ZYGAENIDAE IN FLUX

Yen, Shen-Horn, Robinson, Gaden S. & Quicke, Donald L. J., 2005, The phylogenetic relationships of Chalcosiinae (Lepidoptera, Zygaenoidea, Zygaenidae), Zoological Journal of the Linnean Society 143 (2), pp. 161-341 : 163-165

THE FAMILY ZYGAENIDAE IN FLUX

The Zygaenidae , colloquially Burnet moths ( Zygaeninae ) and Forester moths (European Procridinae ), is one of the largest families within the Zygaenoidea, estimated to include c. 1200 species worldwide ( Bryk, 1936, Epstein et al., 1999). According to Naumann Tarmann & Tremewan (1999) and Epstein et al. (1999), the current concept of zygaenids is not supported by general morphological features but rather by their ability to synthesize two cyanogenic compounds from the amino acids valine and isoleucine ( Witthohn & Naumann, 1984a, b, 1987a, b; Epstein et al., 1999; Naumann et al., 1999).

The chemical defence ecology of Zygaenidae was first reported by Jones et al. (1962) who demonstrated that HCN is released from crushed tissues of all instars of Zygaena filipendulae , and that the highest concentrations of HCN precursors are found in the eggs. Subsequently, various studies on the biochemical mechanisms, interactions amongst hostplants, moths and their parasitoids, and the relevant morphological structures of several representative genera of Zygaenidae were conducted by a number of research teams. The chemical source of HCN in Burnet moths remained unknown until Davis & Nahrstedt (1979) demonstrated that it is derived from two cyanoglucosides, linamarin and lotaustralin. Linamarin and lotaustralin have long been known to occur in a number of plant families, e.g. Fabaceae , widely utilized as a host plant by the species of Zygaena (see Figs 5 , 6 ). However, the fact that some Zygaeninae live on acyanogenic host plants, but remain cyanogenic, suggests that these insects are capable of synthesizing these compounds de novo.

Although cyanogenesis in the surveyed zygaenid species has been considered to be autapomorphic for this family (e.g. Naumann et al., 1999), a similar chemical defence mechanism is known to exist in its potential sister group, the Heterogynidae ( Zilli, 1987; Zilli & Racheli, 1989; Epstein et al., 1999; Fänger & Naumann, 2001), and the current taxonomic composition of the Zygaenidae remains problematic ( Yen, 2003c). The consistency of apomorphies recognized in previous studies has yet to be tested in a comprehensive study.

The chaotic taxonomic history of Zygaenidae has involved most family groups within the superfamily, as well as various non-zygaenoid groups. When established by Latreille (1809) as Zygaenides, only the wellknown western Palaearctic genus Zygaena Fabricius, 1775 was included in Zygaenidae . Subsequently, the following groups were included in the family, and its concept varied between different authors: Heterogynis (in Zygaenides by Walker, 1854), Syntominae and Ctenuchini of Arctiidae (by Walker, 1854), Procridinae Boisduval, 1828 (as Procridae = Pyromorphina Herrich-Shaffer, 1855), Chalcosiinae Walker, 1864 [1865] (as Chalcosiidae), Charideinae Butler, 1876 (as Charideinae in Arctiidae = Glaucopidae Harris, 1839, Pompostolinae Jordan, 1907 ), Himantopteridae Rogenhofer, 1884 , Phaudinae Kirby, 1892 and Anomoeotidae Hering, 1937 . There were, in addition, two little-known groups, Lactura -group (sensu Kyrki,

Boradia 2 Sciodoclea 3 Isocrambia 4' Aphantocephala 87 1' ' Anarbudas Trypanophora 5 Docleopsis 2' Isocrambia 7' Phlebohecta 5 ' Aphantocephala 8 Thaumastophleps 7 Scotopais 10 Arbudas 10 14 1 Caprima Boradiopsis 9 Euxanthopyge 10 0 Phlebohecta Leptozygaena 16 Pollanisus 15' 17 Hestiochora Doclea 16 Levuana ' 19 Eucormopsis ' Trypanophora 20 93 ' ' Cryptophysophilus 82 21 ' Docleopsis ' Pseudoscaptesyle

1

93 Soritia Cyclosia 23 Histia 22 Cadphises Prosopandrophila ' 23 26 ' Docleopsis 25 Allocyclosia 26 Gynautocera

28 15 ' Trypanophora Pollanisus 30 Callizygaena 31 ' Procris Procotes Aphantocephala

16

' 33 Herpolasia ' 34 ' Clematoessa 35 ' Pompelon 48 ' Herpa basiflava

22 ' 73 44 Heteropan 40 90 Herpa 30 42 Rhodopsona ' 45 Aglaope 55 36 ' Pidorus truncatus

Campylotes 73 Psaphis

36'

Doclea 74 Pseudoscaptesyle

73

Chalcophaedra

74

Caprima 77 ' 71 76 ' Amesia

33 77

Soritia

' 80 ' Doclea 79 ' Prosopandrophila 80 Chalcosia Heteropan Barbaroscia 37 39 Hampsonia 40 ' Corma 41 38 ' Herpa ' 55 Hemiscia 43' Barbaroscia

