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. 2022 Jun 24;1108:119–139. doi: 10.3897/zookeys.1108.80783

Molecular phylogeny of Lichen Tiger Moths (Lepidoptera, Erebidae, Arctiinae, Lithosiini): a contribution toward classifying Western Hemisphere genera

John D Palting 1, Wendy Moore 1,✉
PMCID: PMC9848871  PMID: 36760697

Abstract

This study analyzes molecular sequence data from one mitochondrial (COI) and two nuclear (28S, RPS5) genes to test the monophyly of previously proposed subtribes of the Lithosiini (Erebidae: Arctidinae), including subtribal assignment of all North American genera that occur north of Mexico. After transferring Gardinia W.F. Kirby from Lithosiina to Cisthenina, there is strong support for a monophyletic Lithosiina, which includes three originally unplaced Nearctic genera: Agylla Walker, Inopsis Felder, and Gnamptonychia Hampson. The result of this study removes Clemensia Packard and Pronola Hampson from Cisthenina and places them in subtribe Clemensiina. We synonymize Eudesmiina under Cisthenina. After these changes, the phylogeny shows strong support for the monophyly of Cisthenina, which includes a further three unplaced Nearctic genera: Gardinia Kirby, Bruceia Neumögen, and Ptychoglene Felder. The monophyly of Cisthenina (including Eudesmia and Gardinia) is supported by two apomorphies found in adults: the apodemes of the second abdominal sternite are long and the anterolateral processes are fused with the rest of the sternite.

Keywords: Acsalina, Cisthenina, Clemensiina, Eudesmiina, Lithosiina, molecular sequence data, new subtribal classification, phylogenetic analysis

Introduction

Lithosiini (Erebidae: Arctiinae), known as Lichen Tiger Moths, consist of approximately 4000 described species, and have the uncommon ability to feed on lichens (Fig. 1). While other lepidopterans are known to facultatively feed on lichens, only a few groups are known to be obligate lichen feeders. Some authors have suggested most of these are feeding primarily on the algal symbiont of the lichen (Wagner et al. 2008). In the New World, these include members of the Afridini (Nolidae), Elaphriini (Noctuidae) and the Bryophilinae (Noctuidae). Not only do the Lithosiini obligately feed on lichen and algae, they are the only lepidopterans known to sequester phenolics produced by the lichen fungal symbiont (Hesbacher et al. 1995; Wagner et al. 2008; Conner 2009; Scott et al. 2014; Anderson et al. 2017; Scott Chialvo et al. 2018). Lithosiini larvae are secretive, nocturnal, seldom encountered, and poorly known (Wagner 2005; Conner 2009). All Lithosiini larvae that have been examined to date have a mola, a unique flattened, heavily sclerotized area on the inner margin of the mandibles which they use to grind through tough lichen thalli (Fig. 2) (Gardner 1943; Issiki et al. 1965; McCabe 1981; Lafontaine et al. 1982; Rawlins 1984; Garcia-Barros 1985; Habeck 1987; Bendib and Minet 1998; Bendib and Minet 1999; Jacobson and Weller 2002). The ability of the larvae to feed on lichens and sequester associated toxins for their own protection was likely the key innovation that led to the remarkable diversification of this group (Wagner et al. 2008).

Figure 1.

Figure 1.

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Representative Lithosiini larvae ACrambidiamyrlosea Dyar BInopsismodulata (Edwards).

Figure 2.

Figure 2.

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Dissections of the mandible of larvae illustrating two alternate states found among ArctiinaeA mandible of Lerinaincarnata Walker with a blade-like inner margin, as found in Arctiinae tribes other than LithosiiniB mandible of Eudesmiaarida (Skinner), bracket indicates the mola, an apomorphy of Lithosiini.

Defensive chemicals that the larvae acquire from feeding on lichens are maintained through the pupal stage into the adult (Hesbacher et al. 1995; Anderson et al. 2017; Scott Chialvo et al. 2018). Lithosiini adults are small to medium-sized moths (Fig. 3). Some species have white, gray or brown wing scales and others are brightly and aposematically colored. The audible clicks of some adults warn bats of their distastefulness (Acharya and Fenton 1992). Like their better-studied arctiine relatives, it was suggested that the ability of lithosiines to sequester toxic compounds in the larval stages conveys fitness to the adults (Wagner et al. 2008). Among the arctiines, not only do sequestered toxins provide protection from predators (Eisner and Eisner 1991) and parasites (Singer et al. 2004), they are also critical in pheromone production, courtship success, and can be nuptial gifts that the female passes on to protect her eggs (Conner et al. 1981; Eisner and Meinwald 2003; Jordan et al. 2005). The use of sequestered lichen-derived toxins among members of the Lithosiini remains a wide-open area for research.

Figure 3.

Figure 3.

