Developmental origins of normal and anomalous random right-left asymmetry: lateral inhibition versus developmental error in a threshold trait

Abstract

Dramatic examples of right-left asymmetry often inspire adaptive explanations, simply because it is hard to imagine how such forms could not be functionally significant. But are conspicuous morphological asymmetries necessarily adaptive? Surprisingly, in some species where direction of asymmetry is random, asymmetry in bilaterally paired traits may arise as a developmental error in a threshold trait. When cases of asymmetry are rare within a species, they are easily recognized as developmental errors. However, as asymmetrical individuals become more common, or if the asymmetry is in a signaling trait, the temptation to advance an adaptive explanation grows, particularly if the asymmetry is not clearly maladaptive. Several models of the ontogeny of asymmetry are described for both normal and anomalous random asymmetry of bilaterally paired traits. In the absence of selection, each model predicts different expected frequencies of symmetrical and asymmetrical individuals within a species, therefore such frequency distributions can effectively test for different models of development. In normal random asymmetries – where conspicuously asymmetrical individuals predominate – lateral inhibition of one side after the other has transformed appears to be an essential step in development. In anomalous random asymmetries – where conspicuously asymmetrical individuals are relatively rare – no lateral inhibition is required. Other potentially relevant variables include: purely stochastic variation in morphogen levels, useinduced asymmetry, and local (each side independent) versus central (e.g., hormonal) signaling. Examples of normal and anomalous random asymmetries are reviewed for several animal groups. A closer examination of the spectacular forelimb asymmetry in empidid dance flies raises doubts about claims that the asymmetry – both its occurrence and its direction – is adaptive, even though enlargement of the forelimbs likely is. Additional studies are required to conclude that this asymmetry is truly adaptive, as opposed to the outcome of random developmental variation in a threshold trait. This dance-fly leg asymmetry illustrates nicely how alternative hypotheses need to be considered before interpreting such variation as adaptive, even in a signaling trait.

Extreme developmental instability associated with wing plasticity in pea aphids

“…Quantitative traits vary in small ways with increases or decreases of various developmental signals, while threshold traits do not change unless the signal level is at or near the threshold. As noted by Palmer [36,37] when discussing left-right asymmetries, for some traits, thresholds can be achieved or missed independently on each side of an organism. He notes that another Hemipteran, the firebug Pyrrhocoris apterus, also has a wing dimorphism that sometimes yields extreme wing-asymmetry [38], suggesting that this phenomenon might be common among wing-dimorphic insects.…”

Genetic assimilation and the evolution of direction of genital asymmetry in anablepid fishes

“…The new breeding experiment in J. tucumana , a species showing an excess of left-sided males, also suggests a stochastic determination of the direction of the gonopodium, but in this case with a bias towards left-sided offspring. Assuming morphological asymmetries to be threshold traits [12,57,58] allows us to hypothesize how phenotypic variation in the direction of genital asymmetry is assimilated in anablepid fishes (figure 4): under the assumption that variation in a liability factor (e.g. morphogens) is mostly due to developmental stochasticity, individuals with a level of the liability factor above a certain threshold will develop right-sided gonopodia, and below this threshold, left-sided gonopodia.…”