Comprehensive molecular sampling yields a robust phylogeny for geometrid moths (Lepidoptera: Geometridae)

Background

The moth family Geometridae (inchworms or loopers), with approximately 23 000 described species, is the second most diverse family of the Lepidoptera. Apart from a few recent attempts based on morphology and molecular studies, the phylogeny of these moths has remained largely uninvestigated.

Methodology/Principal Findings

We performed a rigorous and extensive molecular analysis of eight genes to examine the geometrid affinities in a global context, including a search for its potential sister-taxa. Our maximum likelihood analyses included 164 taxa distributed worldwide, of which 150 belong to the Geometridae. The selected taxa represent all previously recognized subfamilies and nearly 90% of recognized tribes, and originate from all over world. We found the Geometridae to be monophyletic with the Sematuridae+Epicopeiidae clade potentially being its sister-taxon. We found all previously recognized subfamilies to be monophyletic, with a few taxa misplaced, except the Oenochrominae+Desmobathrinae complex that is a polyphyletic assemblage of taxa and the Orthostixinae, which was positioned within the Ennominae. The Sterrhinae and Larentiinae were found to be sister to the remaining taxa, followed by Archiearinae, the polyphyletic assemblage of Oenochrominae+Desmobathrinae moths, Geometrinae and Ennominae.

Conclusions/Significance

Our study provides the first comprehensive phylogeny of the Geometridae in a global context. Our results generally agree with the other, more restricted studies, suggesting that the general phylogenetic patterns of the Geometridae are now well-established. Generally the subfamilies, many tribes, and assemblages of tribes were well supported but their interrelationships were often weakly supported by our data. The Eumeleini were particularly difficult to place in the current system, and several tribes were found to be para- or polyphyletic.     

Comments on the classification and phylogeny of broad-winged moths (Lepidoptera, Oecophoridae sensu lato)

The broad-winged moths (Oecophoridae sensu lato) belong to the family complex Gelechiiformes with 4 (Kuznetzov and Stekolnikov, 2001) or 6 (Sinev, 1992) superfamilies. The classification of these moths was rather constant in the XX century, but at the turn of the century most researchers concluded that broad-winged moths in the traditional sense (Oecophoridae sensu lato) were a polyphyletic group and that a major revision of their classification was necessary. Many classifications of these families have been proposed recently (Common, 1990; Minet, 1990; Scoble, 1992; Sinev, 1992; Leraut, [1993], 1997; Heppner, 1998; Hodges, 1999; Kuznetzov and Stekolnikov, 2001; Lvovsky, 2002; Kaila, 2004; Bucheli and Wenzel, 2005). This communication presents one more classification variant, based on analysis of the results of the preceding researchers and personal views of the author.     

Molecular phylogeny of Eois (Lepidoptera,Geometridae): evolution of wing patterns and host plant use in a species‐rich group of Neotropical moths

Strutzenberger, P., Brehm, G., Bodner, F. & Fiedler K. (2010). Molecular phylogeny of Eois (Lepidoptera, Geometridae): evolution of wing patterns and host plant use in a species‐rich group of Neotropical moths. —Zoologica Scripta, 39, 603–620. Eois is a pantropical genus of Geometridae moths with currently 250 valid described species, the majority of which occur in the Neotropics. Eois is a prominent component of Andean moth communities locally accounting for up to ～10% of geometrid individuals. We address the evolution of wing patterns and host plant use in Neotropical Eois and provide a preliminary assessment on the monophyly and biogeographic history of the entire genus as well as affinities within the subfamily Larentiinae. We applied Bayesian, maximum likelihood and maximum parsimony methods of phylogenetic reconstruction to a 142 taxon dataset of partial COI (1220 bp) and Ef1α (1066 bp) sequences resulting in the largest taxon set of geometrid moths analyzed in a molecular phylogenetic study so far. Monophyly of Eois was always strongly supported. Ten monophyletic clades were found with good support, seven of which have characteristic wing pattern phenotypes. Only one wing pattern type occurs in two clades. Trophic associations with representatives of the family Piperaceae occur in all 8 (of 9) Neotropical clades for which host information is available. Apart from feeding on Piper, at least two Eois species in Ecuador feed on Peperomia, and one on Manekia (all Piperaceae); two further species live on Hedyosmum (Chloranthaceae). Species feeding on Peperomia, Manekia and Hedyosmum are usually nested in Piper‐associated clades. Single records of associations with Gesneriaceae and Monimiaceae are scattered in otherwise Piperaceae‐associated clades. These patterns suggest multiple parallel host shifts away from Piper as ancestral food plant. Old World Eois were recovered as monophylum and sister to Neotropical Eois. Within the subfamily Larentiinae the genus Eois has previously been placed close to the tribe Eupitheciini, but this was not supported in our phylogenetic analyses.     

