Evolution of sex determination in ants

An important limitation in many social insect species is that they can’t be bred in the lab. Many ants are romantics at heart, and require just the right set of conditions to embark on a mating flight. This aspect of their biology makes them difficult subjects for functional genomic studies, since we are generally limited to the study of just two generations – the queen and her offspring. For many genetic studies, such as pedigree-based mapping of phenotypic traits, we need to analyze at least three generations.

For many years I have sought to find an ant species that could be bred in the lab and had interesting biological features to map. The ant Vollenhovia emeryi seemed like a good candidate. It has a remarkable reproductive strategy, reproducing in at least three different ways:

My former postdoc Misato is an expert at handling these ants and could cross them. Our idea was to map a wide variety of interesting traits, such as genes responsible for caste determination, and the various reproductive strategies. However, to our surprise, families produced by a backcross started to produce sterile diploid males.

In retrospect this should have made sense. It is generally known that ants, bees and wasps have a reproductive system called “complementary sex determination”, and this is what happens when you inbreed them. How sex is determined in clonal ants such as V. emeryi has not been known, but it makes sense that they would also use the same system.

In any case, the backcrossed ants stubbornly refused to produce appreciable numbers of queens and ordinary males, which we wanted to have for our other studies, but we did get plenty of diploid males. So, we pivoted the study to try to understand mechanisms of sex determination in this species, and what they mean for the evolution of sex determination.

Through a series of elegant studies, the research groups of Martin Beye and Martin Hasselmann have determined the specific molecular machinery of sex determination in honey bees, but whether this mechanism is conserved in other species has remained controversial. Our data suggest that V. emeryi also uses this mechanism, but also another completely separate sex determination pathway. This suggests that the honey bee-type mechanism might be very old (> 100 million years), but there might also other pathways that remain to be discovered. We are currently checking whether these loci are involved in other insects, such as wasps and bumblebees, which would suggest that they are even more ancient.

Although this was just side-note in the paper, complementary sex determination may be the reason why so many invasive ants are clonal, or have really bizarre reproductive systems that involve clonality to some extent. By their very nature they have to inbreed, and clonality may be a way around that.

The study was just published in PLoS Genetics and Letizia Diamante from OIST’s media section has written up a nice summary. This study was a tremendous amount of work for just two authors to do, but it is one of my favorite ones to date, because of the clean results that we obtained.

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