Defining the forces that sculpt genome organization is fundamental for understanding the origin, persistence, and diversification of species [1, 2]. The genomic sequences of the nematodes Caenorhabditis elegans and Caenorhabditis briggsae provide an excellent opportunity to explore the dynamics of chromosome evolution [3, 4]. Extensive chromosomal rearrangement has accompanied divergence from their common ancestor, an event occurring roughly 100 million years ago (Mya) ; yet, morphologically, these species are nearly indistinguishable and both reproduce primarily by self-fertilization. Here, we show that genes expressed during spermatogenesis (sperm genes) are nonrandomly distributed across the C. elegans genome into three large clusters located on two autosomes. In addition to sperm genes, these chromosomal regions are enriched for genes involved in the hermaphrodite sperm/oocyte switch and in the reception of sperm signals that control fertilization. Most loci are present in single copy, suggesting that cluster formation is largely due to gene aggregation and not to tandem duplication. Comparative mapping indicates that the C. briggsae genome differs dramatically from the C. elegans genome in clustering. Because clustered genes have a direct role in reproduction and thus fitness, their aggregated pattern might have been shaped by natural selection, perhaps as hermaphroditism evolved.
Bibliographical noteFunding Information:
We thank the Sanger Institute and the Genome Sequencing Center, Washington University, St. Louis, for providing the C. elegans and C. briggsae sequences, and Valerie Reinke for sharing unpublished microarray data. We also thank Robert E. Steele, Ron Ellis, and three anonymous reviewers for their helpful comments on the manuscript. Some strains were provided by the Caenorhabditis Genetics Center and International C. elegans Gene Knockout Consortium. This work was supported by grants from the National Institutes of Health to D.G. and S.W., an American Cancer Society postdoctoral fellowship and UAB Comprehensive Cancer Center Junior Faculty Development Grant to M.A.M., and Department of Defense National Defense Science and Engineering Graduate fellowship and University of Arizona National Science Foundation Integrative Graduate Education and Research Traineeship Genomics Initiative fellowship to A.D.C.