Remodeling of the Platynereis Musculature during Sexual Maturation

SIMPLE SUMMARY: The internal organ transformations associated with sexual maturity in the polychaete worm Platynereis dumerilii have not been systematically analyzed so far. In this study, we focused on the morphology of the longitudinal and transversal muscles in both anterior and posterior regions of the body to understand their transformation during maturation. We found that the longitudinal muscles were smaller and less dense after maturation and were strongly degraded. Moreover, we observed a profound remodeling of the transversal muscles in the posterior segments of both sexes, resulting in strong thickening. Accordingly, the entire musculature in the posterior segments was severely swollen. In addition, we discovered an enormous number of small, blind-ended blood vessels that completely penetrate the musculature in the posterior segments. The different degree of muscle remodeling between anterior and posterior segments reflects the specific tasks of the different body regions after sexual maturation. The anterior segments contain the gametes and thus the degradation of the muscles makes room for the germ cells. By contrast, the swollen muscles and the new blood vessels in the posterior segments coincide with the remodeling of the appendages in this body region into paddle-shaped swimming organs, allowing rapid swimming during nuptial dance and gamete release. ABSTRACT: Background: The external transformations associated with sexual maturation in Platynereis dumerilii (Audouin and Milne Edwards) are well studied, whereas the internal changes along the body axis have not been systematically analyzed. Therefore, we examined muscle morphology in body regions located anterior or posterior to the prospective atokous/epitokous border to generate a structural basis for internal transformations. Results: All dorsal and ventral longitudinal muscles were significantly reduced in size and density after sexual maturation and strongly atrophied, with the greatest decrease in the anterior segments of females. Despite the general reduction in size throughout the longitudinal muscles, we found a specific degradation mechanism for the posterior segments, which were characterized by the formation of secondary bundle-like fibrous structures. In addition, we observed a profound remodeling of the transversal muscles in the posterior segments of both sexes, apparently resulting in excessive thickening of these muscles. Accordingly, the entire transversal muscle complex was severely swollen and ultrastructurally characterized by a greatly increased number of mitochondria. As a possible trigger for this remodeling, we discovered an enormous number of small, blind-ending blood vessels that completely penetrated the longitudinal and transversal muscles in posterior segments. In addition, both the number of visceral muscles as well as their coelothelial covering were reduced during sexual maturation. Conclusions: We hypothesize that a possible reason for the secondary bundling of the longitudinal fibers, as well as the difference in size of the posterior transversal muscles, could be the high degree of posterior vascularization. The different degree of muscle remodeling thus depends on segmental affiliation and reflects the tasks in the motility of the different body regions after maturation. The strongest atrophy was found in the anterior segments, while signs of redifferentiation were encountered in posterior segments, supported by the vigorous growth of vessels supplying the transformed epitokous parapodia and associated muscles, which allows rapid swimming during swarming and gamete release.