Abstract
Somatic and germline sex determination pathways have diverged significantly in animals, making comparisons between taxa difficult. To overcome this difficulty, we compared the genes in the germline sex determination pathways of Caenorhabditis elegans and C. briggsae, two Caenorhabditis species with similar reproductive systems and sequenced genomes. We demonstrate that C. briggsae has orthologs of all known C. elegans sex determination genes with one exception: fog-2. Hermaphroditic nematodes are essentially females that produce sperm early in life, which they use for self fertilization. In C. elegans, this brief period of spermatogenesis requires FOG-2 and the RNA-binding protein GLD-1, which together repress translation of the tra-2 mRNA. FOG-2 is part of a large C. elegans FOG-2-related protein family defined by the presence of an F-box and Duf38/FOG-2 homogy domain. A fog-2-related gene family is also present in C. briggsae, however, the branch containing fog-2 appears to have arisen relatively recently in C. elegans, post-speciation. The C-terminus of FOG-2 is rapidly evolving, is required for GLD-1 interaction, and is likely critical for the role of FOG-2 in sex determination. In addition, C. briggsae gld-1 appears to play the opposite role in sex determination (promoting the female fate) while maintaining conserved roles in meiotic progression during oogenesis. Our data indicate that the regulation of the hermaphrodite germline sex determination pathway at the level of FOG-2/GLD-1/tra-2 mRNA is fundamentally different between C. elegans and C. briggsae, providing functional evidence in support of the independent evolution of self-fertile hermaphroditism. We speculate on the convergent evolution of hermaphroditism in Caenorhabditis based on the plasticity of the C. elegans germline sex determination cascade, in which multiple mutant paths yield self fertility.
Highlights
Sex determination is an ancient and universal feature in metazoans
We provide evidence that the essential role of FOG-2 in C. elegans hermaphrodite spermatogenesis evolved from post-speciation duplication and divergence of the fog-2-related (FTR) gene family and that a fog-2 gene is not present in C. briggsae
Our results indicate that the control of hermaphrodite spermatogenesis is fundamentally different between the sister species C. elegans and C. briggsae at the level of FOG-2/GLD-1/ tra-2 mRNA regulation
Summary
Comparison of distantly related species such as Caenorhabditis elegans and Drosophila melanogaster has revealed little about the evolution of the complex pathways that mediate the sexual fate decision in the soma and germline [1,2,3]. This is likely due to the combination of gross morphological, functional, and behavioral dissimilarity and extensive sequence divergence. One approach is to perform comparative analysis of sex determination genes in species separated by sufficient evolutionary time to allow for changes in pathway components yet retain comparable somatic and germline morphology and function. The clade containing C. elegans and C. briggsae represents an ideal case for this type of study, as the sex determination pathway has been well studied in C. elegans and an abundance of sequence information is available for both species [4,5]
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