Bat-deafness in day-flying moths (Lepidoptera, Notodontidae, Dioptinae)

Assuming that bat-detection is the primary function of moth ears, the ears of moths that are no longer exposed to bats should be deaf to echolocation call frequencies. To test this, we compared the auditory threshold curves of 7 species of Venezuelan day-flying moths (Notodontidae: Dioptinae) to those of 12 sympatric species of nocturnal moths (Notodontidae: Dudusinae, Noctuidae and Arctiidae). Whereas 2 dioptines (Josia turgida, Zunacetha annulata) revealed normal ears, 2 (J. radians, J. gopala) had reduced hearing at bat-specific frequencies (20–80 kHz) and the remaining 3 (Thirmida discinota, Polypoetes circumfumata and Xenorma cytheris) revealed pronounced to complete levels of high-frequency deafness. Although the bat-deaf ears of dioptines could function in other purposes (e.g., social communication), the poor sensitivities of these species even at their best frequencies suggest that these moths represent a state of advanced auditory degeneration brought about by their diurnal life history. The phylogeny of the Notodontidae further suggests that this deafness is a derived (apomorphic) condition and not a retention of a primitive (pleisiomorphic), insensitive state. Accepted: 1 May 1997     

Exploring phenotypic plasticity and biogeography in emerald moths: A phylogeny of the genus Nemoria (Lepidoptera: Geometridae)

The moth genus Nemoria (Lepidoptera: Geometridae) includes 134 described species whose larvae and adults display a considerable range of phenotypic plasticity in coloration and morphology. We reconstructed the phylogeny of 54 species of Nemoria and seven outgroups using characters from the mitochondrial genes, Cytochrome Oxidase I and II (COI and COII), and the nuclear gene, Elongation Factor-alpha (EF-1alpha). Maximum parsimony, maximum likelihood and Bayesian inference were used to infer the phylogeny. The 54 ingroup species represented 13 of the 15 recognized species groups of Nemoria [Ferguson, D.C., 1985. Fasc. 18.1, Geometroidea: Geometridae (in part). In: Dominick, R.B. (Ed.), The Moths of America North of Mexico, Fasc. 18.1. Wedge Entomological Research Foundation, Washington; Pitkin, L.M., 1993. Neotropical emerald moths of the genera Nemoria, Lissochlora and Chavarriella, with particular reference to the species of Costa Rica (Lepidoptera: Geometridae, Geometrinae). Bull. Br. Mus. Nat. Hist. 62, 39-159], and the seven outgroups came from four tribes of Geometrinae. These data support Nemoria as a monophyletic group and largely recover the species groupings proposed in previous taxonomic analyses using morphological characters. Phenotypic plasticity of larvae is not correlated with plasticity of adults among those species of Nemoria where life histories are known, and appears to be evolutionarily labile for both life history stages: Species exhibiting larval phenotypic plasticity, such as N. arizonaria and N. outina, are placed in several distinct clades, suggesting that this trait has evolved multiple times, and species displaying adult phenotypic plasticity are likewise distributed throughout the phylogeny. A comparative analysis of the biogeographic history of Nemoria supports a South American origin for the genus with multiple introductions into North America, and an application of published substitution rates to the phylogram provides an age estimate of 7.5 million years.     

