Evolutionary Solutions to the Hairy Back Problem

Some creationists like to complain about macroevolution. They claim that this microevolution stuff is all well and good, but when has it ever produced any kind of meaningful change at the whole organism level?

This week's paper is an excellent rebuttal. Alistair McGregor of Princeton University has a paper in Nature that details how multiple minor changes to the regulation of the shavenbaby gene add up to a novel morphology in one species of fruit fly.

There's lots of fun to be had with fruit fly (Drosophila) gene names. The names usually describe the phenotype of flies with a mutated copy of the gene in question, so it's no surprise that the usual function of shavenbaby (svb) is in the development of larval trichomes, bristly hairlike structures that protrude from certain cells. The larvae of one Drosophila species (D. sechellia) have the same pattern of ventral trichomes as other related species, but a different pattern of trichomes on their backs. McGregor and colleagues from Princeton and Toulouse, France, set out to determine how this novel trichome pattern evolved.

The first stage of the study was to determine how svb is regulated in D. melanogaster, the standard model of fly genetics. Different sections of the DNA surrounding the svb gene were hooked up to a reporter gene. The reporter was expressed in embryos in visible patterns, as directed by the upstream D. melanogaster DNA. The researchers also stained embryos for the expression of a downstream target of the svb transcription factor. Target genes are only expressed in cells that first express a functional copy of the svb protein, so this second stain ensured that the observed patterns of reporter gene expression matched those of the natural svb gene. Three distinct regions of DNA, known as transcriptional enhancers, were found to control expression of svb in D. melanogaster, with each enhancer responsible for svb expression in different but overlapping cell types.

D. sechellia larvae lack expression of svb in one particular cell type, resulting in their restricted pattern of trichome formation compared to other related species. The researchers hypothesised that a mutation in one of the svb enhancers was to blame. They therefore repeated the first set of experiments using D. sechellia DNA to drive the expression of the reporter gene in D. melanogaster embryos.

Each of the three D. sechellia enhancers behaved slightly differently to the corresponding D. melanogaster sequence, driving expression of the reporter gene in different cell types and at different stages of development. The D. sechellia species has therefore evolved mutations in each of the three enhancers that drive expression of svb.

Interbreeding between D. sechellia and D. mauritiana produced offspring that resembled each parent, but also offspring with one of three different intermediate patterns of trichome formation, each one corresponding to inheritance of a different D. sechellia enhancer. Mutations to the DNA sequence of each svb enhancer (microevolutionary changes) therefore contribute to the novel morphology (macroevolutionary change) of D. sechellia embryos.

The authors state that the enhancer sequences of D. melanogaster and D. sechellia differ by 3-5%. However, they did not discuss whether any specific mutations to the enhancer sequences destroy or create known regulatory sequences that might explain the differential expression of svb in the two species. Hopefully their declared intention to undertake “fine-scale functional analyses of morphological differences between species” will include investigation of these potential evolutionary mechanisms.

The paper's discussion section raises a very interesting possibility. The regulation of svb expression is controlled by multiple upstream transcription factors. However, svb is also a transcription factor in its own right that controls the expression of multiple downstream genes. Mutations to svb are therefore perfectly placed to affect the entire trichome development process without the need to alter expression of an upstream transcription factor, which could have other phenotypic effects on the developing embryo. Evolution of svb may therefore be the only feasible permitted route to novel trichome patterns. I think that more dissection of the upstream and downstream regulatory networks is needed before we can say for sure, but this intriguing hypothesis provides yet another example of the evolutionary importance of changes to the patterns of gene expression.

HT to Chris Harrison for prompting me to get on with writing this summary!