4 - The evolution of spermatogenesis

Abstract

This chapter aims to discern the evolutionary histories leading to the varied types of spermatogenesis seen today. It focuses on three model systems: the nematode Caenorhabditis elegans, the fruit fly Drosophila melanogaster and the mouse Mus musculus. In these and all other animals, the production of sperm has four steps: (1) Establishment of the germline—in C. elegans and D. melanogaster, primordial germ cells are specified by determinants present in the egg. By contrast, in M. musculus they are specified by signals from neighboring cells. In either case, once formed, the primordial germ cells migrate toward the somatic gonad precursors, and together form the gonad. (2) Proliferation of germ cells—in all three species, a somatic stem cell niche stimulates germ cells to proliferate. However, once they lose access to this signal, germ cells eventually enter meiosis and begin the process of spermatogenesis. In nematodes, this transition happens almost immediately—germ cells enter meiosis, become primary spermatocytes, and separate from the rachis, which is a core of cytoplasm that runs through the center of the male germline. In mammals and fruit flies, germ cells first undergo a further series of mitotic divisions. (3) Production of spermatids by meiosis—in all three species, once germ cells become primary spermatocytes, they go through two meiotic divisions, resulting in four haploid spermatids and a residual body, which contains leftover material. (4) Differentiation of mature sperm—at the appropriate time, the spermatids undergo spermiogenesis, producing amoeboid sperm in nematodes or flagellated sperm in most other species. It is only during this final step that spermatids become fully cellularized in fruit flies or mammals. This review explores how these complex processes are evolved.