Pyralid moths (Lepidoptera,Pyraloidea) of Buryatia: Family Pyraustidae

A faunistic survey of 67 species of the family Pyraustidae from Buryatia is presented. Twenty species new to the territory investigated, and one species is new to the Asian part of Russia. For each species, data on the collection localities, general distribution, habitats, and host plants are reported.     

Immunolocalization of odorant-binding proteins in noctuid moths (Insecta, Lepidoptera)

Odorant-binding proteins were studied in the noctuid moths Agrotis segetum, Autographa gamma, Helicoverpa armigera, Heliothis virescens and Spodoptera littoralis using antisera raised against the pheromone-binding protein (PBP) and general odorant-binding protein 2 (GOBP2) of Antheraea polyphemus (Saturniidae). Proteins immunoreacting with these antisera were only found on the antennae and PBP and GOBP2 could be identified on western blots of males and females of all five species. PBPs were predominantly localized in sensilla trichodea and GOBP2 in sensilla basiconica, in good correlation with the stimulus specificity of the receptor cells in these sensilla. In H. armigera and H. virescens the majority of the s. trichodea immunoreacted with the antiserum against PBP of A. polyphemus; in A. segetum, A. gamma and S. littoralis, on the other hand, a high percentage of s. trichodea remained unlabelled. Probably, the PBP expressed in these sensilla is so different that it does not immunoreact with the antiserum used. Such a protein was found by native PAGE of antennal extracts of A. segetum and S. littoralis. These data correlate with the fact that the two heliothine species use pheromones with the same alkyl chain length as A. polyphemus, while the other three species use pheromones with shorter chains. In H. armigera, H. virescens, A. gamma and S. littoralis female antennae were also immunolabelled and a large number of PBP-expressing s. trichodea was consistently found. In S.littoralis this fits with the electrophysiologically recorded high pheromone sensitivity of female s. trichodea, whereas in females of H. armigera and H. virescens no or only weak responses to pheromone stimulation have been reported. Therefore, PBP expression in a sensillum does not necessarily imply pheromone sensitivity of its receptor cells.     

Foreleg stridulation in male Urania moths (Lepidoptera: Uraniidae)

Males of the uraniid moth genus Urania possess a stridulatory organ on the prothoracic leg. This organ represents an autapomorphy for the genus. The sound-producing mechanism consists of a peg formed of specialized scales on the coxa which produces a train of high pitched clicks when scraped against scales on the proximal end of the femur. The proximal end of the femur is enlarged compared with that of the females and would serve to amplify the sound pulse. Stridulation occurs during a series of rapid forward jerks of the forelegs. The sound produced by Urania consists of a low amplitude pulse audible to humans at short range but with a strong ultrasound component. It has not yet been observed in the wild and its function in these moths is unknown, but it may be used during intrasexual or perhaps intersexual communication. This organ is unlikely to have been evolved originally as a defence against nocturnal predators since the genus is a member of an exclusively diurnal clade and females lack the organ. Stridulation occurs in conjunction with fanning-out of the foreleg femoral hair pencil and this invites speculation as to a route for evolution of the organ.     

A multi‐gene phylogeny disentangles the chat‐flycatcher complex (Aves: Muscicapidae)

