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20. Evolution of Larval Food Preferences in Lepidoptera

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20. Evolution of Larval Food Preferences in Lepidoptera

Jerry A. Powell, Charles Mitter & Brian Farrell

Introduction

The Lepidoptera constitute probably the largest radiation of phytophagous insects (Scoble 1992), rivalled only by the coleopteran clade Phyto- phaga (Chrysomeloidea + Curculionoidea; Crowson 1981). The majority of lepidopteran larvae live at the expense of living seed plants, and virtually all orders of both gymnosperms and angiosperms, as well as ferns, liverworts and mosses, are used. The Lepidoptera date at least to the early Jurassic (1-2), and their major radi- ations probably began by at least the early Creta- ceous, at about the same time as those of flower- ing plants. Moreover, many lepidopteran clades are restricted primarily to particular higher taxa of angiosperms. These facts suggest that the di- versification of lepidopteran lineages might have paralleled, perhaps even been promoted by, that of their hostplants (Ehrlich and Raven 1964), and that the present distribution of Lepidoptera among host taxa might reflect such long-stand- ing interactions.

Comprehensive review of larval foods within major clades of Lepidoptera, however, raises doubt that major features of lepidopteran evolu- tion reflect interactive coevolution, or even par- allel phylogenesis, with plants. Larvae of Lepi- doptera feed on a vast array of substrates. in- cluding not only all kinds of living plant materi- als, but detritus of both plant and animal origin and occasionally living insects. Non-phytopha- gous habits, while in the minority, are found pri- marily in basal lineages of some major clades (e. g. Tineoidea), suggesting that these might have had non-phytophagous ancestors. We focus this necessarily brief review on phytophages and to a lesser extent on detritivores, and will only mention carnivores in passing, where these occur in each group. We refer the reader to the recent comprehensive review by Pierce (1995). A strik- ing generalization may be made concerning the origins of lepidopteran carnivory. Of the more than 200 species in eight superfamilies which are known to be obligate carnivores or parasitoids, nearly all attack only sedentary insects encoun- tered on or near hostplants. With a notable ex- ception in the geometrids, these caterpillars largely feed on scale insects or other homopter- ans and/or ant brood or eggs (see Pierce 1995).

Considering just phytophagous lineages, there is scant evidence for correspondence of lepidop-

I teran phylogeny at higher levels to relationships among major plant groups. Thus, analysis of a general survey of larval food records more than

a decade ago (Powell 1980) showed that while a few primitive taxa are associated with primitive plants (bryophytes, gymnosperms), all the larger superfamilies of both non-ditrysian and ditrysian Lepidoptera feed on a wide variety of angio- sperms. No superfamily or higher taxon of Glos- sata is primarily or even primitively associated with non-flowering plants, though there are spo- radic, clearly secondary transfers to such hosts by unrelated species and genera. Moreover, the differences among lepidopteran taxa in how plants are used are often as pronounced as those in which hosts are used. Larvae may bore in roots, under bark, or in stems; feed on leaves or within them as miners; induce galls or feed within galls caused by other insects or patho- gens; or feed in flowers, fruits or immature or mature seeds. It is possible that the plant-re- source "adaptive zones" in which lepidopteran taxa have radiated are better described by such ecological categories or "horizons" (Powell 1980) than by plant taxonomy or chemistry.

In this chapter we summarize the evidence for and against these contrasting views of feeding habit evolution, focusing on the following ques- tions: I . Does specialized feeding on living plants have a single origin in Lepidoptera, or has it arisen multiple times independently? By what interven- ing stages has it arisen from, or given rise to, non-phytophagous habits? 2. Among phytophagous lineages, to what ex- tent does evolution of host use reflect plant tax- onomy or secondary chemistry, as opposed to other ecological aspects of plant resources'? To what extent do extant host associations reflect parallel cladogenesis or reciprocally interactive coevolution with hostplants?

We examine these questions separately for non-ditrysian and ditrysian lineages, and briefly contrast diet-evolutionary patterns in Lepidop- tera to those in two comparably old phyto- phage clades.

