Innovation of heterochromatin functions drives rapid evolution of essential ZAD-ZNF genes in Drosophila

Contrary to prevailing dogma, evolutionarily young and dynamic genes can encode essential functions. Here, we investigate genetic innovation in ZAD-ZNF genes, which encode the most abundant class of insect transcription factors. We find that evolutionarily dynamic ZAD-ZNF genes are more likely to encode essential functions in Drosophila melanogaster than ancient, conserved ZAD-ZNF genes. To understand the basis of this unexpected correlation, we focus on the Nicknack ZAD-ZNF gene. Nicknack is an evolutionarily young, poorly retained in Drosophila species, and evolves under strong positive selection, yet we find that it is necessary for larval development in D. melanogaster. We show that Nicknack encodes a heterochromatin-localizing protein like its closely related paralog Oddjob, also an evolutionarily dynamic, essential ZAD-ZNF gene. We find that the divergent D. simulans Nicknack protein can still localize to D. melanogaster heterochromatin and rescue viability of female but not male Nicknack-null D. melanogaster. Our findings suggest that innovation for rapidly changing heterochromatin functions might provide a general explanation for the essential functions of many evolutionarily dynamic ZAD-ZNF genes in insects.