S CIENCE’ S C OMPASS 65 PERSPECTIVES: DEVELOPMENT (Formica) nitridiventris. For queens, the re- 64 sults were straightforward: Wing development 63 genes highly conserved in other insects 62 Sociogenomics Takes Flight showed the expected expression patterns in all 61 four species. (The same re- 60 Gene E. Robinson sult was obtained for males, 59 which also are winged.) For 58 hese are good times for research on so- logical differences among workers, the results were 57 cial insects. The social Hymenoptera— worker castes in many surprising. Expecting wing- 56 Tants, bees, and wasps—are emerging as species of ants, which re- lessness in the four ant 55 valuable models for the study of molecular flects a further division of species to be associated 54 processes (1). The honey bee Apis mellifera, labor. Smaller workers with a break at the same 53 a social insect, has just been selected by the care for the brood, whereas node of the genetic network, 52 NIH’s National Human Genome Research larger individuals become Abouheif and Wray instead 51 Institute to be among the next group of or- highly specialized as “sol- observed different gene ex- 50 ganisms to have its genome sequenced (2). diers” with powerful jaws pression patterns in different 49 Genes that are important for the organization and potent toxins. species. For example, wing 48 of ant (3) and bee (4) societies have been Insects were the first development in C. lineolata 47 identified during the past year, and the devel- group of animals to fly, and N. nitridiventris workers 46 opment of genomic resources such as ex- more than 100 million was shut down toward the 45 pressed sequence tags and microarrays (5, 6) years before reptiles and end of the process (no ex- 44 is quickening the pace of discovery. Some of birds, and this trait is wide- pression of en), but in P. 43 the genes that are differentially regulated dur- ly seen as a key evolution- morrisi workers the break 42 ing the development of worker and queen ary innovation underlying occurred much more up- 41 honey bees have been identified (7), and their spectacular success. stream, with no expression 40 provocative findings hint at even stronger ge- Ant queens initially have detected of any of the six 39 netic influences on caste determination in wings but shed them after genes. In P. morrisi soldiers, 38 ants (8, 9). On page 249 of this issue, mating when they begin to by contrast, five of the six 37 Abouheif and Wray (10) now formally wel- establish a new colony. genes showed normal ex- 36 come ants into the vigorous field of “evo-de- Workers, in contrast, are pression and only sal, the 35 vo” with a fascinating description of changes born completely wingless. Winging their way to success. most downstream gene ex- 34 in gene expression that are associated with This evolutionary reversal Female ants can develop into ei- amined, was silent, demon- 33 the evolution of the wingless worker caste. is thought to have given ther winged queens or wingless strating differences in gene 32 Winglessness in ants is part of a ants the mobility to search workers. Drawings depict a winged expression even for workers 31 polyphenism, which can be defined as the more efficiently for insects virgin queen (middle), a wingless and soldiers of the same 30 “occurrence of several distinct phenotypes or and other food sources in worker (bottom) and a winged species. male (top) of the American har- 29 forms in a given species, each of which de- the ground, and thus fig- Why are there such vester ant, Pogonomyrmex barba- 28 velops facultatively in response to some cue ures prominently in their tus.Fossil evidence, such as this broad variations in a trait 27 from the internal or external environment” overwhelming ecological specimen in amber, indicates that that is thought to have 26 (11). Polyphenism is not limited to inverte- dominance (these tiny winglessness evolved just once in evolved just once? Abouheif 25 brates, and accounts for some of the remark- creatures constitute 10 to the ants. Shown is a worker ant and Wray suggest that, after 24 able flexibility seen in life forms, including 15% of the entire animal (subfamily Sphecomyrminae) in the wing development gene 23 fish that switch sexes in response to changes biomass in most terrestrial sequoia amber formed about 80 network was inactivated in a 22 in their social environment (12). Polyphenism environments) (14). With million years ago during the Upper basal lineage, either a neu- 21 has figured prominently in the evolution of all known ant species Cretaceous. [Reproduced from tral evolutionary process or 20 one of the defining features of insect soci- sporting wingless workers, (22) with permission] natural selection (perhaps 19 