47

60

36 Pseudonyctemera 46' 52 Pidorus 53 Chalcosia ' 54 ' Pseudoscaptesyle 47 ' Retina 52 Caprima '

56

Eusphalera

37 ' ' 57 ' Eumorphiopais

58 ' 84 Elcysma Pseudonyctemera 47 ' Retina 44 52 ' ' Caprima 56 ' Eusphalera 57 ' Eumorphiopais 46 58 ' ' Allocaprima 59 Chalcosia 8497 Philopator Agalope 47 Retina 60 ' Erasmia 61 64 Eucorma ' 63 Chalcosia 64 ' Amesia 62 66 ' Soritia Eusphalera Heterusia 68 ' Chalcosia 63 ' Milleria 67 ' Chalcosia 71 ' 97

HIMANTOPTERINAE

Anomoeotini ANOMOEOTINAE Dianeurini

Aglaope Aglaopini

Agalope

Boradia

Elcysma

Herpa

Philopator Agalopini Chalcophaedra

Campylotes

Corma

Rhodopsona

Cadphises

Cyclosia Cyclosiini

Hampsonia

Amesia

Anarbudas

Erasmia

Eterusia

Caprima

Chalcosia Docleopsis

Aphantocephala

Erasmiphlebohecta

CHALCOSIINAE

Eusphalera

Gynautocera

Chalcosiini

Histia

Milleria

Pidorus

Pompelon

Prosopandrophila

Psaphis

Pseudoscaptesyle

Pseudonyctemera

Retina

Soritia

Trypanophora

Arbudas

Chalcosiopsis

Heteropanini Eumorphiopais

Heteropan

1984; Common, 1990) and Burlacena -group ( Heppner, 1981), which were transferred from Yponomeutidae and Glyphipterigidae sensu lato, respectively. Consequently, the boundary of Zygaenidae had been extended to include seven subfamilies (see Bryk, 1936; Alberti, 1954; Common, 1970; Scoble, 1992) plus some genera without subfamilial attribution.

When Minet (1986, 1991) started to challenge the traditional classification of the Lepidoptera , he transferred Charideinae to Thyrididae (Thyridoidea) ( Fig. 1C ). He supported Fletcher & Nye’s (1982) viewpoint that Himantopteridae and Anomoeotidae , which are assumed to be related to Megalopygidae + Somabrachyidae ( Fänger et al., 1999) , should be treated as families distinct from Zygaenidae . Eventually, four subfamilies – Zygaeninae , Procridinae , Chalcosiinae and Phaudinae – were retained in Zygaenidae after Minet’s re-arrangement. His proposal that Heterogynidae may be most closely allied to Zygaenidae ( Fig. 1C ) was later followed by Scoble (1992), Naumann et al. (1999), Fänger et al. (1999) and Epstein et al. (1999).

However, the classification proposed by Heppner (1984, 1992, 1998) still lumped Anomoeotidae with Zygaenidae and suggested that the Himantopteridae was the sister group of all the other zygaenid subfamilies ( Fig. 1F ). The Callizygaeninae , as a newly elevated subfamily based on several features of genitalic structures, were separated from Procridinae by Tarmann (1994). Furthermore, Fänger et al. (1999) pointed out that the Phaudinae would probably have to be excluded from Zygaenidae , since this group obviously shared a number of apomorphic characters with the limacodid families; as a result, the inter-subfamilial relationships of the Zygaenidae have become even more contentious. The Lactura -group, which was suggested as belonging to Zygaenidae by Kyrki (1984) and Common (1990), was later established as a new family, Lacturidae , by Heppner (1995) and regarded as the sister group of Zygaenidae by Holloway et al. (2001). As for the Burlacena -group, its taxonomic association has wandered amongst various families ( Glyphipterigidae , Yponomeutidae , Tineidae , Choreutidae ); the Zygaenidae seems to be its current destination, but even this placement is dubious.

In summary, the monophyly of the current concept of Zygaenidae has never been tested cladistically. Scoble’s (1992) placing of the genera Heterogynis Rambur, 1837 and Janseola Hopp, 1923 in Heterogynidae may well be correct. Of the subfamilies Zygaeninae , Procridinae , Callizygaeninae and Chalcosiinae , only the monophyly of Zygaeninae has been established ( Naumann, 1987a, Naumann et al., 1999), although no cladistic analysis is available for any of them. The historical changes of the relationships of zygaenid groups are shown in Figure 1.

Figures

Figure 1. Schematic classifications and phylogenetic concepts of Zygaenoidea and Zygaenidae proposed by different authors. In each of the hypotheses, members of Zygaenidae are in bold and non-zygaenoid groups are in italic. A, Alberti (1954). B, Minet (1986, 1991, 1994). C, Common (1970) and Nielsen & Common (1991). D, Scoble (1992). E, Epstein (1996). F, Heppner (1998). G, Fänger et al. (1999). H, Epstein et al. (1999). I, Holloway et al. (2001).

Figure 5. The two chemically related cyanoglucosides linamarin and lotaustralin are found in comparatively high concentrations in zygaenid moths and form the chemical basis for the evolution of the aposematic and mimicry patterns of this family. The release of hydrocyanic acid (hcn) by chemical decomposition of linamarin or lotaustralin depends on the presence of highly specialized glucosidases and is also ph–dependent (after Naumann et al., 1999).

Figure 6. In the Zygaenidae biosynthesis of the cyanoglucosides linamarin and lotaustralin begins with the universally available amino acids valine and isoleucine, respectively. The cyanoglucosides found in the tissues of most developmental stages of the Zygaenidae are derived from a de novo biosynthesis. Only a relatively small proportion of cyanoglucosides may be plant-derived in species living on cyanogenic hostplants, usually species of Fabaceae (after Witthohn & Naumann, 1987a).