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Dorsal views of representative Lithosiini adults from North America A–DLithosiinaE–LCistheninaAAgyllaseptentrionalis Barnes & McDunnough BGnamptonychiaventralis Barnes & Lindsey CInopsismodulata (Edwards) DCrambidiacephalica (Grote & Robinson) EGardiniaanopla Hering FEudesmiaarida (Skinner) GPtychoglenecoccinea (Edwards) HCisthenetenuifascia Harvey ILycomorpharegulus (Grinnell) JBruceiapulverina Neumögen KHaematomisuniformis Schaus LHypoprepiainculta Edwards. Scale bar: 1 cm.

Monophyly of the Lithosiini is supported by two larval apomorphies, a mandibular mola (Fig. 2B) and the unique arrangement of labral setae, where M1 is more ventral and far from M2 (Bendib and Minet 1999). In the plesiomorphic condition (non-Lithosiini), M1 and M2 are either in a horizontal line or M1 is slightly dorsad of M2 (Habeck 1987). Lithosiini monophyly is further supported by several molecular phylogenetic studies of the Arctiinae (Zahiri et al. 2012; Zaspel et al. 2014; Zenker et al. 2016).

One lingering question is the classification of the Neotropical genus Afrida Möschler which has a confusing taxonomic history. Several authors considered it to belong to Lithosiini (Hampson 1900; Dyar 1913). While the larvae do feed on lichens, they are morphologically distinct, particularly in the shape of their cocoon and that they weave bits of lichen into the structure (Wagner et al. 2011), something no Lithosiini is known to do. Several authors proposed to move this genus from the Erebidae to the family Nolidae, subfamily Afridinae (Holloway 1998; Kitching and Rawlins 1998). More recently, Lafontaine and Schmidt (2010) placed Afridinae as a subfamily of Nolidae, based on COI sequence data and morphology. Although Zahiri et al. (2013a) performed a molecular phylogenetic study of the family Nolidae based on eight gene regions, Afrida was not included in their taxon sampling, and thus the phylogenetic placement of this genus has not been tested by molecular-based analysis.

Knowledge of the relationships among the 350 genera classified within the Lithosiini is not well-resolved. Seven lineages within the Lithosiini were either redefined or first proposed by the seminal work of Bendib and Minet (1999). Based on their extensive analysis of morphological characters in adults and larvae (where known) they described and assigned 49 Lithosiini genera to six of these lineages (here considered subtribes), including Cisthenina (26 genera), Eudesmiina (four genera), Acsalina (one genus), Nudariina (15 genera), Endrosiina (two genera) and Phryganopterygiina (one genus). While this work established a baseline and laid the groundwork for future studies of Lithosiini, their taxon sampling was far from complete. They did not include all genera in their classification, and they did not treat the Lithosiina or assign any genera to this group. Jacobson and Weller (2002) included some lithosiines in their pioneering cladistical study of arctiid adult and larval characters, while Scott and Branham (2012) conducted the largest morphology-based phylogenetic analysis of the Lithosiini, including 76 species in 49 genera from each of the proposed seven subtribes. While these studies again supported the monophyly of the Lithosiini as a group, morphology alone failed to elucidate subtribal relationships.

In this study we conduct a DNA-based phylogenetic analysis of the Lithosiini that builds upon three previously published studies (Scott et al. 2014; Zenker et al. 2016; Scott Chialvo et al. 2018), with the aim of including representatives of all genera known from North America north of Mexico (Schmidt and Opler 2008) as well as published sequences from other Western Hemisphere taxa. We propose a new subtribal classification based upon our analyses. The resulting phylogenetic framework and classification provide a baseline for future systematic and behavioral studies of this charismatic group and evolutionary studies of their remarkable defensive chemistry.

Materials and methods

Gene selection and taxon sampling

Sequences acquired from previous molecular phylogenetic studies of Erebidae (Zahiri et al. 2011; Zahiri et al. 2012; Zahiri et al. 2013b; Scott et al. 2014; Zenker et al. 2016; Scott Chialvo et al. 2018) were downloaded from GenBank and assembled into single gene matrices. Preliminary phylogenetic analyses of the aligned sequences were conducted to determine which gene markers appeared to be most phylogenetically informative and would provide the most complete taxon sampling for our analyses. Based on the results of these preliminary analyses we chose to proceed with one mitochondrial protein-coding gene, cytochrome oxidase I (COI); one nuclear protein-coding gene, ribosomal protein S5 (RPS5); and one nuclear structural gene, the large subunit rRNA D2 loop (28S). Sequences from five species classified in the Erebidae subfamily Aganainae, and representative species of the Arctidinae tribes Arctiniini, Syntomiini, and Amerillini were downloaded from GenBank and included in the single gene matrices as outgroups. Molecular sequence data for 31 additional species, representing 16 genera from the southwestern United States were added. All voucher specimens have been deposited in the University of Arizona Insect Collection (UAIC).

DNA extraction, amplification, and sequencing

Total genomic DNA was extracted from the right mesothoracic leg or the abdomen of single specimens using the Qiagen DNeasy Blood and Tissue Kit (Qiagen, Valencia, CA) according to manufacturer suggested protocols. Total genomic DNA was stored in buffer at -80 °C.

