Development is left–right reversed between dextral and sinistral morphs of snails. In sympatry, they share the same gene pool, including polygenes for shell shape. Nevertheless, their shell shapes are not the mirror images of each other. This triggered a debate between hypotheses that argue either for a developmental constraint or for zygotic pleiotropic effects of the polarity gene. We found that dextrals can be wider or narrower than sinistrals depending on the population, contrary to the prediction of invariable deviation under a developmental constraint. If the pleiotropy is solely responsible instead, the mean shape of each morph should change, depending on the frequency of polarity genotype. Our simulations of this mean shape change under zygotic pleiotropy, however, show that the direction of interchiral difference remains the same regardless of genotype frequency. Our results suggest the presence of genetic variation among populations that changes the maternal or zygotic pleiotropic effect of the polarity gene.
Traditional taxonomy of shell-bearing molluscs does not generally use soft-body coloration. However, the land snails Bradybaena pellucida and B. similaris have been distinguished only on the basis of the color of the soft-body visible through the shell. Thus, the taxonomic status of the two species has traditionally been questionable. We found that dense spots of pigments embedded in the dorsal mantle are responsible for the yellow coloration of B. pellucida . Similar spots in B. similaris are white and less densely aggregated in whorls further from the apex, and the brown color of the hepatopancreas is visible through the shell. The yellow pigments of B. pellucida seep out with mucus from the body in natural and laboratory conditions. The two species became externally indistinguishable after 30 days of laboratory feeding, because the yellow spots disappeared in B. pellucida and the color of the hepatopancreas changed from dark brown to pale brown in both species. Irradiation with ultraviolet A demonstrated that the yellow pigment of B. pellucida fluoresces. Adult specimens of the two species were distinct in penial microsculpture, with F(1) hybrids intermediate in form. Populations of the two species differed significantly in allelic frequencies at four allozyme loci. Therefore, B. pellucida and B. similaris are morphologically and genetically distinct. The fluorescent yellow pigment distinguishes B. pellucida from B. similaris under natural conditions despite its environmental dependence.
The generality of asymmetric reproductive isolation between reciprocal crosses suggests that the evolution of isolation mechanisms often proceeds in reciprocal asymmetry. In hermaphroditic snails that copulate simultaneously and reciprocally, asymmetry in premating isolation may not be readily detectable because the failure of the symmetric performance of courtship would prevent copulation from occurring. On the other hand, through their prolonged copulation, snails discriminate among mates when exchanging spermatophores for their benefit and thus may exhibit asymmetric reproductive isolation during interspecific mating. However, no clear case of reciprocal asymmetry has been found in reproductive isolation between snail species. Here we show a discrete difference in hybridization success between simultaneous reciprocal copulations between two species of pulmonate snails. Premating isolation of Bradybaena pellucida (BP) and Bradybaena similaris (BS) is incomplete in captivity. In interspecific copulation, BP removes its penis without transferring a spermatophore, while BS sires hybrids by inseminating BP. Thus, 'male' BP or 'female' BS rejects the other individual, while female BP and male BS accept each other, so that the two sexes of either BP or BS oppose each other in mate discrimination. Our results are a clear example of asymmetry in reproductive isolation during simultaneous reciprocal mating between hermaphroditic animals.
Depending on fitness consequences, hybridization may rescue inbred populations; generate premating barriers, reproductive interference, or hybrid species; or extinguish a species. However, the fitness of hybrids is unpredictable without direct quantification of their performance in fitness components across multiple generations. The land snails Bradybaena pellucida and B. similaris, which are indigenous and non-indigenous in Japan, respectively, copulate with each other simultaneously and reciprocally. However, only B. pellucida produces hybrids, because it ends mating by removing the penis before transferring a spermatophore, while B. similaris inseminates B. pellucida. To evaluate the strength of an intrinsic postzygotic barrier against the hybrids produced by B. pellucida, we conducted breeding experiments in the laboratory and measured six life-history traits: (1) growth rate, (2) body weight at maturity, (3) number of days to first oviposition after being permitted to mate, (4) clutch size, (5) fecundity, and (6) hatchability. We also calculated the relative intrinsic fitness based on five of these trait values (excluding clutch size). F1 hybrids exhibited heterosis in growth rate, body weight at maturity and relative intrinsic fitness. F2 hybrids also showed heterosis in body weight at maturity. Nevertheless, the F2 hybrids produced significantly fewer progeny than the mid-point value of the parental species. Thus, the F2 hybrids exhibited weak outbreeding depression in reproduction, offsetting their vigor in body size. These results indicate that only a weak postzygotic barrier, contrasting with strong F1 heterosis, has evolved during genetic divergence of the two sibling species in allopatry.
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