Population stochasticity, random determination of handedness, and the genetic basis of antisymmetry

Conspicuous lateral asymmetries of organisms are classified into two major categories: antisymmetry (AS), characterized by almost equal frequencies of dextral and sinistral morphs, and directional asymmetry (DA), in which one morph dominates. I compared and characterized two types of genes, both with existing examples, in their roles in the evolutionary transitions between AS and DA for the first time. Handedness genes (HGs) determine the chirality in a strict sense, while randomization genes (RGs) randomize the chirality. A theory predicts that, in an AS population maintained by HGs under negative frequency-dependent selection, RGs harness fluctuation of the morph frequencies as their driving force and thus increase their frequency until half of the population flips the phenotype. These predictions were confirmed by simulations. Consequently, RGs mask the genetic effects of HGs, which provides a possible explanation for the apparent lack of a genetic basis for AS in empirical AS studies.

► Dextrals and sinistrals are equally frequent in some organisms (antisymmetry: AS).
► Handedness-determining or randomizing genes (HGs and RGs, respectively) can cause AS.
► Theory predicted that negative frequency-dependent selection prefers both HGs and RGs.
► Population stochasticities caused prevalence of RGs, resulting in masking of HGs.
► The results provide an explanation for the apparent lack of a genetic basis in AS.