Gene fragments were PCR amplified for COI using the primers LCO1490 and HCO2198 (Hebert et al. 2003); the nuclear protein-coding gene RPS5 and nuclear large subunit 28S were amplified using primers and PCR protocols as provided in Scott et al. (2014). PCR products were cleaned, quantified, normalized and sequenced in both directions at the University of Arizona’s Genomic and Technology Core Facility using a 3730 or 3730XL Applied Biosystems automatic sequencer. Chromatograms were assembled into contigs and initial base calls were made for each gene with Phred (Green and Ewing 2002) and Phrap (Green 1999) as orchestrated by Chromaseq ver. 1.5 in Mesquite ver. 3.6 (Maddison and Maddison 2017, 2018). Final base calls were made in Mesquite and ambiguous bases were designated by standard ambiguity codes. GenBank accession numbers for all sequences used in this study are listed in Table 1.

Table 1.

Sampling of Lithosiini and outgroup species and GenBank accession numbers for sequences used in this study.

UAIC Specimen Number RpS5 28S rDNA COI
Family Nolidae
Afridaexegens Dyar USA: AZ, Cochise Co., Huachuca Mts. UAIC1148036, UAIC1148037 OM990708 ON006455 ON000160
ON006456 ON000161
Family Erebidae
Subfamily Aganainae
Asotaheliconia (Linnaeus) KC571142 KC570976 KC571044
Asotaorbona Vollenhoven KC571143 KC570977 GWORG305-08
Neocheradominia Cramer KC571144 KC570978 JZAGA909-12
Peridromeorbicularis Walker JN401903 JN401280
Subfamily Arctiinae
Tribe Amerilini
Amerillabrunnea Hampson KX300895 KX300223
Tribe Arctiini
Cycniatenera Hübner KF533651 KF533380 KF533458
Halysidotatessellaris J. E. Smith KF533658 KF533469
Leucanopsissetosa Rothschild KJ723700 KF533400 KJ723706
Phragmatobiaamurensis Seitz KF533679 KF533419 KF533492
Pygoctenuchaterminalis Walker Mexico: Sonora, SSW Mesa Tres Rios UAIC1128849 OM990703 ON006450
Virbiacostata (Stretch) USA: AZ, Pima Co., Santa Catalina Mts. UAIC1128305 OM990695 ON006437 MF923392
Tribe Syntomiini
Amataphegea (Linnaeus) HQ006749 KF533352 HQ006238
Apisacanescens Walker HQ006663 HQ006146
Automolisferrigera Druce KF533641 KF533447
Ingroup
Tribe Lithosiini
Subtribe Acsalina
Acsalaanomala Benjamin KC571145 KC570980 KJ378646
Subtribe Cisthenina
Abrochocisesperanza Dyar KC570979 KC571047
Ardoneatenebrosa (Walker) KX361016 KX360798
Arhabdosia sp. KX361034 KX360800
Balburadorsisigna Walker KC570986 KC571053
Balburaintervenata Schaus KX361017 KC570987 KX360802
Bruceiahubbardi Dyar USA: AZ, Pima Co., Santa Catalina Mts. UAIC1128313 OM990689 ON006431 ON000141
Bruceiapulverina Neumögen Mexico: Sonora, Sierra del Tigre UAIC1128312 OM990704 ON006451 KC571055
ON000157
Bruceia sp. 1 Mexico: Sonora, Sierra del Tigre UAIC1128309 OM990692 ON006434 ON000146
Bruceia sp. 2 USA: AZ, Pima Co., Santa Catalina Mts. UAIC1148030 OM990697 ON006439 ON000144
Chrysochlorosiamagnifica Schaus KC570996 KC571057
Cistheneangelus (Dyar) USA: AZ, Pima Co., Tucson Mts. UAIC1128316 ON006426 ON000136
Cisthene sp. USA: AZ, Pima Co., Santa Catalina Mts. UAIC1148032 OM990690 ON006432 ON000142
Cisthenemartini Knowlton USA: AZ, Cochise Co., Huachuca Mts. UAIC1128318 ON006427 ON000137
Cisthenekentuckiensis (Dyar) USA: Texas, Travis Co., Austin UAIC1148031 OM990698 ON006440 ON000143
Cisthenetenuifascia Harvey USA: AZ, Pima Co., Santa Catalina Mts. UAIC1128319 ON006430 ON000140
Clemensiamarmorata (Schaus) KX300811 KX300245
Cloesiadigna Schaus KC570995 JQ561796
Cloesia sp. KX361038 KX360809
Dipaenaecontenta (Walker) KX361018 KX360815
Dolichesiafalsimonia Schaus KC571000 KC571062
Eudesmiaarida (Skinner) Mexico: Sonora, Municipio de Nacori Chico UAIC1128306 OM990701 ON006448 ON000156
Eudesmiamenea (Drury) MF922663.1
Euthyonegrisescens (Schaus) KC571010 KC571073
Euthyonepurpurea (E. D. Jones) KX361046 KX360823
Gardiniaanopla Hering KC571159 KC571012 KC571075
Gardiniaanopla Hering USA: AZ, Pima Co., Santa Catalina Mts. UAIC1128297 ON006425 ON000135
Gardiniaparadoxa Hering KX361019 KX360825
Hypermaepha sp. KX361049 KX360828
Hypoprepiacadaverosa Strecker USA: AZ, Apache Co., Greer UAIC1148028 ON006446
