Remodeling of the Platynereis Musculature during Sexual Maturation

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.

Antero-posterior gradients of cell plasticity and proliferation modulate posterior regeneration in the annelidPlatynereis

“…Cells labelled with a 5h-long EdU pulse in S6/S7 were mainly delineating a central and circular epithelium, which appears to be the gut (Fig. 1C, C') (Žídek et al, 2018;Dahlitz et al, 2023).…”

The cost and payout of age on germline regeneration and sexual maturation inPlatynereis dumerilii

“…However, the growth rate difference was not drastic enough to be the only factor explaining the difference in time to maturation. Other factors in the anterior 8 segments remaining after amputation could be physiological, morphological, and molecular changes that occur in P. dumerilii before the visible onset of maturation (Dahlitz et al, 2023;Fischer et al, 2010;Fischer and Hoeger, 1993;Schenk et al, 2019Schenk et al, , 2016. For example, there may be differential storage of nutrients, including lipids, that could enable the rapid growth observed in older amputated worms.…”