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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.

SUBMITTER: Torres-Dowdall J

PROVIDER: S-EPMC7423465 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Fertilization mode may affect sperm characteristics, such as morphology, velocity, and motility. However, there is little information on how fertilization mode affects sperm evolution because several factors (e.g., sperm competition) are intricately intertwined when phylogenetically distant species are compared. Here, we investigated sperm characteristics by comparing seven externally and four internally fertilizing marine fishes from three different groups containing close relatives, considering sperm competition levels. The sperm head was significantly slenderer in internal fertilizers than in external fertilizers, suggesting that a slender head is advantageous for swimming in viscous ovarian fluid or in narrow spaces of the ovary. In addition, sperm motility differed between external and internal fertilizers; sperm of external fertilizers were only motile in seawater, whereas sperm of internal fertilizers were only motile in an isotonic solution. These results suggest that sperm motility was adapted according to fertilization mode. By contrast, total sperm length and sperm velocity were not associated with fertilization mode, perhaps because of the different levels of sperm competition. Relative testis mass (an index of sperm competition level) was positively correlated with sperm velocity and negatively correlated with the ratio of sperm head length to total sperm length. These findings suggest that species with higher levels of sperm competition have faster sperm with longer flagella relative to the head length. These results contradict the previous assumption that the evolution of internal fertilization increases the total sperm length. In addition, copulatory behavior with internal insemination may involve a large genital morphology, but this is not essential in fish, suggesting the existence of various sperm transfer methods. Although the power of our analyses is not strong because of the limited number of species, we propose a new scenario of sperm evolution in which internal fertilization would increase sperm head length, but not total sperm length, and change sperm motility.

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

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