Volume 48, Issue 3 p. 445-462
Original Article
Open Access

Evolutionary history of Euteliidae (Lepidoptera, Noctuoidea)

Reza Zahiri

Corresponding Author

Reza Zahiri

Canadian Food Inspection Agency, Ottawa Plant Laboratory, Entomology Laboratory, Ottawa, Ontario, Canada

Correspondence

Reza Zahiri, Canadian Food Inspection Agency, Ottawa Plant Laboratory, Entomology Laboratory, 960 Carling Ave., Ottawa K1A 0C6 ON, Canada.

Email: [email protected]

Niklas Wahlberg, Department of Biology, Lund University, Lund, Sweden.

Email: [email protected]

Contribution: Conceptualization, ​Investigation, Funding acquisition, Writing - original draft, Methodology, Validation, Visualization, Writing - review & editing, Software, Formal analysis, Project administration, Data curation, Supervision, Resources

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Jeremy D. Holloway

Jeremy D. Holloway

Science Group, Natural History Museum, London, UK

Contribution: ​Investigation, Validation, Visualization, Writing - review & editing, Supervision, Conceptualization, Resources

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Jadranka Rota

Jadranka Rota

Department of Biology, Lund University, Lund, Sweden

Contribution: Writing - review & editing, Methodology, Data curation, Conceptualization

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B. Christian Schmidt

B. Christian Schmidt

Agriculture and Agri-Food Canada, Biodiversity Program, Canadian National Collection of Insects, Arachnids, and Nematodes, Ottawa, Ontario, Canada

Contribution: Conceptualization, ​Investigation, Funding acquisition, Writing - review & editing, Validation, Resources

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Markku J. Pellinen

Markku J. Pellinen

175, M1 Muuban Phichai, Muang Lampang, Lampang, Thailand

Contribution: Validation, Resources, Visualization

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Ian J. Kitching

Ian J. Kitching

Science Group, Natural History Museum, London, UK

Contribution: Resources, Writing - review & editing, Validation

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Scott E. Miller

Scott E. Miller

National Museum of Natural History, Smithsonian Institution, Washington, DC, USA

Contribution: Resources, Writing - review & editing, Data curation, Project administration

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Niklas Wahlberg

Corresponding Author

Niklas Wahlberg

Department of Biology, Lund University, Lund, Sweden

Correspondence

Reza Zahiri, Canadian Food Inspection Agency, Ottawa Plant Laboratory, Entomology Laboratory, 960 Carling Ave., Ottawa K1A 0C6 ON, Canada.

Email: [email protected]

Niklas Wahlberg, Department of Biology, Lund University, Lund, Sweden.

Email: [email protected]

Contribution: Resources, Supervision, Data curation, Methodology, Validation, Writing - review & editing, Conceptualization, Funding acquisition

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First published: 13 April 2023
Citations: 1

Abstract

We performed a molecular phylogenetic analysis on the family Euteliidae to clarify deep divergences and elucidate evolutionary relationships at the level of the subfamily, tribe, and genus. Our dataset consists of 6.3 kbp of one mitochondrial and seven nuclear DNA loci and was analysed using model-based phylogenetic methods, that is, maximum likelihood and Bayesian inference. Based on the recovered topology, we recognize two subfamilies, Euteliinae and Stictopterinae, and the tribes Stictopterini and Odontini. We identify apomorphic morphological character states for Euteliidae and its component subfamilies and tribes. Several genera (e.g., Targalla, Paectes, Marathyssa, Eutelia) were found polyphyletic and require taxonomic revision. Two new genera (Niklastelia Zahiri & Holloway gen.nov. and Pellinentelia Holloway & Zahiri gen.nov.) are described and a number of taxonomic changes (new combinations and new synonymies) are established. The Neotropical genus Thyriodes, currently included in Euteliidae, is found to be associated with Erebinae (Erebidae). The divergence time estimate for the split between the Euteliidae and Noctuidae is at 53 Ma, and the Euteliidae subfamilies Euteliinae and Stictopterinae are estimated to have diverged at 42 Ma. In Stictopterinae, the tribes Stictopterini and Odontodini split at 31 Ma, while Euteliinae began diversifying at 34 Ma. Malpighiales are inferred to have been the ancestral larval hostplant order for Euteliidae. The ancestors of Stictopterinae also appear to have been Malpighiales feeders, but then diverged to Malvales specialists (Odontodini) and Malpighiales specialists (Stictopterini) hostplants. Larvae of Stictopterini appear to be restricted primarily to Clusiaceae, apart from a few records from Dipterocarpaceae. In Euteliinae, Anacardiaceae are predominant as larval hosts. Thus, all hosts in the family are lactiferous, possibly providing some degree of pre-adaptation for exploiting Dipterocarpaceae.

INTRODUCTION

Current status of Euteliidae

The family Euteliidae is one of the four major lineages of the quadrifid noctuoids recognized in Zahiri et al. (2011), being a rather homogeneous and small group of 34 genera and 520 species (Nieukerken et al., 2011). Euteliidae are the only quadrifid noctuoid lineage without even a preliminary molecular phylogeny. The diversity of euteliid moths is concentrated in the tropics, although they tend to be poorly documented, except for Borneo (Holloway & Barlow, 2011). Euteliidae along with three other major lineages (i.e., Nolidae, Erebidae, and Noctuidae) form a robust monophyletic assemblage, informally referred to as the quadrifid noctuoids, which was discussed in detail by Zahiri et al. (2011, 2012). However, the relationships among these four families are not fully understood yet, even though collectively the group has very strong support. Quadrifid noctuoids, along with the trifid noctuoids (i.e., Oenosandridae and Notodontidae), comprise the superfamily Noctuoidea, which contains the largest radiation of Lepidoptera (moths and butterflies).

Family rank was first proposed for Euteliidae by Mitchell et al. (2006), but both current subfamilies of Euteliidae (i.e., Euteliinae and Stictopterinae) were treated as distinct families (i.e., Euteliidae and Stictopteridae) in their phylogenetic hypothesis. The molecular analyses of Mitchell et al. (2006) corroborated these two groups as sister taxa, and in turn placed them as sister to their LAQ clade (i.e., Lymantriidae, Arctiidae, and Quadrifine Noctuoidea) within which the rest of the Erebidae groups were embedded. The close relationship between Euteliinae and Stictopterinae was also demonstrated by Kitching (1987) and Holloway (1985) based on morphological characters. Kitching (1987) proposed 11 unique, unreversed synapomorphies uniting the two (with nine apomorphies lost in one of the included genera). Synapomoprohies uniting Euteliinae and Sticopterinae include a reduced female frenulum; a clypeofrons scaled only at the edge; weak hindtarsal spinning; hindlegs shorter than midlegs; a small oval plate in the ductus ejaculatorius; ovipositor lobes (anal papillae) with inner surfaces facing at least partially posteriorly. The close relationship of Euteliinae + Stictopterinae was also discussed by Kitching and Rawlins (1998), who noted that the counter-tympanal hood has a unique double structure, although differently modified in each group. Fibiger and Lafontaine (2005) also recognized the two taxa as sister-groups, placing them as subfamilies within their concept of Erebidae. Holloway (2011) concluded that it was more informative to treat them as distinct subfamilies within one family, for which Euteliidae is the oldest name. This arrangement was fully supported by the molecular analysis of Zahiri et al. (2011).

Diagnostic characters of Euteliidae

Adult characteristics of Euteliinae include the shape of the forewing, which is either elongate or squarish, and a hindwing that usually has a subtornal mark, often incorporated in a broad, dark border contrasting with a paler ground colour (Holloway, 1985). Lateral scale tufts at the apex of the male abdomen often give it a squared-off appearance. The male antennae are characteristically broadly bipectinate over the basal half or two-thirds, narrowly so or only ciliate in the distal third; the antennae of females are usually filiform though occasionally partially bipectinate as in the male (Holloway, 1985). Partially bipectinate antennae of this form may be unique to Euteliinae within the quadrifid Noctuoidea but are paralleled in other families such as Notodontidae, Cossidae, and Limacodidae. The cryptic resting posture of adults of the subfamily is unusual with an upcurved abdomen that may be facilitated by musculature attached to the curved flanges of the ventral sternite at the base of the abdomen (Holloway, 1985). These flanges are distinctive and may serve to stiffen the sclerite and its development from a groove to a flange and could be a further adaptation associated with the characteristic resting posture of adults. Larval traits of Euteliidae include anterior prolegs that are not reduced, or only slightly reduced; short setae; a moderately elongate parallel-sided spinneret, and narrow spiracles (Figure 1a, b).

