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Sci Adv. 2019 Jun 12;5(6):eaau3648. doi: 10.1126/sciadv.aau3648. eCollection 2019 Jun.

Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of lepidopteran chromosome evolution.

Author information

1
Population Genetics, Department of Zoology, Stockholm University, Stockholm, Sweden.
2
Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.
3
Institute of Biotechnology, University of Helsinki, Helsinki, Finland.
4
Department of Zoology, University of Cambridge, Cambridge, UK.
5
Institute of Integrative Biology, University of Liverpool, Liverpool, UK.
6
Department of Vector Biology, Liverpool School of Tropical Medicine, Liverpool, UK.
7
Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, PA 15260, USA.
8
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USA.
9
Department of Evolutionary Biology, Ecology and Environmental Sciences, University of Barcelona, 08028 Barcelona, Spain.
10
CREAF, Global Ecology Unit, Autonomous University of Barcelona, 08193 Cerdanyola del Vallès, Spain.
11
Functional Morphology, Department of Zoology, Stockholm University, Stockholm, Sweden.
12
INRA, Department of Sensory Ecology, Institute of Ecology and Environmental Sciences of Paris, Route de Saint-Cyr, 78026 Versailles Cedex, France.
13
Department of Ecology, Evolution and Behavior, University of Minnesota, St Paul, MN 55108, USA.
14
Department of Biology, University of Mississippi, University, MS 38677, USA.
15
Department of Entomology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.
16
Center for Developmental Genetics, Department of Biology, New York University, 100 Washington Square East, New York, NY 10003, USA.
17
Department of Biological Sciences University of South Carolina, Columbia, SC 29208, USA.

Abstract

Chromosome evolution presents an enigma in the mega-diverse Lepidoptera. Most species exhibit constrained chromosome evolution with nearly identical haploid chromosome counts and chromosome-level gene collinearity among species more than 140 million years divergent. However, a few species possess radically inflated chromosomal counts due to extensive fission and fusion events. To address this enigma of constraint in the face of an exceptional ability to change, we investigated an unprecedented reorganization of the standard lepidopteran chromosome structure in the green-veined white butterfly (Pieris napi). We find that gene content in P. napi has been extensively rearranged in large collinear blocks, which until now have been masked by a haploid chromosome number close to the lepidopteran average. We observe that ancient chromosome ends have been maintained and collinear blocks are enriched for functionally related genes suggesting both a mechanism and a possible role for selection in determining the boundaries of these genome-wide rearrangements.

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