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A molecular phylogeny for yponomeutoidea (insecta, Lepidoptera, ditrysia) and its implications for classification, biogeography and the evolution of host plant use - PubMed

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A molecular phylogeny for yponomeutoidea (insecta, Lepidoptera, ditrysia) and its implications for classification, biogeography and the evolution of host plant use

Jae-Cheon Sohn et al. PLoS One. 2013.

Abstract

Background: Yponomeutoidea, one of the early-diverging lineages of ditrysian Lepidoptera, comprise about 1,800 species worldwide, including notable pests and insect-plant interaction models. Yponomeutoids were one of the earliest lepidopteran clades to evolve external feeding and to extensively colonize herbaceous angiosperms. Despite the group's economic importance, and its value for tracing early lepidopteran evolution, the biodiversity and phylogeny of Yponomeutoidea have been relatively little studied.

Methodology/principal findings: Eight nuclear genes (8 kb) were initially sequenced for 86 putative yponomeutoid species, spanning all previously recognized suprageneric groups, and 53 outgroups representing 22 families and 12 superfamilies. Eleven to 19 additional genes, yielding a total of 14.8 to 18.9 kb, were then sampled for a subset of taxa, including 28 yponomeutoids and 43 outgroups. Maximum likelihood analyses were conducted on data sets differing in numbers of genes, matrix completeness, inclusion/weighting of synonymous substitutions, and inclusion/exclusion of "rogue" taxa. Monophyly for Yponomeutoidea was supported very strongly when the 18 "rogue" taxa were excluded, and moderately otherwise. Results from different analyses are highly congruent and relationships within Yponomeutoidea are well supported overall. There is strong support overall for monophyly of families previously recognized on morphological grounds, including Yponomeutidae, Ypsolophidae, Plutellidae, Glyphipterigidae, Argyresthiidae, Attevidae, Praydidae, Heliodinidae, and Bedelliidae. We also assign family rank to Scythropiinae (Scythropiidae stat. rev.), which in our trees are strongly grouped with Bedelliidae, in contrast to all previous proposals. We present a working hypothesis of among-family relationships, and an informal higher classification. Host plant family associations of yponomeutoid subfamilies and families are non-random, but show no trends suggesting parallel phylogenesis. Our analyses suggest that previous characterizations of yponomeutoids as predominantly Holarctic were based on insufficient sampling.

Conclusions/significance: We provide the first robust molecular phylogeny for Yponomeutoidea, together with a revised classification and new insights into their life history evolution and biogeography.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Previous hypotheses of phylogenetic relationships in Yponomeutoidea.

A. Moriuti (1977), B. Heppner (1998), C. Kyrki (1990). All figures are redrawn with nomenclature following the original.

Figure 2
Figure 2. The best ML tree found for nt123 analysis of the deliberately incomplete 8–27 gene, 139-taxon data set, showing Yponomeutoidea only.

Bootstrap supports shown above branches: partitioned 8–27 gene nt123/unpartitioned 8–27 gene nt123/8-gene nt123/8–27 gene degen1/8–27 gene codon model/rogue-pruned 8–27 gene nt123 (121 taxa). ‘−’ = node not recovered in the ML tree for that analysis. ‘*’ = bootstrap value <50%. ‘NA’ = bootstrap value undefined because data were obtained for ≤1 taxon in that clade for that analysis. Dotted lines indicate alternative topologies strongly supported by either degen1 or the codon model. Node numbers for selected nodes (solid circles) are provided to facilitate discussion. Thickened terminal branches denote yponomeutoid species feeding on Celastraceae.

Figure 3
Figure 3. The best ML tree found for nt123 analysis of the deliberately incomplete 8–27 gene, 139-taxon data set (continued from Fig. 2), showing outgroups only.

See Figure 2 for notes on bootstrap supports and node numbers. Terminal taxa shown in pink were initially thought to be yponomeutoids.

Figure 4
Figure 4. Phylogram representation of ML tree shown in Figures 2 and 3.

Branch lengths are proportional to total number of substitutions per site. Thickened branches are supported by ≥70% bootstrap in at least one analysis summarized in Figures 2 and 3.

Figure 5
Figure 5. Representative adult habitus images of all yponomeutoid families and subfamilies recognized in this study.

Scale bar = 5 mm. A. Glyphipterigidae: Glyphipteriginae, Glyphipterix bifasciata (Walsingham); B. Glyphipterigidae: Acrolepiinae, Acrolepia xylophragma (Meyrick); C. Glyphipterigidae: Orthoteliinae, Orthotelia sparganella (Thunberg); D. Plutellidae, Plutella xylostella (Linnaeus); E. Ypsolophidae: Ypsolophinae, Ypsolopha blandella (Christoph); F. Ypsolophidae: Ochsenheimeriinae, Ochsenheimeria vacculella Fisher von Roeslerstamm; G. Yponomeutidae: Yponomeutinae, Yponomeuta padellus Linnaeus; H. Yponomeutidae: Saridoscelinae, Saridoscelis kodamai Moriuti; I. Argyresthiidae, Argyresthia brockeella (Hübner); J. Lyonetiidae: Lyonetiinae, Lyonetia ledi Wocke; K. Lyonetiidae: Cemiostominae, Leucoptera spartifoliella (Hübner); L. Praydidae, Prays fraxinella (Bjerkander); M. Attevidae, Atteva aurea (Fitch); N. Heliodinidae, Embola ciccella (Barnes et Busck); O. Bedelliidae, Bedellia somnulentella (Zeller); P. Scythropiidae stat. rev., Scythropia crataegella (Linnaeus).

Figure 6
Figure 6. Host plant families of 16 major yponomeutoid lineages.

The cladogram is simplified from figure 2, annotated with predominant growth form of host plants (‘W’ for woody plants vs. ‘H’ for herbaceous plants). Fractions below yponomeutoid taxon names denote host record completeness for genera and species (in that order), calculated from the number of genera or species with host records relative to the total number of known genera or species. Host plant families used by each lineage are denoted by gray cells showing the numbers of species feeding on that plant family. Symbols denote the dominant growth-forms of each plant family: shaded circles = trees and shrubs; open circles = herbs; and shaded stars = veins and lianas. Capital letters next to host plant orders denote membership in clades above the order level: A – magnoliids, B – commelinids, C – fabids, D – malvids, E – lamiids, F – campanulids, G – Gnetophyta, and H – Pinophyta.

Figure 7
Figure 7. Species diversity, feeding mode, diet breadth and geographic distribution of 16 major yponomeutoid lineages.

The tree topology is that of Figure 6. Branch colors indicate predominant feeding modes: black = internal feeding; blue = external feeding; alternating black and blue = state ambiguous under parsimony optimization.

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Financial support was provided by the U.S. National Science Foundation’s Assembling the Tree of Life program, award number 0531769, and the Maryland Agricultural Experiment Station. This is contribution 244 of the Evolution of Terrestrial Ecosystems consortium of the National Museum of Natural History, in Washington, D.C. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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