Hypoprepiafucosa Hübner KC571162 KC571017 KC571078
Hypoprepiafucosa tricolor (Fitch) KC571163 KC571018 KC571079
Hypoprepiainculta Edwards USA: AZ, Cochise Co., Chiricahua Mts. UAIC1128315 OM990706 ON006453 MH337839
Hypoprepialampyroides Palting & Ferguson USA: AZ, Greenlee Co., Blue Ridge Primitive Area UAIC1128324 ON006441 MH337834
Hypoprepiaminiate (Kirby) MF923793
Illiceendoxantha Hampson KX361050 KX360831
Lycomorphafulgens (H. Edwards) USA: AZ, Apache Co., Hannagan Meadow UAIC1148033 ON006447
Lycomorphagrotei (Packard) USA: AZ, Apache Co., Greer UAIC1148029 OM990702 ON006449
Lycomorpharegulus (Grinnell) USA: AZ, Greenlee Co., Blue Ridge Primitive Area UAIC1148034 OM990693 ON006435 ON000147
Lycomorphodescorrebioides Schaus KC571027 KC571088
Lycomorphodessordida (Butler) KC571028 KC571089
Lycomorphodesstrigosa (Butler) KX361051 KX360833
Metalobosiavarda (Schaus) KX361052 KX360836
Meterythrosiasangala (H. Druce) KC571030 KC571030
Nodozanacf.coresa Schaus KX361055 KX360839
Prepiellasesapina (Butler) KX361057 KX360844
Pronolamagniplaga Schaus KX300812 KX300312
Ptychoglenecoccinea (H. Edwards) KC571036 HQ918634
Ptychoglenephrada H. Druce KF533681 KF533497
Rhabdatomiscoracoroides Schaus KC571037 KC571094
Rhabdatomislaudamia (H. Druce) UAIC1128848 ON006429 ON000139
Mexico: Sonora, Sierra La Madera
Rhabdatomismandana (Dyar) KX361058 KX360845
Rhabdatomismelinda (Schaus) KC571039 KC571096
Talaracara Schaus KC571041 KC571098
Talaralepida Schaus KC571042 KC571099
Talaranr.mona Dyar KC571043 KC571100
Talarasemiflava Walker KX361060 KX360847
Subtribe Endrosina
Eugoabipunctata Walker JN401906 KF533390 JN401906
Setinairrorella (Linnaeus) KX050605 KX050282
Stigmatophoramicans (Bremer & Grey) KF704470
Trischalis sp. HM906475
Subtribe Lithosiina
Agkoniaovifera Dognin KX300816 KX300221
Agyllaargentea Walker KX300817 KX300220
Agyllaargentifera Walker KC570981 KC571048
Agyllaseptentrionalis Barnes & McDunnough USA: AZ, Cochise Co., Chiricahua Mts. UAIC1148038 OM990705 4167 ON000158
Apistosiajudas Hübner KX300815 KX300230
Arevatrigemmis Hübner KX300814 KX300233
Atolmisrubricollis (Linnaeus) KC571147 KC570985 ABOLA126-14
Bruniaantica (Walker) HQ006706 KF533366 HQ006193
Calamidiahirta Walker KC571148 KC570990 KC571056
Crambidiacephalica (Grote & Robinson) USA: AZ, Navajo Co., Showlow UAIC1128271 OM990699 ON006442 ON000152
Crambidiaimpura Barnes & McDunnough USA: AZ, Gila Co., N. of Winkelman UAIC1128280 OM990688 ON006428 ON000138
Crambidiamyrlosea Dyar Mexico, Sonora, Sierra Alacran UAIC1148035 OM990696 ON006438 ON000150
Crambidiapallida Packard USA: NC, Macon Co, Slick Rock UAIC1128304 OM990691 ON006433 ON000145
Crambidiaxanthocorpa Lewis USA: IN, Tippecanoe Co., Purdue University UAIC1128323 OM990694 ON006436 ON000148
Cybosiamesomella (Linnaeus) KC570999 ABOLA124-14
Eilemacomplanum (Linnaeus) Romania: Torda, Torocko UAIC1128295 ON006443 ON000153
Gnamptonychiaflavicollis (H. Druce) KC571158 KC571013 KC571076
Gnamptonychiaventralis Barnes & Lindsey Mexico: Sonora, Sierra del Tigre UAIC1128300 OM990707 ON006454
Hieragyge H. Druce KC571161 KC571015
Inopsismodulata (H. Edwards) KC571164 KC571020 KC571082
Lithosiaquadra (Linnaeus) Bulgaria: Kalimantsi UAIC1128303 ON006444 ON000154
Manuleabicolor (Grote) USA: CO, Gilpin Co., Golden Gate Canyon UAIC1128293 OM990700 ON006445 ON000155
Mintopolabraziliensis Schaus KX300290
Subtribe Nudariina
Asuracervicalis Walker KC570983 KC571050
Barsine sp. JN401878 KF533364 JN401286
Cyanameyricki Rothschild & Jordan KC571151 KC570998 KC571061
Cyana sp. JN401876 KF533379 JN401285
Lyclenepyraula (Meyrick) KC571165 KC571022 KC571084
Lyclenequadrilineata (Pagenstecher) KC571172 KC571035 KC571093
Lyclenereticulata (C. Felder) KC571166 KC571023 KC571085
Lyclene sp. KC571168 KC571024 KC571086
Miltochristaminiata (Forster) KC571170 KC571031 KC571090
Miltochrista sp. KC571171 KC571032 KC571091
unplaced
Heliosiajucunda Walker KC571160 KC571014 KC571077
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Sequence alignment and phylogenetic analyses

