Gene Gain and Loss from the Asian Corn Borer W Chromosome

Dai, Wenting; Mank, Judith E.; Ban, Liping

doi:10.1101/2022.10.21.512844

Cited by 3 publications

(12 citation statements)

References 86 publications

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“…Using homology tests between the W and remaining 31 chromosomes in H. misippus and other Lepidoptera we show that there is a degree of similarity between the W and the Z chromosome, suggesting a possible common origin. These results differ from the homology tests performed in Danaus plexipuss (Lewis et al 2021), Kallima inachus (Yang et al 2020) and Dryas iulia (Lewis et al 2021), where no similarity was found between the W and the Z chromosome and are more in line with results in the Asian corn borer, Ostrinia furnacalis, a moth belonging to the Pyraloidea, which suggests a common autosomal origin of the Z and the W chromosome (Dai et al 2022). Contrastingly, the lack of similarity between the W and the Z in five of the seven species studied could suggest a B chromosome origin or could be the result of the rapid evolution of the W, which could be interfering with the inference of homology (Yoshido et al 2013;Vítková et al 2007).…”

Section: Discussioncontrasting

confidence: 99%

“…Furthermore, and irrespective of the specific origin, the number of evolutionary events leading to the formation of the W chromosome has also been debated. That is whether all W chromosomes in the Lepidoptera share a common evolutionary origin of if their inception was the result of multiple independent events, with the most recent evidence supporting the latter (Dai et al 2022;Lewis et al 2021)(Figure 1D-E). hypothesis is that the W chromosome evolved from a B chromosome, which are non-essential chromosomes that vary in number in populations and species.…”

Section: Introductionmentioning

confidence: 99%

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TheHypolimnas misippusgenome supports a common origin of the W chromosome in Lepidoptera

Orteu

McCarthy

Hornett

et al. 2023

Preprint

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Moths and butterflies (Lepidoptera) have a heterogametic sex chromosome system with females carrying ZW chromosomes and males ZZ. The lack of W chromosomes in early diverging lepidopteran lineages has led to the suggestion of an ancestral Z0 system in this clade and a B chromosome origin of the W. This contrasts with the canonical model of W chromosome evolution in which the W would have originated from the same homologous autosomal pair as the Z chromosome. Despite the distinct models proposed, the rapid evolution of the W chromosome has hindered the elucidation of its origin. Here, we present high-quality, chromosome-level genome assemblies of two Hypolimnas species (Hypolimnas bolina and Hypolimnas misippus) and use the H. misippus assembly to explore the evolution of W chromosomes in butterflies and moths. We show that in H. misippus the W chromosome has higher similarity to the Z chromosome than any other chromosome, which could suggest a possible origin from the same homologous autosome pair as the Z chromosome. However, using genome assemblies of closely related species (ditrysian lineages) containing assembled W chromosomes, we present contrasting evidence suggesting that the W chromosome might have evolved from a B chromosome instead. Crucially, by using a synteny analysis to infer homology, we show that W chromosomes are likely to share a common evolutionary origin in Lepidoptera. This study highlights the difficulty of studying the evolution of W chromosomes and contributes to better understanding its evolutionary origins.

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Section: Discussioncontrasting

confidence: 99%

Section: Introductionmentioning

confidence: 99%

TheHypolimnas misippusgenome supports a common origin of the W chromosome in Lepidoptera

Orteu

McCarthy

Hornett

et al. 2023

Preprint

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“…1). This view aligns with evidence of a key role of major rearrangements in the evolution of sex chromosomes in other advanced Lepidoptera (Smith et al 2016;Mongue et al 2017;Carabajal-Paladino et al 2019;Hill et al 2019;Yoshido et al 2005Yoshido et al , 2020Hejnickova et al 2021), and with the recent demonstration of a shared Z-origin of the W chromosomes in two species of Crambidae (also advanced Lepidoptera) (Dai et al 2022).…”

