P ERSPECTIVES tulates that sets of two “true” segments are shared by other members of this group, in- dividual features that are serially repeated incompletely fused to form “diploseg- cluding those with a more typical cylindri- along the main body axis. These features are ments.” In pill —short-body cal shape (5)? The basal position of pill not integrated into anatomically and func- that roll up like armadillos— millipedes among the Diplopoda (8) sup- tionally individual segments, as is usually the there is another complication due to the pu- ports this prediction. case in the thorax and abdomen. Far tative fusion of anterior dorsal plates (see the Second, within arthropods, is segmenta- from being a primitive feature of arthro- figure). tion in the pill a primitive or de- pods, these units may be the product of his- Developmental genetics had been com- rived event? I suspect that the mismatch in torical changes in the genetic mechanisms pletely silent about the mechanisms of mil- gene expression between dorsal and ventral of segmentation that have been fostered by lipede segmentation, until Janssen et al. segments is an ancient feature, particularly the adaptive value gained from the different analzyed segmentation in the given the morphology of several long- resulting morphologies (11, 12). extinct groups. It is possible that those Paleozoic arthropods with different serially References repeated structures may eventually be 1. P. H. W. Holland, Semin. Dev. Biol. 1, 135 (1990). 2. P. A. Lawrence, The Making of a Fly (Blackwell, Oxford, grouped with millipedes in a clade that ex- 1992). cludes other modern arthropods. Recent ad- 3. V. Braun et al., Bioinformatics 19, 851 (2003). vances in molecular phylogeny 4. A. Minelli, The Development of Form (Cambridge Univ. Press, Cambridge, 2003). make this a hypothesis worth testing (9, 10). 5. R. Janssen et al., Dev. Biol. 268, 89 (2004). marginata (5). They report that A better understanding of segmentation 6. A. Ansenne, P. Compere, G. Goffinet, in Proceedings of the 7th International Congress of Myriapodology, A. segmentation genes in the dorsal and ven- mechanisms will enable the validity of the Minelli, Ed. (Brill, Leiden, Netherlands, 1990), pp. tral sides of the embryo are expressed inde- recently defined subphylum Myriochelata 125–134. pendently. They argue that the dorsal and (the Chelicerata plus the ) (9) to 7. D. K. Jacobs et al., Evol. Dev. 2, 340 (2000). 8. P. Sierwald et al., J. Zool. Syst. Evol. Res. 41, 87 (2003). ventral segments are independent units and be tested. In members of this putative group, 9. D. Pisani et al., BMC Biol. 2, 1 (2004). not dorsal and ventral aspects of trunk seg- both extinct and extant, there is nothing com- 10. E. Negrisolo et al., Mol. Biol. Evol. 21, 770 (2004). ments or diplosegments. They discovered parable to the “textbook” segments regarded 11. G. E. Budd, Evol. Dev. 3, 332 (2001). that the wingless gene is expressed in ven- as the true building blocks of arthropod bod- 12. A. Minelli, G. Fusco, Trends Ecol. Evol. 19, 423 (2004). tral segments only, whereas engrailed, ies. All of these share a series of in- 10.1126/science.1098138 hedgehog, and cubitus interruptus are ex- pressed both dorsally and ventrally but in EVOLUTION different expression patterns. The major divergence from the develop- mental gene expression patterns of the fruit Sex…Only If Really Necessary fly Drosophila and other arthropods is the dorsal expression of these genes, which is shifted by half a segmental unit that is de- in a Feminine Monarchy limited by intersegmental grooves in the growing embryo. In the pill millipede, gene Raghavendra Gadagkar expression seems to mark the posterior bor- ders of the millipede’s dorsal plates. As he honey bee society was famously de- by a highly variable sex determination locus these plates are mineralized (6), they may scribed as “The Feminine Monarchy” by such that homozygosity (a very rare possibil- be analogous to the shell of mollusks, the Tthe cleric Charles Butler in 1634. Honey ity, given the low probability of a female mat- margin of which is demarcated by expres- bees and their relatives—including all hy- ing with a male having the same allele as her- sion of the engrailed gene (7). Dorsal ex- menopteran societies—qualify for this label self) or hemizygosity (expected in all haploid pression of engrailed in the pill millipede because their colonies are headed by one or a individuals) results in male development, could be related to biomineralization rather small number of fertile queens. These queens whereas heterozygosity results in female de- than to segmentation. This does not imply produce a large number of sterile or nearly velopment (4). In social Hymenoptera, virgin conservation of biomineralization from sterile daughter workers and, later, with their queens make nuptial flights during which mollusks to arthropods, but rather provides assistance, produce a smaller number of fertile they acquire sperm from one or more males evidence of repeated independent co- sons and daughter queens (1). The complex and store and nurture the sperm in their sper- option of the engrailed gene among differ- and diverse life cycles and social organization matheca—a tiny gland that opens into the ent phyla. Later in development, the dorsal of the feminine monarchies are matched by oviduct. Queens have perfect control over the and ventral segments of the pill millipede their equally complex and diverse strategies sex of their offspring. To produce daughters, become aligned, giving rise to the serial or- for sexual and asexual reproduction (2). On a queen lets sperm flow from the spermathe- ganization of the animal’s trunk. In terms page 1780 of this issue, Pearcy et al. (3) un- ca into her oviduct and then lays fertilized of function, the result is no different than if cover a new dimension in the complexity of diploid eggs. Whether the diploid eggs devel- the trunk had been built out of a series of hymenopteran reproduction. op into sterile workers or fertile queens de- “true” segments. It is clear that the milli- In the Hymenoptera, males are typically pends on the nutritional environment of the pede body is not formed by serially adding haploid and females are diploid (see the fig- young larvae. To produce sons, however, a complete segmental units one after the oth- ure). It has been shown that sex is determined queen prevents the flow of sperm into the er. “True” segments simply do not exist, at oviduct and lays unfertilized haploid eggs. least in this arthropod. The author is in the Centre for Ecological Sciences, Such parthenogenetic development of The Janssen et al. findings raise two in- Indian Institute of Science, 560 012 Bangalore, India, males—known as arrhenotoky—is a univer- teresting phylogenetic questions. First, are and the Evolutionary and Organismal Biology Unit, sal and well-known feature of the Jawaharlal Nehru Centre for Advanced Scientific the independent expression patterns of seg- Research, Jakkur, 560 064 Bangalore, India. E-mail: Hymenoptera. Less widely known (and ap-

