Origin of a function by tandem gene duplication limits the evolutionary capability of its sister copy

Abstract

The most remarkable outcome of a gene duplication event is the evolution of a novel function. Little information exists on how the rise of a novel function affects the evolution of its paralogous sister gene copy, however. We studied the evolution of the feminizer (fem) gene from which the gene complementary sex determiner (csd) recently derived by tandem duplication within the honey bee (Apis) lineage. Previous studies showed that fem retained its sex determination function, whereas the rise of csd established a new primary signal of sex determination. We observed a specific reduction of nonsynonymous to synonymous substitution ratios in Apis to non-Apis fem. We found a contrasting pattern at two other genetically linked genes, suggesting that hitchhiking effects to csd, the locus under balancing selection, is not the cause of this evolutionary pattern. We also excluded higher synonymous substitution rates by relative rate testing. These results imply that stronger purifying selection is operating at the fem gene in the presence of csd. We propose that csd's new function interferes with the function of Fem protein, resulting in molecular constraints and limited evolvability of fem in the Apis lineage. Elevated silent nucleotide polymorphism in fem relative to the genome-wide average suggests that genetic linkage to the csd gene maintained more nucleotide variation in today's population. Our findings provide evidence that csd functionally and genetically interferes with fem, suggesting that a newly evolved gene and its functions can limit the evolutionary capability of other genes in the genome. A n important question in genome evolution is how the rise of a gene with a novel function influences the genomic region around that gene and the evolution of other genes in the genome. Under neofunctionalization, the newly arisen gene gains a function not present in the progenitor gene, whereas the original copy retains its function (1). Thus, duplicated genes that have evolved under a model of neofunctionalization provide an interesting case for exploring this question. Although the rise of novel gene functions has been studied in great detail in some examples of duplicated genes (2-4), how selection and the rise of a new function in the duplicated copy affects the evolution of the sister copy remains unclear. This evolutionary interference has not yet been studied in paralogous genes. This process differs from coevolutionary effects that implicate bidirectional interference between the tandem duplicated genes. Coevolution has been intensively studied in interacting protein systems, such as the cellular signaling pathway of protein ligands and their receptors (5, 6).By examining the paralogous genes feminizer (fem) and complementary sex determiner (csd), which control sex determination in honey bees (7, 8), we can explore whether evolutionary interference plays a role in the evolution of tandemly arranged genes. We previously showed that after the duplication event in the honey bee lineage, fem preserved its ancestral ...

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Sex Determination in Insects: Variations on a Common Theme

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