The phylogeny of the Noctuidae (Lepidoptera)

A new phylogenetic system of the Noctuidae is proposed. The system should, however, be regarded as provisional because it is primarily based on only two character complexes: the male genitalia and the tympanal region. The presence of preabdominal brush-organs and the length of tibial spurs in the adult male, the presence of a ventral cervical gland and the lack of the SV 2 setae on the first abdominal segment of the larvae are considered. The results confirm the monophyly of the Noctuidae. The Herminiinae are considered to represent the sister-group of all other Noctuidae. Remaining noctuid subfamilies are grouped in a series of clades for which the corresponding autapomorphies are given. Some formerly accepted subfamilies, such as the Acontiinae, prove to be polyphyletic. Accordingly, these subfamilies are subdivided into separate lineages. A sister-group relationship between the Noctuidae and the Aganaidae is supported. These two families may be united with the Arctiidae to form a still broader clade. Introduction superficial resemblance and vaguely defined characters, rather than on rigorous application of cladistic principles. In an attempt to progress beyond the age of traditional Seven moth families, the Oenosandridae, Doidae, noctuid taxonomy we started a morphological investigation, Notodontidae, Lymantriidae, Arctiidae, Aganaidae and based on a set of characters, which we considered particularly Noctuidae, are currently recognized in the large superfamily useful in elucidating the basic relationships of the noctuid Noctuoidea (Miller, 1991), comprising some 40 000 described subfamilies. species (Heppner, 1991). Monophyly of the Noctuoidea is The tympanal region was chosen because it was demonstrated based on the presence of a metathoracic tympanal organ (Miller, by Eggers (1919) to be structurally heterogeneous within the 1991). With almost 25 000 included species, the Noctuidae Noctuidae. Richards (1932) proposed a noctuid classification form the largest family within the superfamily, and within the based on a comparative study of the tympanal region. order Lepidoptera as a whole (Heppner, 1991). Nevertheless, Unfortunately, Richard’s system relies exclusively on intuitive our understanding of the phylogenetic affinities of the Noctuidae character interpretation; characters or character states to delimit to other noctuoid families, as well as interrelations among the subfamily groups were not provided. various noctuid subfamilies, is still in its infancy. The male genitalia and their associated muscles were Holloway (1988) noted that the Aganaidae and Noctuidae considered because they are thought to evolve quickly share a similar number of thoracic subventral setae in the (Eberhard, 1985), and may thus provide considerable larvae, and both have an orbicular stigma in the forewing cell. information. Tikhomirov (1979a,b,c), in a series of valuable On these grounds he relegated the Aganaidae to a subfamily papers, has demonstrated that some noctuid subfamilies share of the Noctuidae. However, there is homoplasy in the the unique presence of an additional (novel) male genitalic distribution of the subventral setae among the families under muscle. consideration. We prefer to retain family rank for the Aganaidae, The males of most ‘higher’ Noctuidae are characterized by because this corresponds better with the historical development the presence of a paired brush-organ, situated on the second of noctuoid classification, and because the sister-group relationabdominal segment, that is presumably responsible for the ship is still weakly supported. dissemination of male sexual pheromones (reviewed in Birch Kitching (1984) published an historical review of noctuid et al., 1990). We investigated the distribution of this character subfamily relationships. His synopsis shows that current ideas in order to find the point at which it evolved within the family. on the higher classification of the Noctuidae are based on During our studies we suspected that the spurs of noctuid species might be relatively long. We