A rearrangement of the Z chromosome topology influences the sex-linked gene display in the European corn borer, Ostrinia nubilalis

Abstract

Males are homogametic (ZZ) and females are heterogametic (WZ) with respect to the sex chromosomes in many species of butterflies and moths (insect order Lepidoptera). Genes on the Z chromosome influence traits involved in larval development, environmental adaptation, and reproductive isolation. To facilitate the investigation of these traits across Lepidoptera, we developed 43 degenerate primer pairs to PCR amplify orthologs of 43 Bombyx mori Z chromosome-linked genes. Of the 34 orthologs that amplified by PCR in Ostrinia nubilalis, 6 co-segregated with the Z chromosome anchor markers kettin (ket) and lactate dehydrogenase (ldh), and produced a consensus genetic linkage map of ~89 cM in combination with 5 AFLP markers. The O. nubilalis and B. mori Z chromosomes are comparatively co-linear, although potential gene inversions alter terminal gene orders and a translocation event disrupted synteny at one chromosome end. Compared to B. mori orthologs, O. nubilalis Z chromosome-linked genes showed conservation of tissuespecific and growth-stage-specific expression, although some genes exhibited species-specific expression across developmental stages or tissues. The O. nubilalis Z chromosome linkage map provides new tools for isolating quantitative trait loci (QTL) involved in sex-linked traits that drive speciation and it exposes genome rearrangements as a possible mechanism for differential gene regulation in Lepidoptera. Abstract Males are homogametic (ZZ) and females are heterogametic (WZ) with respect to the sex chromosomes in many species of butterflies and moths (insect order Lepidoptera). Genes on the Z chromosome influence traits involved in larval development, environmental adaptation, and reproductive isolation. To facilitate the investigation of these traits across Lepidoptera, we developed 43 degenerate primer pairs to PCR amplify orthologs of 43 Bombyx mori Z chromosomelinked genes. Of the 34 orthologs that amplified by PCR in Ostrinia nubilalis, 6 co-segregated with the Z chromosome anchor markers kettin (ket) and lactate dehydrogenase (ldh), and produced a consensus genetic linkage map of *89 cM in combination with 5 AFLP markers. The O. nubilalis and B. mori Z chromosomes are comparatively co-linear, although potential gene inversions alter terminal gene orders and a translocation event disrupted synteny at one chromosome end. Compared to B. mori orthologs, O. nubilalis Z chromosomelinked genes showed conservation of tissue-specific and growth-stage-specific expression, although some genes exhibited species-specific expression across developmental stages or tissues. The O. nubilalis Z chromosome linkage map provides new tools for isolating quantitative trait loci (QTL) involved in sex-linked traits that drive speciation and it exposes genome rearrangements as a possible mechanism for differential gene regulation in Lepidoptera.

Genetic mapping of male pheromone response in the European corn borer identifies candidate genes regulating neurogenesis

“…An inversion between bgi03892 and another marker was also detected in O. nubilalis by Kroemer et al (Fig. 2) (37). Finally, we found that the Z-linked marker bgi002071 in B. mori was autosomal in O. nubilalis, as was also shown for marker G23 just above kettin by Kroemer et al (37).…”

“…2) (37). Finally, we found that the Z-linked marker bgi002071 in B. mori was autosomal in O. nubilalis, as was also shown for marker G23 just above kettin by Kroemer et al (37). Thus, the segment of the Z chromosome above kettin in B. mori appears to be autosomal in O. nubilalis and therefore segregates independently from the behavioral response trait.…”

“…Although mapping of Resp was based on phenotype data from 78 males (13), it is difficult to judge the significance of this result, because the accuracy of the behavioral scoring is unknown. Furthermore, independent replicate backcrosses using the E and Z strains by another group showed a high variability in recombination rates among Z-linked genetic markers (37).…”

A recombination suppressor contributes to ecological speciation in OSTRINIA moths

“…The ECB diverged from Bombyx mori (the silk moth)~100 Mya (Pringle et al, 2007); however, the species pair shows a high degree of conservation in gene order like many other Lepidoptera (Pringle et al, 2007;d'Alencon et al, 2010;Kroemer et al, 2011). Therefore, we relied on the B. mori genome to identify evenly spaced sex-linked mapping loci for the ECB, whose genome is incomplete.…”

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

“…In contrast, lepidopteran autosomes are far less distinct because they are cytogenetically uniform as a result of their holokinetic arrangement (that is, lacking a primary constriction, the centromere; Murakami and Imai, 1974;Carpenter et al, 2005), large number, small size and insusceptibility to banding techniques. 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.…”