Evolutionary transition to XY sex chromosomes associated with Y-linked duplication of a male hormone gene in a terrestrial isopod

Russell, Aubrie; Borrelli, Sevarin; Fontana, Rose; Laricchiuta, Joseph; Pascar, Jane; Becking, Thomas; Giraud, Isabelle; Cordaux, Richard; Chandler, Christopher H.

doi:10.1038/s41437-021-00457-2

Cited by 8 publications

(10 citation statements)

References 109 publications

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“…The f element induces female development, as a W chromosome does, and it shows non-Mendelian inheritance, making it an SRD [21,22]. These SRD may cause turnovers in sex determination mechanisms [6,15,23] and they could explain why sex chromosome systems are so variable in terrestrial isopods [24][25][26][27].…”

Section: Introductionmentioning

confidence: 99%

Heterogeneous distribution of sex ratio distorters in natural populations of the isopod Armadillidium vulgare

et al. 2023

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In the isopod Armadillidium vulgare , many females produce progenies with female-biased sex ratios, owing to two feminizing sex ratio distorters (SRD): Wolbachia endosymbionts and the f element. We investigated the distribution and population dynamics of these SRD and mitochondrial DNA variation in 16 populations from Europe and Japan. Confirming and extending results from the 1990s, we found that the SRD are present at variable frequencies in populations and that the f element is overall more frequent than Wolbachia . The two SRD never co-occur at high frequency in any population, suggesting an apparent mutual exclusion. We also detected Wolbachia or the f element in some males, which probably reflects insufficient titer to induce feminization or presence of masculinizing alleles. Our results are consistent with a single integration event of a Wolbachia genome in the A. vulgare genome at the origin of the f element, which contradicts an earlier hypothesis of frequent losses and gains. We identified strong linkage between Wolbachia strains and mitochondrial haplotypes, but no association between the f element and mitochondrial background. Our results open new perspectives on SRD evolutionary dynamics in A. vulgare , the evolution of genetic conflicts and their impact on the variability of sex determination systems.

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Section: Introductionmentioning

confidence: 99%

Heterogeneous distribution of sex ratio distorters in natural populations of the isopod Armadillidium vulgare

et al. 2023

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“…Genome sequencing of 17 crustacean genomes yielded 19 to 25 gigabases (Gb) of Illumina reads per genome and 769 Mb to 16.8 Gb of ONT reads per genome (Supplementary Table 1). We also analyzed publicly available sequence data of the swimming crab Portunus trituberculatus (14) and the terrestrial isopod Trachelipus rathkii (15).…”

Section: Resultsmentioning

confidence: 99%

“…Porcellio scaber clopovirus (PsCLPV) was identified from the shotgun sequencing data of Porcellio scaber . The genome sequence of Trachelipus rathkii clopovirus (TrCLPV; Supplementary Files 1 and 2) was identified from the shotgun sequencing data of Trachelipus rathkii , a species native to Europe but introduced into North America (15). TrCLPV has a genome size of 579 kb, the largest of all nimaviruses discovered so far.…”

Section: Resultsmentioning

confidence: 99%

“…Repeat-specific integration is believed to be a survival strategy employed by transposable elements in order to minimize negative effects on host fitness (52)(53)(54). The prevalence of telomere-repeat-specific nimaviruses in penaeid shrimps and terrestrial isopods may be due to a combination of this viral survival strategy and the abundance of simple sequence repeats, including telomere-like repeats (55), in the genomes of these organisms (15,(56)(57)(58)(59).…”

Section: Discussionmentioning

confidence: 99%

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Integrase-associated niche differentiation of endogenous large DNA viruses in crustaceans

Kawato

Kondo

Hirono

2023

Preprint

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Crustacean genomes harbor sequences originating from nimaviruses, a family of large double-stranded DNA viruses infecting crustaceans. In this study, we recovered metagenome-assembled genomes of 25 endogenous nimaviruses from crustacean genome data. Phylogenetic analysis revealed four major lineages within Nimaviridae, and for three of these lineages, we propose novel genera of endogenous nimaviruses: Majanivirus and Pemonivirus identified from penaeid shrimp genomes, and Clopovirus identified from terrestrial isopods. Majanivirus genomes contain multiple eukaryotic-like genes such as baculoviral inhibitor of apoptosis repeat-containing genes, innexins, and heat shock protein 70-like genes, some of which contain introns. An alignment of long reads revealed that that each endogenous nimavirus species specifically inserts into host microsatellites or within 28S rDNA. This insertion preference was associated with the type of virus-encoded DNA recombination enzymes, the integrases. Majaniviruses, pemoniviruses, some whispoviruses, and possibly clopoviruses specifically insert into the arthropod telomere repeat motif (TAACC/GGTTA)n and all possessed a specific tyrosine recombinase family. Pasiphaea japonica whipovirus and Portunus trituberculatus whispovirus, the closest relatives of white spot syndrome virus, integrate into the host 28S rDNA and are equipped with members of another family of tyrosine recombinases that are distantly related to telomere-specific tyrosine recombinases. Endogenous nimavirus genomes identified from sesarmid crabs, which lack tyrosine recombinases and are flanked by a 46-bp inverted terminal repeat, integrate into (AT/TA)n microsatellites through the acquisition of a Ginger2-like cut-and-paste DDE transposase. These results suggest that endogenous nimaviruses are giant transposable elements that occupy different sequence niches through the acquisition of different integrase families.

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Section: Introductionmentioning

confidence: 99%

Heterogeneous distribution of sex ratio distorters in natural populations of the isopodArmadillidium vulgare

Durand

Lheraud

Giraud

et al. 2022

Preprint

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In the isopod Armadillidium vulgare, many females produce progenies with female-biased sex ratios, due to two feminizing sex ratio distorters (SRD): Wolbachia endosymbionts and the f element. We investigated the distribution and population dynamics of these SRD and mitochondrial DNA variation in 16 populations from Europe and Japan. Confirming and extending results from the 1990's, we found that the SRD are present at variable frequencies in populations, and that the f element is overall more frequent than Wolbachia. The two SRD never co-occur at high frequency in any population, suggesting an apparent mutual exclusion. We also detected Wolbachia or the f element in some males, which likely reflects insufficient titer to induce feminization or presence of masculinizing alleles. Our results are consistent with a single integration event of a Wolbachia genome in the A. vulgare genome at the origin of the f element, which contradicts an earlier hypothesis of frequent losses and gains. We identified strong linkage between Wolbachia strains and mitochondrial haplotypes, but no association between the f element and mitochondrial background. Our results open new perspectives on SRD evolutionary dynamics in A. vulgare, the evolution of genetic conflicts and their impact on the variability of sex determination systems.

show abstract

Evolutionary transition to XY sex chromosomes associated with Y-linked duplication of a male hormone gene in a terrestrial isopod

Cited by 8 publications

References 109 publications

Heterogeneous distribution of sex ratio distorters in natural populations of the isopod Armadillidium vulgare

Heterogeneous distribution of sex ratio distorters in natural populations of the isopod Armadillidium vulgare

Integrase-associated niche differentiation of endogenous large DNA viruses in crustaceans

Heterogeneous distribution of sex ratio distorters in natural populations of the isopodArmadillidium vulgare

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