Developmental "noise" -- the imprecision in molecular pathways that leads to minor slip-ups in development -- creates fodder for evolution. That's the conclusion of a paper published online yesterday (July 5) in Nature, which shows that a single mutation in bacterial spore formation that affects individuals in different ways generates morphological diversity that can then be genetically fine-tuned to maximize an organism's fitness.

"Noise may help in the evolutionary transition from one fate to another," Avigdor Eldar of the California Institute of Technology in Pasadena, the study's lead author, told The Scientist.

B. subtilis cells sporulating into a forespore (green) and mother-cell (red) Image: Avigdor Eldar, Caltech

Many genetic mutations often cause different phenotypes in different individuals, even under identical environmental and genetic backgrounds. This phenomenon, known as partial or incomplete penetrance, has been well documented in myriad developmental systems, but its underlying genetic basis and adaptive value have remained elusive.

Eldar and his colleagues at Caltech and Temple University in Philadelphia studied partial penetrance in spore formation in the rod-shaped bacterium Bacillus subtilis. Under stress, a B. subtilis cell normally doubles its chromosomes and divides unevenly into a smaller cell, which develops into a heat- and desiccation-resistant spore, and a larger "mother" cell, which nurtures and supports the spore. But identical individuals with mutations in the spoIIR gene, which codes for a secreted protein involved in the mother-spore cell differentiation, can adopt any of four different fates, depending on the number of cellular compartments and chromosomes: normal single spores, defective double spores, spores with polyploid mother cells, and functional "twin" spores.

Twin spores can be beneficial under particularly harsh conditions, but jumping from single spores to twin spores requires changing cell signaling, division, and chromosomal replication. This is a difficult evolutionary feat because the intermediate steps can be non-adaptive or come with serious fitness costs. But the partial penetrance associated with developmental noise can help bridge the genetic gap. If a mutation in any one of these processes creates a low-level occurrence of the twin phenotype, as spoIIR does, then "additional mutations can assimilate the noise so [the bacteria] become less dependent on the noise and more dependent on the developmental program for making twins," said Eldar, a postdoc with Caltech's Michael Elowitz, the paper's senior author.

C. oceanicum twinning into two white spores within the darker cells Image: Avigdor Eldar, Caltech

Eldar's team modulated the levels of other genes involved in the sporulation pathway and found that they could tip the balance toward twinning or other mutant traits. They also looked at another microbe called Clostridium oceanicum, which is known to naturally form twin spores, and showed that the spore-forming process was similar to that in the B. subtilis spoIIR mutants. Together, said Eldar, this shows that partial penetrance creates the necessary variation for an organism to evolve toward an adaptive trait -- twin sporulation in this case.

The study "opens a new door in our understanding of the molecular underpinnings of phenotypic evolution," Heather Maughan, an evolutionary microbiologist at the University of Toronto, wrote in an email. "Perhaps it is the case that phenotypes with large noise components are more evolvable; this is a fascinating hypothesis."


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