Heads or tails: How different species of flies repurpose genes to determine which end is up

Animals have many genes in common, but up to one third of the genes in a given species are only found in that species or its close relatives. One might think that those “orphan genes” are what truly distinguish a species, i.e., genes that control the body shape, size, or behavior. But a new study by scientists from the University of Chicago shows how even genes with a fundamental role early development of an embryo can change over relatively short time without changing the resulting body parts and functions of the fly.

One of the most consequential developments in the life of an insect is determining its polarity, or which end of an egg will develop the head and which will develop the tail. In Drosophila, the common fruit fly studied as a model species by biologists the world over, a gene called bicoid controls embryo polarity. The gene produces messenger RNA that congregates in one end of the egg, which becomes the head. In another type of fly, the common midge Chironomus, a gene called panish fills this role. The bicoid and panish genes are dedicated to establishing embryo polarity. Most fly species don’t have these genes, though, and yet they all manage to produce offspring with a head and tail. So, how did these new genes acquire the job of controlling embryo polarity?

In a new study published in eLife, biologist Urs Schmidt-Ott, PhD, and his collaborators, including Yoseop Yoon, a graduate student in Schmidt-Ott’s lab and first author of the study, identified three older genes that adopted this function in other fly species. They found genes with other, unrelated functions took on the job of establishing head-to-tail polarity in developing embryos by stashing their RNA in the anterior end of the egg (the part that ultimately forms the head).

“These genes come and go in evolution all the time, although they clearly control very important things in development,” Schmidt-Ott said.

Yoon’s experiments in moth flies show that a gene can keep its old function while evolving a new role, such as establishing embryo polarity. To do so, the mother deposits RNA of that gene at the anterior end of the egg. RNA from corresponding genes of Drosophila or Chironomus could play the same role for the moth fly’s gene function in specifying embryo polarity, too.

That means the new function for regulating polarity adopted by the old moth fly gene was the result of placing an alternative transcript of this gene at the right time and location in the egg, rather than evolving a new protein product, Schmidt-Ott said.

In other species, the polarity function may have evolved by the same mechanism, even when the species used a new gene with only this function. For example, the study suggests that the panish gene, which establishes embryo polarity in the Chironomus midge, inherited its function from an alternative localized RNA transcript of an older gene. Later, this gene duplicated and diverged, resulting in the unique panish gene. Yoon and Schmidt-Ott believe that panish diverged rather than acquiring the new function because it had fewer genetic constrains than its precursor.

Schmidt-Ott says this study gives his team new directions to explore in their research. “We want to understand why there are certain developmental mechanisms that frequently exchange key players in evolution,” he said. “What is it that allows this kind of evolutionary plasticity?”

The study, “Embryo Polarity in Moth Flies and Mosquitoes Relies on Distinct Old Genes with Localized Transcript Isoforms,” was supported by the National Science Foundation, the National Institute of General Medical Science, the University of Chicago, the National Center for Advancing Translational Sciences of the National Institutes of Health, and the National Institute of Allergy and Infectious Diseases. Additional authors on the study include Jeff Klomp from the University of North Carolina, Ines Martin-Martin, Frank Criscione, Eric Calvo, and José Ribeiro from the National Institute of Allergy and Infectious Diseases.