A transposon origin of large tandem repeats in the butterfly Papilio bianor

Abstract

Without single centromeres, holocentric chromosomes do not accumulate repetitive DNA in the same way as their monocentric ancestors. In holocentric butterflies and moths, large tandem repeats are rare compared to other insects with monocentric chromosomes. We discover in the butterfly Papilio bianor that nearly half of its chromosomes have large tandem repeats composed entirely of transposons. These transposon arrays are formed by concerted expansion of multiple families, often locked together as a single repeating unit of 100kb-200kb in length. On Hi-C contact maps, transposon arrays partition chromosomes into distinct "arms" and insulate the inter-arm contact. Chromosomes with transposon arrays are also more compact than those without the arrays. In male meiosis, transposon arrays facilitate double crossovers, likely by reducing crossover interference between the flanking arms. As a result, chromosomes with transposon arrays exhibit increased recombination rates. Taken together, we demonstrate that large tandem repeats can affect multiple aspects of holocentric chromosomes, and in many ways, the effects resemble those of centromeres in monocentric organisms.