Zuccon, D. & Ericson, P. G. P. (2010). A multi‐gene phylogeny disentangles the chat‐flycatcher complex (Aves: Muscicapidae).—Zoologica Scripta, 39, 213–224. We reconstructed the first well‐sampled phylogenetic hypothesis in the chat‐flycatcher complex combining nuclear and mitochondrial sequences. The dichotomy between chats‐terrestrial feeders and flycatchers‐aerial feeders does not reflect monophyletic groups. The flycatching behaviour and morphological adaptations to aerial feeding (short tarsi, broad bill, rictal bristles) evolved independently from chat ancestors in three different lineages. The genera Alethe, Brachypteryx, and Myiophonus are nested within the Muscicapidae radiation and their morphological and behavioural similarities with the true thrushes Turdidae are presumably the result of convergence. The postulated close relationships among Erithacus, Luscinia and Tarsiger cannot be confirmed. Erithacus is part of the African forest robin assemblage (Cichladusa, Cossypha, Pogonocichla, Pseudalethe, Sheppardia, Stiphrornis), while Luscinia and Tarsiger belong to a large, mainly Asian radiation. Enicurus belongs to the same Asian clade and it does not deserve the recognition as a distinct subfamily or tribe. We found good support also for an assemblage of chats adapted to arid habitats (Monticola, Oenanthe, Thamnolaea, Myrmecocichla, Pentholaea, Cercomela, Saxicola, Campicoloides, Pinarochroa) and a redstart clade (Phoenicurus, Chaimarrornis and Rhyacornis). Five genera (Muscicapa, Copsychus, Thamnolaea, Luscinia and Ficedula) are polyphyletic and in need of taxonomic revision.     

Phylogenetic utility of the nuclear gene dopa decarboxylase in noctuoid moths (Insecta: Lepidoptera: noctuoidea)

Phylogenetic utility for the nuclear gene encoding dopa decarboxylase (DDC), little used in systematics, was recently demonstrated within the noctuid moth subfamily Heliothinae. Here we extend the test of the utility of a 709-bp DDC fragment to deeper levels, analyzing 49 species representing major groups across the superfamily Noctuoidea. Parsimony, distance, and maximum-likelihood analyses recover all or nearly all of a set of "test clades" supported by clear morphological synapomorphies, spanning a wide range of taxonomic levels. DDC also upholds a recent proposal that the Noctuidae are paraphyletic. Nt3 contributes a majority of the signal and recovers the basal split between Notodontidae and all other noctuoids, despite a plateau of nt3 divergence at this level. However, nonsynonymous changes also support groups at all levels, and in contrast to nt3, amino acid divergence shows no plateau. The utility of DDC promises to extend back to the early Tertiary and Cretaceous, a time span for which few suitable genes have been identified.     

Little-known accessory glands in female Zygaena moths (Lepidoptera, Zygaenidae)

In the female genital system of Zygaena moths, an additional pair of accessory glands is present besides the Y-shaped sebaceous gland. The term 'Petersen's glands' is proposed for these organs. Anatomy, histology, histochemistry and cytology of Petersen's glands of Zygaena trifolii are described. The sac-like glands, situated in the extreme dorsocaudal part of the abdomen, can be divided into a purely secretory part consisting of acini with large pear-shaped gland cells and a reservoir part with combined secretory and storage function. The secretory cells of the acini are penetrated by long curved ductules or secretory end apparatuses having feltwork consisting of very fine filaments. The cytoplasm is characterized by abundance of smooth tubular endoplasmic reticulum (ATER) and the presence of peroxisomes. This cytoplasmic organization is in accordance with the chemical composition of the sticky secretion, which evidently consists completely of lipids. The ultrastructure of the epithelium lining the reservoir of the glands has both traits of secretory and of transporting epithelia. Besides contributing to the secretion, it may be involved in absorption of residual aqueous phase from the contents of the reservoir.     

Acoustic irradiation produced by flying moths (Lepidoptera,Noctuidae)

Characteristics of acoustic waves accompanying the flight of noctuid moths (Noctuidae) were measured. The low-frequency part of the spectrum is formed of a series of up to 17 harmonics of the wingbeat frequency (30–50 Hz) with a general tendency toward the decrease in the spectral density and the increase in the sound frequency. The root-mean-square level of the sound pressure from flapping wings was found to be 70–78 dB SPL. Besides low-frequency components, the flight of moths was accompanied by short ultrasonic pulses, which appeared with every wingbeat. Most of the spectral energy was concentrated within a range of 7–150 kHz with the main peaks at 60–110 kHz. The short-term pulses were divided into two or more subpulses with different spectra. The high-frequency pulses were produced at two phases of the wingbeat cycle: during the pronation of the wings at the highest point and at the beginning of their upward movement from the lowest point. In most of the specimens tested, the peak amplitude of sounds varied from 55 to 65 dB SPL at a distance of 6 cm from the insect body. However, in nine noctuid species, no high-frequency acoustic components were recorded. In these experiments, the acoustic flow from the flying moth within a frequency range of 2 to 20 kHz did not exceed the self-noise level of the microphone amplifier (RMS 18 dB SPL). Probable mechanisms of the high frequency acoustic emission during flight, the effect of these sounds on the auditory sensitivity of moths, and the possibility of their self-revealing to insectivorous bats are discussed. In addition, spectral characteristics of the moth echolocation clicks were more precisely determined within the higher frequency range (>100 kHz).     

