Jae-Cheon Sohn

A Large-Scale, Higher-Level, Molecular Phylogenetic Study of the Insect Order Lepidoptera (Moths and Butterflies)

Background Higher-level relationships within the Lepidoptera, and particularly within the species-rich subclade Ditrysia, are generally not well understood, although recent studies have yielded progress. We present the most comprehensive molecular analysis of lepidopteran phylogeny to date, focusing on relationships among superfamilies. Methodology / Principal Findings 483 taxa spanning 115 of 124 families were sampled for 19 protein-coding nuclear genes, from which maximum likelihood tree estimates and bootstrap percentages were obtained using GARLI. Assessment of heuristic search effectiveness showed that better trees and higher bootstrap percentages probably remain to be discovered even after 1000 or more search replicates, but further search proved impractical even with grid computing. Other analyses explored the effects of sampling nonsynonymous change only versus partitioned and unpartitioned total nucleotide change; deletion of rogue taxa; and compositional heterogeneity. Relationships among the non-ditrysian lineages previously inferred from morphology were largely confirmed, plus some new ones, with strong support. Robust support was also found for divergences among non-apoditrysian lineages of Ditrysia, but only rarely so within Apoditrysia. Paraphyly for Tineoidea is strongly supported by analysis of nonsynonymous-only signal; conflicting, strong support for tineoid monophyly when synonymous signal was added back is shown to result from compositional heterogeneity. Conclusions / Significance Support for among-superfamily relationships outside the Apoditrysia is now generally strong. Comparable support is mostly lacking within Apoditrysia, but dramatically increased bootstrap percentages for some nodes after rogue taxon removal, and concordance with other evidence, strongly suggest that our picture of apoditrysian phylogeny is approximately correct. This study highlights the challenge of finding optimal topologies when analyzing hundreds of taxa. It also shows that some nodes get strong support only when analysis is restricted to nonsynonymous change, while total change is necessary for strong support of others. Thus, multiple types of analyses will be necessary to fully resolve lepidopteran phylogeny.

A Molecular Phylogeny for Yponomeutoidea (Insecta, Lepidoptera, Ditrysia) and Its Implications for Classification, Biogeography and the Evolution of Host Plant Use

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.

The fossil record and taphonomy of butterflies and moths (Insecta, Lepidoptera): implications for evolutionary diversity and divergence-time estimates

BackgroundIt is conventionally accepted that the lepidopteran fossil record is significantly incomplete when compared to the fossil records of other, very diverse, extant insect orders. Such an assumption, however, has been based on cumulative diversity data rather than using alternative statistical approaches from actual specimen counts.ResultsWe reviewed documented specimens of the lepidopteran fossil record, currently consisting of 4,593 known specimens that are comprised of 4,262 body fossils and 331 trace fossils. The temporal distribution of the lepidopteran fossil record shows significant bias towards the late Paleocene to middle Eocene time interval. Lepidopteran fossils also record major shifts in preservational style and number of represented localities at the Mesozoic stage and Cenozoic epoch level of temporal resolution. Only 985 of the total known fossil specimens (21.4%) were assigned to 23 of the 40 extant lepidopteran superfamilies. Absolute numbers and proportions of preservation types for identified fossils varied significantly across superfamilies. The secular increase of lepidopteran family-level diversity through geologic time significantly deviates from the general pattern of other hyperdiverse, ordinal-level lineages.ConclusionOur statistical analyses of the lepidopteran fossil record show extreme biases in preservation type, age, and taxonomic composition. We highlight the scarcity of identified lepidopteran fossils and provide a correspondence between the latest lepidopteran divergence-time estimates and relevant fossil occurrences at the superfamily level. These findings provide caution in interpreting the lepidopteran fossil record through the modeling of evolutionary diversification and in determination of divergence time estimates.

New fossil Lepidoptera (Insecta: Amphiesmenoptera) from the Middle Jurassic Jiulongshan Formation of Northeastern China.

