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

Abstract

Contrary to dogma, evolutionarily young and dynamic genes can encode essential functions. We find that evolutionarily dynamicZAD-ZNFgenes, which encode the most abundant class of insect transcription factors, are more likely to encode essential functions inDrosophila melanogasterthan ancient, conservedZAD-ZNFgenes. We focus on theNicknack ZAD-ZNFgene, which is evolutionarily young, poorly retained inDrosophilaspecies, and evolves under strong positive selection. Yet we find that it is necessary for larval development inD. melanogaster.We show thatNicknackencodes a heterochromatin-localizing protein like its paralogOddjob, also an evolutionarily dynamic yet essentialZAD-ZNFgene. We find that the divergentD. simulansNicknack protein can still localize toD. melanogasterheterochromatin and rescue viability of female but not maleNicknack-nullD. melanogaster. Our findings suggest that innovation for rapidly changing heterochromatin functions might generally explain the essentiality of many evolutionarily dynamicZAD-ZNFgenes in insects.