Details are in the caption following the image
Caterpillars of Euteliidae (photographs by M. Pellinen) (a, b) 5th instar of Penicillaria jocosatrix (Euteliinae); (c, d) 5th and 4th instars of Odontodes aleuca (Stictopterinae, Odontodini), respectively.

The prefix ‘sticto’ means dappled, mottled, or spotted (Holloway, 1985), and the majority have fine, complex markings on the forewings (often an etched, reticulate patterning) and many genera contain species with hindwings distinctively hyaline in their basal half, particularly Stictoptera Guenée, Aegilia Walker, and Lophoptera Guenée (Holloway, 1985). The antennae of both sexes are filiform, sometimes finely ciliate. The frenulum in the female is reduced to a single spine. A tuft of fine scales extends obliquely in a posterior ventral direction from anterior to the tympanum as in the Euteliinae but not to such a pronounced extent. The male eighth sternite typically bears a pair of coremata. The posture of Stictopterinae contrasts strikingly with the resting postures of Euteliinae. Species tend to rest with wings folded at an acute angle or, in Stictoptera and the more narrow-winged species, with them rolled around the body giving the appearance of a short, broken twig. Caterpillars of Stictopterinae have a complete set of four equal pairs of prolegs with uniordinal crochets, variably homoideous (Lophoptera), or heteroideous (Odontodes Guenée) (Figure 1c, d). Ventral prolegs are complete and equal, setae short and integument smooth (Figure 1c, d).

Hostplant associations of Euteliidae

There is a heavy bias within the Euteliinae towards the plant family Anacardiaceae. Genera of Anacardiaceae from which euteliines have been reared in the Indo-Australian tropics are: Anacardium L., Buchanania Spreng., Holigarnia Bell, Lannea (A. Rich.), Schinus L., Semecarpus L., and Spondias L. as well as Mangifera L. Other families recorded are Burseraceae (Bursera Jacq., Canarium L., Garuga Roxb.), Dipterocarpaceae (Anisoptera Korth., Shorea Roxb.), Fabaceae (Cajanus DC., Mucuna Adans.), Moraceae (Ficus L., Morus L.), myrtaceae (Eucalyptus L Her., Eugenia P. Michel., Myrtus L., Syzygium P. Browne; the Targalla delatrix group especially), Sapindaceae (Nephelium L., Pometia G. R. Forst), and Lamiaceae (Tectona L. f.) (Holloway, 1985). In southern Africa (Pinhey, 1975) Anacardiaceae are also recorded as hostplants (Pistacia L., Rhus L. for Eutelia adulatrix Hübner) but also Fabaceae (Brachystegia Benth., Baikiaea B. & H. for Targallodes polychondra Hampson), Myricaceae (Myrica L. for Eutelia bowkeri Felder), and Rutaceae (Citrus L. for Targallodes subrubens Mabille). In Nearctic, three species have been recorded from Rhus (Paectes oculatrix Guenee, Manathyssa basalis Walker and M. inficita Walker) but M. inficita includes Tsuga Carr. (Pinaceae) and Ulmus L. (Ulmaceae) in its host range (Tietze, 1972). P. pygmaea Hübner, the type species of Paectes, is recorded from Liquidambar L. (Hamamelidaceae) and P. burserae Dyar from Bursera (Burseraceae), the last family shared with the Oriental list.

The hostplant relationships within the Stictopterinae (e.g., Stictoptera, Aegilia, and Savoca) are mostly from the genera Garcinia L. (Clusiaceae, formerly Guttiferae), Calophyllum L. and Mesua L. of the family Calophyllaceae. Records from Odontodes and Lophoptera (both from the tribe Odontodini) are few but show a high frequency in the family Dipterocarpaceae (Shorea). Some Lophoptera species have shown host range extensions to other plant families, for example, Lophoptera squammigera Guenée is known from Shorea but also Grewia L. (Malvaceae) and Mallotus Lour. and Bridelia Willd. (Phyllanthacaceae) (Gardner, 1948; Holloway, 1985; Mathur, 1942).

Economic importance of Euteliidae

Euteliidae are of some minor economic importance according to records in Zhang (1994), a compendium of almost a century's records in the Review of Applied Entomology. An indication of economic importance can be reflected in the number of years in which records occur. Most Euteliinae pests defoliate fruit crops, particularly mango (Mangifera) (Anacardiaceae) with eight records for Penicillaria jocosatrix Guenée and a total of 12 for Chlumetia transversa (Walker) and C. euthysticha (Turner), although this genus also attacks young twigs and shoots. Eutelia adulatrix (Hübner) has three records from Pistacia (pistachio), also Anacardiaceae, but E. blandiatrix Hampson has a single record from Altingia Noronha (Hamamelidaceae), which is harvested for its scented resin and timber. Targalla palliatrix (Guenée) has two records of feeding on fruits in Myrtaceae, such as Eugenia L. and Syzygium P. Browne ex Gaertn. Fruit pests are also recorded in Stictopterinae: the Stictoptera species S. bisexualis Hampson, S. cucullioides Guenée and S. grisea Moore have five records collectively on Garcinia L. (mangosteen) and Phyllanthus L. (perfumes, oilseed, and some timber). Both subfamilies have also been recorded as forestry pests, particularly on Shorea Roxb. ex C.F. Gaertn. (Dipterocarpaceae), with three records for Paectes subapicalis (Walker) and one for Lophoptera illucida (Walker).

The goals of this study are first to assess the previous phylogenetic hypotheses with significantly expanded taxon sampling and then to focus on the ecology of Euteliidae, particularly the unique specialization of the early stages on a few plant groups with high levels of resin or latex in their sap and foliage that is not seen in any other group of the Macroheterocera to the same degree. In addition, we test putative morphological synapomorphies for the various groups of Euteliidae against the molecular phylogeny.

MATERIALS AND METHODS

Taxon sampling

To infer the phylogenetic hypothesis of Euteliidae, two taxon sampling strategies were adopted.

First, we inferred a backbone phylogenetic hypothesis based on a dataset of DNA sequences of up to eight independent protein-coding gene (PCG) regions from 183 terminal taxa, including 142 representatives of euteliid moths as the ingroup and 41 exemplars from four other families of Noctuoidea: Oenosandridae (two species), Notodontidae (three species), Noctuidae (eight species), Nolidae (four species), Erebidae (six species), and one species of Geometridae as outgroups to test the monophyly of Euteliidae (Table S1). The ingroup included representatives for all known major lineages of euteliids to date (subfamilies Euteliinae and Stictopterinae (including two tribes, Odontodini and Stictopterini)) and represents 20 of the 34 known genera of euteliids (Table S2). Table S2 also indicates which genera are represented by their type species (TS). This selection was mainly based on the results of previous morphological and molecular works (Fibiger & Lafontaine, 2005; Lafontaine & Fibiger, 2006; Lafontaine & Schmidt, 2010; Zahiri et al., 2011; Zahiri et al., 2012; Zahiri, Lafontaine, Holloway, et al., 2013; Zahiri, Lafontaine, Schmidt, et al., 2013). Cladograms were rooted with Geometridae, which represents the hypothesized sister taxon to Noctuoidea (Mutanen et al., 2010; Nieukerken et al., 2011; Regier et al., 2009).

Second, to find a home for a wide range of euteliids currently considered incertae sedis we added DNA barcode data from 243 specimens to the dataset in A (Table S3) to produce a 425-specimen dataset of Euteliidae (384 ingroup and 41 outgroup exemplars) (Table S3). This dataset includes 26 of the 34 currently recognized genera of euteliids (Table S2). A phylogeny was then generated that highlighted potential taxonomic misplacements, unrecognized major clades, and positions for incertae sedis taxa. We use these results to make systematic rearrangements within the family Euteliidae.