Background The early history of the Lepidoptera is poorly known, a feature attributable to an inadequate preservational potential and an exceptionally low occurrence of moth fossils in relevant mid-Mesozoic deposits. In this study, we examine a particularly rich assemblage of morphologically basal moths that contribute significantly toward the understanding of early lepidopteran biodiversity. Methodology/Principal Findings Our documentation of early fossil moths involved light- and scanning electron microscopic examination of specimens, supported by various illumination and specimen contrast techniques. A total of 20 moths were collected from the late Middle Jurassic Jiulongshan Formation in Northeastern China. Our principal results were the recognition and description of seven new genera and seven new species assigned to the Eolepidopterigidae; one new genus with four new species assigned to the Mesokristenseniidae; three new genera with three new species assigned to the Ascololepidopterigidae fam. nov.; and one specimen unassigned to family. Lepidopteran assignment of these taxa is supported by apomorphies of extant lineages, including the M1 vein, after separation from the M2 vein, subtending an angle greater than 60 degrees that is sharply angulate at the junction with the r–m crossvein (variable in Trichoptera); presence of a foretibial epiphysis; the forewing M vein often bearing three branches; and the presence of piliform scales along wing veins. Conclusions/Significance The diversity of these late Middle Jurassic lepidopterans supports a conclusion that the Lepidoptera–Trichoptera divergence occurred by the Early Jurassic.

A molecular phylogeny and revised higher-level classification for the leaf-mining moth family Gracillariidae and its implications for larval host-use evolution

Gracillariidae are one of the most diverse families of internally feeding insects, and many species are economically important. Study of this family has been hampered by lack of a robust and comprehensive phylogeny. In the present paper, we sequenced up to 22 genes in 96 gracillariid species, representing all previously recognized subfamilies and genus groups, plus 20 outgroups representing other families and superfamilies. Following objective identification and removal of two rogue taxa, two datasets were constructed: dataset 1, which included 12 loci totalling 9927 bp for 94 taxa, and dataset 2, which supplemented dataset 1 with 10 additional loci for 10 taxa, for a total of 22 loci and 16 167 bp. Maximum likelihood analyses strongly supported the monophyly of Gracillariidae and most previously recognized subfamilies and genus groups. On this basis, we propose a new classification consisting of eight subfamilies, four of which are newly recognized or resurrected: Acrocercopinae Kawahara & Ohshima subfam. n.; Gracillariinae Stainton; Lithocolletinae Stainton; Marmarinae Kawahara & Ohshima subfam. n.; Oecophyllembiinae Réal & Balachowsky; Parornichinae Kawahara & Ohshima subfam. n.; Ornixolinae Kuznetzov & Baryshnikova stat. rev.; and Phyllocnistinae Zeller. The subfamily Gracillariinae is restricted to the monophyletic group comprising Gracillaria Haworth and closely related genera. We also formally transfer Acrocercops scriptulata Meyrick to Ornixolinae and use the name Diphtheroptila Vári, creating Diphtheroptila scriptulata comb. n. An exploratory mapping of larval host‐use traits on the phylogeny shows strong conservation of modes of leaf mining but much higher lability of associations with host plant orders and families, suggesting that host shifts could play a significant role in gracillariid diversification.

A molecular phylogeny and revised classification for the oldest ditrysian moth lineages (Lepidoptera: Tineoidea), with implications for ancestral feeding habits of the mega-diverse Ditrysia

The Tineoidea are the earliest‐originating extant superfamily of the enormous clade Ditrysia, whose 152 000+ species make up 98% of the insect order Lepidoptera. Though more diverse than all non‐ditrysian superfamilies put together (3719 vs 2604 species), the tineoids are not especially species‐rich among ditrysian superfamilies. Their phylogenetic position, however, makes tineoids potentially important for understanding the causes of ditrysian hyperdiversity, through their effect on inferences about the traits of ancestral ditrysians. To reconstruct early ditrysian evolution, we need a firmly established ground plan for tineoids themselves, which in turn requires a robust knowledge of their biodiversity and phylogeny. Tineoid systematics is under‐studied. The description of the world fauna remains very patchy, especially in the largest family, Tineidae, and phylogenetic studies within and among families have been few. Recently, molecular analyses have shown strong promise for advancing tineoid systematics. Here we present the largest tineoid molecular study to date, sampling five to 19 nuclear gene regions (6.6–14.7 kb) in 62 species, representing all tineoid groups ever assigned family rank, 25 of the 31 subfamilies recognized in recent classifications, and 40 genera spanning the morphological diversity of Tineidae, for which monophyly has not been established. Phylogenetic analysis used maximum likelihood, with synonymous substitutions alternatively included and excluded. The main findings confirm and extend those of other recent studies, as follows: (i) monophyly is strongly supported for Psychidae subsuming Arrhenophanidae, for Eriocottidae, and for Tineidae subsuming Acrolophidae but excluding Dryadaulinae and two genera previously assigned to Meessiinae; (ii) two new families are described, Dryadaulidae stat. rev. and Meessiidae stat. rev., based on subfamilies previously included in Tineidae but strongly excluded from this and all other families by our molecular results; (iii) Doleromorpha, formerly placed in Meessiinae sensu lato, is likewise here excluded from Tineidae, but left incertae sedis pending better characterization of what is potentially another new family; (iv) basal division of Tineidae sensu novo into ‘tineine’ and ‘acrolophine’ lineages is moderately to strongly supported, but most subfamily relationships within these lineages are very weakly supported, and polyphyly is confirmed for Meessiinae and Myrmecozelinae as previously defined; (v) basal division of Psychidae sensu novo into ‘arrhenophanine’ and ‘psychine’ lineages is moderately to strongly supported, as are most subfamily relationships within these lineages; (vi) Tineoidea are paraphyletic with respect to all other Ditrysia when synonymous substitutions are eliminated, with branching order (Meessiidae stat. rev. (Psychidae sensu novo ((Eriocottidae (Dryadaulidae stat. rev. + Doleromorpha)) (Tineidae sensu novo + all other Ditrysia)))). Support for tineoid non‐monophyly varies, among the relevant nodes and among analyses, from weak to moderate to strong; and (vii) paraphyly of Tineoidea, coupled with parsimony mapping of feeding habits on the molecular phylogeny, suggests that the earliest ditrysians may typically have been detritivores and/or fungivores as larvae, like most extant tineoids, rather than host‐specific feeders on higher plants, as in most non‐ditrysians and most non‐tineoid Ditrysia, i.e., the great majority of Lepidoptera. Thus, radiation of Ditrysia, a leading example of insect diversification linked to that of higher plants, may have started with reversion to feeding habits more like those of ancestral amphiesmenopterans.