eties: a division of labor for reproduction. as well as some telling fos- related to pleiotropy) could 18 Eggs of female social Hymenoptera can sil finds (see the figure), ant specialists be- have acted in different species to change 17 develop into either queens or workers (see lieve that worker ant winglessness evolved when wing development is halted. They also 16 the figure). Queens specialize in reproduc- only once (10). speculate that similar evolutionary lability 15 tion, whereas workers engage in little or no Abouheif and Wray (10) compared gene underlies other polyphenisms, making it 14 reproduction and perform all tasks related to expression profiles during development of the risky to generalize about molecular pathways 13 colony maintenance and growth (13). A queens and workers of several ant species. on the basis of data from a single species. 12 colony of social insects may have just one or Their study draws on an elegant body of work Their results provide a good example of how 11 a few queens but from tens to millions of (15) that has elucidated a hierarchical gene different genomes can achieve the same end 10 workers. In many insect societies, there are network underlying wing development in the in different ways, thus highlighting the im- 9 profound morphological differences between fruit fly Drosophila melanogaster and other portance of comparative genomics. 8 queens and workers. For example, queens insects. These authors studied the expression The heightened interest in social insects 7 have huge ovaries and often lay thousands of of six wing development genes—ultrabitho- reflects the sense that the time has come to 6 eggs per day, whereas workers may com- rax (Ubx), extradenticle (exd), engrailed (en), develop a comprehensive understanding in 5 pletely lack ovaries. There are also morpho- wingless (wg), scalloped (sd), and spalt molecular terms of social life: how it 4 (sal)—in the ant Pheidole morrisi. Mean- evolved, how it is governed (16, 17), and 3 The author is in the Department of Entomology and while, they analyzed expression of Ubx, exd, how it influences all aspects of genome 2 the Neuroscience Program, University of Illinois, Ur- and en in the ant species Myrmica americana, structure, gene expression and organismal 1 bana, IL 61801, USA. E-mail: [email protected] Crematogaster lineolata, and Neomormica development, physiology and behavior (18). CREDITS: TOP, JOHN P. GEOGRAPHIC SOCIETY; DAWSON/NATIONAL BOTTOM, FRANK M. CARPENTER 204 12 JULY 2002 VOL 297 SCIENCE www.sciencemag.org S CIENCE’ S C OMPASS 65 The nascent field of sociogenomics is pred- parative analysis and facilitate gene identifi- References 64 icated on two of the most significant ideas cation in other social insect species. It will 1. R. E. Page et al., Genetics 160, 375 (2002). 2. www.nhgri.nih.gov/NEWS/sequencing.html (2002). 63 in biology to emerge from the latter half of boost sociogenomics enormously and fur- 3. M. J. Krieger,K.G.Ross,Science 295, 328 (2002). 62 the 20th century. First, many aspects of so- ther enhance the value of social insects as 4. Y. Ben-Shahar et al., Science 296, 741 (2002). 61 cial life, including social behavior, have a models in diverse fields of biology. 5. C.W. Whitfield et al., Genome Res. 12, 555 (2002). 6. R. Kucharski, R. Maleszka, Genome Biol. 3,RE- 60 biological basis and are thus influenced to By now, you’re probably muttering that SEARCH0007 (2002). 59 some extent by genes and the forces of evo- the only topic for which social insects have 7. J. D. Evans, D. E. Wheeler, Genome Biol. 2,RE- 58 SEARCH0001 (2002). lution (13). Second, the functions of many not been promoted in this article is world 8. G. E. Julian et al., Proc. Natl. Acad. Sci. U.S.A. 99, 57 genes are highly conserved between inver- peace. In fact, I don’t have to, because The 8157 (2002). 56 tebrates and vertebrates even for complex New York Times (19) already did! In their 9. V. P. Volny, D. M. Gordon, Proc. Natl. Acad. Sci. U.S.A. 99, 6108 (2002). 55 traits (15), so that much can be learned news story entitled “A lesson in détente 10. E. Abouheif, G. A.Wray, Science 297, 249 (2002). 54 from strategically chosen models. Appro- from the insect world” they discuss Giraud 11. H. F. Nijhout, Insect Hormones (Princeton Univ. Press, 53 priately, social insects and developmental et al.’s (20) remarkable work on the Argen- Princeton, NJ, 1994). 12. R. D. Fernald, Novartis Found. Symp. 244, 169 (2002). 52 biology, the subjects of Abouheif and tine ant Linepithema humile. This creature, 13. E. O. Wilson Sociobiology: The New Synthesis (Belk- 51 Wray’s (10) paper, contributed profoundly normally a highly territorial species in its nap, Cambridge, MA, 1975). 50 to these hard-won insights.