Gene sampling

Total genomic DNA was extracted from one or two legs, dried or freshly preserved in 96% ethanol, using the DNeasy tissue extraction kit (Qiagen, Hilden, Germany) or the NucleoSpin Tissue 250 kit (Macherey-Nagel, Düren, Germany) and following the manufacturers' instructions. For each specimen, we sequenced eight protein-coding exons that have previously been found to be highly informative in higher-level lepidopteran phylogeny (Keegan et al., 2019; Keegan et al., 2021; Mutanen et al., 2010; Rota et al., 2016; Wahlberg et al., 2009; Wahlberg & Wheat, 2008; Zahiri et al., 2011; Zahiri et al., 2012; Zahiri, Lafontaine, Holloway, et al., 2013; Zahiri, Lafontaine, Schmidt, et al., 2013). The gene regions were single-copy from the nuclear genome: elongation factor-1α (EF-1α; 1240 bp), ribosomal protein S5 (RpS5; 603 bp), carbamoylphosphate synthase domain protein (CAD; 862 bp), cytosolic malate dehydrogenase (MDH; 407 bp), glyceraldehyde-3-phosphate dehydrogenase (GAPDH; 691 bp), isocitrate dehydrogenase (IDH; 722 bp) and wingless (400 bp) genes, and, from the mitochondrial genome, cytochrome c oxidase subunit I (COI, contains both COI5P (i.e., barcode region) and COI3P fragments giving a total of 1476 bp). We followed the protocols from Wahlberg and Wheat (2008) for DNA amplification (PCR) and pre-sequencing methods. We sequenced our PCR products at the CFIA Ottawa Plant Laboratory (Fallowfield, Ontario, CA), or sent them to either Macrogen Europe Inc. (Amsterdam, The Netherlands) or Macrogen, Seoul, Korea for Sanger sequencing. For the majority of loci, we used single forward reads, although for some fragmented PCR products we used reverse reads as well (Wilson, 2012). We have deposited the sequences generated for this study in GenBank (GenBank accession numbers will be added to Table S1).

DNA sequence data and quality controls

We inspected sequence chromatograms visually for base call errors and heterozygous loci, and produced consensus sequences in Geneious® version 10.2.5 (http://www.geneious.com, Kearse et al., 2012), BioEdit (Hall, 1999), or Mesquite version 3.2 (Maddison & Maddison, 2017). Alignment was trivial and the few insertion/deletion events that were detected were of entire codons that could be easily aligned. To minimize the risk of any confusion during the sequencing protocol and errors in alignments, we constructed Neighbour-Joining and Maximum Likelihood trees separately for each gene region and checked them carefully for identical sequences and other doubtful patterns. In addition, to minimize the risk of incorrect identifications, all the specimens with COI sequences were cross-checked with their DNA barcodes in BOLD (Barcode of Life Data System, http://www.boldsystems.org) (Ratnasingham & Hebert, 2007), where reference specimens were available for many of the species used in this study.

Phylogenetic analyses

The aligned DNA sequences were added to a VoSeq version 1.7.4 database (Peña & Malm, 2012) from which we generated aligned datasets. The gene regions were explored using model-based phylogenetic approaches including Maximum Likelihood (ML) and Bayesian Inference (BI) methods. The dataset was analysed using the maximum likelihood framework in the program IQ-TREE V1.6.12 (Nguyen et al., 2015). The dataset, for a total of 6401 aligned nucleotide sites, was partitioned by gene into eight partitions. The best-fitting substitution models were selected by ModelFinder (Kalyaanamoorthy et al., 2017). Support for nodes was evaluated with 1000 ultrafast bootstrap (UFBoot2) approximations (Hoang et al., 2018), and SH-like approximate likelihood ratio test (Lanfear et al., 2012). To reduce the risk of overestimating branch supports in UFBoot2 test, we implemented the –bnni option, which optimizes each bootstrap tree using a hill-climbing nearest neighbour interchange (NNI) search. BI analyses were carried out using the software MrBayes v3.1 (Ronquist & Huelsenbeck, 2003) on the freely available Bioportal server (http://www.bioportal.uio.no). The Bayesian analyses were run independently twice for 20 million generations, with every 1000th tree sampled. The dataset was divided into two partitions, mtDNA and nDNA, as partitioning by gene resulted in poor mixing of chains and problems with convergence. We modelled the evolution of sequences according to the GTR+ Γ model independently for the two partitions using the “unlink” command in MrBayes. Clade robustness was estimated by posterior probabilities in MrBayes. Convergence was determined when the standard deviation of split frequencies went below 0.05 and the PSRF (Potential Scale Reduction Factor) approached 1, and both runs had properly converged to a stationary distribution after the burn-in stage (which was 1000 sampled generations). The Interactive Tree Of Life (https://itol.embl.de) was applied for the display, manipulation, and annotation of phylogenetic trees (Letunic & Bork, 2021).

Time of divergence

The multi-locus dataset with 183 taxa (Table S4) was used to estimate dates of cladogenetic events at the family level as well as lower taxonomic groupings (e.g., subfamilies, tribes, and generic level). Times of divergence were estimated using a Bayesian lognormal relaxed clock with uncorrelated rates to each clock model as implemented in BEAST 2.6.3.0 (Bouckaert et al., 2019). The dataset was partitioned by genes and the best-fit model of evolution of sequences, according to BIC, was found using ModelFinder (Kalyaanamoorthy et al., 2017) in IQ-TREE (Nguyen et al., 2014; Trifinopoulos et al., 2016). As a result, we unlinked the partitions for the substitution models, allowing partitions to independently evolve under different substitution models (see Table S4). However, we linked the partitions for the clock and tree models (the list of best-fit substitution models per partition can be found in Table S4). The tree prior was set to a Birth-Death Model in one run, and a Yule Model in another run. Ditrysian Lepidoptera are unfortunately characterized by a lack of fossils that can be confidently assigned to extant clades (Grimaldi & Engel, 2005; Wahlberg et al., 2013), and Euteliidae are no exception. Fossils assigned to the Noctuoidea (Sohn et al., 2012) are either ambiguously assigned taxonomically, incomplete, or too recent to use for purposes of calibration (Kristensen, 1998). We used the recent phylogenomic study of Kawahara et al. (2019) to apply secondary calibration points for the estimation of divergence times within Euteliidae. We constrained the root of the superfamily Noctuoidea (69 Ma) with normal distributions encompassing the 95% credibility intervals estimated in Kawahara et al. (2019). We then constrained the roots of the family Erebidae and the subfamily Arctiinae to 47.8 and 30 Ma, respectively, with normal distributions encompassing the 95% credibility intervals (see Dataset S11 Kawahara et al., 2019). The MCMC parameters were fixed to 150 million generations for two separate runs (tree priors set to a. Birth-Death Model and b. Yule Model) with sampling every 5000 generations and the first 25% discarded as burn-in.

Hostplant data acquisition and ancestral state reconstruction

Our review of host use draws data from the Robinson et al. (2001) compendium of Lepidoptera host records for the Oriental tropics to provide a ‘metasample’ with a fixed dateline. Though many of the groups have records from a wide range of plant families, they mostly show a preference for just one or only a few plant families. The overview attempts to establish a ranking for this by summing as units every plant genus record for a moth species across the tribe or subfamily. These were summed for plant families and higher categories within insect genera and higher categories. It is restricted to genera known to occur in Borneo as representative of the fauna of the Sunda Shelf, to allow standardization following ‘Moths of Borneo’ (Holloway, 2011). See Holloway (2017, 2019a, 2019b) for details. For Lepidoptera host records of Nearctic region, we use Caterpillars of Eastern North America (Wagner, 2005).

Ancestral state reconstruction was conducted using RASP (Reconstruct Ancestral State in Phylogenies, version 4.2) (Yu et al., 2015) using the Bayesian Binary Markov Chain Monte Carlo (BBMCMC) analysis (BBM; Ronquist & Huelsenbeck, 2003) for hostplant order association: (A) Sapindales, (B) Fagales, (C) Rosales, (D) Myrtales, (E) Malpighiales, (F) Malvales, (G) Fabales, (H) Laurales, (I) Saxifragales (Table S5). Hostplant information was compiled from the literature (Gardner, 1948; Holloway, 1985; Janzen & Hallwachs, 2016, 2022; Mathur, 1942; Robinson, 1974; Robinson et al., 2010; Sevastopulo, 1941; Staude et al., 2020). Higher-level classification and nomenclature of plants are based on the Angiosperm Phylogeny Group (APG) classification of the orders and families of angiosperms (The Angiosperm Phylogeny Group et al., 2016). BBM analysis was based on 10,001 trees, of which 3000 were discarded (burn-in 30%), sampled from one run of a Bayesian inference calculated by MrBayes 3.2 as outlined above but using a reduced alignment (122 terminal leaves) to include only ingroups with reliable foodplant records (Table S5). A condensed tree was calculated and the outgroups were removed using the tools provided by RASP. The MCMC analysis was set to one million generations and the model of DNA evolution to Estimated + Gamma distribution.