mentation genes found in the pill millipede [email protected] parently rather infrequent) is another form of CREDIT: MARCO ULIANA

1694 3 DECEMBER 2004 VOL 306 SCIENCE www.sciencemag.org Published by AAAS PERSPECTIVES parthenogenesis known as driven by a genetic predispo- thelytoky, which permits the sition for task specialization production of diploid daugh- Haploid son Diploid daughter queen Diploid daughter worker (8). Daughter queens, by con- ters without the need for a trast, are the mode for trans- paternal genome (1). Diploid ovum Diploid zygote mitting genes to future gener- Thelytoky (of the kind re- ations, making the twofold ferred to as automictic) in- cost of sex entirely relevant Syngamy Sexual reproduction volves the secondary fusion during their production. of two nonsister haploid nu- Pearcy et al. (3) make the rea- clei after the meiotic second 2nd meiotic division sonable argument that queens division. Automictic thely- (equational) are relatively protected from

toky restores diploidy and yet 1st meiotic division the environment, so that the has the potential for maintain- (reductional) lack of genetic variability

ing heterozygosity at the sex Primary oocyte Primary oocyte Primary oocyte may not be as serious a prob- determination locus, so that lem for them. In short, C. the sex of the resulting adult is cursor queens seem to have female. Although thelytoky Sexual the best of both worlds—they has been suspected as a minor Arrhenotoky Thelytoky reproduction reap the benefit of sex where form of reproduction in many it is most needed and the ben- species, it has been unequivo- efit of thelytoky where it is cally demonstrated in one most affordable. honey bee species (Apis mel- Diploid inseminated mother queen If C. cursor uses such a lifera capensis) and five phy- wonderful strategy, why don’t logenetically distant species Diversity of reproductive strategies. The European C. cursor uses arrhenotoky to other social Hymenoptera do of . In all of these six cas- produce haploid sons, thelytoky to produce diploid daughter queens, and normal sexual so? One possibility is that too es, workers use thelytoky to reproduction to produce diploid daughter workers (3).The process of oogenesis results in few species have been studied one egg pronucleus and four polar bodies at the end of the meiotic second division. The produce diploid female off- in sufficient detail to conclude polar bodies degenerate (indicated by an X). During arrhenotoky, the cell bearing the egg spring, even though they can- pronucleus develops parthenogenetically into a haploid adult male. During sexual repro- that this strategy is not more not mate. Thelytoky thus duction, the cell bearing the egg pronucleus is fertilized by a sperm from the queen’s sper- widespread (1 ). Alternatively, gives workers a degree of matheca to produce a diploid zygote that develops into a female offspring, a daughter this may be an artifact of gyne freedom from their queens, worker. In thelytoky, two nonsister haploid nuclei produced during the second meiotic di- production in the laborato- inasmuch as they themselves vision fuse secondarily to restore diploidy without the need for a paternal genome. The ry—an unlikely possibility can produce both male and fe- resulting diploid ovum develops into a viable female offspring, a daughter queen. but one that has not yet been male offspring. For this rea- ruled out. Perhaps the most son, thelytoky may also be interpreted as an ny, and thelytoky to produce daughter queens interesting possibility is that the luxury of mix- attempt by the workers to revolt against the (see the figure). The most striking conse- ing sex and nonsex in this way is not available hegemony of the queen, and as a potential ear- quence of this complex strategy, which the au- to all. What