Evolution of heteroneuran Lepidoptera (Insecta) and the utility of dopa decarboxylase for Cretaceous-age phylogenetics

Abstract

This study tests the utility of the nuclear gene encoding dopa decarboxylase (DDC) for recovering Cretaceous-age divergences within the lepidopteran clade Heteroneura, which contains 98% of lepidopteran species. A 709-bp fragment of DDC has been sequenced in 32 species, including representatives of all major lineages of Heteroneura plus outgroups from more basal lepidopteran groups and the related order Trichoptera. Pairwise divergences across the first and second codon positions and amino acids increase with depth throughout the taxonomic hierarchy, indicating that non-synonymous substitutions are not fully saturated; whereas, divergences across the third codon position level off at the family to superfamily level. Inclusion of non-neolepidopteran outgroups results in phylogeny estimates that contradict well established groups, almost surely due to sparse taxon sampling and high character divergence. When these taxa and an equivalently divergent basal ditrysian are excluded, DDC trees show nearly complete recovery of ten uncontroversial basal heteroneuran «test clades» of family rank and higher, about half with strong bootstrap support. Thus, DDC clearly carries phylogenetic signal at these levels. Bootstrap support for resolution of the controversial relationships among the five main heteroneuran groups (four monotrysian superfamilies plus Ditrysia) is individually low, but two of three previous hypotheses were statistically rejected overall by DDC. DDC trees within the primitive heteroneuran superfamily Incurvarioidea, though modestly supported, closely resemble a previous morphological hypothesis, while removing the requirement for reversal in a possible «key adaptation», the larval case. Taxon overlap with a previous mtDNA study of Prodoxidae (Incurvarioidea), which includes much-studied mutualist pollinators, permits a comparison of substitution rates with the conservative mitochondrialCOI +COII region, as well as combined-data re-examination of generic reltionships. Non-synonymous substitution is about 25% slower in DDC than in COI+COII, though synonymous substitution is faster. With additional taxon sampling, and in combination with other genes, DDC promises to be a powerful tool for reconstructing among-superfamily relationships within Lepidoptera and probably other insect groups.