Single gene matrices were aligned using default settings in MAFFT v7.474 (Katoh and Standley 2013) and were concatenated in Mesquite. Maximum likelihood analyses were conducted on each gene individually and on the concatenated dataset using IQ-TREE ver. 1.6.10 (Nguyen et al. 2015), as orchestrated by Mesquite. The ModelFinder feature within IQ-TREE (Kalyaanamoorthy et al. 2017) was used to find the optimal character evolution models. The MFP model option was used for 28S, and the TESTMERGE option for the protein-coding genes. The TESTMERGE option sought the optimal partition of sites, beginning with the codon positions in different parts. Analyses of the concatenated data matrix were conducted using the TESTMERGE option, beginning with each codon position for each gene as a separate part (thus, the analysis began allowing for up to 7 parts, three for both of the protein-coding genes and one for 28S). One hundred searches were conducted for the maximum likelihood tree for each matrix. One thousand replicates were used for bootstrap analyses.

Results

A summary diagram of the ML tree for the concatenated dataset is shown in Fig. 4. The full ML tree and all bootstrap values recovered from analyses of the concatenated dataset are shown in Suppl. material 1: Fig. S1. Based on our results we propose several changes to the subtribe classification within Lithosiini as discussed below and summarized in Table 2.

Figure 4.

Figure 4.

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Maximum likelihood tree for the concatenated matrix. Branch lengths are proportional to relative divergence, as estimated by IQ-TREE. Bootstrap values are depicted below branches. Western Hemisphere monophyletic genus-level clades are collapsed and subtribes are colored. Clades that do not include Western Hemisphere species are collapsed and colored gray. See Suppl. material 1: Fig. S1 for the full tree.

Table 2.

Proposed classification of Western Hemisphere genera of Lithosiini based on this study with reference to their original placement by Bendib and Minet (1999). Plus symbols (+) indicate that that genus was included in one or more of three molecular-based studies of Lithosiini, including Zenker et al. (2016) (column A), Scott Chialvo et al. (2018) (column B), and this study (column C), and that results support its position in the subtribal classification proposed here. Dashes indicate that that genus was not included in the molecular-based studies. When dashes occur in all three columns, that genus was placed in the proposed subtribal classification by morphology alone.

Proposed subtribal classification Placement by Bendib and Minet 1999 A B C
Acsalina Bendib and Minet
Acsala Benjamin Acsalina - - +
Cisthenina Bendib and Minet
Abrochocis Dyar unplaced - - +
Ardonea Walker unplaced + - +
Arhabdosia Dyar Cisthenina + + +
Ascaptesyle Dyar Cisthenina + - +
Balbura Walker unplaced + - +
Barsinella Butler Cisthenina - - -
Bruceia Neumoegen unplaced - + +
Callisthenia Hampson Cisthenina - - -
Chrysochlorosia Hampson unplaced - - +
Chrysozana Hampson Cisthenina - - -
Cisthene Walker Cisthenina + + +
Cloesia Hampson unplaced + - +
Dipaenae Walker unplaced + - +
Dolichesia Schaus Cisthenina - - +
Eudesmia Hübner Eudesmiina - - +
Euryptidia Hampson Eudesmiina - - +
Euthyone Watson Cisthenina + - +
Gardinia Kirby‎ unplaced + - +
Haematomis Hampson unplaced - + -
Hypermaepha Hampson Cisthenina - - -
Hypoprepia Hübner Cisthenina + + +
llice Walker unplaced + - +
Josiodes Felder Eudesmiina - - +
Leucorhodia Hampson Cisthenina - - -
Lycomorpha Harris Cisthenina - - +
Lycomorphodes Hampson Cisthenina + - +
Maepha Walker Cisthenina - - -
Metallosia Hampson Cisthenina - - -
Metalobosia Hampson unplaced + - +
Meterythrosia Hampson‎‎ unplaced - - +
Neotalara Hampson Cisthenina - - -
Neothyone Hampson Cisthenina - - -
Nodozana H. Druce unplaced + - +
Odozona Walker Cisthenina - - -
Paratype Felder Eudesmiina - - +
Prepiella Schaus Cisthenina + - +
Ptychoglene Felder unplaced + + +
Rhabdatomis Dyar Cisthenina + + +
Seripha Walker Cisthenina - - -
Talara Walker Cisthenina + + +
Clemensiina Bendib & Minet
Clemensia Packard Cisthenina + - +
Pronola Schaus Cisthenina + - +
Lithosiina Stephens not treated
Agylla Walker not treated + - +
Apistosia Hübner not treated + - +
Areva Walker not treated + - +
Atolmis Hübner not treated - - +
Crambidia Packard not treated + - +
Cybosia Hübner not treated - - +
Eilema Hübner not treated - - +
Gnamptonychia Hampson not treated - - +
Hiera Druce not treated - - +
Inopsis Felder not treated - - +
Lithosia Fabricius not treated - - +
Manulea Wallengren not treated - + +
Mintopola Hampson not treated + - +
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Discussion

