Academic journal article Genetics

Synteny and Chromosome Evolution in the Lepidoptera: Evidence from Mapping in Heliconius Melpomene

Academic journal article Genetics

Synteny and Chromosome Evolution in the Lepidoptera: Evidence from Mapping in Heliconius Melpomene

Article excerpt

ABSTRACT

The extent of conservation of synteny and gene order in the Lepidoptera has been investigated previously only by comparing a small subset of linkage groups between the moth Bombyx mori and the butterfly Heliconius melpomene. Here we report the mapping of 64 additional conserved genes in H. melpomene, which contributed 47 markers to a comparative framework of 72 orthologous loci spanning all 21 H. melpomene chromosomes and 27 of the 28 B. mori chromosomes. Comparison of the maps revealed conserved synteny across all chromosomes for the 72 loci, as well as evidence for six cases of chromosome fusion in the Heliconius lineage that contributed to the derived 21-chromosome karyotype. Comparisons of gene order on these fused chromosomes revealed two instances of colinearity between H. melpomene and B. mori, but also one instance of likely chromosomal rearrangement. B. mori is the first lepidopteran species to have its genome sequenced, and the finding that there is conserved synteny and gene order among Lepidoptera indicates that the genomic tools developed in B. mori will be broadly useful in other species.

THE domesticated silkmoth Bombyx mori (Bombycidae: Bombycinae) was the first lepidopteran species to become a focus of genomic studies, due to its tractability as a study organism and importance to the silk industry. In combination with a draft genome sequence completed in 2004 (Xia et al. 2004), recent high-density linkage maps provide a comprehensive picture of chromosomal linkage in B. mori (Yasukochi 1998; Miao et al. 2005; Yoshido et al. 2005; Yasukochi et al. 2006). Increasingly, however, genetic studies of other Lepidoptera are also reaching genomic scale as similar tools are applied in nonmodel species (Papanicolaou et al. 2005; Beldade et al. 2006; Turner et al. 2006). In particular, these studies have focused on groups of specific ecological and evolutionary interest. Heliconius butterflies (Nymphalidae: Heliconiinae: Heliconiini) are one such group, notable for their highly accurate Müllerian mimicry in which unpalatable species converge in apo-sematic coloration.

Genome mapping studies in diverse taxa, such as in the Heliconiini, will allow the first comparisons of linkage across the Lepidoptera. To draw conclusions from comparative mapping between B. mori and Heliconius, it is necessary to consider the phylogenetic relationships and evolution of karyotype in the Lepi-doptera as a whole. Rhopalocera, the lineage that contains heliconiines and the rest of the true butterflies (Papilionoidea) is younger than the Bombycoidea, the lineage that contains the silkworm moths (Grimaldi and Engel 2005). Derived heliconiines have a chromosome number of 21, contrasting with the 31 chromosomes of the basal genera in the Heliconiini and basal Lepidoptera (Suomalainen 1979). Thus, both B. mori (28 chromosomes) and derived Heliconiini appear to have undergone independent karyotype reductions from more basal taxa.

Studies using traditional genetic methods located several chromosomal regions responsible for color-pattern changes in the comimicking species Heliconius melpomene and H. erato (Sheppard et al. 1985; Mallet 1989; Jiggins and Mc M illan 1997; Gilbert 2003; Naisbit et al. 2003). However, it is only very recently that genomic tools, including high-density linkage maps and expressed sequence tag (EST) libraries have begun to be developed for these butterflies as a means for identifying the particular genes underlying changes in color patterns (Jiggins et al. 2005; Tobler et al. 2005; Joron et al. 2006b; Kapan et al. 2006; Kronforst et al. 2006). An earlier linkage map of H. melpomene localized amplified fragment length polymorphisms (AFLPs), microsatellites, and single-copy nuclear loci (SCNLs) to 21 distinct linkage groups (LGs) (Jiggins et al. 2005), which correspond to the 21 H. melpomene chromosomes. Importantly, that study identified and mapped 19 SCNLs that are homologous to annotated genes from other organisms and represent anchor loci for comparisons with B. …

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