New discoveries often highlight just how counter-intuitive and complex evolution can be. Take, for example, the gene that determines which end of a fly embryo will develop into the head and which end will develop into the tail. In the common fruit fly Drosophila and related flies, the gene bicoid controls this crucial function. When it is artificially turned off, larva develop in a dramatically abnormal fashion (with two heads and no tail, or two tail ends and no head, depending on the experiment). However, most flies and other insects lack bicoid, and how they establish their head-to-tail polarity has been poorly understood.
In a study published today in the journal Science, a team of UChicago scientists present their discovery of a new gene, called panish, that controls head-to-tail patterning — but only in a specific group of midge flies. They found that panish, which appears to have evolved more recently, has the same developmental role as bicoid. Moreover, the team found that bicoid appears to have been lost or altered in certain fly families during evolution. One would assume that the genes that regulate such a critical developmental process would be incredibly resilient against change, but the new findings suggest that these evolutionary “innovations” happen all the time, in flies at least.
“The genes that drive embryonic polarity are not conserved across flies and their evolutionary replacement does not seem to be rare at all,” said study senior author Urs Schmidt-Ott, PhD, associate professor of organismal biology and anatomy at the University of Chicago. “The hijacking of this early developmental pathway by novel or newly evolved genes happens at a much higher frequency than previously thought.”
Early studies of chironomids, a group of mosquito-like midges, found that ultraviolet light or a chemical which destroys RNA targeted toward the front portion of embryos led to double-abdomen formation (two tail ends and no head), which suggested that localized RNA in the anterior egg might function as head determinant.
To identify which gene products were being disrupted, Schmidt-Ott and his colleagues profiled and compared gene expression levels between the front and rear halves of Chironomus embryos. Out of thousands of candidates, the team identified a specific gene that appeared to be necessary for the formation of head-to-tail polarity. Double-abdomen formation occurred when this gene, called panish, was silenced in early Chironomus embryos. These embryos could be returned to normal with the addition of an independent source of panish gene product.
Although panish and bicoid perform essentially the same function, they are structurally unrelated and found in completely separate families of flies. Both genes act by regulating other genes involved in genetic patterning, but panish represses them while bicoid activates them.
The team found no evidence of panish in flies other than Chironomus, suggesting that panish is a newly evolved gene that appropriated the function of regulating head-to-tail polarity. They also reexamined the occurrence of bicoid and discovered that the gene has been repeatedly lost or substantially altered in certain fruit flies and tsetse flies during evolution.
Despite the importance of head-to-tail patterning in early embryonic development, it appears that genes that regulate the process are poorly conserved in flies, and that new genes took over the role far more often than previously thought.
The discovery of this phenomenon now opens a multitude of new research avenues. Schmidt-Ott and his colleagues are now investigating questions such as how do genes appropriate new roles, why it happens so frequently, and whether such instances share common features.
“It’s astonishing how a newly evolved gene can, in a very short amount of time, take over control of such a fundamental process,” Schmidt-Ott said. “Given that a small sample of examined genomes already suggests four independent fundamental substitutions, we probably are looking at the ‘tip of the iceberg’ for these events.”
The study, “A cysteine-clamp gene drives embryo polarity in the midge Chironomus,” was supported by the National Institutes of Health, the National Science Foundation and the University of Chicago. Additional authors include Jeff Klomp, Derek Athy, Chun Wai Kwan, Natasha I. Bloch, Thomas Sandmann and Steffen Lemke.