Afridaexegens Dyar was initially included in the taxon sampling to test its potential placement within the Lithosiini or as an outgroup in this analysis. Including it caused long branch attraction, so the ssequences were removed from the matrices. GenBank BLAST searches of 28S, RPS5 and COI all confirm that Afrida, long considered by some an arctiine based on hindwing venation, does not belong to Erebidae, supporting the conclusions of Kitching and Rawlins (1998), Holloway (1998), Lafontaine and Schmidt (2010) and Zahiri et al. (2013a), who regarded the Afridinae as a subfamily of the family Nolidae.

Monophyly of Lithosiini

Lithosiini monophyly is supported by two morphological apomorphies found in the larvae. Both the unique arrangement of labral setae M1 and M2 and the mandibular mola were present in all Lithosiini larvae reared as part of this study, many of which were previously unknown, including Agyllaseptentrionalis Barnes & McDunnough, Cisthenekentuckiensis (Dyar), Gardiniaanopla Hering, Crambidiamyrlosea Dyar, Eudesmiaarida (Skinner), Hypoprepialampyroides Palting & Ferguson, Inopsismodulata (Edwards) and Lycomorphafulgens (Edwards).

Subtribe Acsalina

Acsalaanomala Benjamin occurs on a long branch by itself, supporting the placement of this species in a monotypic subtribe Acsalina. This enigmatic species was placed among the Lymantriidae, however following description of the larval stages feeding on lichens and the presence of a mandibular mola (Lafontaine et al. 1982) it was considered Lithosiini. Bendib and Minet (1999) list many unique apomorphies of the Acsalina, including flightless females, translucent wing vestiture, compound eyes with interommatidial setae, and a primitive hindwing ground plan not found among other Lithosiini. From a biogeographic perspective it is interesting that the Acsalina does not seem to be recently derived from any other temperate lineage contrary to virtually all other Lepidoptera endemic to the Arctic.

Subtribe Cisthenina (includes Gardinia and Eudesmiina)

When Bendib and Minet (1999) erected the tribe Cisthenini they divided it into the Cistheniti (containing Cisthene Walker, Clemensia Packard, Hypoprepia Hübner, Lycomorpha Harris, Lycomorphodes Hampson, and Rhabdatomis Dyar) and Clemensiiti (containing Clemensia Packard, Pronola Schaus, Siccia Walker, Hyposiccia Hampson and Parasiccia Hampson). They noted Cistheniti have an unusual resting posture with the antennae facing forward, while Clemensiiti exhibit the plesiomorphic folding backwards of the antennae. They also noted that Clemensiiti rested with the wings flattened rather than roof-like over their back as in Cistheniti.

We find strong support to remove Clemensia and Pronola (as discussed below) and include thirteen Neotropical genera that were unplaced by Bendib and Minet (1999). These include nine genera (Balbura Walker, Cloesia Hampson, Dipaenae Walker, Dolichesia Schaus, Ilice Walker, Metalobosia Hampson, Nodozona Druce, Ptychoglene Felder, and Talara Walker) which were found to be cisthenines in previous studies molecular-based studies (Zenker et al. 2016; Scott Chialvo et al. 2018) as well as four genera (Abrochocis Dyar, Bruceia Neumögen, Chrysochlorosia Hampson, Meterythrosia Hampson) which we include in a molecular-based study and classify for the first time (Table 2). We were not able to obtain fresh specimens of Haematomis Hampson for inclusion in our phylogeny, however we speculate based on its small size and resting posture that Haematomis belongs to Cisthenina. The wing pattern, particularly the distinctive pink basal wing markings, are consistent with other cisthenines that are thought to be Mullerian mimics of lampyrid beetles, especially some Hypoprepia species (H.lampyroides and H.inculta, for example).

