Cryptic, extensive and non-random chromosome reorganization revealed by a butterfly chromonome

Chromosome evolution, an important component of mico- and macroevolutionary dynamics 1-5, presents an enigma in the mega-diverse Lepidoptera6. While most species exhibit constrained chromosome evolution, with nearly identical haploid chromosome counts and chromosome-level shared gene content and collinearity among species despite more than 140 Million years of divergence7, a small fraction of species independently exhibit dramatic changes in chromosomal count due to extensive fission and fusion events that are facilitated by their holocentric chromosomes7-9. Here we address this enigma of simultaneous conservation and dynamism in chromosome evolution in our analysis of the chromonome (chromosome level assembly10) of the green-veined white butterfly, Pieris napi (Pieridae, Linnaeus, 1758). We report an unprecedented reorganization of the standard Lepidopteran chromosome structure via more than 90 fission and fusion events that are cryptic at other scales, as the haploid chromosome number is identical to related genera and gene collinearity within the large rearranged segments matches other Lepidoptera. Furthermore, these rearranged segments are significantly enriched for clusters of functionally related genes and the maintenance of ancient telomeric ends. These results suggest an unexpected role for selection in shaping chromosomal evolution when the structural constraints of monocentricq chromosomes are relaxed.