then is special about C. cursor? ly step in the eventual loss of sociality (5 ). thors emphasize, is in the context of the cost Do their queens not need genetic variability, or But what Pearcy et al. (3) have found in of sex. Sexual reproduction involves a twofold do they mix sex and nonsex even while pro- the European formicine ant, Cataglyphis cost because, relative to a parthenogenetic ducing queens in nature? Genetic variability cursor, is radically different. In this species, mother, a sexually reproducing mother trans- may, of course, be more important in some en- workers in orphaned colonies were already mits only half the number of her genes to each vironments than others and more important for known to produce diploid female offspring offspring (6). This genetic cost is thought some species than others. There is also the in- (both workers and queens). Now it appears (more precisely, hoped!) to be offset by the ad- triguing possibility that the advantage of thely- that queens themselves use thelytoky to pro- vantages of sexual reproduction in terms of toky for queens may be offset by the danger of duce daughter queens. The authors geno- enhanced genetic variability of the offspring. such a powerful tool falling into the clutches of typed workers and queens collected from Such genetic variability is expected to be use- the workers, who could then use it for subver- field colonies as well as laboratory-raised ful in dealing with variable environments— sive purposes. Clearly, the time is ripe for the- workers and gynes (queens) at four highly the physical environment to some extent, but oretical and empirical investigations of a new polymorphic microsatellite loci. Their results biological environments such as rapidly paradigm: sex versus nonsex in the service of provide unambiguous evidence that perhaps adapting parasites in particular (7). C. cursor queens and workers. a small fraction of the workers but certainly queens appear to forgo this benefit and save the large majority of laboratory-raised gynes on the cost of sex while producing daughter References (54 of 56 gynes studied) were produced by queens, but reap the benefits of sex while pro- 1. E. O. Wilson, The Insect Societies (Belknap/Harvard, Cambridge, MA, 1971). the queens through thelytoky. Confidence in ducing daughter workers. Because workers 2. R. H. Crozier, P. Pamilo, Evolution of Social Insect thelytoky as the mode of production of the are generally sterile and do not constitute a Colonies—Sex Allocation and Kin Selection (Oxford gynes arises from the fact that all of them on- way for the queens to transmit their genes to Univ. Press, Oxford, 1996). ly carried alleles that could be attributed to future generations, the twofold cost of sex is 3. M. Pearcy, S. Aron, C.Doums, L. Keller, Science 306, 1780 (2004). the mother queen. The probability that this irrelevant during their production. On the oth- 4. M. Beye et al., Cell 114, 419 (2003). could be the result of a chance mating of the er hand, the benefits of sexual reproduction 5. R. Gadagkar, Curr. Sci. 72, 950 (1997). queens with males carrying alleles identical are expected to be profound. Workers are 6. J. Maynard Smith, The Evolution of Sex (Cambridge Univ. Press, Cambridge, 1978). to their own is estimated at less than 10–28! much more exposed than queens to different 7. W. D. Hamilton, Oikos 35, 282 (1980). Apparently, then, C. cursor queens use ar- physical and biological environments. More 8. R. E. Page Jr. et al., Nature 338, 576 (1989). TAINA LITWAK TAINA rhenotoky to produce male offspring, normal important, genetic diversity among workers is

CREDIT: sexual reproduction to produce worker proge- known to facilitate efficient division of labor, 10.1126/science.1106673

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