Contrary to previous classifications, this study finds support to include two genera, Eudesmia and Gardinia, within Cisthenina. Bendib and Minet (1999) classified Eudesmia in subtribe Eudesmiina along with three other Western Hemisphere genera: Euryptidia Hampson, Josiodes Felder, and Paratype Felder. This is the first molecular-based phylogenetic study to include a member of the subtribe Eudesmiina. Results indicate that recognizing Eudesmiina as a valid subtribe would render Cisthenina polyphyletic. Therefore, as first revisers we place Eudesmiina in synonymy under Cisthenina, with an expanded concept of the latter. Both names, Cisthenina and Eudesmiina, were published at the same time (Bendib and Minet 1999), so neither name has priority (ICZN Article 24.2). We choose Cisthenina since it is a much more diverse lineage. Given the apomorphies presented by Bendib and Minet for uniting the four genera they placed within the Eudesmiini, we tentatively place them all within Cisthenina (Table 2).

While Gardinia was unplaced by Bendib and Minet (1999) it was treated as a member of Lithosiina by several authors (Scott and Branham 2012; Scott et al. 2014). Gardinia is a Neotropical genus containing five species, including one species from southeastern Arizona, Gardiniaanopla Hering (Fig. 1E). Gardiniaanopla is the largest lichen moth in North America with an average forewing length of 25 mm, making it more than twice as large as other Cisthenina (typically with forewing lengths of 10 mm or less). When captured, adults of this nocturnal species produce audible clicks. Among Cisthenina, adults of Cisthenemartini are known to produce clicks in response to bat echolocation and are generally avoided by bats (Dowdy and Conner 2016). The clicks of Gardinia might be used similarly to warn bats of their distastefulness.

Cisthenina larvae generally have short, sparse setae and they lack verrucae, which was proposed as an apomorphy for the subtribe (Bendib and Minet 1999). However, the larvae of Gardinia (Fig. 5A) and of Eudesmia (Fig. 5B), reared as part of this study, possess verrucae making species in these genera the only members of Cisthenina known to have them. Eudesmiaarida (Skinner) larvae possess exceedingly long, soft setae, unlike the short, stiff setae characteristic of other Cisthenina (Fig. 5B).

Figure 5.

Figure 5.

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Representative Cisthenina larvae AEudesmiaarida (Skinner) BGardiniaanopla Hering.

All members of the Cisthenina, as defined here, are endemic to the Western Hemisphere. Among Cisthenina adults, apodemes on the second abdominal sternite are long and the anterolateral processes are fused with the rest of the sternum (Fig. 6). We find that these character states are present in Eudesmia and Gardinia (Fig. 6) which hold as a strong apomorphies of Cisthenina as redefined in this study.

Figure 6.

Figure 6.

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Dissections of the second abdominal sternites of adults illustrating two alternate states found among subtribes of LithosiiniA apodemes of Pygarctiaroseicapitis (Neumoegen & Dyar) are relatively short and the anterolateral processes articulate with the sternal plate as found in most members of Lithosiina (other than Agylla) and in ArctiiniB apodemes of Gardiniaanopla Hering are relatively long and the anterolateral processes are fused with the rest of the sternum as found in members of the Cisthenina, including Eudesmia and Gardinia.

Subtribe Clemensiina Bendib & Minet

Type-genus: Clemensia Packard.

When Bendib and Minet (1999) erected the tribe Cisthenini they divided it into the Cistheniti and Clemensiiti, with the latter housing Clemensia, Pronola, Siccia, Hyposiccia and Parasiccia. In addition to the differences they noted in resting posture between the subtribes, they noted three apomorphies of the Clemensiiti, including the presence of a pair of metascutal membranous areas, sternite A2 possessing curved movable anterolateral processes and the presence of a corethrogyne in females.

In this study Clemensia falls outside Cisthenina and it forms a highly supported clade with the small neotropical genus Pronola Schaus (5 species), the adults of which are similarly sized and have a similar peculiar rounded wing shape. Zenker et al. (2016) found Clemensia + Pronola were the sister group of the Oriental genus Garudinia Moore. Additional taxon sampling from around the world will be needed to determine the extent of this clade, with the genera Sicia, Hyposiccia and Parasiccia from the Western Hemisphere likely to be included within it. Future research on this clade is likely to be fruitful. Not only is a larger molecular and morphological analysis required, the limited information available on the immatures of species in this clade (McCabe 1981) suggests they are strictly algivores, refusing to feed on lichen at all. This observation, combined with their somber coloring, might indicate they do not sequester lichen phenolics for protection as do all other lithosines.

Subtribe Lithosiina

Bendib and Minet (1999) did not treat or assign genera to the Lithosiina. Results of this study indicate the following 13 genera are included in this well-supported clade: Agylla Walker, Apistosia Hübner, Areva Walker, Atolmis Hübner, Crambidia Packard, Cybosia Hübner, Eilema Hübner, Gnamtonychia Hampson, Hiera Druce, Inopsis Felder, Lithosia Fabricius, Manulea Wallengren, Mintopola Hampson.

