No sex please

Once upon a time, if there was something that could be taken for granted about ants, it was that reproduction depends on mating, that is, sex. Admittedly, males come from unfertilized eggs; but against that, all females have a father from whom they receive half of their genome. However, ants are full of surprises; and though most species do in fact follow the norm, there is at least one that contradicts it. This is Cataglyphis cursor, whose queens behave with reckless abandon, sometimes using male sperm to have daughters and sometimes not bothering. Sexual and asexual reproduction are all the same to them.

Sexual reproduction has been a bother to biologists for a long time. What is sex for? Why should sexual reproduction be so widespread throughout the animal kingdom? If you think about it, this way of having children is rather inconvenient, given that it requires two partners of opposite sex to come together and that this is a matter of chance. From the genetic point of view, this is particularly unprofitable for the mother, since it restricts her to passing on only half of her genes. In addition, she invests half of her reproductive energy in having male offspring, who are not very useful except for fertilizing eggs. This makes for a very wasteful system, marked by what the British biologist John Maynard Smith famously defined as 'the twofold cost of sex'. Nevertheless, there is much to be said in favour of sexual reproduction. For a start, the mix of parental genes passed on to children makes for increased genetic diversity in the population. Over evolutionary time, this constant mingling of genetic inheritances leads to the elimination of deleterious genes and the preservation of functional ones. A noteworthy long-term consequence of this is that it produces individuals who are more resistant to parasites and other pathogens.

This is the reason why, although asexual reproduction has appeared many times, species that go in for it do not last long in evolutionary terms. Some species of arthropods, some insects, and some lizards still contrive to do without sex, but they are a tiny minority in the animal world. Ants, however, do not belong to that small category; and myrmecologists were for a long time convinced that all queens had recourse to sexual reproduction. Witness any mating flight and it will be apparent that queens are not averse to copulating with males. However, close study of Cataglyphis cursor, with Morgan Pearcy and Serge Aron of ULB and Claudie Doums from the University of Paris VI, led us to recognize that there was more to it than that. The interesting point about this particular species was that some of the behaviours of its queens are unusual. In these monogynous colonies, the young virgin queen does not fly away in search of a mate. All she does is leave the nest and wait until males come to her; at that point she copulates with them, still on the ground close to the nest, before going back inside as soon as the love-making is over. She stays in the nest only as long as it takes to gather together a party of her sister workers, then sets off with her troops to found her own nest a few metres away.

Intrigued by Cataglyphis cursor, we collected thirty-eight colonies in the south of France and analysed their DNA, using genetic markers, with the object of determining who had begotten whom and how. To our great surprise, we discovered that the genotype of the young queens was not the same as that of their sister workers. It eventually turned out that the vast majority, 90 per cent, of young queens were the outcome of asexual reproduction. They had not hatched from fertilized eggs but were produced via parthenogenesis. What is going on here? Remember that all female ants (queens and workers) are diploid, that is their cells contain one set of chromosomes from each parent, whereas male cells are haploid, as they receive only the maternal chromosomes. Thus daughters born via sexual reproduction inherit two sets of chromosomes, one maternal and one paternal. In the case of parthenogenesis, however, there are no paternal chromosomes. The maternal cell divides, each of its two parts bearing a set of chromosomes, which then recombine to form the daughter cell (see Figure 3). This means that young Cataglyphis cursor females of royal caste, having no father, inherit all their genes from their mother. Workers, on the other hand, follow the standard pattern of females and hatch from fertilized eggs.

Thus the queen has it both ways, eating her cake and having it. By producing new queens via asexual reproduction, she avoids paying the cost of sex, because she hands on all her genes to her reproductive daughters. But by using sexual reproduction to give birth to barren daughters, she manages to maintain the colony's queen male

male future queen worker

Figure 3 Parthenogenesis In Cataglyphis cursor ants, queens produce their sons and their worker daughters by the 'normal' method. Thus males, from unfertilized eggs, receive half the genes of their mother (1), while the workers, produced by sexual reproduction (3), inherit half their mother's genes and all their father's. On the other hand, mothers produce young queens asexually, by parthenogenesis (2). In this case, the maternal cells divide in two, each of them bearing a set of chromosomes that recombine to make a daughter cell. So the young queen inherits genes only from its mother and the two females have a degree of kinship (r) equal to 1. However, because of the chromosome recombinations that occur during parthenogenesis, the genomes of the mother and daughter are not identical.

genetic diversity and reinforce the workers' resistance to parasites. This, as the workers are in constant contact with the outside world, is very advantageous for them. If the queens, by being produced asexually, are more prone to pathogens, their risk of being infected is reduced, as they are constantly protected by the workers.

In all of this, the males are once again the losers. If they are to pass on copies of their genes to posterity, their only hope is to find one of the rare queens hatched from a fertilized egg, a thing which can happen, given that there are always exceptions to the rule and about 10 per cent of the female reproducers are not born via parthenogenesis. Even so, the males' reproduction rate is pretty low. The only way they can improve it is if the queen dies, because then the workers make haste to replace her by producing young queens. Being unmated, they can of course only do this via parthenogenesis; but that is immaterial, since they are passing on their paternal genes to the future queens, who will transmit them in their turn to their own progeny. All things considered, the males hand on very little of themselves to posterity and appear to be duped all along the line.

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