Section: Discussionsupporting

confidence: 86%

“…Our data further support the notion that W chromosome evolution is extraordinarily rapid (Vitkova et al 2007; Sahara et al 2012; Hejnickova et al 2021). The evolution of lepidopteran W chromosomes frequently involves sequence deletions, the incorporation of autosomal segments, and extensive sequence multiplication (Abe et al 2005a, 2005b; Traut et al 2013; Lewis et al 2021; Dai et al 2022). Our identification of autosomal segments copied into and expanding on the W chromosome in P. mannii exemplifies some of these processes.…”

Section: Discussionmentioning

confidence: 99%

Chromosome-level assemblies of thePieris manniibutterfly genome suggest Z-origin and rapid evolution of the W chromosome

Blattner

Ruffener

Berner

2023

Preprint

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The insect order Lepidoptera (butterflies and moth) represents the largest group of organisms with ZW/ZZ sex determination. While the origin of the Z chromosome predates the evolution of the Lepidoptera, the W chromosome is considered younger, but its origin is debated. To shed light on the origin of the lepidopteran W, we here produce chromosome-level genome assemblies for the butterfly Pieris mannii, and compare the sex chromosomes within and between P. mannii and its sister species P. rapae. Our analyses clearly indicate a common origin of the W chromosomes of the two Pieris species, and reveal similarity between the Z and W in chromosome sequence and structure. This supports the view that the W originates from Z-autosome fusion rather than from a redundant B chromosome. We further demonstrate the extremely rapid evolution of the W relative to the other chromosomes and argue that this may preclude reliable conclusions about the origin of the W based on comparisons among distantly related Lepidoptera. Finally, we find that sequence similarity between the Z and W chromosomes is greatest toward the chromosome ends, perhaps reflecting selection for the maintenance of recognition sites essential to chromosome segregation. Our study highlights the utility of long-read sequencing technology for illuminating chromosome evolution.

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“…We suspect that Pelw30 is a neo-chromosome or W sex chromosome. Specifically, the high content of repetitive sequences in Pelw30 is particularly similar to that of the W sex chromosome [ 25 , 27 , 81 ], but there is no clear evidence for this at present. Chromosome 15 of P. machaon (Pmac15) was collinear to chromosomes 15 (Pelw15) and 28 (Pelw28) of P. elwesi .…”

Section: Resultsmentioning

confidence: 99%

Chromosome-Level Genome Assembly of Papilio elwesi Leech, 1889 (Lepidoptera: Papilionidae)

Pan

Ding²,

Zhang³

et al. 2023

Insects

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A rarely seen butterfly species, the large swallowtail butterfly Papilio elwesi Leech, 1889 (Lepidoptera: Papilionidae), endemic to the Chinese mainland, has been declared a state-protected animal in China since 2000, but its genome is not yet available. To obtain high-quality genome assembly and annotation, we sequenced the genome and transcriptome of P. elwesi using the PacBio and PromethION platforms, respectively. The final assembled genome was 358.51 Mb, of which 97.59% was anchored to chromosomes (30 autosomes and 1 Z sex chromosome), with a contig/scaffold N50 length of 6.79/12.32 Mb and 99.0% (n = 1367) BUSCO completeness. The genome annotation pointed to 36.82% (131.99 Mb) repetitive elements and 1296 non-coding RNAs in the genome, along with 13,681 protein-coding genes that cover 98.6% (1348) of the BUSCO genes. Among the 11,499 identified gene families, 104 underwent significantly rapid expansions or contractions, and these rapidly expanding families play roles in detoxification and metabolism. Additionally, strong synteny exists between the chromosomes of P. elwesi and P. machaon. The chromosome-level genome of P. elwesi could serve as an important genomic resource for furthering our understanding of butterfly evolution and for more in-depth genomic analyses.

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Gene Gain and Loss from the Asian Corn Borer W Chromosome

Cited by 3 publications

References 86 publications

TheHypolimnas misippusgenome supports a common origin of the W chromosome in Lepidoptera

TheHypolimnas misippusgenome supports a common origin of the W chromosome in Lepidoptera

Chromosome-level assemblies of thePieris manniibutterfly genome suggest Z-origin and rapid evolution of the W chromosome

Chromosome-Level Genome Assembly of Papilio elwesi Leech, 1889 (Lepidoptera: Papilionidae)

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