RESULTS

Phylogenetic hypothesis

Based on two model-based phylogenetic approaches (ML and BI) for the combined datasets, our results strongly support the monophyly of Euteliidae (100/1/100/1; numbers in parentheses are SH-aLRT support (%)/aBayes support / ultrafast bootstrap support (%)/Posterior Probability respectively) (Figure 2a, b). SH-Like ≥80 and UFBoot2 ≥ 95 values indicate well-supported clades. Euteliidae consist of two strongly supported lineages corresponding to the subfamilies Euteliinae (100/1/100/1) and Stictopterinae (100/1/100/1) (Figure 2a, b). The optimal topologies from the two analyses are very similar, with slight variation observed mostly in the terminal branches and branch supports. The analysis of the partitioned dataset by mtDNA and nDNA genes, as well as the dataset omitting the mitochondrial COI gene, did not differ substantially in topology and node supports.

Details are in the caption following the image
Phylogenetic hypothesis of Euteliidae and out-groups based on Maximum Likelihood and Bayesian inference analyses. Clades representing outgroups are collapsed and coloured. Support values shown next to the branches are SH-aLRT support (%)/aBayes support/ultrafast bootstrap support (%)/posterior probabilities, respectively. The names of the moths in the figure are associated with the terminal leaves marked with red stars. (a) Out-groups and Stictopterinae; (b) Euteliinae.

Relationships among the four families within the quadrifid Noctuoidea (i.e., Euteliidae, Noctuidae, Erebidae, and Nolidae) are not clear, although they form a strongly supported (100/1/100/1) monophyletic group (Figure 2a, b) with Euteliidae sister to Noctuidae and Nolidae sister to Erebidae in both ML and BI analyses (80/0.997/93/0.99; 59.5/0.95/94/0.99 respectively, Figure 2a, b).

Subfamily Stictopterinae

Stictopterinae are recovered as a strongly-supported monophyletic group including two moderately supported major lineages corresponding to the tribe Stictopterini comprising the genera Stictoptera, Aegilia, Nagara Walker, and Gyrtona Walker (48.7/0.923/83/0.9) and the Odontodini (99.4/1/100/1), which includes [((Odontodes), (Lophoptera/Sigmuncus Holloway/Savoca Walker))] (Figure 2a). Lophoptera huma (Swinhoe) appears as sister to Gyrtona clade.

Subfamily Euteliinae

Our analysis recovered three strongly supported generic groupings, together with a weakly supported lineage (87.1/0.999/73/0.85) represented by the six genera Aplotelia Warren (Type Species = TS) (including Aplotelia diapera (Hampson) see below); Chlumetia Walker (TS); Caedesa Walker, Pataeta Walker (TS), Anuga Guenée (TS), and Targalla Walker, within Euteliinae (Figure 2b). The Eutelia clade (99.4/1/100/1) includes the genera Eutelia Hübner (TS), Targallodes Holland, Marathyssa Walker (TS), and Penicillaria Guenée. The Anigraea clade (96.7/1/97/0.99) comprises the monophyletic genus Anigraea Walker (TS) and the Oriental Marathyssa (i.e., M. harmonica (Hampson) and M. incisa Kobes). And finally, the Paectes clade (100/1/100/1) contains the Nearctic and Old World Paectes Hübner (TS) + Callingura Butler, monophyletic genus Atacira Swinhoe (TS), and Targalla apicifascia (Hampson) (Figure 2b).

Within the Eutelia clade, the Eutelia-group (represented by the TS) is associated with the Afro-Oriental genus Targallodes with weak support (43.6.7/0.9/92/0.7). This clade (Eutelia/Targallodes) is associated with a monophyletic group (95/1/99/1) that contains the Nearctic Marathyssa (represented by the TS) and Eutelia (E. pyrastis Hampson and E. pulcherrimus (Grote)), forming a moderately-supported lineage (90.2/1/99/1) (Figure 2b). Eutelia is polyphyletic, with the Old World type species (E. adulatrix) associated with E. geyeri (Felder and Rogenhofer) (TL: Japan) and E. adulatricoides (Mell) (TL: China), whereas two Nearctic species (E. pyrastis and E. pulcherrimus) are allied with the Nearctic genus Marathyssa, and finally, two exemplars of the Asian species, E. cuneades (Draudt) are associated with the Indo-Australian genus Penicillaria with moderate support (87.1/0.998/97/0.99). E. cuneades was originally placed in the genus Marathyssa but Sugi (2000) transferred it to Eutelia based on its similarity to E. favillatrixoides Poole. Moreover, in our analysis Marathyssa is polyphyletic, with the New World type-species (M. basalis Walker) forming a strongly supported clade with three Nearctic species (M. minus Dyar, E. pyrastis and E. pulcherrimus) (95.1/1/99/1) the other two Oriental species M. harmonica and M. incisa are placed with strong support (96.7/1/91/0.99) as sister to the monophyletic assemblage that includes the type-species of the Indo-Australian Anigraea (100/1/100/1) (Figure 2b).

The Indo-Australian genus Penicillaria is supported as monophyletic (Figure 2b). Our results suggest paraphyly of the Indo-Australian genus Aplotelia (Figure 2b) with A. diapera grouped as sister to monophyletic Afro-Oriental genus Chlumetia (71.8/0.784/88/0.54) represented by the TP (C. transversa Walker), and A. diplographa Hampson placed as sister to A. diapera/Chlumetia (93.7/1/81/0.98) (Figure 2b).

The Indo-Australian genus Targalla appears polyphyletic since T. apicifascia is not associated with the seven other Targalla species that form a monophyletic group (99.3/1/100/1). The latter clade arises as a sister to the type species of the Old World Tropical genus Pataeta Walker with weak supports (80/0.921/58/0), and the former clade (three representatives of T. apicifascia) as sister to Paectes clade with no support (Figure 2b). The Southeast Asian genus Caedesa is paired with the Anuga clade (94.2/1/100/1)—represented by the TS—with weak support (94.1/0.967/62/0) (Figure 2b).

Multi-locus phylogenetic analyses showed a strong relationship between the New World Paectes clade represented by the TS, P. pygmaea Hübner (98.1/1/100/1), and the Old World Paectes (Callingura) (100/1/100/1) with strong support (100/1/100/1). This pair [Nearctic Paectes/Old World Paectes (Callingura)] is sister to Targalla apicifascia with no support (Figure 2b). This triplet is sister to the monophyletic assemblage of nine species of Atacira (represented by the TS) with strong support (100/1/100/1).

Backbone phylogeny and barcode data

Our results based on ML analysis of 435-specimen dataset of Euteliidae and outgroups with nearly 43% of representative species included in the multigene backbone and the remaining 57% included only by mitochondrial COI barcode data, provide strong support (BS = 99) for the monophyly of Euteliidae comprising two strongly supported clades (i.e., subfamilies): Euteliinae (BS = 98) and Stictopterinae (BS = 98) (Figure 3).

Details are in the caption following the image
Phylogenetic hypothesis of Euteliidae and outgroups inferred by Maximum Likelihood analysis. The MLtree contains 425 terminal taxa in total: 183 with multi-locus sequence data and 242 terminals represented only by mitochondrial COI barcode data. Bootstrap values (please see legend) are displayed as grey circles (five various sizes) on the tree branches. The scale bar shows the estimated number of substitutions per site. The colour bars represent gene regions used in the ML analysis for each leaf: red represents COI-barcode and the rest represent COI3P (mtDNA), EF1a, GAPDH, IDH, MDH, RpS5, Wgl400, CAD (nDNA), respectfully. Type species are marked with red stars.

