Study begins to unravel mysterious evolution of fatherless male insects

It’s not often you see genetic systems described as “bizarre” in the title of a scientific research paper. Unless it comes from the lab of Scott Roy, an associate professor of biology at San Francisco State University, who has a particular penchant for strange genetics.

In his latest paper for PNAS †Proceedings of the National Academy of Sciences), Roy and his collaborators provide the first empirical evidence supporting a hypothesis for the evolution of haplodiploidy, the unusual sex-determining system found in species such as bees, ants and wasps.

The most well-known sex-determining system is the XX/XY system, where women usually have a pair of X sex chromosomes and males have an X and Y. In many species (such as humans), a sperm and egg haploid cells each containing a single copy of genetic material, including a single sex chromosome, come together to create a diploid individual with two copies of genetic material. However, in haplodiploidy, females follow the egg-sperm system while males only emerge from an egg. This means that males only have half the genetic information of their female counterparts (all from their mother).

“There’s kind of a fundamental puzzle in biology, and how do weird things get there?” said Roy. “Either the weird thing evolved in one step, or it must have happened through a series of steps, each of which was accepted by evolution.”

The problem is that it’s difficult to explain the evolutionary transition from the more familiar sex-determining system to haplodiploidy, Roy says. Because haploid men have less genetic material and no paternal genes (Reduce) genetic diversity), we would expect them to have a lower survival rate. So how did species sustain haploid males?

The key may lie in intragenomic conflicts (ie conflicts between different genes within an individual) that destabilize genetic systems and promote the origin of new systems (such as haplodiploidy). According to this hypothesis, genes linked to the father’s X chromosome may bias sperm production toward making more X-containing sperm, leading to more daughters (XX) than sons. If so, it could boost production of haploid males to rebalance the male-to-female ratio. Researchers suspect this would happen in the presence of a larger X chromosome.

“The idea that a conflict between genes in a single organism could drive evolution has been around for some time, but to date there are few, if any, empirical tests of it,” Roy said.

That’s because it’s a difficult hypothesis to test in known species and differentiate from other possible explanations, he adds. But that didn’t stop him and his associates.

They sequenced the entire genome of dark-winged fungus gnats, gall midges/mosquitoes and springtails to circumvent some of their experimental challenges. These species are essentially haplodiploid, but would allow the researchers to separate the conflict hypothesis from other proposed hypotheses.

The analysis found that these species indeed have very large X chromosomes compared to related diploid species. Their large X chromosomes took between 16% and 66% of a. confiscated typesgenome.

“Normally 1 to 5% of the genome is about the X chromosome, but in these systems it’s almost half the genome. That’s a very big and obvious difference,” said first author Noelle Anderson, a University of California , Merced Ph.D. † student in Roy’s lab. (Roy holds a secondary adjunct professorship at UC Merced.)

The exciting thing is how clear the data is, Roy explains. “We’re talking more than tens of millions of years of evolution, maybe hundreds. And to see this clearly, a pattern in bioinformatics data is almost unheard of,” he added.

This evidence supports the idea that intragenomic conflict could drive the evolution of new biological systems, Roy says. He credits the culture of SF State for encouraging him to pursue this tricky project.

“I would never have developed the skills or the confidence for us to get started with this [research] direction, so it’s kind of a tribute to the state of San Francisco,” Roy said. “I feel a lot of intellectual freedom here.”

Anderson, who initially worked with Roy in the summer of 2014 as an SF State NSF Research Experience for Undergraduates researcher, will return to college after graduating as a bioinformatics lecturer.