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4.3 Brief Comms Am 26/2/04 6:00 Pm Page 1 4.3 brief comms am 26/2/04 6:00 pm Page 1 brief communications Ant parasite queens revert to mating singly A parasitic ant has abandoned the multiple mating habit of the queens of its related host. ultiple mating (polyandry) is would apply equally to social parasites widespread among animal and free-living species. Other likely ASH 1 Mgroups, particularly insects .But benefits (greater sperm store, conver- D. R. N the factors that maintain it and under- gence of sex-allocation interests lie its evolution are hard to verify between queens and workers, reduced because benefits and costs are not easily fitness cost of producing sterile diploid quantified and they tend to be similar males and increased genetic diversity in related species. Here we compare the among workers3) are specific to free-liv- mating strategies of the leaf-cutting ant ing social insects and so are the most Acromyrmex echinatior and its recently likely explanations for polyandry in derived social parasite Acromyrmex Acromyrmex ants. The benefits of insinuator,which is also its closest rela- polyandry in these ants are therefore tive2 (see Fig. 1). We find that although related to their social lifestyle, indicat- the host queens mate with up to a ing that the selective forces affecting the dozen different males, the social para- evolution of polyandry in free-living site mates only singly. This rapid and Figure 1 A multiply mated queen of the leaf-cutting ant Acromyrmex echinatior social insects differ from those in other surprising reversion to single mating in (right) and its singly mated socially parasitic companion queen A. insinuator (left) animals. We would expect workerless a socially parasitic ant indicates that the on their joint fungus garden. Small worker ants cluster around the parasite queen. social parasites of other polyandrous costs of polyandry are probably specific social insects to have also reverted to to a free-living lifestyle. Pǃ0.0006), and genetic relatedness among mating singly. The identification of addi- In social insects, obligate polyandry has the offspring was 0.380DŽ0.042 versus tional reversions to single mating, both in evolved independently in four groups 0.693DŽ0.053 (t-test, Pǃ0.0002) for the host social and non-social animals,will be impor- (honeybees,vespid wasps,harvester ants and and parasite,respectively.The difference can- tant in further distinguishing the factors leaf-cutting ants3), among which every not be attributed to low variability in the species was previously believed to be multi- genetic markers8,sampling error8 or inbreed- ply mated. All free-living leaf-cutting ants ing: neither species was inbred (Fǃ0.006, 4 are multiply mated , so the common ances- nǃ10, Pǃ0.19 and Fǃǁ0.035, nǃ19, 48891010 10 11 11 12 1.0 tor of both parasite and host ants must have Pǃ0.88 for A. echinatior and A. insinuator, had multiply mated queens. Because social respectively). 0.8 Host parasite queens exploit the resources and These findings provide insight into the 0.6 workers of a host colony to produce repro- selective forces affecting the evolution of 0.4 ductive offspring (sexuals) without investing polyandry. Like its host, A. insinuator is out- 0.2 in a large worker force of their own5–7,we bred and produces hundreds of winged sex- 0 investigated whether this dramatic change in uals in discrete batches that leave their natal 7 1111111111122 lifestyle could have altered the costs and colonies within the same brief time period . 1.0 benefits of polyandry, and thereby driven a This indicates that females of both species 0.8 shift in mating strategy. mate with unrelated males in swarms outside 0.6 Parasite Parasitized A. echinatior colonies were the colony. The parasite is also very abun- 0.4 collected from Gamboa, Panama, where the dant, infecting 44% of host colonies at our Frequency of patrilines within progeny 0.2 species is common7.We compared the mat- study site7.Mating behaviour,mate availabil- ing frequencies of host and parasite by ity and thus the costs of mating are therefore 0 analysing the genotypes of queens and their likely to be similar for the two species. That Queens female offspring to estimate the number of A. insinuator has reverted to single mating fathers contributing to a queen’s progeny. suggests that the benefits of polyandry are Figure 2 The observed frequency distributions of patrilines Host queens mated with 10.6DŽ1.0 males reduced for the social parasite.The reversion (offspring sired by different males) of the social parasite (meanDŽs.e; nǃ10) but social parasite to single mating seems to have been rapid Acromyrmex insinuator (nǃ13) and its host A. echinatior queens were