Our analysis places the Neotropical Thyriodes Guenée outside Euteliidae, among the Zale Hübner and Catocala Schrank lineages of Erebidae (subfamily Erebinae) (Figure 3), with strong support (BS = 100). The rest of the Euteliidae exemplars represented only by barcode data fall within the Euteliidae. Within Stictopterinae, there are two well-supported major lineages corresponding to tribes Stictopterini and Odontodini. Stictopterini contains the monophyletic genera Stictoptera, Nagara, Aegilia, and Gyrtona (Figure 3). Gyrtona appears to be sister to the rest of the genera within Stictopterini (Figure 3). The tribe Odontodini comprises monophyletic genera Odontodes and Lophoptera (Figure 3). Sigmuncus forms a monophyletic group as sister to a group of Bornean Lophoptera species within a larger species-group of Lophoptera (Figure 3). Diascoides Holloway, represented only by barcode data from a single species falls between Lophoptera and Odontodes (Figure 3). Finally, representatives of Savoca fall within a clade sister to Bornean Lophoptera univalva Holloway within a larger group of Lophoptera species (Figure 3).

Within the subfamily Euteliinae, Penicillaria is recovered as monophyletic (BS = 100) and sister (BS = 97) to a strongly supported clade (BS = 100) that contains Eutelia cuneades from Thailand and Marathyssa cuneata (Saalmüller) from South Africa (Figure 3). This latter pair is weakly (BS = 80) associated with a clade (BS = 77) consisting of [((Targallodes/Phlegetonia Guenée), (Eutelia TS/Phlegetonia TS)), (Marathyssa TS/Eutelia)] (Figure 3).

Aplotelia (represented by the TS) is recovered as monophyletic and placed weakly supported as sister (BS = 69) to a poorly supported clade (BS = 83) that contains the monophyletic Afro-Oriental genus Chlumetia represented by the TS and a South Asian species (diapera) of Aplotelia (Figure 3). Two exemplars of the Old World tropical genus Mimanuga Warren from PNG and a singleton Bornean Anuga (see below) are well supported within a larger clade (BS = 94) that contains the true Anuga clade (BS = 100) and Phalga Moore (Figure 3). This clade ([Anuga TS/Phalga TS/Mimanuga]) is placed as a sister to Caedesa with moderate support (BS = 87). The Bornean Anuga canescens appears to be more associated with Mimanuga than with the core Anuga clade (Figure 3).

Targalla appears to be polyphyletic. The Indomalayan Targalla apicifascia is weakly supported as sister to Paectes (BS = 67) within a strongly supported clade (BS = 100) that also contains Atacira. Targalla plumbea (Walker) is placed as a sister lineage to Pataeta (represented by the TS), with good support (BS = 96), and a large group of Targalla species is strongly supported (BS = 100) as sister to (Pataeta/Targalla plumbea) (Figure 3).

Old World Paectes form a strongly supported monophyletic group with Callingura Butler (Figure 3). This assemblage (Paectes/Callingura) is weakly supported as sister to Indomalayan Targalla apicifascia (BS = 67). This pairing is sister to the monophyletic genus Atacira (represented by the TS) (BS = 100), with a strong support value (BS = 100) (Figure 3). This triplet is in turn sister to another well-supported clade (BS = 95) comprising (Anigraea [represented by the TS]/Marathyssa incisa/harmonica), but this relationship is poorly supported (BS = 80) (Figure 3).

Time of divergence

Our divergence time analysis suggests a median age of 41.87 Ma (mid-Eocene) for the crown clade of Euteliidae, with 95% highest posterior densities (HPD) of 34.7–49.43 Ma (Figure 4). Euteliidae diverged from its common ancestor with Noctuidae approximately 53.10 Ma (95% HPD: 45.04–61.28 Ma). Our analysis suggests that the two subfamilies of Euteliidae split in the early Oligocene ~31–34 Ma (Figure 4). Within Stictopterinae, beginning with the bifurcation of Stictopterini from Odontodini, there appear to have been several branching events throughout the late Oligocene (Figure 4). Diversification within Euteliinae appears to have been simultaneous with that of the Stictopterinae tribes, that is, ~ 25–28 Ma (Figure 4).

Details are in the caption following the image
Maximum credibility tree with median ages (Ma) from the Bayesian uncorrelated uniform analysis under BEAST for the superfamily Noctuoidea. A five Myr-timescale is placed at the top and bottom of the chronogram and spans the Cretaceous to the Holocene. Black hourglasses at the corresponding nodes indicate the calibration points used to ultrametrize the topology. For the groups of major interest, the name is given above the branch leading to the group. The tree includes 95% credibility intervals for the age estimates of each node.

Reconstruction of ancestral character states (hostplant associations)

The hostplant order Malpighiales is recovered as the most probable ancestral state for the crown of Euteliidae (Figure 5). The ancestral nodes for both the subfamily Stictopterinae (69.49%) and the tribe Stictopterini (96.33%) appear to have been Malpighiales feeders (Figure 5). However, our phylogenetic reconstructions suggest that there was a split between Malvales+Malpighiales specializations (Malvales+Malpighiales [71.99%]/Malvales [25.89%]) in Odontodini and Malpighiales specializations (96.33%) in Stictopterini (Figure 5). For Euteliinae, the inferred ancestral hostplants were in Sapindales (94.63%). Our results suggest that there were multiple shifts at the generic level from Sapindales to new hostplant orders: to Laurales, Malvales, Fagales, Fabales, and Myrtales (Paectes); to Fabales and Fagales (Eutelia, Marathyssa); to Fabales (Pataeta); to Myrtales (Targalla); to Fagales, Fabales, and Myrtales (Anigraea); and to Fabales (Anuga) (Figure 5).

Details are in the caption following the image
Ancestral trait reconstruction for Euteliidae hostplant Orders using RASP 4.2. Stochastic character mapping with 100,000 replicates. Most Likely States (MLS) at each node are displayed in the centre of pie charts. Hostplant Orders are: (a) Sapindales, (b) Fagales, (c) Rosales, (d) Myrtales, (e) Malpighiales, (f) Malvales, (g) Fabales, (h) Laurales, (i) Saxifragales.

DISCUSSION

Systematics and taxonomy

Euteliidae are a well-defined group of quadrifid noctuoids, deserving family status based on the multi-locus phylogenies (Zahiri et al., 2011, 2012; Zahiri, Lafontaine, Holloway, et al., 2013; Zahiri, Lafontaine, Schmidt, et al., 2013) and morphology and biology (Holloway, 1985, 2011; Kitching, 1987; Lafontaine & Schmidt, 2010). The relationship of Euteliidae to the three remaining quadrifid Noctuoidea families has been unclear. In this study, Euteliidae are associated with Noctuidae, and Nolidae are sister to Erebidae in both ML and BI analyses (Figure 2). This is in contrast to the results of Mitchell et al. (2006) where both Euteliinae s.s. + Stictopterinae s.s. grouped as the sister group to Erebidae. However, the sister group relationship between Euteliidae and Noctuidae was also recovered by Zahiri et al. (2011, 2012), in a more recently study based on mitochondrial genomes (Yang et al., 2015), as well as in a new study based on ca. 2600 loci using hybridization capture (Mayer et al., 2021).

The close association of Euteliinae and Stictopterinae had already been examined and suggested by Richards (1933), Holloway (1985), and Kitching (1987). Numerous synapomorphies have been proposed to unite Euteliinae + Stictopterinae, including reduced female frenulum, modified basiconic sensilla on the proboscis, presence of a small oval plate in the ductus ejaculatorius, inner surface of anal papillae directed posteriorly, and the counter-tympanal hood consisting of a unique double structure (Holloway, 1985; Kitching, 1987; Kitching & Rawlins, 1998; Richards, 1933).

Within the Euteliinae there is strong support for the relationships among the genera Eutelia (represented by the TS), Targallodes, Marathyssa (represented by the TS), Phlegetonia (represented by the TS), and Penicillaria (Figures 2, 3). Our analysis confirmed polyphyly of the genus Marathyssa. The two Oriental species M. harmonica and M. incisa from Thailand and Borneo appear more closely related to the Oriental genus Anigraea and these need to be examined morphologically more critically (Figures 2, 3). Our phylogenetic hypothesis also revealed a deep split within the Paectes + Callingura clade (Figure 3), with the New World species (represented by the TS of Paectes) and the Oriental species being sister to each other. Kobes (19942008) revived Callingura as a full genus (the name Callingura is available as a subgenus for the Indo-Australian taxa; Holloway, 1985), distinct from the New World Paectes Hübner. However, Kobes did not revise Callingura but simply preferred to use it for the Oriental taxa, whereas Holloway (1985) recognized the monophyly of Paectes as a whole to retain the New World/Oriental connection. Afterwards, Kononenko and Pinratana (2013) followed Holloway (1985, 2011) and treated Callingura as a synonym of Paectes, for example, ‘Paectes gertae (Kobes, 2008)’. In fact, they go as far as saying ‘NOTE: The species [gerthae], described in Callingura (Kobes, 2008) belongs to the genus Paectes (Holloway, pers. comm.).’ So unless someone reinstated Callingura as a (sub)genus after that, or we ignore the non-explicit synonymy in Moths of Thailand, this is a stat. rev. here. As a result, those Oriental species that are currently treated in the nominate genus Paectes (i.e., P. roseovincta, P. cristatrix) should be included in the subgenus Paectes (Callingura), and those New World species that are currently treated in the genus Paectes (Table S6) should be included in the subgenus Paectes (Paectes). Our divergence time analysis suggests split between the New World species and Oriental species of Paectes occured roughly 19 Ma (Figures 2b, 3, 4).