This is the first study to include specimens of Gnamtonychia Hampson and Inopsis Felder in a molecular-based phylogenetic analysis. Including them in Lithosiina is also supported by the shape of the second abdominal sternite (Fig. 6A) and their resting posture with their wings held somewhat flattened and rolled around their abdomen, two traits typical of Lithosiina. Gnamtonychiaventralis Barnes and Lindsey occurs in southeastern Arizona and New Mexico and Inopsismodulata Edwards occurs in Mexico and is rarely found in southeastern Arizona. These two species are remarkably similar in external appearance as adults, however side-by-side I.modulata is a slightly smaller moth with shorter, more rounded wings than G.ventralis (Fig. 3B, C). Both species are evidently part of a Mullerian mimicry complex that includes the arctiine Pygotenuchaterminalis (Walker) (included here as an outgroup), which is similarly colored and a toxic milkweed-feeder in the larval stages. The larvae of G.ventralis are unknown. The larvae of I.modulata have distinctive orange to red verrucae and a dark bodies (Fig. 5B), making them conspicuous as they feed on lichens growing on tree branches.

In agreement with Zenker et al. (2016), the molecular phylogeny in this study places Agylla within Lithosiina. Agylla represents the single largest radiation among Western Hemisphere Lithosiini, with 101 described species found in the Neotropics. Primarily an Old World group, Zenker et al. (2016) proposed the Lithosiina colonized South America from the Holarctic in one or more events. In fact, results presented here likely confirm that there have been at least three incursions from the Old World to the New World (assuming the group originated in Asia as proposed by Zenker et al. 2016). In our analyses we added A.septentrionalis Barnes and McDunnough (Fig. 1A), which is restricted to the mountains of southeastern Arizona. Adults of this species look similar to some European members of the genus Lithosia Fabricius such as male L.quadra Linnaeus included in our analyses. However, the results of this analysis show that these two genera are not closely related, Crambidia is instead closely related to Manulea+Eilema (Palaearctic/Oriental), whereas Agylla is part of a Neotropical clade. We note that adults of A.septentrionalis hold their wings “tent-like” over the body rather than flattened and rolled around their abdomens like most Lithosiina. In addition, the adults possess a Cisthenina-like second abdominal sternite (Fig. 6B). Thus, the placement of Agylla within Lithosiina, means that these morphological characteristics are more labile than previously thought.

Concluding remarks

With a tribe as large as Lithosiini, it is surprising that a subtribal classification was neglected for so long, yet understandable given their worldwide diversity and confounding variation of morphological characters. Beginning with Bendib and Minet (1999), we started to conceptualize how Lithosiini genera might be related. Some of our placements here, such as Gardinia among Cisthenina, show that the appearance of the adults does not belie their phylogenetic relatedness. With the apparent lack of morphological apomorphies identified thus far that support subtribal alliances, molecular techniques provide a useful tool for understanding how their diversity evolved. As additional molecular data are published and made available, their evolutionary relationships will become more apparent and hopefully lead to the discovery of morphological apomorphies in both larvae and adults. Presently the whole life history is known for only a small percentage of species. Thus, we have barely scratched the surface in understanding these remarkable lepidopterans and their unique relationship to their lichen hosts and to each other.

Acknowledgements

We are grateful to Ray Nagle and David Wagner for their generous help in procuring fresh specimens of numerous Lithosiini and for their photographs used in this work, to Reilly McManus for her assistance in the lab, and Christopher Palting for his computer help during this study. We thank James Adams, Tim Anderson, Barbara Bartell, Eric Wallace, Dave Marsden, Cliff Ferris, Ann Hendrickson, Chris Schmidt, Christi Yeager, Ana Lilia Reina and Tom VanDevender for their help in collecting specimens. We thank three anonymous reviewers and Doug Yanega for sharing his expertise on ICZN rules. This work is in partial fulfillment of JDP’s Doctorate of Philosophy degree from the Graduate Interdisciplinary Program in Entomology and Insect Science (GIDP-EIS) at the University of Arizona and is a product of the Arizona Sky Island Arthropod Project (ASAP) based in WM’s laboratory. Funding for this work was provided by WM, and JDP is grateful for her patient mentoring in molecular systematics. JDP also thanks Molly Hunter, the GIDP-EIS Program, and his committee members Wendy Moore, Yves Carriere, Ray Nagle, Carol Schwalbe and Bruce Walsh for their support and mentoring.

Citation

Palting JD, Moore W (2022) Molecular phylogeny of Lichen Tiger Moths (Lepidoptera, Erebidae, Arctiinae, Lithosiini): a contribution toward classifying Western Hemisphere genera. ZooKeys 1108: 119–139. https://doi.org/10.3897/zookeys.1108.80783

Supplementary materials

Supplementary material 1

Figure S1

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

John D. Palting, Wendy Moore

Data type

Image.

Explanation note

Maximum likelihood tree for the concatenated matrix. Branch lengths are proportional to relative divergence, as estimated by IQ-TREE, scale bar indicates 0.05 units. Bootstrap values are depicted below branches. Clades are colored by subtribe.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary material 1

Figure S1

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

John D. Palting, Wendy Moore

Data type

Image.

Explanation note

Maximum likelihood tree for the concatenated matrix. Branch lengths are proportional to relative divergence, as estimated by IQ-TREE, scale bar indicates 0.05 units. Bootstrap values are depicted below branches. Clades are colored by subtribe.

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