Progress towards unraveling the influences of genetics, ecology and function in shaping the evolution of germline stem cell genes in Drosophila

Thu, Apr 15, 2021, 12:30 pm

Germline stem cells (GSCs) in the gonads of animals are responsible for the sustained production of sperm and eggs, known as spermatogenesis and oogenesis, respectively. The Bag of marbles (bam) gene is essential for male and female fertility in the fruitfly Drosophila melanogaster and signals self-renewal and differentiation of GSCs. Surprisingly, we found that this gene has undergone strong positive selection for amino acid diversification in several closely related Drosophila species, but not in others. Using CRISPR/Cas9 gene editing to produce new bam nulls in five species, we also recently demonstrated that bam’s key role in gametogenesis, that had been demonstrated as essential in D. melanogaster, is not conserved nor even required for fertility in the related species D. teissieri and D. ananassae. How does such a critical developmental process like the production of gametes have its key “switch” gene evolve rapidly in sequence and function? Are these changes due to evolving regulation of GSCs or to an evolutionary conflict such as with the intracellular bacteria, Wolbachia pipientis, which is known to manipulate reproduction in many insects? Remarkably given its central role in GSC regulation, bam is a novel gene restricted to the genus Drosophila and, reportedly, a few closely related Diptera. How a novel gene can take the lead role in such a developmentally important process is a major puzzle. Current work focuses on the extent to which bam’s new roles may be independent of W. pipientis interaction as the hypotheses of coevolution and novel function are not mutually exclusive of each other. For example, conflicts between GSC function and W. pipientis could drive gene innovation for control of this process. Changes in life history between species could also drive the evolution of bam’s function through its role in the “schedule” of reproduction during the fly’s lifespan.

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