The Asian genus Targalla is found to be polyphyletic since T. apicifascia is not associated with other Targalla (represented by the TS), as first suggested by Holloway (1985). It clearly requires a new genus, more closely related to the Paectes clade (Paectes [Paectes] and Paectes [Callingura]) (Figures 2b, 3), which we describe below. Eutelia is recovered as polyphyletic, with the Nearctic species and E. cuneades from Thailand falling outside the true Eutelia group (Figures 2b, 3). Two Nearctic species (E. pyrastis and E. pulcherrimus) are grouped within the Nearctic Marathyssa (represented by the TS), and E. cuneades from Thailand is closely associated with Penicillaria (Figures 2b, 3). By expanding taxon sampling of the New World Eutelia (from Costa Rica, Bolivia, USA, and French Guiana) in our COI + multi-locus phylogeny (Figure 3), we found that they were all nested within the Nearctic Marathyssa, corroborating the results of the multi-locus phylogeny. As a result, the New World species of Eutelia (e.g., E. pyrastis and E. pulcherrimus) are transferred to Marathyssa (comb nov.) (Table S6). Eutelia cuneades + Marathyssa cuneata (Figure 3) together form the sister-group of Penicillaria and require further morphological study (Table S6). Phlegetonia violescens Hampson appears to be closely related to the Targallodes species group (Figures 3), and the new combination Targallodes violescens comb nov. is implemented here (Table S6). Furthermore, a detailed investigation of the original description and barcode analysis of the African species, Eutelia megacycla Berio, revealed that this taxon should be synonymized with Targallodes violescens. The TS of the African genus Phlegetonia (catephioides Guenée) is grouped within the true Eutelia clade (Figure 3). Thus, Phlegetonia should be synonymized with Eutelia as suggested by Holloway (1985), although the name has been used in many publications and online databases, such as Afromoths (de Prins & de Prins, 2011). Holloway (1985) concluded that the male and female genitalia of catephioides are of the same general form as those of the type species of Eutelia, the Mediterranean E. adulatrix. Therefore, Phlegetonia is once again here placed as a junior subjective synonym of Eutelia (Table S6). Our time of divergence analysis reveals that the initial split between the Old World Eutelia + the Afro-Oriental Targallodes and the Nearctic Marathyssa began in the late Oligocene (~ 25 Ma), resulting in the trans-Atlantic split into two distinct lineages (Eutelia + Targallodes and Marathyssa) (Figure 4). Following this, the Eutelia + Targallodes lineage diverged between the Old World lineage (Eutelia) and the Afro-Oriental lineage (Targallodes) (~ 22 Ma).

Mimanuga + Anuga canescens (Walker) are together recovered as the sister to the Anuga clade + Phalga. Poole (1989) placed Mimanuga as a synonym of Anuga but our results support the monophyly of Anuga (excluding Anuga canescens) and a close relationship between Mimanuga and Anuga canescens (Figure 3). As a result, we reinstate Mimanuga from synonymy and transfer Anuga canescens into Mimanuga as Mimanuga canescens comb. nov.

Our coverage of New World taxa included all five genera previously assigned to the family in this geographic realm (Poole, 1989). Neotropical Euteliidae are comparatively few, the majority comprising a moderately large diversification of Paectes with about 30 described and at least as many undescribed species. The Neotropical genus Thyriodes has been included in Euteliidae (Poole, 1989), but examination of the larval morphology and hostplant (Janzen pers. comm.), in addition to adult morphology, suggested that this genus belongs to the Erebinae. Our results corroborate a close relationship of Thyriodes with members of the subfamily Erebinae within Erebidae (Figure 3), and we accordingly transfer Thyriodes to Erebidae: Erebinae. Tribal placement within Erebinae will require greater coverage of taxa and gene sampling. Stictopterinae are very poorly represented in the Neotropics, Nagara being the only genus confirmed there. Thus, only three unrelated and relatively small lineages of Euteliidae occur in the New World: Nagara (Stictopterinae: Stictopterini), Marathyssa (= Eutelia) (Euteliinae), and Paectes (Paectes) (Euteliinae).

Based on our phylogenetic hypothesis, minimally three faunal interchanges occurred between the New and Old World. In Stictoperinae, New World Nagara (N. vitrea) is sister to Southeast Asian Stictoptera, and Marathyssa (as redefined here) is sister to Old World Eutelia + Targallodes (Euteliinae). Similar divergence time estimates of 25–26 Ma could be indicative of colonization into the New World roughly during the late Oligocene. The third New World lineage comprises the western hemisphere Paectes (subgenus Paectes), sister to Paectes subgenus Callingura, with a slightly younger divergence time estimate of about 19 Ma (early Miocene).

Aplotelia diapera is placed between the remainder of Aplotelia and Chlumetia (Figure 3). Although we would note that it is also treated as Eutelia diapera in numerous resources (Poole, 1989; https://ftp.funet.fi/pub/sci/bio/life/insecta/lepidoptera/ditrysia/noctuoidea/euteliidae/), our results suggest the species requires morphological study and potentially a new genus.

The two tribes of Stictopterinae identified in the previous studies (Holloway, 2011) were recovered here as monophyletic groups with good support (Figure 2). Odontodes, Lophoptera (both represented by TS), Sigmuncus, Savoca and a singleton Diascoides with only COI data are the main genera of the tribe Odontodini (Figure 3). Lophoptera is found to be polyphyletic since the Southeast Asian species Lophoptera huma is not associated with other Lophoptera (represented by the TS) and needs to be included in a new genus that is more likely associated with the Gyrtona clade (Figures 2b, 3). Below, we describe a new genus to accommodate it, as it is evidently distinct from Lophoptera species-group.

Holloway (1985) found it difficult to establish clear morphological differences between Odontodes and Lophoptera, but based on morphological features of male and female genitalia, he established a system that recognized a series of groupings. However, many of these were monobasic or with just two species. Our analysis supports the distinction of the two genera and also supports two of Holloway's larger groups within Lophoptera. His groups B1 and B6 fall into our clade from L. stipata (Walker) to L. nama (Swinhoe) (Figure 3) that contains the type-species of the synonym genus Evia Walker, E. ferrinalis Walker. His group D1 is recovered as our clade from L. melanesigera Holloway to L. squammlinea Holloway, and includes L. squammigera Guenée, the type-species of Lophoptera (Figure 3). In contrast, we found (Figure 3) that the genus Sigmuncus falls into a clade from L. brunnistis Holloway to L. arcuata (Hampson), the latter being the second species included in Sigmuncus by Holloway (1985) besides the here unsampled type species, S. albigrisea (Warren). Most of these species have a modification like a twist or scroll to the apex of a slender uncus, which can be treated as a synapomorphy for the whole clade that unites species from groups A1 and D5, and thus Sigmuncus is better treated as a synonym: Lophoptera = Sigmuncus syn. nov.

Like Sigmuncus, the sampled members of the genus Savoca are nested within Lophoptera based on both nDNA and barcode data (Figure 3). This is a group of small species that were distributed among the genera Lophoptera and Gyrtona in previous classifications (Holloway, 1985). The species are relatively small, with rectangular forewings patterned usually with a distinctive basal zone and a postmedial that is fine, double, biarcuate, roughly perpendicular to the dorsum. The hindwings often grade paler based but are not hyaline. Hence Savoca is here treated as a synonym: Lophoptera = Savoca syn. nov.

