The direction of genital asymmetry is expressed stochastically in internally fertilizing anablepid fishes

Abstract

Animal genitalia vary considerably across taxa, with divergence in many morphological traits, including striking departures from symmetry. Different mechanisms have been proposed to explain this diversity, mostly assuming that at least some of the phenotypic variation is heritable. However, heritability of the direction of genital asymmetry has been rarely determined. Anablepidae are internally fertilizing fish where the anal fin of males has been modified into an intromittent organ that transfers sperm into the gonopore of females. Males of anablepid fishes exhibit asymmetric genitalia, and both left- and right-sided individuals are commonly found at similar proportions within populations (i.e. antisymmetry). Although this polymorphism was described over a century ago, there have been no attempts to determine if genital asymmetry has a genetic basis and whether the different morphs are accumulating genetic differences, as might be expected since in some species females have also asymmetric gonopores and thereby can only be fertilized by compatible asymmetric males. We address this issue by combining breeding experiments with genome-wide data (ddRAD markers) in representative species of the two anablepid genera with asymmetric genitalia: Anableps and Jenynsia . Breeding experiments showed that all offspring were asymmetric, but their morphotype (i.e. right- or left-sided) was independent of parental morphotype, implying that the direction of asymmetry does not have a strong genetic component. Consistent with this conclusion, association analyses based on approximately 25 000 SNPs did not identify markers significantly associated with the direction of genital asymmetry and there was no evidence of population structure between left- and right-sided individuals. These results suggest that the direction of genital asymmetry in anablepid fishes might be stochastic, a commonly observed pattern in species with antisymmetry in morphological traits.

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

“…Antisymmetry is likely the ancestral state in the two extant genera with gonopodia (figure 2). Previously, we predicted that the probabilities of observing transitions from antisymmetry to directional asymmetry were low, considering the small additive genetic variation observed for the direction of genital asymmetry [28]. Here, we show that in the family Anablepidae the transition from antisymmetry to directional asymmetry indeed occurred multiple times, suggestive of recurrent genetic assimilation of the direction of asymmetry in this group of fishes.…”

“…To sum up, this model might help reconcile the lack of heritability of sidedness (e.g. [28,61]), and the lack of response to artificial selection on the direction of asymmetry (e.g. [14,15,62,63]), with the fact that the direction of asymmetry certainly evolves [11,17].…”

“…To determine if variation in the direction of asymmetry has a heritable component, we conducted crosses with J. tucumana following previously described protocols [28]. Females of this species have symmetrical genitalia.…”

“…Additionally, Anableps females also possess an asymmetric structure that laterally covers the gonopore, called a foriculum [20]. The antisymmetric pattern in males is associated with an apparent lack of heritability for bending sidedness, as the direction of asymmetry was found to be expressed stochastically in anablepid fishes [28]. However, some populations have been reported to be monomorphic in terms of genital sidedness [29,30].…”

“…However, some populations have been reported to be monomorphic in terms of genital sidedness [29,30]. This could indicate possible transitions between antisymmetry and directional asymmetry, which would suggest genetic assimilation of this character because of its lack of heritability [28]. Yet, these reports are anecdotal and not associated with particular populations or species [29,30].…”