, , , , , , , , , , ,

Solenopsis invicta (Photo credit: AJC1)An international team of researchers studying fire ants have discovered the first “social chromosome”.  While this is obviously exciting to those of us who are fascinated by the advanced social organization of ants, the discovery also has broader implications.  The mechanism the researchers uncovered is similar to how sex is determined in many animals, creating the tantalizing possibility that it might be an example of a more general mechanism for evolving distinctly different complex behaviours.

Despite their regal title, ant queens aren’t the rulers of a colony, but rather its reproductive heart; without a queen, dying workers wouldn’t be replaced and the colony would wither away.* The queen also gives birth to the young, virgin queens and short-lived males who go on to found new colonies. Unlike the workers, these winged ants are fertile; when conditions are just right, they fly off to join sexual ants from other colonies in a gigantic ‘nuptial flight’ — the only time in their life they will mate. Having served their purpose, the males die shortly afterwards; the young queens live on, however, carrying within them enough sperm to produce the hundreds of thousands of workers needed over the life of a colony.

What happens next depends on whether the queen tries to found a new colony alone or with help.  Although popular depictions tend to include only a single queen, ant colonies can also have many queens, several of which might be reproductively active. In the fire ant Solenopsis invicta, as in many other species, the single-queen and multi-queen colonies are quite distinct forms of social organization. Queens from multi-queen colonies tend to have help from workers when starting a new colony; they are also smaller and produce less offspring than queens in single-queen colonies.  Workers from these colonies are also smaller, while the males tend to produce less sperm.  These consistent differences have been described as a “multi-queen syndrome”, a collection of physical and behavioral characteristics that distinguish multi-queen and single-queen colonies.

Over a decade ago, Laurent Keller and Kenneth Ross discovered that fire ants from the two colony types had different versions of a gene, Gp-9, which produces a protein involved in scent perception. Despite the importance of chemical signalling in ant society, the researchers weren’t convinced that a single gene could affect the diverse range of traits involved in the multi-queen syndrome.  Keller and his colleagues therefore speculated that Gp-9 might in fact be part of a “supergene” cluster that was responsible for these differences. In a paper appearing this week in Nature, they used several thousand markers to map the genes in ants from the two colony types; based on these maps, they found a cluster of over 600 genes around Gp-9 that are all always inherited together. Only one version of this cluster of genes is found in single-queen colonies, while multi-queen colonies can have both versions.  The cluster takes up more than half the chromosome on which it’s found, leading the team to dub this the “social chromosome”.

What keeps this cluster together, though? Normally, a process called “crossing over” swaps DNA between the maternal and paternal chromosomes in a pair, ensuring that different versions of genes get mixed together. In order for the cluster of genes around Gp-9 to be Inversion blocking crossing overinherited together, something has to interfere with this process. One way this might happen is if there was a structural change that stopped the two chromosomes in a pair from properly lining up during crossing over. To test this idea, the teams used fluorescent markers to label specific positions on the “social” chromosome. Some of the markers showed up in a different order on the two versions, showing that a stretch of the chromosome had somehow become inverted during the evolution of S. invicta.  The inversion stops the chromosomes in a pair from lining up, preventing crossing over and thereby ensuring that the cluster remains intact.

A similar mechanism is at play in how sex is determined in mammals. In what is called the “XY system“, individuals with two X chromosomes develop as females while XY individuals develop into males. Like the two forms of the social chromosome, the X and Y forms of the sex chromosome can’t line up together and undergo crossing over. This is because a variety of traits have to be coordinated differently during the developments of males and females, just as multi-queen colonies consistently differ from single-queen colonies. In both cases, the collection of traits is kept together by ensuring that the genes responsible for them are inherited as a single unit; the cluster of genes is maintained because structural differences in the two versions of the chromosome prevent crossing over between them. Crossing over is also repressed in the ZW sex determination system used by reptiles, birds, and some other organisms, although in that case ZZ individuals are male and ZW individuals are female.

Despite the similarity in their genetic underpinnings, social organization and sex determination are vastly different processes; they rely on similar mechanisms because in both cases a set of traits need to be inherited together consistently.  Rather than trying to compare the social organization of fire ants to sex determination in mammals, I’d prefer to take this as a chance to see sex through a different lens: as a complex collection of traits associated with a particular biological or reproductive organization which we’ve come to label “male” and “female”.  The inhibition of crossing over, which seems to maintain both the “multi-queen syndrome” and the “sex syndrome”, might also underlie other complex behaviours or characteristics that have evolved into two distinctly different forms.

*This is true of most ant species. In some cases, though, workers are fertile and can reproduce; there’s even a species in which the workers reproduce asexually. Although infertile workers can’t keep the colony alive, they can produce males since male ants (and bees and wasps) are born from unfertilized eggs.

Wang, J., Wurm, Y., Nipitwattanaphon, M., Riba-Grognuz, O., Huang, Y., Shoemaker, D., & Keller, L. (2013). A Y-like social chromosome causes alternative colony organization in fire ants Nature, 493 (7434), 664-668 DOI: 10.1038/nature11832