therefore compared spur length of the Noctuidae with that of outgroups. Correspondence: Dr W. Speidel, Zoologisches Forschungsinstitut The presence of a ventral cervical gland in noctuid larvae und Museum Alexander Koenig, Adenauerallee 160, D-53113 Bonn, Germany. has been known for quite a long time (e.g. Gardner, 1941; © 1996 Blackwell Science Ltd 219 220 W. Speidel, H. Fänger and C. M. Naumann Peterson, 1962). Curiously, the precise distribution of this Character system 1: the tympanal region character within Noctuoidea has never been investigated. We therefore decided to include this character in our analysis. General description The absence of seta SV 2 on the first abdominal segment of the larva has been considered to represent an apomorphic The term tympanal region is used here in a rather broad character for the higher Noctuidae (Poole, 1995). We also sense. It refers to the area around the waist-like cleft separating included this important character. the thorax and abdomen, commonly known in the Noctuoidea as the tympanal cavity (Figs 2 and 3). Thus, the tympanal region includes the tympanal organ proper as well as functionally related structural modifications of the metathorax Material and methods and first abdominal segment. Sexual dimorphism in tympanal morphology is probably restricted to species with wingless For the study of cuticular structures, the specimens were females, e.g. the lymantriid genus Orgyia (Eggers, 1919). The cleared in hot aqueous KOH (10%) for about 10 min. In some sex of the specimens investigated is therefore not noted. cases the specimens were later stained in an aqueous solution of We focus on external structures of the tympanal region. An Evan’s Blue in order to clearly visualize delicate membraneous overview of structures and morphological terms is presented structures. in Fig. 2, showing the metathorax and the first two abdominal Specimens to be studied by scanning electron microscopy segments of a higher noctuid species, Agrotis exclamationis (SEM) were either macerated in KOH, or fixed in an aqueous (Noctuinae). The following structures are of particular interest: solution of picric acid. In both cases they were dehydrated through a graded series of ethanol before being transferred to hexamethyldisilazan. Specimens were then air-dried and 1 Hood structures of the A1 pleuron sputter-coated with gold prior to SEM examination. For the investigation of genitalic muscles, male moths were The presence of a metathoracic tympanum has influenced stored in a saturated aqueous solution of picric acid until the structure of the pleural region of the first abdominal dissection. Penetration of the aqueous solution into the segment (A1). The anterior parts of A1, forming the posterior specimens was greatly facilitated by first soaking them briefly wall of the tympanal cavity, are often prominently expanded. in 70% ethanol. Prolonged storage in picric acid stains the There are three principal configurations. A prespiracular hood, muscles a bright yellow colour, while they simultaneously i.e. a pleural evagination situated anterior to the A1 spiracle, remain soft and flexible. During dissection, which was carried is present in the Oenosandridae, Lymantriidae, Arctiidae and out in 70% ethanol, specimens were occasionally dipped in a in a strongly reduced form in the Aganaidae (Fig. 4). The diluted alcoholic solution of Evan’s Blue in order to obtain Herminiinae are the only noctuids possessing this configuration enhanced contrast. (Fig. 5). A postspiracular hood originating immediately behind We obtained fixed male specimens from the noctuoid families the A1 spiracle is typical for the remaining Noctuidae (Figs 2, Oenosandridae, Notodontidae, Lymantriidae, Arctiidae, 6, 7). Reduction of the hood to simple dorsal remnants occurs Aganaidae and from most subfamilies of the Noctuidae in the Nolinae (Fig. 8). Finally, a perispiracular cup on the A1 (Table 1a). Unfortunately, we were unable to obtain fixed male pleura is typical for all Notodontidae (Fig. 9). In some cases specimens of the Doidae, a small family confined to the the cup