The neuroethology of sound production in tiger moths (Lepidoptera,Arctiidae)

When stimulated either acoustically or tactually, certain species of arctiid moths rhythmically emit trains of clicks from metathoracic tymbals. The purpose of the experiments presented here was to determine the location within the central nervous system (CNS) of the proposed tymbal central pattern generator (CPG) in Cycnia tenera. Motor neuron impulses that underlie tymbal activation were recorded extracellularly from the tymbal nerve while moths were subjected to selective severing of the suboesophageal, prothoracic, pterothoracic and abdominal ganglia connectives. Motor output evoked by either acoustic or tactile stimulation originates from a common CPG because tymbal nerve spikes in both cases are similar in amplitude, waveform and rhythmicity. Our results showed: (1) removal of the CNS posterior of the second abdominal neuromere had no effect, (2) removal of the head decreased the responsiveness of the animal to acoustic stimulation and, (3) severing the connectives between the prothoracic and pterothoracic ganglia abolished responses to acoustic stimuli and diminished responses to tactile stimuli. We conclude that although the minimal circuitry sufficient for activating the tymbals resides in the pterothoracic ganglion, the prothoracic and cephalic ganglia are required for the normal, and in particular, auditory-evoked operation of the tymbal CPG.Abbreviations ASR acoustic startle response - CNS central nervous system - CPG central pattern generator - dB peSPL decibel peak equivalent sound pressure level (rms re 20 Pa) - ISI inter-spike interval     

Pyralid moths (Lepidoptera,Pyraloidea) of Buryatia. Family Crambidae

All the known bibliographical and original data on grass moths (Pyraloidea, Crambidae) of Buryatia (Western Transbaikalia) are summarized. Regional fauna is represented by 46 species, including 24 species recorded for the first time, 1 species new for Asian part of Russia, and 1 species new for Russia. The distribution and bionomics of each species are described in brief.     

Carpenter moths (Lepidoptera,Cossidae) of the Altai Mountain Range

An annotated species list of carpenter moths (Lepidoptera, Cossidae) of the Altai Mountain Range is presented. It includes 26 species from 3 subfamilies. Two species are new to science: Semagystia tarbagataica Yakovlev, sp. n. and Dyspessa saissanica Yakovlev, sp. n. The former differs from the other species of the genus (except Semagystia enigma Yakovlev, 2007 from southeastern Turkey whose wing pattern is totally reduced) in the absence of wing pattern; a specific clavate shape of the process on the costal margin of valve is also its important diagnostic character. Dyspessa saissanica Yakovlev, sp. n. belongs to the well-revised Dyspessa salicicola (Eversmann, 1848) species group (Yakovlev, 2005); the closest species is D. salicicola, which also has elongate processes of the pectinate antennae and a weakly developed ridge on the costal marginof valve. The newly described species is different in having a poorly developed dark pattern on the forewings, very broad bases of the processes of the transtilla, a thinner base of the aedeagus, and thinner lateral processes of the juxta. In conclusion, the carpenter moth fauna of the Altai Mountains is briefly analyzed.     