The Stictopterini includes the genera Stictoptera (represented by the TS), Aegilia (represented by the TS), Gyrtona, the new genus described below for Lophoptera huma, and the Neotropical genus Nagara (represented by the TS).

Niklastelia description

Niklastelia Zahiri & Holloway gen. Nov.

Type species: Eutelia apicifascia Hampson, 1894 (Figure 6a–f), by present designation.

Details are in the caption following the image
Photos of the new genera Niklastelia and Pellinentelia: (a) adult male of Niklastelia apicifascia (coll. RMNH) (photo by Rob de Vos), Indonesia, Papua Kab, Yahukimo, WALMAK (distr. Nipsan), 4° 07′ S–138° 36′ E//1710 m. at light, 20-25.ix.2011, leg. F. Groenen//RMNH.INS.1557720; (b) adult female of Niklastelia apicifascia (coll. RMNH) (photo by Rob de Vos), Fort de Kock (Sumatra), 920 m., November 1921, leg. E. Jacobson//RMNH.INS.1557723; (c) male genitalia of Niklastelia apicifascia (RMNH.INS.1557722) (dissection and photo by Rob de Vos); (d) eighth abdominal segment of male of Niklastelia apicifascia with coremata (RMNH.INS.1557722) (dissection and photo by Rob de Vos); (e) female genitalia of Niklastelia apicifascia (RMNH.INS.1557721) (dissection and photo by Rob de Vos); (f) bursa copulatrix of female genitalia of Niklastelia apicifascia with a pair of scobinate signa (RMNH.INS.1557723) (dissection and photo by Rob de Vos); (g) Pellinentelia huma from Thailand (photo by M. Pellinen); (h) male genitalia of Pellinentelia huma from Thailand (dissection and photo by M. Pellinen).

LSID: urn:lsid:zoobank.org:act:22F2BCA5-92F7-439C-83FB-968,810,657,353.

The type species has been placed variously in Eutelia, Phlegetonia, and Targalla, but was indicated to be somewhat atypical for all of these by Holloway (1985). The male antennae are weakly bipectinate basally (filiform in typical Targalla). The male genitalia are distinctive with valves reduced, slender, strongly upcurved at the apex (Figure 6c). The genus lacks the marked flexing of the tegumen of the male seen in typical Targalla. The eighth abdominal segment bears coremata as in other Targalla (Figure 6d). In the female, the bursa copulatrix has a pair of scobinate signa rather than several patches of some weak scobination basally (Figure 6e, f).

Our analysis places the genus in a position well separated from typical Targalla or its subgenus Euteliella Roepke, but associates it instead with Paectes and Atacira, further support for its generic status.

The genus consists of the type species, Niklastelia apicifascia comb. nov., which occurs throughout the Indo-Australian tropics as far east as the Solomon Islands, and Niklastelia barbara (Robinson) comb. nov. from Fiji and Samoa.

Etymology: the genus is named for Niklas Wahlberg in recognition of his work on the phylogeny of the Noctuoidea.

Pellinentelia description

Pellinentelia Holloway & Zahiri gen.nov.

Type species: Stictoptera huma Swinhoe, 1903 (Figure 6g, h), by monotypy.

LSID: urn:lsid:zoobank.org:act:A2CC2497-A688-4D7D-88F2-A7E96E1951AA.

The type species, Stictoptera huma, was originally placed in Stictoptera by Swinhoe (1903) and then transferred to Lophoptera by Hampson (Hampson, 1912). Holloway (1985) placed it in his ‘D group’ of Lophoptera, which was characterized by a synapomorphy of the female genitalia: the presence of both the post-ostial invagination and lateral lobes. It was placed as the sole species in subgroup ‘D2’. The post-ostial invagination is short, triangular, and the lateral lobes are small semicircular flaps. The male genitalia have a basally swollen uncus, a rod-like costal process almost as long as the valve, and a small, centrally placed harpe (Figure 6h). These last two features only came into focus when our analysis placed the species well within the Stictopterini and not in the Odontodini, as they represent synapomorphies that are masked by the enlargement of the sacculus.

Pellinentelia huma comb nov., the only included species, is distinguished from the smaller Lophoptera and Gyrtona by its robustness, the marked basal hyaline area of the hindwing, and the presence of two black patches on the costal margin of the forewing (Figure 6g). In the male genitalia, the sacculus bears an oval bulge, with a process on the apex.

As indicated earlier, our analyses placed the genus in a position well separated from typical Lophoptera, but in a sister relationship with Gyrtona, further support for its generic status.

The genus occurs throughout Thailand, Sumatra, Borneo, Sulawesi, Seram, and New Guinea (Holloway, 1985), and China (Hainan, Guangxi) (Qi et al., 2011).

Etymology: The genus is named for Markku Pellinen in recognition of his work on the Moths of Thailand.

Hostplant associations and divergence time of major lineages of Euteliidae

The vast majority of studies on the evolution of hostplant use in Lepidoptera have focussed on butterflies (e.g., Janz et al., 2006), and our understanding of the evolution of hostplant associations in other groups of Lepidoptera is not as well developed. Noctuoids can be highly polyphagous (e.g., Wang et al., 2017), but Euteliidae show specialization at the host plant family level. We found that the ancestral hostplant for Euteliidae was likely to be in Malpighiales and/or Sapindales. There appears to be a clear split into Sapindales feeders in the ancestor of the subfamily Euteliinae, and Malpighiales feeders in the ancestor of Stictopterinae.

In the subfamily Euteliinae, the plant family Anacardiaceae (order Sapindales) provides the majority of the larval hostplants (Figure 5). There have been multiple colonizations of other plant families at the species and genus levels, general patterns that have been observed in butterflies (Janz et al., 2006), and suggesting that the evolution of hostplant use is linked to diversification of Euteliinae moths. A common feature of the hostplants is that they tend to be lactiferous, suggesting constraints on what kinds of hostplants can be utilized by euteliine (and indeed more generally euteliid) species.

Our ancestral trait reconstruction identified the plant order Malpighiales (e.g., Clusiaceae and Euphorbiaceae) as the ancestral hostplant for the subfamily Stictopterinae and the tribe Stictopterini. The sister lineage (Odontodini) appears to have switched from Malpighiales to Malvales (e.g., Dipterocarpaceae) once they became available as a resource. Our divergence time analysis also suggests that the diversification of major lineages of Stictopterinae began in the Middle Miocene (12–14 Ma). These estimates are similar to those recovered in divergence time estimates for the age of Dipterocarpaceae (Cvetković et al., 2022), which suggested that species diversification began in the Late Oligocene–Early Miocene (21–27 Ma).

Dipterocarpaceae are a highly diverse family in Southeast Asia that are a significant component of the plant foliage biomass yet have a low load of defoliators (Holloway, 1989). For example, in Bornean forests, dipterocarps are represented in most moist lowland forest types, with ten genera and at least 267 species, and usually about three-quarters of large trees in Bornean lowland forest are dipterocarps (Whitmore, 1984). This dominance is thought to have developed from the Middle Miocene (12–14 Ma) in response to climatic shifts (Cvetković et al., 2022). Dipterocarps, unlike the majority of flowering plants, are resinous like gymnosperms. In mixed temperate forests, the diversity of gymnosperm feeding Macroheterocera tends to be much lower than that of angiosperm feeders (Holloway & Hebert, 1979). In temperate forests, only highly polyphagous species such as in the erebid subfamily Lymantriinae and the geometrid subfamily Ennominae appear able to span this discontinuity and feed on both angiosperms and gymnosperms (Figure 7). It is therefore perhaps not surprising that very few Lepidoptera made the switch to dipterocarps and are now specialists on the family. The high species richness of Odontodini in these habitats might thus be explained by their specialization on dipterocarp hostplants.

Details are in the caption following the image
Lepidopteran lineages feeding on the Dipterocarpaceae, the dominant family in most moist lowland forest types of the Oriental tropics.