has shifted anterad to such an extent that it bears Americas. superficial resemblance to a postspiracular hood, and may even A list of the species examined for the other characters is be mistaken for that structure. given on Table 1(b–d). In addition, the pleural region posterior to the A1 hood is, at least in the Noctuidae, provided with a lateral sclerotization (Figs 5–7). This lateral A1 sclerotization should not be confused Results with the hood itself. This sclerotization may be an autapomorphy of the Noctuidae 1 Aganaidae (Minet, 1986; At the outset, the phylogenetic system we propose as a result character a), but has not been studied here in detail. of our morphological investigations will be briefly introduced. Family relationships between the Arctiidae, Aganaidae and 2 The alula Noctuidae, and the principal noctuid subfamily arrangements, are depicted in Fig. 1. For each taxon the approximate number of species has been added in parentheses, mainly following The alula, the posterobasal lobe of the wing, forms a thin membraneous flap covering the dorsal part of the tympanal Heppner (1991). Information concerning the monophyly and composition of individual noctuid subfamilies is presented later region. Its tubular posterior margin (axillary cord) is continued into the scutellar arm, connecting the hindwing with the in the discussion. The cladogram is accompanied by a list of the presumed autapomorphies for each of the ten clades metanotum (Fig. 14). Generally, the insect metanotum houses a pulsatile wing-heart that is responsible for sucking indicated (Table 2). In the following pages the apomorphies in Table 2 are detailed through successive treatment of the five haemolymph out of the hindwings along the scutellar arm (e.g. Krenn & Pass, 1994, 1995). Because of its large size the alula character systems examined. © 1996 Blackwell Science Ltd, Systematic Entomology, 21, 219–251 Phylogeny of Noctuidae 221 Table 1 List of families and species investigated. (a) For the survey of the muscles in the male genitalia* Oenosandridae Oenosandra boisduvalii Newman, 1856 Notodontidae Cerura vinula (Linnaeus, 1758) Phalera bucephala (Linnaeus, 1758) Thaumatopoea solitaria (Freyer, 1838) Traumatocampa pityocampa ([Denis & Schiffermüller], 1775) Lymantriidae Calliteara pudibunda (Linnaeus, 1758) Lymantria dispar (Linnaeus, 1758) Arctiidae Eilema complana (Linnaeus, 1758) Euplagia quadripunctaria (Poda, 1761) Aganaidae Asota caricae (Fabricius, 1775) Noctuidae Herminia grisealis ([Denis & Schiffermüller], 1775) (Herminiinae) Hydrillodes moloalis (Walker, 1859) (Herminiinae?) Rivula sericealis (Scopoli, 1763) (Rivulinae) Hypena proboscidalis (Linnaeus, 1758) (Hypeninae) Penicillaria simplex (Walker, 1865) (Euteliinae) Stictoptera cucullioides Guenée, 1852 (Stictopterinae) Catocala fraxini (Linnaeus, 1758) (Catocalinae) Oxyodes scrobiculata (Fabricius, 1775) (Catocalinae?) Panthea coenobita (Esper, 1785) (Pantheinae) Colocasia coryli (Linnaeus, 1758) (Pantheinae) Diloba caeruleocephala (Linnaeus, 1758) (Pantheinae) Camptoloma interiorata (Walker, 1865) (Camptolominae) Maurilia iconica (Walker, 1858) (Chloephorinae) Pseudoips prasinana (Linnaeus, 1758) [ 5 fagana (Fabricius, 1781)] (Chloephorinae) Blenina lucretia (Dalman, 1823) [ 5 accipiens Walker, [1858]] (Sarrothripinae) Blenina quinaria Moore, 1882 (Sarrothripinae) Meganola albula ([Denis & Schiffermüller], 1775) (Nolinae) Meganola strigula ([Denis & Schiffermüller], 1775) (Nolinae) Abrostola triplasia (Linnaeus, 1758) [ 5 trigemina (Werneburg, 1864)] (Plusiinae) Autographa gamma (Linnaeus, 1758) (Plusiinae) Acronicta rumicis (Linnaeus, 1758) (Acronictinae) Cryphia algae (Fabricius, 1775) (Bryophilinae) Sarbanissa sp. (Agaristinae) Heliothis virescens (Fabricius, 1777) (Heliothinae) Noctua pronuba Linnaeus, 1758 (Noctuinae) Hecatera bicolorata (Hufnagel, 1766) (Hadeninae) (b) For the survey of the presence of a ventral cervical gland in the larvae Notodontidae Phalera bucephala (Linnaeus, 1758) Pheosia gnoma (Fabricius, 1776) Stauropus fagi (Linnaeus, 1758) Lymantriidae Lymantria dispar (Linnaeus, 1758) Orgyia sp.