Step-by-step evolution of neo-sex chromosomes in geographical populations of wild silkmoths, Samia cynthia ssp.

Yoshido, Atsuo; Sahara, Ken; Marec, František; Matsuda, Yoichi

doi:10.1038/hdy.2010.94

Cited by 27 publications

(30 citation statements)

References 41 publications

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“…The gene composition of the Z chromosome is conserved in Lepidoptera, although not as strongly as some of the autosomes (Beldade et al, 2009;Baxter et al, 2011;Kroemer et al, 2011). A number of genes, such as kettin, tpi, 6-PGD, period, apterous and Ldh, have been assigned to the Z chromosomes of various Lepidoptera (Johnson and Turner, 1979;Gotter et al, 1999;Suzuki et al, 1999;Dopman et al, 2004;Narita et al, 2006;Pringle et al, 2007;Putnam et al, 2007;Van't Hof et al, 2008;Kroemer et al, 2011;Yoshido et al, 2011) and are now established lepidopteran Z-genes. The silkworm (Bombyx mori) whole-genome sequence assembly (The International Silkworm Genome Consortium, 2008) includes a large number of additional Z-linked genes, many of which have since also been found on the Z chromosome in other Lepidoptera (Beldade et al, 2009;Baxter et al, 2011;Kroemer et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism

et al. 2012

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We have constructed a linkage map for the peppered moth (Biston betularia), the classical ecological genetics model of industrial melanism, aimed both at localizing the network of loci controlling melanism and making inferences about chromosome dynamics. The linkage map, which is based primarily on amplified fragment length polymorphisms (AFLPs) and genes, consists of 31 linkage groups (LGs; consistent with the karyotype). Comparison with the evolutionarily distant Bombyx mori suggests that the gene content of chromosomes is highly conserved. Gene order is conserved on the autosomes, but noticeably less so on the Z chromosome, as confirmed by physical mapping using bacterial artificial chromosome fluorescence in situ hybridization (BAC-FISH). Synteny mapping identified three pairs of B. betularia LGs (11/29, 23/30 and 24/31) as being orthologous to three B. mori chromosomes (11, 23 and 24, respectively). A similar finding in an outgroup moth (Plutella xylostella) indicates that the B. mori karyotype (n ¼ 28) is a phylogenetically derived state resulting from three chromosome fusions. As with other Lepidoptera, the B. betularia W chromosome consists largely of repetitive sequence, but exceptionally we found a W homolog of a Z-linked gene (laminin A), possibly resulting from ectopic recombination between the sex chromosomes. The B. betularia linkage map, featuring the network of known melanization genes, serves as a resource for melanism research in Lepidoptera. Moreover, its close resemblance to the ancestral lepidopteran karyotype (n ¼ 31) makes it a useful reference point for reconstructing chromosome dynamic events and ancestral genome architectures. Our study highlights the unusual evolutionary stability of lepidopteran autosomes; in contrast, higher rates of intrachromosomal rearrangements support a special role of the Z chromosome in adaptive evolution and speciation.

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Section: Introductionmentioning

confidence: 99%

Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism

et al. 2012

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“…Neo-sex chromosome evolution via multiple sex chromosome-autosome fusions was described in moths with highly derived karyotypes, Orgyia antiqua and Orgyia thyellina (Lymantriidae), and in geographical subspecies of Samia cynthia (Saturniidae) (13). Recently, it has been suggested that the sex chromosome rearrangements in S. cynthia populations may contribute to the formation of reproductive barriers and facilitate divergence toward speciation (14).…”

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Neo-sex chromosomes and adaptive potential in tortricid pests

