Decay of the CTCF paralog BORIS in neognathous birds

Abstract

BORIS (brother of the regulator of imprinted sites), the paralog of the genome organizer CTCF, originated at least 318 million years ago (Mya), in the ancestor of amniotes (mammals, reptiles, and birds). Based on results from chicken (Gallus gallus), the gene was thought to be absent from birds. Using comparative genomics of 59 bird species, we show that birds possess BORIS, but frequently experience severe degradation of the gene, as observed in Gallus gallus. The degradation events are restricted to neognathous birds, specific for the BORIS coding sequence, and occur multiple times independently on different branches. They comprise a wide range of molecular decay, from individual point mutations to the inactivation and/or loss of particular zinc fingers, to the almost complete disintegration of the gene. The decay is accompanied by relaxed evolutionary constraints on BORIS codons across neognathous birds and coincides with the accumulation of species-specific repetitive elements in degenerate loci. BORIS represents a case of a presently ongoing, convergent, and specific gene loss within a lineage. As possible explanation, we propose a link between the loss of BORIS and a shift in sperm and/or genital morphology during the evolution of Neognathae. Significance StatementThe gene BORIS was believed to be absent from birds. However, genome analysis of 59 bird species reveals its presence, though it often underwent severe degradation in neognathous birds. These independent degradation events affect the BORIS coding sequence and range from point mutations to near complete gene disintegration. This decay correlates with relaxed evolutionary constraints and species-specific accumulation of repetitive elements. A potential link between BORIS loss and changes in sperm or genital morphology during neognathous bird evolution is suggested.