Cell and Evolutionary Biology of Gametogenesis: Where Did Sex Come From?
Germ cells, the family of "sex cells" that give rise to eggs and sperm in higher animals, are particularly interesting to cell and evolutionary biologists for a number of reasons. First, unlike the somatic cells that make up the majority of our bodies, they are potentially immortal. Fusion of germ cells at fertilization constitutes the first cell of the next generation. Second, the pathways from undifferentiated germline stem cell to highly specialized sperm or egg involve extraordinary changes in cell structure, entailing extensive, coordinated changes in many organelle systems. This affords the cell biologist with the opportunity to probe inter-organelle communications. Since all contemporary biological pathways and life cycles are presumably evolved from simple, more primitive biological activities, we expect that a good understanding of the structural basis of gametogenesis will also yield insights into how germ cells have evolved to behave the way they do. We are using a combination of genetic, molecular biological, and structural approaches to understand the extensive reorganization of the cysts that give rise to sperm in the fruit fly, Drosophila melanogaster. In all organisms, cytokinesis following each of the mitotic and meiotic nuclear divisions in the cell lineages leading to sperm is incomplete. The result is that sperm morphogenesis takes place in a large communal cytoplasm. Only very late in sperm formation are the individual cells separated from each other and encased in their own membranes. We are studying the specialized cellular machinery of sperm individualization in Drosophila. Surprisingly, mitochondria appear to play an active and central role in this process, and in a number of other specialized pathways of germ cells. We are working on a hypothesis that these otherwise unexplained mitochondrial behaviors reflect an endosymbiotic origin to gametogenic pathways. Since mitochondria are descended from microbes that invaded ancient proto-eukaryotic cells, a simple way of rationalizing these mitochondrial behaviors in the germ cell life cycle is that they are evolved from the life cycle of the ancient endosymbiont from which mitochondria are descended. In recent years, much work has been done by cell biologists to understand the mechanisms by which several classes of bacteria, having gained access to the cytoplasm of cells they are parasitizing, "hijack" the actin based cytoskeleton and use it to move about within the host cell. Detailed studies have shown that these bacteria promote the polymerization of actin fibers into a comet-tail like structure that propels them through the cell. We are exploring the hypothesis that sperm mitochondria, during Drosophila sperm individualization, recapitulate the "comet-tail" motility of their endosymbiotic ancestor.
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