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

Hill, Jason; Rastas, Pasi; Hornett, Emily A.; Neethiraj, Ramprasad; Clark, Nathan L.; Morehouse, Nathan I; Celorio‐Mancera, Maria de la Paz; Cols, Jofre Carnicer; Dircksen, Heinrich; Meslin, Camille; Keehnen, Naomi; Pruisscher, Peter; Sikkink, Kristin L.; Vives, María; Vogel, Heiko; Wiklund, Christer; Woronik, Alyssa; Boggs, Carol L.; Nylin, Sören; Wheat, Christopher W.

doi:10.1126/sciadv.aau3648

Cited by 71 publications

(105 citation statements)

References 83 publications

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“…Strong syntenic correspondence between S. exigua and S. litura (Fig. 4b) indicated the conserved chromosomelevel gene collinearity, which was also reported previously [81,82]. litura.…”

Section: Genome Annotationsupporting

confidence: 85%

A chromosome-level genome assembly for the beet armyworm (Spodoptera exigua) using PacBio and Hi-C sequencing

Zhang

Yang

et al. 2019

Preprint

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The beet armyworm, Spodoptera exigua (Hübner), is a worldwide, polyphagous agricultural pest feeding on vegetable, field, and flower crops. However, the lacking of genome architecture severely limits our understanding of its rapid adaptation and the development of efficient pest managements. We report a chromosome-level genome assembly using single-molecule real-time PacBio sequencing and Hi-C data. The final genome assembly was 446.80 Mb with a scaffold N50 of 14.36 Mb, and captured 97.9% complete arthropod Benchmarking Universal Single-Copy Orthologs (n=1,658). A total of 367 contigs were anchored to 32 pseudo-chromosomes, covering 96.18% (429.74 Mb) of the total genome length. We predicted 17,707 protein-coding genes, of which 81.69% were supported by transcriptome evidence and 97.94% matched the UniProt protein records. We also identified 867,102 (147.97 Mb/33.12%) repeats and 1,609 noncoding RNAs. Synteny analyses indicated a strong collinearity between three lepidopteran species. Our high-quality genome information provides a valuable resource for better understanding and management of the beet armyworm.

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“…Strong syntenic correspondence between S. exigua and S. litura (Fig. 4b) indicated the conserved chromosomelevel gene collinearity, which was also reported previously [81,82]. litura.…”

Section: Genome Annotationsupporting

confidence: 85%

A chromosome-level genome assembly for the beet armyworm (Spodoptera exigua) using PacBio and Hi-C sequencing

Zhang

Yang

et al. 2019

Preprint

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“…Consequently, the Leptidea species do not exhibit a conserved macrosynteny of genes compared with the putative ancestral karyotype of Lepidoptera (Van’t Hof et al 2013 ; Ahola et al 2014 ). The recent genome assembly of another pierid butterfly, Pieris napi , showed conserved microsynteny blocks of genes in autosomes but broken macrosynteny blocks, also suggesting dynamic genome rearrangements (Hill et al 2019 ).…”

Section: Discussionmentioning

confidence: 99%

Evolution of multiple sex-chromosomes associated with dynamic genome reshuffling in Leptidea wood-white butterflies

et al. 2020

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Sex-chromosome systems tend to be highly conserved and knowledge about their evolution typically comes from macroevolutionary inference. Rapidly evolving complex sex-chromosome systems represent a rare opportunity to study the mechanisms of sex-chromosome evolution at unprecedented resolution. Three cryptic species of wood-white butterflies-Leptidea juvernica, L. sinapis and L. reali-have each a unique set of multiple sex-chromosomes with 3-4 W and 3-4 Z chromosomes. Using a transcriptome-based microarray for comparative genomic hybridisation (CGH) and a library of bacterial artificial chromosome (BAC) clones, both developed in L. juvernica, we identified Z-linked Leptidea orthologs of Bombyx mori genes and mapped them by fluorescence in situ hybridisation (FISH) with BAC probes on multiple Z chromosomes. In all three species, we determined synteny blocks of autosomal origin and reconstructed the evolution of multiple sex-chromosomes. In addition, we identified W homologues of Z-linked orthologs and characterised their molecular differentiation. Our results suggest that the multiple sex-chromosome system evolved in a common ancestor as a result of dynamic genome reshuffling through repeated rearrangements between the sex chromosomes and autosomes, including translocations, fusions and fissions. Thus, the initial formation of neo-sex chromosomes could not have played a role in reproductive isolation between these Leptidea species. However, the subsequent species-specific fissions of several neo-sex chromosomes could have contributed to their reproductive isolation. Then, significantly increased numbers of Z-linked genes and independent neo-W chromosome degeneration could accelerate the accumulation of genetic incompatibilities between populations and promote their divergence resulting in speciation.

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“…Lepidoptera have long been recognized as exhibiting striking variation in chromosome number [ 39 ]. The extreme distribution of chromosome number observed in lepidoptera has been a driving force in the development of the hypothesis that holocentricity allows for rapid changes in chromosome number [ 19 , 20 ]. Our results find little support for this hypothesis.…”

Section: Discussionmentioning

confidence: 99%

“…Because chromosomal rearrangements are thought to often be deleterious or underdominant, they should be more likely to fix in populations with meiotic drive or low effective population size [ 5 , 17 , 18 ]. However, centromeric structure may modulate the fitness effects of fusions and fissions [ 19 , 20 ]. In species with monocentric chromosomes fusions and fissions can lead to multiple or no centromeres along the length of a chromosome which leads to failed segregation [ 21 , 22 ].…”

Section: Introductionmentioning

confidence: 99%

Chromosome number evolves at equal rates in holocentric and monocentric clades

et al. 2020

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Despite the fundamental role of centromeres two different types are observed across plants and animals. Monocentric chromosomes possess a single region that function as the centromere while in holocentric chromosomes centromere activity is spread across the entire chromosome. Proper segregation may fail in species with monocentric chromosomes after a fusion or fission, which may lead to chromosomes with no centromere or multiple centromeres. In contrast, species with holocentric chromosomes should still be able to safely segregate chromosomes after fusion or fission. This along with the observation of high chromosome number in some holocentric clades has led to the hypothesis that holocentricity leads to higher rates of chromosome number evolution. To test for differences in rates of chromosome number evolution between these systems, we analyzed data from 4,393 species of insects in a phylogenetic framework. We found that insect orders exhibit striking differences in rates of fissions, fusions, and polyploidy. However, across all insects we found no evidence that holocentric clades have higher rates of fissions, fusions, or polyploidy than monocentric clades. Our results suggest that holocentricity alone does not lead to higher rates of chromosome number changes. Instead, we suggest that other co-evolving traits must explain striking differences between clades.

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

Cited by 71 publications

References 83 publications

A chromosome-level genome assembly for the beet armyworm (Spodoptera exigua) using PacBio and Hi-C sequencing

A chromosome-level genome assembly for the beet armyworm (Spodoptera exigua) using PacBio and Hi-C sequencing

Evolution of multiple sex-chromosomes associated with dynamic genome reshuffling in Leptidea wood-white butterflies

Chromosome number evolves at equal rates in holocentric and monocentric clades

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