In Euteliidae, dipterocarp feeding predominates in Odontodini with eight records, followed by four for Euphorbiaceae. The sister-tribe, Stictopterini, has one record, possibly an error through past confusion of generic concepts, as most records (12) are from the Clusiaceae. Euteliinae have four records, though this subfamily feeds predominantly on Anacardiaceae (32 records) with a subgroup of Targalla and the genus Pataeta on Myrtaceae. Thus, no clear instance in the Macroheterocera of exclusive specialization at a generic level has been discovered, and genera with a high incidence of dipterocarp feeding are few and far between, but three such genera are among the more species-rich in the region: Arhopala in Lycaenidae; the related genera Lophoptera and Odontodes (tribe Odontodini of the Stictopterinae) in Euteliidae; and Arctornis in Lymantriinae. Two other genera in Geometridae, Ornithospila Warren in Geometrinae and Ectropidia Warren in Ennominae, each have a unique record from Dipterocarpaceae. This is not significant in itself but species of both genera have been found to decline in numbers or be absent in samples from forests where dipterocarps had been logged out compared with undisturbed forests of the same type (Intachat et al., 1999), and five species of Ornithospila were almost exclusive to a sample from an indigenous plantation consisting mainly of dipterocarps compared with those from three other areas that had undergone various intensities of logging (Intachat et al., 1997). These observations were made in Peninsular Malaysia. Thus, the three genera most successful at exploiting the dipterocarps seem to have achieved this by slightly different evolutionary routes. Though none of the genera is exclusively specialist on dipterocarps, all three are species-rich in SE Asia, particularly Borneo, where current lists have 48 species for Lophoptera, 77 for Arctornis and 89 for Arhopala (Seki et al., 1991).

With a few notable exceptions, hostplant families of the three New World Euteliidae clades are consistent with that of their nearest Old World relatives: Anacardiaceae and Burseraceae (both Sapindales) predominate in subgenus Paectes and Marathyssa, and like other Stictopterini, Nagara specializes on either Clusiaceae or Calophyllaceae (both Malpighiales). Marathyssa exclusively feeds on Rhus / Toxicodendron (Anacardiaceae). No New World representatives of the dipterocarp-feeding Odontodini are known, and only one (recently discovered) species of dipterocarp is native to the Neotropics (Londoño et al., 1995). It is likely that New World colonization by Stictopterini (~26 Ma, based on the NagaraStictoptera split) preceded diversification of dipterocarp-feeding by Odontodini, if the latter occurred primarily in the mid to late Miocene as suggested above. Within subgenus Paectes, degree of specialization varies somewhat, but a number of species are oligophagous on members of Anacardiaceae plus Burseraceae. These two plant families are closely allied and share many biochemical and structural similarities (Pell et al., 2010), including the production of terpene-based resin. Some Paectes include non-native plants from these two families in their diet (e.g., Paectes nana; Pogue, 2013), a prime example of plasticity in hostplant use. Two Paectes that appear as sister species in our analysis feed exclusively (so far as known) on non-Sapindales: P. devincta on Myrtaceae (Myrtales) and P. nubifera on Fagaceae (Fagales).

CONCLUSIONS

Despite the rather weak support for deep internal nodes and short branches that are not well supported, we consider our phylogenetic hypothesis firm enough to inform a stable classification for Euteliidae. As we found previously (Zahiri et al., 2011), the results of the current study continue strongly to support the monophyly of four quadrifid noctuoid families. For Euteliidae, we have been able to resolve the relationships of major lineages within the family and we have elucidated the phylogenetic positions of many previously unplaced taxa. Furthermore, as previously demonstrated in the subtribe Polyommatina (Lepidoptera: Lycaenidae) (Talavera et al., 2022), DNA barcodes combined with multigene backbone DNA data can be used successfully to generate reliable phylogenetic hypotheses and significantly improve higher-level systematics in large datasets.

The diversification of phytophagous insects is likely associated with their tendency to specialize on specific hostplants. This specialization may induce host shifts with numerous expansions and reductions of the hostplant range (Janz et al., 2006) that eventually promote the evolution of new specialist species. This study reveals that conservatism in utilizing lactiferous hostplant families is prevalent in the moth family Euteliidae. Lophoptera and Odontodes are the main genera of the tribe Odontodini with strong larval feeding preferences for species of Dipterocarpaceae. The Stictopterini appears to be restricted to Clusiaceae, apart from two records from Dipterocarpaceae. In the other subfamily, Euteliinae, Anacardiaceae are predominant as larval hosts. Thus, all hosts of Euteliidae are lactiferous, perhaps causing specialization of hostplant use. All these plant families have their highest diversity in the Oriental tropics, hence the occurrence of over 30% of known Euteliidae in Borneo is not surprising.

AUTHOR CONTRIBUTIONS

Reza Zahiri: Conceptualization; investigation; funding acquisition; writing – original draft; methodology; validation; visualization; writing – review and editing; software; formal analysis; project administration; data curation; supervision; resources. Jeremy D. Holloway: Investigation; validation; visualization; writing – review and editing; supervision; conceptualization; resources. Jadranka Rota: Writing – review and editing; methodology; data curation; conceptualization. B. Christian Schmidt: Conceptualization; investigation; funding acquisition; writing – review and editing; validation; resources. Markku J. Pellinen: Validation; resources; visualization. Ian J. Kitching: Resources; writing – review and editing; validation. Scott E. Miller: Resources; writing – review and editing; data curation; project administration. Niklas Wahlberg: Resources; supervision; data curation; methodology; validation; writing – review and editing; conceptualization; funding acquisition.

ACKNOWLEDGMENTS

This work was supported financially by the Academy of Finland and the Kone Foundation awarded to N. Wahlberg; CIMO + Finnish Cultural Foundation + Alfred Kordelin Foundation awarded to R. Zahiri; CeNak, University of Hamburg, Germany (supported by Dr. Martin Husemann) to R. Zahiri; Canadian National Collection of Insects, CNC (provided by Chris Schmidt) to R. Zahiri; Canadian Food Inspection Agency, CFIA to R. Zahiri. The main sources of samples, other than those collected by the authors (MJP, BCS, IJK), are the LepTree project, headed by Charles Mitter et al. (US NSF award #0531769); the Natural History Museum, London, UK; Daniel H. Janzen (US NSF #DEB0072730 and DEB0515699); Roger C. Kendrick (Kadoorie Farm and Botanic Garden, Hong Kong); Pasi Sihvonen (Helsinki, Finland); Henry Barlow (International Trust for Zoological Nomenclature, UK & Malaysia). The authors also acknowledge Rob de Vos (Naturalis Biodiversity Center, The Netherlands) for the specimen dissection and photography of Niklastelia apicifascia. The Papua New Guinea specimens come from a rearing campaign by the Binatang Research Centre led by Vojtech Novotny, George Weiblen, Yves Basset, and Scott Miller, and supported by the US National Science Foundation (grant DEB-0211591 and others), Czech Science Foundation grant 206/09/0115 and others, and Czech Ministry of Education & European Union grant CZ.1.-07/2.3.00/20.0064. DNA barcodes were largely provided by Paul Hebert through a grant from Genome Canada to the iBOL project. DNA barcodes were largely provided by Paul Hebert through a grant from Genome Canada to the iBOL project. All Costa Rican specimens in iBOL's BOLD public database were collected, exported and DNA barcoded under Costa Rican government permits issued to BioAlfa (Janzen, Hallwachs 2019) (R-054-2022-OT-CONAGEBIO; R-019-2019-CONAGEBIO; National Published Decree #41767), JICA-SAPI #0328497 (2014) and DHJ and WH (ACG-PI-036-2013; R-SINAC-ACG-PI-061-2021; Resolución N 001-2004 SINAC; PI-028-2021).

    FUNDING INFORMATION

    RZ: CIMO + Finnish Cultural Foundation + Alfred Kordelin Foundation + Canadian Food Inspection Agency + Canadian National Collection of Insects + CeNak, University of Hamburg + Academy of Finland + Kone Foundation.

    CONFLICT OF INTEREST STATEMENT

    The authors declare that they have no competing interests.

    ZOOBANK REGISTRATION

    1. ZooBank publication URL:http://zoobank.org/urn:lsid:zoobank.org.pub: C0ABC829-938D-4409-B544-BB90F69D55EA
    2. ZooBank nomenclatural act registration code:

      Niklastelia: http://zoobank.org/urn:lsid:zoobank.org:act: 22F2BCA5-92F7-439C-83FB-968,810,657,353.

      Pellinentelia: http://zoobank.org/urn:lsid:zoobank.org:act: A2CC2497-A688-4D7D-88F2-A7E96E1951AA.

    DATA AVAILABILITY STATEMENT

    All data generated or analysed during this study are accessible in GenBank through accession numbers provided in Tables S1–S3.