Heteroceran moths (Lepidoptera,Heterocera) of the Don River delta

A list of the Heterocera (Lepidoptera) found in the Don River delta is given. The investigated fauna is several times less species-rich than the faunas of the neighboring territories but includes some species not found in other parts of Rostov Province. These are Epischnia prodromella (Hb.), Euzophera alpherakyella Ragonot, Ancylosis samaritanella (Zeller, 1867), Ancylolomia tentaculella (Hb.), Nymphula nitidulata (Hufn.), Megaspilates mundataria (Stoll), and Chrysodeixis chalcites (Esp.). Population densities of some species, e.g., Loxostege deliblatica Szent-Ivány & Uhrik-Meszáros, 1942, Atychia appendiculata (Esper, 1779), Eublemma minutata (Fabricius, 1794), Oxytripia orbiculosa (Esper, 1799), in the Don Delta are the greatest within Rostov Province. The data obtained emphasize the importance of this natural refuge of the regional insect fauna.     

Higher phylogeny of zygaenid moths (Insecta: Lepidoptera) inferred from nuclear and mitochondrial sequence data and the evolution of larval cuticular cavities for chemical defence

Zygaenid moths are capable of releasing hydrogen cyanide in their defense by enzymatic break-down of cyanoglucosides, but only larvae of chalcosiine and zygaenine moths store cyanogenic compounds in cuticular cavities and thus are able to discharge defense droplets, which effectively deter potential predators. A previously proposed phylogeny of Zygaenidae hypothesized a sister group relationship of chalcosiine and zygaenine moths because of their similar larval defense system. Not all chalcosiine taxa possess cuticular cavities, however, and a comparable defense mechanism has been reported in larvae of the zygaenoid family Heterogynidae. Considering sequence data of seven molecular loci, the present study estimates the posterior probability of phylogenetic hypotheses explaining the occurrence of larval cuticular cavities. The molecular data confirm the previous exclusion of Himantopteridae from Zygaenidae and suggest their close affinity to Somabrachyidae. The sequence data also corroborate the recently proposed exclusion of the Phaudinae from the Zygaenidae, because this subfamily is recovered in a reasonably well supported species cluster consisting of members of the families Lacturidae, Limacodidae, Himantopteridae, and Somabrachyidae. We consequently agree to raise Phaudinae to family rank. Within Zygaenidae, the subfamilies Callizygaeninae, Chalcosiinae, and Procridinae most likely constitute a monophyletic group, which is sister to the Zygaeninae. Our results imply that cuticular cavities were probably present in the larvae of the most recent common ancestor of Zygaenidae. Heterogynidae cannot be confirmed as sister taxon to this family, but appear at the very first split of the Zygaenoidea, although with poor support. The specific pattern of taxa in the molecular phylogeny showing larval cuticular cavities opens the possibility that these structures could have been already present in the most recent common ancestor of the Zygaenoidea.     

Higher level phylogeny of Satyrinae butterflies (Lepidoptera: Nymphalidae) based on DNA sequence data

We have inferred the first empirically supported hypothesis of relationships for the cosmopolitan butterfly subfamily Satyrinae. We used 3090 base pairs of DNA from the mitochondrial gene COI and the nuclear genes EF-1alpha and wingless for 165 Satyrinae taxa representing 4 tribes and 15 subtribes, and 26 outgroups, in order to test the monophyly of the subfamily and elucidate phylogenetic relationships of its major lineages. In a combined analysis, the three gene regions supported an almost fully resolved topology, which recovered Satyrinae as polyphyletic, and revealed that the current classification of suprageneric taxa within the subfamily is comprised almost completely of unnatural assemblages. The most noteworthy findings are that Manataria is closely related to Melanitini; Palaeonympha belongs to Euptychiina; Oressinoma, Orsotriaena and Coenonympha group with the Hypocystina; Miller's (1968). Parargina is polyphyletic and its components group with multiple distantly related lineages; and the subtribes Elymniina and Zetherina fall outside the Satyrinae. The three gene regions used in a combined analysis prove to be very effective in resolving relationships of Satyrinae at the subtribal and tribal levels. Further sampling of the taxa closely related to Satyrinae, as well as more extensive sampling of genera within the tribes and subtribes for this group will be critical to test the monophyly of the subfamily and establish a stronger basis for future biogeographical and evolutionary studies.