Innovation of heterochromatin functions drives rapid evolution of essential ZAD-ZNF genes in <i>Drosophila</i>.

Abstract

Contrary to dogma, evolutionarily young and dynamic genes can encode essential functions. We find that evolutionarily dynamic <i>ZAD-ZNF</i> genes, which encode the most abundant class of insect transcription factors, are more likely to encode essential functions in <i>Drosophila melanogaster</i> than ancient, conserved <i>ZAD-ZNF</i> genes. We focus on the <i>Nicknack ZAD-ZNF</i> gene, which is evolutionarily young, poorly retained in <i>Drosophila</i> species, and evolves under strong positive selection. Yet we find that it is necessary for larval development in <i>D. melanogaster.</i> We show that <i>Nicknack</i> encodes a heterochromatin-localizing protein like its paralog <i>Oddjob</i>, also an evolutionarily dynamic yet essential <i>ZAD-ZNF</i> gene. We find that the divergent <i>D. simulans</i> Nicknack protein can still localize to <i>D. melanogaster</i> heterochromatin and rescue viability of female but not male <i>Nicknack-</i>null <i>D. melanogaster</i>. Our findings suggest that innovation for rapidly changing heterochromatin functions might generally explain the essentiality of many evolutionarily dynamic <i>ZAD-ZNF</i> genes in insects.