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bioRxiv · 10.1101/2024.09.11.612556

A Newborn F-box Gene Blocks Gene Flow by Selectively Degrading Phosphoglucomutase in Species Hybrids

Xie, D.·Ma, Y.·Ye, P.·Liu, Y.·Ding, Q.·Huang, G.·Felix, M.-A.·Cai, Z.·Zhao, Z.
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Abstract

The establishment of reproductive barriers such as postzygotic hybrid incompatibility (HI) remains the key to speciation. Gene duplication followed by differential functionalization has long been proposed as a major model underlying HI, but few supporting evidence exists. Here, we demonstrate that a new-born F-box gene, Cni-neib-1, of the nematode Caenorhabditis nigoni specifically inactivates an essential phosphoglucomutase encoded by Cbr-shls-1 in its sister species C. briggsae and their hybrids. Zygotic expression of Cni-neib-1 specifically depletes Cbr-SHLS-1, but not Cni-SHLS-1, in approximately 40 minutes starting from gastrulation, causing embryonic death. Cni-neib-1 is one of thirty-three paralogues emerging from a recent surge in F-box gene duplication events within C. nigoni, all of which are evolving under positive selection. Cni-neib-1 undergoes turnover even among C. nigoni populations. Differential expansion of F-box genes between the two species could reflect their distinctive innate immune responses. Collectively, we demonstrate how recent duplication of genes involved in protein degradation can cause unintended destruction of targets in hybrids that leads to HI, providing an invaluable insight into mechanisms of speciation. Significance statementUnderstanding how reproductive isolation forms and triggers speciation remains a central topic in evolutionary biology. In this study, the authors reveal a novel molecular mechanism that obstructs gene flow between the nematodes Caenorhabditis briggsae and C. nigoni. A recently evolved, species-specific F-box gene in C. nigoni selectively depletes an essential phosphoglucomutase enzyme in C. briggsae, leading to embryonic lethality in hybrids. This mechanism effectively prevents gene flow from C. nigoni to C. briggsae. This discovery underscores how a newborn gene, arising from recent gene duplication, can contribute to reproductive isolation by inadvertently disrupting a functionally important protein in hybrid offspring.

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Xie, D., Ma, Y., Ye, P., Liu, Y., Ding, Q., Huang, G., Felix, M.-A., Cai, Z., Zhao, Z.. 2024-09-13. A Newborn F-box Gene Blocks Gene Flow by Selectively Degrading Phosphoglucomutase in Species Hybrids. https://doi.org/10.1101/2024.09.11.612556

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