Gene-by-gene or localized dosage compensation on the neo-X chromosome in Drosophila miranda

Nozawa, Masahiro; Ikeo, Kazuho; Gojobori, Takashi

doi:10.1093/gbe/evy148

Cited by 12 publications

(33 citation statements)

References 30 publications

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“…Such findings support the idea that many of the patterns seen in sex chromosomes are representative of supergenes in general. Indeed, rapid evolution of dosage compensation similarly occurred in the 10 million-year-old sex chromosomes of the plant Silene latifolia ( Muyle et al, 2012 ) and in two Drosophila species neo-sex chromosomes that are only a few million years old ( Nozawa et al, 2014 ; Alekseyenko et al, 2013 ; Nozawa et al, 2018 ).…”

Section: Discussionmentioning

confidence: 99%

“…For instance, in male Drosophila melanogaster the entire X chromosome is expressed at roughly twice the level of autosomes to compensate for the lack of expression in the highly degenerated Y chromosome ( Conrad and Akhtar, 2012 ). In species with much younger sex chromosomes such as Drosophila miranda , dosage compensation instead occurs only at a gene-by-gene level ( Alekseyenko et al, 2013 ; Nozawa et al, 2018 ). Because the fire ant supergene is young, we hypothesize that individual genes for which the Sb allele has begun to degenerate would show evidence of dosage compensation.…”

Section: Introductionmentioning

confidence: 99%

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Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants

Martínez-Ruiz

Pracana

Stolle

et al. 2020

eLife

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Supergene regions maintain alleles of multiple genes in tight linkage through suppressed recombination. Despite their importance in determining complex phenotypes, our empirical understanding of early supergene evolution is limited. Here we focus on the young "social" supergene of fire ants, a powerful system for disentangling the effects of evolutionary antagonism and suppressed recombination. We hypothesize that gene degeneration and social antagonism shaped the evolution of the fire ant supergene, resulting in distinct patterns of gene expression. We test these ideas by identifying allelic differences between supergene variants, characterizing allelic expression across populations, castes and body parts, and contrasting allelic expression biases with differences in expression between social forms. We find strong signatures of gene degeneration and gene-specific dosage compensation. On this background, a small portion of the genes has the signature of adaptive responses to evolutionary antagonism between social forms.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants

Martínez-Ruiz

Pracana

Stolle

et al. 2020

eLife

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“…Therefore, in D. miranda, not only XF-YP genes, but also XF-YF genes showed RLin values significantly greater than 0.5, the expected RLin value under no DC (Fig. 3A) (see also Nozawa et al 2018). In contrast, XF-YF gene upregulation was not necessarily conspicuous in D. albomicans and D. americana.…”

Section: Gene-by-gene and Global DC On Neo-xsmentioning

confidence: 73%

“…Using the RLin index (Lin et al 2012), Nozawa et al (2018) reported gene-by-gene DC on the D. miranda neo-X. Specifically, the DC level (i.e., the RLin value) for the neo-X-linked genes with pseudogenized neo-Y-linked homologs (XF-YP) was significantly greater than that for the neo-X-linked genes with functional neo-Y-linked homologs (XF-YF).…”

Section: Gene-by-gene and Global DC On Neo-xsmentioning

confidence: 99%

“…CC-BY-NC 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made The copyright holder for this preprint this version posted March 12, 2021. ; https://doi.org/10.1101/2021.03.11.435033 doi: bioRxiv preprint In addition to global DC, Nozawa et al (2018) reported that individual neo-X-linked genes may be upregulated in response to pseudogenization of neo-Y-linked homologs in D. miranda [i.e., gene-bygene or localized DC; see also Nozawa et al (2014)]. The presence of gene-by-gene DC seems particularly important at the initial stage of sex chromosome evolution when global DC has not yet been established, to counteract the deleterious effects caused by the sequential losses of individual neo-Ylinked genes.…”

Section: Introductionmentioning

confidence: 99%

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Evolutionary trajectories of three independent neo-sex chromosomes inDrosophila

Nozawa

Minakuchi

Satomura

et al. 2021

Preprint

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Dosage compensation (DC) on the X chromosome is a mechanism to counteract the deleterious effects by gene loss from the Y chromosome. However, DC cannot work efficiently if the X chromosome also degenerates. This indeed occurs in the neo-sex chromosomes in Drosophila miranda, where neo-X as well as neo-Y chromosomes are under accelerated pseudogenization. To examine the generality of this pattern, we investigated the evolution of two additional neo-sex chromosomes that independently emerged in D. albomicans and D. americana and compared their evolutionary processes with that in D. miranda. Comparative genomic and transcriptomic analyses revealed that the pseudogenization rate on neo-X is also accelerated in the two species (though lesser extent in D. americana). We also found that neo-X-linked genes whose neo-Y homologs are pseudogenized tend to be upregulated more stringently than those whose neo-Y homologs remain functional. Moreover, the genes under strong functional constraints and highly expressed in the testis tended to remain functional on neo-X and neo-Y, respectively. Focusing on the D. miranda and D. albomicans neo-sex chromosomes that independently emerged from the same autosome, we further found that the same genes tend to have been pseudogenized in parallel on neo-Y. Those genes include Idgf6 and JhI-26 whose functions seem to be unnecessary or could be even harmful for males. These results indicate that neo-sex chromosomes in Drosophila share a common evolutionary trajectory after their emergence, which may be applicable to other sex chromosomes in a variety of organisms to avoid being an evolutionary dead-end.

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Evolution of sex‐biased genes in Drosophila species with neo‐sex chromosomes: Potential contribution to reducing the sexual conflict

Minovic,

Nozawa

2024

Ecology and Evolution

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An advantage of sex chromosomes may be the potential to reduce sexual conflict because they provide a basis for selection to operate separately on females and males. However, evaluating the relationship between sex chromosomes and sexual conflict is challenging owing to the difficulty in measuring sexual conflict and substantial divergence between species with and without sex chromosomes. We therefore examined sex‐biased gene expression as a proxy for sexual conflict in three sets of Drosophila species with and without young sex chromosomes, the so‐called neo‐sex chromosomes. In all sets, we detected more sex‐biased genes in the species with neo‐sex chromosomes than in the species without neo‐sex chromosomes in larvae, pupae, and adult somatic tissues but not in gonads. In particular, many unbiased genes became either female‐ or male‐biased after linkage to the neo‐sex chromosomes in larvae, despite the low sexual dimorphism. For example, genes involved in metabolism, a key determinant for the rate of development in many animals, were enriched in the genes that acquired sex‐biased expression on the neo‐sex chromosomes at the larval stage. These genes may be targets of sexually antagonistic selection (i.e., large size and rapid development are selected for in females but selected against in males). These results indicate that acquiring neo‐sex chromosomes may have contributed to a reduction in sexual conflict, particularly at the larval stage, in Drosophila..

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Gene-by-gene or localized dosage compensation on the neo-X chromosome in Drosophila miranda

Cited by 12 publications

References 30 publications

Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants

Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants

Evolutionary trajectories of three independent neo-sex chromosomes inDrosophila

Evolution of sex‐biased genes in Drosophila species with neo‐sex chromosomes: Potential contribution to reducing the sexual conflict

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