Phylogeny and feeding trait evolution of the mega-diverse Gelechioidea (Lepidoptera: Obtectomera): new insight from 19 nuclear genes

The Gelechioidea (>18 000 species), one of the largest superfamilies of Lepidoptera, are a major element of terrestrial ecosystems and include important pests and biological model species. Despite much recent progress, our understanding of the classification, phylogeny and evolution of Gelechioidea remains limited. Building on recent molecular studies of this superfamily and a recently revised family/subfamily classification, we provide an independent estimate of among‐family relationships, with little overlap in gene sample. We analysed up to five nuclear genes, totalling 6633 bp, for each of 77 gelechioids, plus up to 14 additional genes, for a total of 14 826 bp, in 45 of those taxa and all 19 outgroup taxa. Our maximum‐likelihood (ML) analyses, like those of previous authors, strongly support monophyly for most multiply‐sampled families and subfamilies, but very weakly support most relationships above the family level. Our tree looks superficially divergent from that of the most recent molecular study of gelechioids, but when the previous tree is re‐rooted to accord maximally with ours, the two phylogenies agree entirely on the deepest‐level divergences in Gelechioidea, and strongly though incompletely on among‐family relationships within the major groups. This concordance between independent studies is evidence that the groupings (or at least the unrooted branching order) are probably accurate, despite the low bootstrap values. After re‐rooting, both trees divide the families into three monophyletic groups: a ‘Gelechiid Assemblage,’ consisting of Gelechiidae and Cosmopterigidae; a ‘Scythridid Assemblage,’ consisting of Stathmopodidae, Scythrididae, Blastobasidae, Elachistidae, Momphidae, Coleophoridae and Batrachedridae; and a ‘Depressariid Assemblage,’ consisting of Autostichidae, Xyloryctidae, Lecithoceridae, Oecophoridae, Depressariidae and Lypusidae. Within the largest family, Gelechiidae, our results strongly support the pairing of Anomologinae with Gelechiinae, in accordance with a recent study of this family. Relationships among the other subfamilies, however, conflict moderately to strongly between studies, leaving the intrafamily phylogeny unsettled. Within the ‘Scythridid Assemblage,’ both trees support an ‘SSB clade’ consisting of Blastobasidae + (Scythrididae + Stathmopodidae), strongly resolved only in our results. Coleophoridae + Batrachedridae is supported, albeit weakly, in both trees, and only Momphidae differ in position between studies. Within the ‘Depressariid Assemblage,’ both trees support an ‘AXLO’ clade consisting of Autostichidae, Xyloryctidae, Lecithoceridae and Oecophoridae. The monophyly of this clade and relationships therein are supported weakly in previous results but strongly in ours. The recently re‐defined family Depressariidae is paraphyletic in our tree, but the evidence against depressariid monophyly is very weak. There is moderate support for a core group of Depressariidae consisting, among the seven subfamilies we sampled, of Depressariinae, Aeolanthinae and Hypertrophinae. We show that gelechioids have a higher total number and percentage of species that are saprophagous as larvae than any other apoditrysian superfamily, that saprophagy is concentrated primarily in the ‘AXLO clade,’ and that the ancestral gelechioid condition was probably feeding on live plants. Among the living‐plant feeders, concealed external feeding was probably the ancestral state. The multiple origins of internal feeding of various kinds, including leaf mining (otherwise almost unknown in Apoditrysia), are restricted mostly to the Scythridid and Gelechiid Assemblages. The traits that predispose or permit lineages to adopt these unusual life histories are worthy of study.