predominantly singly mated compared with the evolution of other adap- (nǃ10), as derived from genetic analysis of the progeny of (average number of matings per queen, tive traits5–7,supporting the widely held but single queens. Patrilines are shown by alternate shading patterns, 1.19DŽ0.10; only 2 out of 13 queens doubly rarely demonstrated assumption1,2 that with their total number in each colony given above the bars. Host mated;see Fig.2). multiple mating is costly. queens and an average of 203 (range, 35–672) female offspring This difference is statistically highly sig- The association between a reversion to per queen were genotyped at four microsatellite loci (Ech1390, nificant (Mann–Whitney U-test,P<0.0001) single mating and a switch to social para- Ech3385, Ech4126 and Ech4225)9.Parasite queens and an and robust to alternative measures of queen- sitism indicates that the benefits of average of 14.7 (6–20) female progeny per queen were geno- mating frequency. For example, the observed polyandry for Acromyrmex ants may be spe- typed at two loci (Trachy11_12 and Ech3385)9,10. Genotypes of number of queen matings was 9.3DŽ0.7 cific to being free-living and social.Four pro- queens and their offspring were analysed using the software versus 1.15DŽ0.10 (P<0.0001), the effective posed benefits of multiple mating for social MATESOFT 1.0b (by A. Moilanen, L. Sundström and J. S. P.; avail- number of queen matings was 5.3DŽ0.6 insect queens (nutrient transfer,sperm com- able at http://www.zi.ku.dk/popecol/personal/JSPedersen/Mate- versus 1.09DŽ0.09 (P<0.0001),the estimated petition, variable daughter queens and Soft.htm) to obtain mating-frequency statistics8, and the total proportion of multiply mated queens was avoidance of genetic incompatibility3) are mate number for host queens was further estimated using a 1.00 (95% confidence interval, 0.69–1.00) unlikely to be important in the maintenance modified version of the coverage statistics calculated by the versus 0.19 (0.034–0.51; binomial test, of polyandry in Acromyrmex,because they program CHAO11. NATURE | VOL 428 | 4 MAR CH 2004 | www.nature.com/nature 35 © 2004 Nature Publishing Group 4.3 brief comms am 26/2/04 6:00 pm Page 2 brief communications involved in the evolution and maintenance the basis of previous correlations with 3 of multiple mating by females. spreading rate” .Owing to the high enrich- a Seirian Sumner*, William O. H. Hughes, ment of the hydrothermal fluids in mantle 25 3 4 ) Jes S. Pedersen, Jacobus J. Boomsma –1 He (typically a factor of 10 relative to ambi- 20 Biological Institute, Department of Population ent sea water), this abundant hydrothermal km Biology, University of Copenhagen, activity should logically correspond to an –1 15 3 yr Rainbow –1 2100 Copenhagen, Denmark enhanced He output from the ridge. Lucky Strike e-mail: [email protected] At a global scale, three-dimensional 10 Red Sea *Present addresses: Smithsonian Tropical Research oceanic general circulation models make a 5 He (mmol Institute, Unit 0948, APO AA 34002, USA, and good job of simulating the oceanic distribu- 3 Gakkel Ridge Institute of Zoology, Zoological Society of London, tion of hydrothermal 3He by using the simple 0 3 010203040506070 Regents Park, London N1 4RY, UK. assumption that the He source intensity is Spreading rate (mm per year) 1. Simmons, L. W. Sperm Competition and its Evolutionary linearly correlated with the spreading rate5,6. Consequences in the Insects (Princeton University Press, 3 b Princeton, 2001). The slope of the He flux–spreading rate rela- Barents Sea 3 ǁ2 2. Sumner, S., Aanen, D. K., Delabie, J. & Boomsma, J. J. Insectes tionship is close to 330 He mol km of 39 ± EBDW+EBDW Ar: 92 6% Soc. 51, 37–42 (2004). crustal spreading, translating into a world 3He: 0.6±0.3% 3. Crozier, R. H. & Fjerdingstad, E. J. Ann. Zool. Fenn. 38, 267–285 3 ǁ2 (2001). average He annual flux of 0.33 mmol km 39Ar: 60.1±6.6% 4. Villesen, P., Murakami, T., Schultz, T. R. & Boomsma, J. J. of ridge and per mm yrǁ1 of full spreading Proc. R. Soc. Lond. B 269, 1541–1548 (2002). 3He: 4.1±0.7% NSDW 3 5. Sumner, S., Nash, D. R. & Boomsma, J. J. Proc. R. Soc. Lond. B rate.Available He fluxes determined for 39Ar: 83±5% 270, 1315–1322 (2003). active portions of ridge show results consis- 3He: 1.9±0.6% 6. Sumner, S., Hughes, W. O. H. & Boomsma, J. J. Behav. Ecol. Sociobiol. 54, 256–263 (2003). tent with this global trend (Fig.1a). 7. Bekkevold, D. & Boomsma, J. J. J. Evol. Biol. 13, 615–623 (2000). Gakkel Ridge stretches 1,800 km across the Figure 1 3He fluxes at mid-ocean ridges. a,3He annual flux per 8. Pedersen, J. S. & Boomsma, J. J. Mol. Ecol. 8, 577–587 (1999). kilometre of ridge as a function of spreading rate.
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