Nguyen

Sýkorová

Šíchová

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

115

133

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Changes in genome architecture often have a significant effect on ecological specialization and speciation. This effect may be further enhanced by involvement of sex chromosomes playing a disproportionate role in reproductive isolation. We have physically mapped the Z chromosome of the major pome fruit pest, the codling moth, Cydia pomonella (Tortricidae), and show that it arose by fusion between an ancestral Z chromosome and an autosome corresponding to chromosome 15 in the Bombyx mori reference genome. We further show that the fusion originated in a common ancestor of the main tortricid subfamilies, Olethreutinae and Tortricinae, comprising almost 700 pest species worldwide. The Z-autosome fusion brought two major genes conferring insecticide resistance and clusters of genes involved in detoxification of plant secondary metabolites under sex-linked inheritance. We suggest that this fusion significantly increased the adaptive potential of tortricid moths and thus contributed to their radiation and subsequent speciation.adaptive evolution | leaf-rollers | performance genes | sex chromosome-autosome fusion | sex-linkage

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“…We observed this phenomenon also in the progenies of backcrosses (data not shown). In S. cynthia ssp., the W (neo-W) chromosome is generally inherited only by females of the respective geographical populations with the exception of two cases, a part of the S. c. pryeri Kagoshima population that lost the W chromosome (Yoshido et al, 2013) and S. c. ricini, which has a Z0/ZZ sex chromosome system (Yoshido et al, 2011a). To our knowledge, transmission of the W (or neo-W) chromosomes to males is limited to hybrids produced by F 1 females of crosses between S. cynthia ssp.…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, an increasing number of reports point to a major role of sex chromosomes in postzygotic and/or prezygotic reproductive barrier in some lepidopteran species (e.g., Naisbit et al, 2002;Dopman et al, 2005). Moreover, recent results suggest that structural rearrangements of sex chromosomes which involve autosomes, the so-called neo-sex chromosomes, can also contribute to reproductive isolation and speciation in Lepidoptera (Yoshido et al, 2011a;Nguyen et al, 2013). However, little is known about the actual impact of sex chromosomes and their meiotic behaviour on fitness of hybrids between distinct populations or closely related species.…”

Section: Introductionmentioning

confidence: 99%

“…indet. (Nagano, Japan) with 2n = 25♀/26♂, and neo-Wneo-Z/neo-Zneo-Z in S. c. walkeri (Sapporo, Japan) with 2n = 26♀/26♂ (Yoshido et al, 2005(Yoshido et al, , 2011a(Yoshido et al, , 2013. The variations in the constitution of sex chromosomes were derived from the loss of W chromosome and fusion between the sex chromosomes and autosomes, resulting in different chromosome numbers (Yoshido et al, 2011a, b;Sahara et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

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The fate of W chromosomes in hybrids between wild silkmoths, Samia cynthia ssp.: no role in sex determination and reproduction

2016

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Moths and butterflies (Lepidoptera) have sex chromosome systems with female heterogamety (WZ/ZZ or derived variants). The maternally inherited W chromosome is known to determine female sex in the silkworm, Bombyx mori. However, little is known about the role of W chromosome in other lepidopteran species. Here we describe two forms of the W chromosome, W and neo-W, that are transmitted to both sexes in offspring of hybrids from reciprocal crosses between subspecies of wild silkmoths, Samia cynthia. We performed crosses between S. c. pryeri (2n = 28, WZ/ZZ) and S. c. walkeri (2n = 26, neo-Wneo-Z/neo-Zneo-Z) and examined fitness and sex chromosome constitution in their hybrids. The F 1 hybrids of both reciprocal crosses had reduced fertility. Fluorescence in situ hybridization revealed not only the expected sex chromosome constitutions in the backcross and F 2 hybrids of both sexes but also females without the W (or neo-W) chromosome and males carrying the W (or neo-W) chromosome. Furthermore, crosses between the F 2 hybrids revealed no association between the presence or absence of W (or neo-W) chromosome and variations in the hatchability of their eggs. Our results clearly suggest that the W (or neo-W) chromosome of S. cynthia ssp. plays no role in sex determination and reproduction, and thus does not contribute to the formation of reproductive barriers between different subspecies.

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Step-by-step evolution of neo-sex chromosomes in geographical populations of wild silkmoths, Samia cynthia ssp.

Cited by 27 publications

References 41 publications

Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism

Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism

Neo-sex chromosomes and adaptive potential in tortricid pests

The fate of W chromosomes in hybrids between wild silkmoths, Samia cynthia ssp.: no role in sex determination and reproduction

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