TWO NEW SPECIES OF WOCKIA HEINEMANN (LEPIDOPTERA: URODIDAE) FROM COASTAL DRY-FORESTS IN WESTERN MEXICO

Abstract Two new species of Wockia Heinemann, 1870 (Lepidoptera: Urodidae), W. chewbacca and W. mexicana, are described from primary dry-forests in western México. A new host record is reported for the genus from larvae of W. chewbacca feeding on leaves of Casearia nitida (L.) Jacq. (Salicaceae). Several shared genitalic features and DNA barcode similarities suggest a congeneric relationship between the two Mexican species but uncertain generic placement within Urodidae. Scanning electron micrographs of the larva and illustrations of the larva and pupa of Wockia chewbacca are provided, along with illustrations of male and female genitalia of both Mexican species. Three unusual features found in the larval stage are documented for W. chewbacca include; a multi-lobed integument, recurved D2 seta on the shield of T1, and a “hydroid bush” consisting of multiple sensilla trichoidea on the apical turret of the antenna. Locality data indicate the existence of Neotropical elements of Wockia and an expanded distributional range for the genus.

A revised checklist of Nepticulidae fossils (Lepidoptera) indicates an Early Cretaceous origin

With phylogenetic knowledge of Lepidoptera rapidly increasing, catalysed by increasingly powerful molecular techniques, the demand for fossil calibration points to estimate an evolutionary timeframe for the order is becoming an increasingly pressing issue. The family Nepticulidae is a species rich, basal branch within the phylogeny of the Lepidoptera, characterized by larval leaf-mining habits, and thereby represents a potentially important lineage whose evolutionary history can be established more thoroughly with the potential use of fossil calibration points. Using our experience with extant global Nepticulidae, we discuss a list of characters that may be used to assign fossil leaf mines to Nepticulidae, and suggest useful methods for classifying relevant fossil material. We present a checklist of 79 records of Nepticulidae representing adult and leaf-mine fossils mentioned in literature, often with multiple exemplars constituting a single record. We provide our interpretation of these fossils. Two species now are included in the collective generic name Stigmellites: Stigmellites resupinata (Krassilov, 2008) comb. nov. (from Ophiheliconoma) and Stigmellites almeidae (Martins-Neto, 1989) comb. nov. (from Nepticula). Eleven records are for the first time attributed to Nepticulidae. After discarding several dubious records, including one possibly placing the family at a latest Jurassic position, we conclude that the oldest fossils likely attributable to Nepticulidae are several exemplars representing a variety of species from the Dakota Formation (USA). The relevant strata containing these earliest fossils are now dated at 102 Ma (million years ago) in age, corresponding to the latest Albian Stage of the Early Cretaceous. Integration of all records in the checklist shows that a continuous presence of nepticulid-like leaf mines preserved as compression-impression fossils and by amber entombment of adults have a fossil record extending to the latest Early Cretaceous.

Systematics, phylogeny and biology of a new genus of Lithocolletinae (Lepidoptera: Gracillariidae) associated with Cistaceae

The gracillariid genus Triberta gen. nov. (Lepidoptera: Gracillariidae: Lithocolletinae Stainton, 1854) is described to accommodate two species formerly assigned to the genus Phyllonorycter Hübner, 1822: Triberta helianthemella (Herrich-Schäffer, 1861) comb. nov. and T. cistifoliella (Groschke, 1944) comb. nov. Triberta cistifoliella bona sp. is restored from synonymy based on morphological characters. The new genus is biologically associated with the plant family Cistaceae of the order Malvales and is endemic to the Palaearctics. Our molecular analysis of eleven nuclear genes failed to unambiguously place Triberta in the lithocolletine phylogeny, but revealed that this genus is distinct from either clade Phyllonorycter + Cremastobombycia and Cameraria. The distinctiveness of Triberta is also supported by inferred traits in wing venation, micro morphology of the last instar larva, pupa, genital morphology of the adult and life history. A key to the species of Triberta is provided. The interspecific homogeneity in external morphology, coupled with minor differences in genital traits, an apparent narrow specialization on Cistaceae host plants, restricted geographical range and molecular evidence based on multi-nuclear genes jointly suggest that the generic diversification of Triberta is a relatively old phenomenon and driven strongly by host selection.