COMMENTARY

The birth of ant genomics

Raghavendra Gadagkar1 Centre for Ecological Sciences and Centre for Contemporary Studies, Indian Institute of Science, Bangalore 560 012, India; and Evolutionary and Organismal Biology Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore 560 064, India

oday science is in the age of bi- social organization (11), mechanisms of ology and biology is in the age of caste determination (12), and the organi- T genomics. Sequencing the entire zation of labor (13). The fire ant S. invicta, genome of an organism, an en- introduced from South America, has terprise that could not have been imagined spread across the United States and has barely 50 y ago, is being thought of as the become one of the most serious pests first step toward a complete understand- threatening agriculture and human life ing of its biology. If I had been asked to and defying most extermination efforts recommend just two families of living (14). C. floridanus, found in the south- organisms from which to pick the first two eastern United States, is perhaps the most species for whole-genome sequencing, I nondescript of the lot but it is good to would surely have suggested Hominidae have to compare with the others, especially (with ourselves) and Formicidae (with all because of its well organized, monogy- ants). My choice of the ant family is easy nous colonies with only two worker castes to justify. The family Formicidae consists (15). H. saltator is rather special, a jumping of approximately 14,000 species of ants, ant from India whose workers can copu- all of which exhibit advanced and sophis- late with males from their own colonies ticated social life, not unlike our own in and contribute to egg-laying, alongside many respects and perhaps surpassing us the queens, as gamergates (i.e., married in some ways. The ants live in colonies workers) (16). Finally, A. cephalotes is an- headed by one or a small number of fertile other “star” as ants go, being an extremely queens and large number (which can serious pest of agriculture in the Neo- sometimes run into millions) of sterile tropics, a status achieved as a result of workers, and display sophisticated division its habit of harvesting leaves and using them of labor and most impressive levels of to cultivate fungal gardens—a 50-million- communication and coordination among year-old form of ant agriculture (17). colony members (Fig 1). One of the With the publication of these six ant many features of great interest is the vastly genomes, we have thus obtained a total of different phenotypes and lifespans of approximately 1.5 billion base pairs’ worth queens and workers, despite developing of new data. What can we do with this from the same genome. Ants have a- massive amount of data? Are the data chieved spectacular ecological success and worth the time, effort, and money that dominance, accounting for more than a went into their collection? The answers to third of all insect biomass and, along with these questions should not be taken as termites, for more than 25% of all Fig. 1. (A) A portion of the nest of the invasive obviously being in the affirmative, but animal biomass in some tropical forests (1). Argentine ant L. humile showing workers tending should be examined very carefully. In ad- brood (photo: Marc Dantzker). (B) A small portion Whole-genome sequencing was, until of a laboratory colony of a red imported fire ant S. dition to the actual genome sequences, recently, a relatively expensive and time- invicta (photo: Yannick Wurm). (C) An example of most of these articles provide basic in- consuming affair, so many organisms had the fungus garden of the leaf-cutter ant A. ceph- formation such as genome size, expected to wait in a queue for their turn. We hu- alotes (photo: Jarrod Scott) with a single ant car- number of genes, transcriptome sequences, mans had to wait until the year 2001 and rying a leaf also shown (Inset; photo: Alex Wild). and information about duplicated genes, the ants have had to wait until hundreds of missing genes, and transposable elements. other animals, plants, and microbes had Each article makes preliminary compar- been sequenced. However, fortunately, the bee genome has already been sequenced isons with some of the other related ge- wait is now over. The genomes of the in- (7), taking the number of eusocial species nomes to point out similarities and vasive Argentine ant Linepithema humile to seven, and because three species of differences. Each article also lists several (2), the red harvester ant Pogonomyrmex the parasitic wasp Nasonia have also been pleasing results. For example, the Argen- barbatus (3), and the fire ant Solenopsis sequenced (8), we have 10 hymenopteran tine ant genome has expansions and/or invicta (4) are being simultaneously un- genome sequences for comparative study. abundance of gustatory, odorant receptor, veiled in PNAS. The genome sequences of The Argentine ant L. humile is re- cytochrome P450, royal jelly protein, and two other ants, Camponotus floridanus and markable in many ways, especially because methylation-related genes and a paucity of Harpegnathos saltator (5), were also pub- of its successful invasion from South immune genes. The harvester ant genome lished recently. In addition the genome America to every Mediterranean-type cli- shows expansion of chemoreception and sequence of the leaf-cutter ant Atta ceph- mate, including most of Europe and North cytochrome P450 genes. The fire ant alotes will soon be published in another America (9), and even more so because journal (6), taking the total to six. Thus, we it appears to form mega-supercolonies are truly witnessing the birth of ant ge- ranging over hundreds of thousands of Author contributions: R.G. wrote the paper. nomics, indeed, of comparative ant geno- kilometers (10). The harvester ant P. bar- The author declares no conflict of interest. mics. Actually, we now find ourselves in an batus is a rather famous granivore, being See companion articles on pages 5667, 5673, and 5679. even better situation because the honey- a favorite model to study variations in 1E-mail: [email protected].

