Internal Selection Against the Evolution of Left-Right Reversal

Abstract

Among metazoan species, left-right reversals in primary asymmetry have rarely gone to fixation. This suggests that a general mechanism suppresses the evolution of polarity reversal. Most metazoans appear externally symmetric and reproduce by external fertilization or copulation with genitalia located in the midline. Thus, reversal should generate little exogenous disadvantage when interacting with the external environment or in mating with the common wild-type. Accordingly, an endogenously caused fitness reduction may be responsible for the general absence of reversed species. However, how this selection operates is little understood.Phenotypic changes associated with reversal are usually inseparable from zygotic pleiotropy. By exploiting hermaphroditism and the maternal inheritance of left-right polarity, we generated dextral and sinistral snails that share the same zygotic genotype.Before hatching, these sinistrals developed lethal morphological anomalies more frequently than dextrals. Their shell shape at maturity differed from the mirror image of the dextral shell. These interchiral differences demonstrate pleiotropy in maternal effects of the polarity or linked genes. Variation in interchiral differences between parental crosses suggests the presence of epistatic variation in relative performance of sinistrals. Our results show that internal selection operates against polarity reversal, and we suggest that this is due to changes in blastomere configuration.K E Y W O R D S : Chirality, homochirality, maternal epistasis, maternal inheritance, maternal pleiotropy, situs inversus.

Phylogenetic reconstruction and shell evolution of the Diplommatinidae (Gastropoda: Caenogastropoda)

“…Transitioning from dextral (the most common state) to sinistral is probably rare due to frequency dependent selection, as inter-chiral mating is difficult to impossible due to physical limitations of mismatching anatomy, at least in pulmonate land snails (Gittenberger, 1988;Schilthuizen and Davison, 2005). However, developmental constraints might also affect the appearance of species with chirality reversals (Schilthuizen and Haase, 2010;Utsuno et al, 2011).…”

Analyzing Fluctuating Asymmetry with Geometric Morphometrics: Concepts, Methods, and Applications

“…Such differences have been found for snail shells in species with dimorphism due to sinistral and dextral coiling [111][112][113][114] as well as for the "left-sided" and "right-sided" forms of the European flounder [183].…”

“…More recently, dozens of studies in a wide range of different animal taxa have found statistically significant directional asymmetry of shape [13,16,. Even in snails where morphs with opposite directions of shell coiling occur within populations, a subtle directional pattern of asymmetry is superimposed on the dimorphism, because the average shell shapes of the two morphs are not precise mirror images of each other [111][112][113][114]. Therefore, just as conspicuous directional asymmetry of internal organs is near-ubiquitous among bilaterian animals, it seems that, for a wide range of animals, even structures that seem superficially symmetric show a subtle directional asymmetry of shape.…”

Development of a feeding trochophore in the polychaete Hydroides elegans

“…In gastropods, dextral and sinistral species have been described (Schilthuizen and Davison, 2005). Some species maintain dimorphism among individuals, although selection generally favors the consolidation of chirality (Utsuno et al, 2011). Cytoskeletal differences implementing alternative chirality within species have been identified in Lymnaea stagnalis (Shibazaki et al, 2004), but the earliest genetic mechanisms that determine spindle orientation among dextral and sinistral species remain unknown.…”