Role of lepidopteran sex chromosomes in sex determination and speciation

Moths and butterflies (Lepidoptera) represent the largest group of organisms with female heterogamety and WZ/ZZ sex chromosome system. The basal moth lineages have a primitive sex chromosome constitution, Z0/ZZ (female/male) and also some species of advanced lineages lost the W chromosome. We study the structure, composition and evolution of the lepidopteran sex chromosomes by molecular cytogenetic methods and synteny mapping of sex-linked genes with the aim to (i) uncover the W chromosome origin, (ii) determine the role of sex chromosomes in sex determination, and (iii) clarify their role in ecological adaptation and speciation.

The maternally inherited W chromosome is known to determine female sex in the silkworm, Bombyx mori. However, the primary trigger of the sex-determining pathway as well as the role of W and Z sex chromosomes in sex determination remained a mystery until recently. The breakthrough came with the discovery a small W-encoded RNA (named Fem piRNA) that has been shown to control female-specific splicing of the B. mori doublesex (Bmdsx) gene by downregulating expression of the Z-linked Masculinizer (Masc) gene. A question remains whether this pathway is evolutionary conserved in Lepidoptera (see comments in Marec, 2014). By means of a detailed analysis of hybrids originating from crosses between geographical races of wild silkmoths, Samia cynthia ssp., we have shown that the W chromosome is transmitted to both sexes in offspring of the hybrids. Our results clearly suggest that the W chromosome of S. cynthia ssp. plays no role in sex determination and reproduction (Yoshido et al., submitted).

In another recent study, we revealed a curious sex determination system with 3–4 W and 3–4 Z chromosomes in three cryptic species of wood white butterflies of the genus Leptidea, emerging models of evolutionary genetics. This system is unique not only in the Lepidoptera but also in all organism with female heterogamety such as birds and reptiles. Our results point to a possible role of the multiple sex chromosomes in the speciation of Leptidea butterflies (Šíchová et al., 2015).

In the major pome fruit pest, the codling moth Cydia pomonella (Tortricidae), we performed gene-based physical mapping of the Z chromosome and showed that it is a neo-Z chromosome that arose by fusion between an ancestral Z chromosome and an autosome corresponding to chromosome 15 in the B. mori reference genome. We further showed 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, which significantly increased the adaptive potential of tortricid moths. Our findings thus not only contribute to management of tortricid pests but also allow a unique perspective concerning the role of neo-sex chromosomes in the adaptive radiation and speciation of phytophagous insects (Nguyen et al., 2013; Carabajal Paladino et al., 2014).

Fig. Mapping of sex-linked genes in the codling moth: a) pachytene chromosomes; b) gene map. Credit: Nguyen_et_al_2013_PNAS_codling_moth_neo-Z_mapping.jpg

Our research is also motivated by the need to develop efficient genetic sexing strains in pest speciessuch as the codling moth in order to facilitate their control by the Sterile Insect Technique (SIT), which currently relies on the mass rearing and release of sterile insects of both sexes into wild populations of the pest. Male-only releases could significantly reduce costs and increase efficiency of SIT. Knowledge of sex chromosomes and sex-determining genes is essential for the successful development of genetic sexing strains for SIT programmes against key pests. 

Author: prof. RNDr. František Marec, CSc.

We acknowledge the use of research infrastructure that has received funding from the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement n° 316304.

This issue is processed e.g. in:

Yoshido A., Marec F., Sahara K. (submitted) The fate of W chromosomes in hybrids between wild silkmoths, Samia cynthia ssp.: no role in sex determination and reproduction. Heredity

Šíchová J., Voleníková A., Dincă V., Nguyen P., Vila R., Sahara K., Marec F. (2015) Dynamic karyotype evolution and unique sex determination systems in Leptidea wood white butterflies.  BMC Evolutionary Biology 15: 89.

Marec F. (2014) Female silkworms have the sex factor. Nature 509: 570-571.

Carabajal Paladino L.Z., Nguyen P., Šíchová J., Marec F. (2014) Mapping of single-copy genes by TSA-FISH in the codling moth, Cydia pomonella. BMC Genetics 15: S15.

Nguyen P., Sýkorová M., Šíchová J., Kůta V., Dalíková M., Čapková Frydrychová R., Neven L.G., Sahara K., Marec F. (2013) Neo-sex chromosomes and adaptive potential in tortricid pests.  Proceedings of the National Academy of Sciences of the United States of America 110: 6931-6936.