www.pnas.org/cgi/doi/10.1073/pnas.1100765108 PNAS | April 5, 2011 | vol. 108 | no. 14 | 5477–5478 Downloaded by guest on October 1, 2021 genome has multiple copies of vitelloge- should permit a more detailed comparison promises are being made. For example, nin, hundreds of olfactory receptors, and of the available sequences and provide the Camponotus–Harpegnathos article an expansion of lipid-processing genes. greater insights into the biology of these claims to help “provide experimental ave- The Camponotus and Harpegnathos ge- fascinating organisms. The sequencing of nues to address long-standing hypotheses nomes reveal many ant-specific genes (as more ant and social insect genomes, which on the relationships among epigenetics, opposed to other hymenopteran genes) is sure to follow, should add exponentially neurobiology, and behavior, as well as life- and have already revealed interesting span regulation” (5); the Argentine ant fi caste-speci c differences in gene expres- With the publication of article promises that “these tools will likely sion. The Atta genome shows reduction in find widespread application and produce genes related to nutrition acquisition and these six ant genomes, tangible benefits for agriculture, societies digestion. The honeybee genome shows and ecosystems” and “will be productive a paucity of genes related to immunity and we have thus obtained detoxification, an excess of genes for che- avenues for future research that explores the basis of eusociality, and the cause and moreception and pollen and nectar utili- a total of approximately ” zation, and an interesting diversification of consequences of biological invasions (2); fi “ genes coding for royal jelly proteins. Al- 1.5 billion base pairs’ the re ant article claims to provide the though sometimes claimed to be tests of foundation for future evolutionary, bio- a priori predictions, these pleasing fea- worth of new data. medical, sociogenetic, and pest-manage- tures should only be considered as being ment studies...” (4); and the Nasonia “not inconsistent” with what one might article claims that the genomic data “will expect on the basis of prior knowledge of to the success of this enterprise. The ad- ultimately provide tools and knowledge for the biology, behavior, and evolution of dition of every new genome sequence to further increasing the utility of parasitoids social insects, especially the high fecundity our toolkit should also add significantly to as pest insect-control agents” (8). Can of their queens, great significance of our ability to apply the tools of genomics these promises ever be met? I think the chemical communication in their lives, and to species whose genomes have not been answer is yes. Will these promises be met high levels of social hygiene. In short, sequenced. Gene hunting and gene ex- in the foreseeable future? Probably, but there are no surprises, at least so far. pression studies, which can now be applied not unless we consciously encourage diverse Is this all we learn? Certainly not. The ever more widely to sequenced as well as approaches in the study of social (and fi facts gleaned and described in the rst unsequenced species, should help unravel nonsocial) hymenopteran insects, ensure the underlying genetic architecture of article reporting the sequence of an or- adequate opportunities for researchers ganism’s genome should really be thought many ecologically and socially interesting continuing to use classical methods, and of as no more than a postcard sent home traits (18). However, is that enough? A thus work hard to make the new and by a visitor giving first impressions of a creative scholar studying the city of New city—say, New York—after spending just York for many years should also attempt spectacular genomic resources of real a day. The longer the visitor stays, the to explain why the city has come to be utility available to those who are not in- more he learns, and if he stays for years, he what it is, why it has this architecture and vestigating genomics themselves. In other may write books about the architecture, not that, why the art and fashion scene is words, we must take care not to make “ ” the art and fashion scene, the crime scene, different from that of Paris, why some genomics so fashionable that there is no the ethnic composition of the city, and so areas are safe and some are not, and why one left to apply genomics to the real on. We should expect something similar the city has this ethnic composition and problems that we sought to tackle in the from those who will continue to study not another—àlaJared Diamond (19, 20). first place. If we succeed in this, I believe these genome sequences for many years to Will something like this happen with the genomics can indeed revolutionize the come. Even a more complete annotation ant genomes? We should hope so because study of ant and social insect biology.

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