Biology

Same genes, different body: the making of a queen

English: Biston betularia caterpillars on birc...

An example of polyphenism: Biston betularia caterpillars on birch (left) and willow (right). (Photo credit: Wikipedia)

How tall are you? Almost everyone I know (myself being an exception) is taller than their same-sex parent, who is, in turn, taller than their same-sex parent. Over recent generations, average height has increased in many parts of the world. This is far too quick to put it down to an evolutionary change based on shifting genetics. Most of us are taller than our parents and grandparents because of our environment — better nutrition, fewer diseases, and less hard labour in our developing years.

But if you really want to see what environmental cues can do to body shape and function, consider the case of social insects. The environment in which a larva is nurtured determines whether it goes on to be a queen or a worker. The caste system of insects is an example of a phenomenon called polyphenism, where the same set of genes (genotype) can result in vastly different body forms (phenotypes). Unlike height in humans, which varies along a continuum, polyphenism in insects creates discrete types. There’s no half-way point between worker and queen; you’re either one or the other. In the one case, you are bound for reproductive glory, in the other, you remain sterile. 

English: Profile view of ant Pogonomyrmex rugo...

Pogonomyrmex rugosus (Photo credit: Wikipedia)

For a wide range of insects — from aphids to firebugs to locusts — environmental conditions that the mother is exposed to affect the form that her offspring will take. These intergenerational maternal effects are at play in determining whether firebugs turn into winged or wingless morphs, and whether a locust will become a homebody (solitary morph) or catch the travel bug (dispersal morph).

In seed harvester ants (Pogonomyrmex rugosus), exposure of a queen to the cold hibernating temperatures of winter and the queen’s age have been found to play a role in determining whether her female offspring are able to become queens — the first described case of maternal effects playing a role in caste determination. Eggs laid by young queens invariably produce worker ants. The same is true for eggs laid by queens who have never experienced the bitter cold of winter. But if a queen has reached the ripe old age of 2 years, and has gone through a period of hibernation, new queens will be found in her brood. This is irrespective of whether or not her worker colony-mates have also undergone hibernation.

In a follow-up to their original study, Laurent Keller and colleagues have picked apart some of the mechanisms responsible for caste determination in seed harvester ants. They suspected that hormonal cues in the queen and her developing larvae were responsible for translating environmental conditions experienced by the queen into caste instructions for her offspring.

In bees, a diet of royal jelly is the difference between a larva becoming a queen bee or an ordinary worker. The diet, laced with the active ingredient royalactin, bumps up activity in two hormonal pathways: the insulin/insulin-like growth factor signalling (IIS) pathway, and the juvenile hormone (JH) pathway. With JH being pumped out at higher levels, a third pathway — the vitellogenin (Vg) pathway — is triggered, a process essential for the making of a queen.

To determine whether IIS, JH or Vg are responsible for conveying the maternal messages in seed harvester ants, Keller and colleagues tried to override the ants’ natural cues by tinkering with their hormones. The first hormone that they tested was juvenile hormone (JH), an insect hormone essential for larval development, but which prevents progression into adulthood. JH is also necessary for egg production by the queen. Queen ants fed on a diet of artificial JH (methoprene) produced a higher number of queens than those that weren’t given the hormone analog. The treatment was effectively able to mimic queen hibernation.

A fried egg, sunny side up.

Queens can only develop when the egg yolk protein, Vitellogenin, is abundant. (Photo credit: Wikipedia)

Genes in both the JH and IIS pathways were cranked up in hibernated and methoprene-treated queens. While this doesn’t answer the chicken and egg question of which pathway is triggering the other, it does suggest that both pathways are important for passing on the intergenerational message necessary for queen-making.

The researchers also measured the content of the egg-yolk protein, Vg, in the ant eggs. Those with higher levels of Vg were more likely to develop into queens. Just as the bright yellow egg yolk of a chicken egg feeds the developing chicken embryo, the egg yolk protein Vg is thought to be a source of nutrients for the developing ant embryo.

Why more Vg pushes an embryo down the developmental pathway towards a queen is not yet known, but it is interesting that a nutritional factor is at play, just as it is in bees.

References: 

  1. Schwander, Humbert, Brent, Cahan, Chapuis, Renai & Keller. 2008. Maternal effect on female caste determination in a social insect. Current Biology. 18: 265-9. doi:10.1016/j.cub.2008.01.024
  2. Libbrecht, Corona, Wende, Azevedo, Serrão & Keller. 2013. Interplay between insulin signaling, juvenile hormone, and vitellogenin regulates maternal effects on polyphenism in ants. Proceedings of the National Academies of Science USA. Published ahead of print June 10, 2013, doi:10.1073/pnas.122178111
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