to fertilize eggs for as long as two decades, and ant workers forage, nurse and defend brood, and die early.

Since the 1960s, we know that Darwin’s hypothesis is correct as it follows directly from the kin-selection idea that brothers and sisters are as effective in passing on gene copies to future generations as offspring are. A higher ergonomic efficiency of rearing siblings could thus gradually modify ant genomes to encode queen and workers castes in parallel, similar to how the genomes in a fertilized egg encode the differentiated cell-lineages of a multicellular body.

But how such complete rewiring of genomes into parallel developmental trajectories for reproductives and workers could happen was anybody’s guess. A new study, initiated 9 years ago at the Section for Ecology and Evolution in the Copenhagen Department of Biology, now provides an entire array of answers to this fundamental question – published in the journal Cell – biology’s most influential international journal in terms of impact factor.

Comparing more than 130 high-quality genomes from ants around the world shows that very little of ant genomic organization makes sense except to illuminate the origin and secondary elaboration of queen and worker castes. After the ants originated in the late Jurassic, the international consortium identified many signatures of natural selection affecting ant genomes while connecting them to increases in colony size, queen-worker size difference and further differentiation of the worker caste itself, including the emergence of sterile soldiers.

Once the ancestral ant genome had become evolutionary stable in the early Cretaceous, their genes were reshuffled to a degree not known from any other animals. As it turned out, the extent to which this happened predicted a good part of how many species the various ant subfamilies managed to evolve. At the same time, smaller clusters of linked genes that mediate reproductive division of labor between queens and workers tended to stay together for more than 100 million years, explaining many details of how the ants diversified.

The new Cell paper saw the light by an unusually fruitful collaboration between Professors Guojie Zhang and Jacobus (Koos) Boomsma, colleagues at the Copenhagen Section for Ecology and Evolution for almost a decade until Guojie Zhang returned to China to start the Center for Evolutionary & Organismal Biology at Zhejiang University in Hangzhou. Both were among the global pioneers of ant genome sequencing in 2010-11, using technology that was cutting edge then, but allowed little more than obtaining fragmented genomes of single ant species at the time.

To realize fundamental innovation of social insect genomics, Professors Zhang and Boomsma started GAGA - the Global Ant Genomics Alliance https://db.cngb.org/antbase/project, in 2016 to use long-read sequencing technology and new generations of bioinformatic analysis while asking global collaborators to collect ant samples, which ultimately produced this new milestone publication.

Contact:

China : Prof. Guojie Zhang at Zhejiang University guojiezhang@zju.edu.cn, Associate Professor Weiwei Liu at Kunming Institute of Zoology, liuweiwei@mail.kiz.ac.cn

Denmark : Prof. Jacobus (Koos) J. Boomsma at University of Copenhagen  jjboomsma@bio.ku.dk

German: Associate Professor Lukas Schrader at University of Münster lukas.schrader@uni-muenster.de

 

 

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