Why do queen fungus-growing ants mate with so many males?

There are several hypotheses that have been put forward to explain why female fungus-growing ants should gain an advantage from mating with many different males.

Sperm supply

A queen fungus-growing ant must store all the sperm from her nuptial flight that she will need to fertilise her eggs for the rest her life. In the higher attines, this can be as long as 20 years, and she must fertilise hundreds of eggs every day. This means that the queen needs to store millions of spermatozoa. It is possible that mating with only one or a few males would not provide the queen with enough sperm. Hence it might be advantageous for her to mate with many males.

Genetic diversity

Most fungus-growing ant colonies have only a single queen, and all the workers and reproductives produced by the colony are her offspring. This means that they will all share some of her genes. If she mates with only one male, all the worker offspring and new queens will also share some of his genes (males are special in ants, they have no father and only have the genes from their mother, the queen). If she mates with more than one male, however, the genetic diversity of the colony will increase, because although all the offspring will share some genes from the queen, the offspring of different males will have genes from the different fathers. The more males she mates with, the greater will be the genetic diversity of the colony. Why might there be an advantage to having greater genetic diversity within the ant colony? There are several hypotheses:

Increased efficiency through division of labour.
 
If the genetic make-up of a worker makes it particularly suitable for a particular task, then a colony which has a higher genetic diversity may be able to carry out more tasks more efficiently.
 
Decreased susceptibility to diseases and parasites.
 
If the genetic make-up of a worker makes it particularly resistant to a particular disease or parasite (even if it is more susceptible to other diseases and parasites), then a colony which has a higher genetic diversity may be better able to withstand attack by a wider variety of parasites and pathogens.
 
Decreased risk of diploid male production.
 
Sex determination in ants is thought to be through a system using a single locus with multiple alleles. Each worker ant receives two copies of the locus, one from its mother and one from its father. If these two copies are different (ie. the alleles are different) then the ant will develop as a normal female worker. However, if the two alleles are the same, the ant will develop as a sterile diploid male who cannot work and will be a drain on colony resources. If the queen mates with several males, then the consequence of one of them having the same allele as her will be less serious as a smaller proportion of her offspring will develop as diploid males.

Genetic conflict within the colony

Ants, bees and wasps are haplodiploid. This means that unfertilised eggs develop as males, and are haploid (they only have one set of genes, those from their mother), while fertilised eggs normally develop as females, and are diploid (they have two sets of genes, one from their mother and one from their father). Diploid males are an exception (see above) where because there are two copies of the same allele at the sex determining locus they are effectively haploid at this locus and so develop as males that are sterile because they are diploid.

The haplodiploid system means that if a queen has only mated once, then workers are more closely related to the new queens produced by a colony than to the males produced by a colony. However, the queen is equally related to both new queens and males. This leads to a genetic conflict over the production of new queens and males between the queen and the workers. The workers will do best by producing more new queens than males, while the queen will do best by producing them in roughly equal numbers. This genetic conflict can lead to actual conflicts in which males produced by the queen are killed by the workers before they mature. If the queen mates with more than one male, however, the average relatedness of workers to the new queens decreases, because the worker and new queen may be half-sisters instead of full sisters. The relatedness of workers to the males does not change, because male ants only have genes form the queen. Hence as the number of males with which the queen mates increases, the genetic conflict between the workers and the queen decreases. This may lead to a reduction in actual conflict in the colony, which may allow the colony to be more efficient.

Colony size and mating frequency

Many of the possible advantages of multiple-mating vary depending on the colony size of the fungus-growing ant colony. If the colony has relatively few workers, then the queen will not need to store so much sperm to produce all the ants that the colony needs. Similarly, in a smaller colony each worker will have to perform several different tasks regardless of its genetic make-up, so that it would not be possible to increase the efficiency of division of labour with increased genetic diversity.

The advantages of reduction in the effect of diploid males and reduction in genetic conflict are independent of colony size. Hence it is potentially possible to distinguish between some of these hypotheses by examining the relationship between colony size and multiple mating across the fungus-growing ants.

Phylogeny and mating frequency

The phylogenetic position of any fungus-growing ant species may be correlated with the number of males with which a queen is likely to mate. This can be through the correlation between position in the phylogeny and factors such as colony size and exposure and susceptibility to pathogens, which are likely to influence the advantage of multiple mating. However, ancestry is also important. Species that have evolved from a common ancestor that shows single-mating are more likely to show single-mating than species that have evolved from a common ancestor that shows multiple-mating. Hence, the phylogenetic position of each species of fungus-growing ant must be taken into account when multiple-mating is studied. Conversely, the patterns of mating strategy found in the different fungus-growing ants can give information about how the group is likely to have evolved, what their nearest common ancestor was likely to have been like.