Our review benefits from major advances in paleontology and phylogeny reconstruction, par- ticularly for primitive Lepidoptera, during the past 20 years. However, enormous gaps remain in our knowledge, which impose limits on our ability to draw conclusions. Lepidopteran fossils are scarce compared with those for many hard bodied insects (Labandeira and Sepkoski 1993), larval fossils are virtually non existent, and it is rarely possible to interpret the larval foods of fossil taxa, though leaf miners are an important exception (Labandeira et al. 1994). Hence, recon- struction of the evolution of feeding habits de-

NON-DlTRYSIANS appro*. no. typical larval descr. spp. feeding sitelhabit

Micropterigidae 100 humid forest floor Agathiphagidae 2 seed borers Heterobathmiidae 10 leaf miners

I' Eriocraniidae Acantherop- f l teroctetidae Lophocoronidae

kP Neopseustidae d I Mnesarchaeidae

oY C Hepialo~dea &J

I Nepticulidae

Opostegidae i

Prodoxidae

25 leaf miners 5 [leaf miner]

3 ?? miner 10 ?? miner 6 humid forest floor

500+ underground or in roots or stems

600+ leaf mlners

100 miners- leaves,bark, stems, fruits

100 leaf miners; pupate in case

44 borers- stems,seeds

7 gal formers 1 mine from portable case

80 leaf miners 30 [twig or leaf t~ers]

2)

Jerry A. Powell, Charles

typical larval hosts

bryophytes; herbs; detritus Agathis (Araucariaceae) Nothofagus

90 % on Fagales [Rhamnaceae]

unknown unknown spores; algae; bryophytes generalists (a l r40 fam., esp. Fagales. Rosales (b)Myrtaceae (a) Nothofagus (b)Betulac., Saxifragac., Ranuncul., Polygon., others

217 fam., esp. Corn., Vit.(Holarc.), Myrt. (Aus.)

218 families

(a) Myrt., Proteac; Nothofagus (b) > 12 fam.; some polyphag.

(a)?My rtaceae (b)Rosac., Saxifr., Eric.; Prodoxinae on Agavaceae

Anacardiaceae Cistaceae

Fagac., Rosac., Asterac.,others [Verben.;Proteac.]

Mitter & Brian Fa1

chief distribution

cosmopolitan Aus., S.W . Pacific S. So. Am.

Holarctic

W. No.Am. S. Aus.

S. Asia, S. So. Am. New Zealand cosmop., esp.

Australia (a)cosmopolitan (b) Australia (a)Chile (b)cosmopolitan

cosmopolitan

(a)Afr., So, Am. (b) Holarcbc

(a)Aus., S: So. Am., (b)Holarctic

(a)S. So. Am. (b) Holarctic

S. So. Am; S. Afr.

Europe

mostly Holarctic S. So. Am., Aus.

Afr.

Fig. 20.1. Phylogenetic synopsis of larval feeding habits in primitive moths (non-Ditrysians). Cladogram follows Kristensen and Nielsen (1 -2, 5); sources for within-superfamily phylogeny, and all other information, in text. (a) and (b) denote basal dichotomies within families. Square brackets denote habits inferred from very few observa- tions or species. Habits of Lophocoronidae, Neopseustidae inferred from ovipositor morphology. Except as noted, hosts indicated to family only.

pends largely on phylogenetic inference from liv- ing species. If changes in host are more frequent than speciation, or if species with ancestral hab- its are extinct, such reconstructions may be mis- leading; for example, Van Nieukerken (1986) ar- gued that in Nepticulidae, many extant primitive genera may have derived hostplant preferences.

A second limitation is the preliminary state of knowledge of extant larval feeding habits, espe- cially for tropical and Southern Hemisphere fau- nas. Probably 75'2'0 of available larval food re- cords for Cepidoptera come from temperate zones, while as many as 75%) of the described species of Lepidoptera may be tropical (Heppner 1991), with the true disparity undoubtedly still greater. Given the floristic differences among re- gions, this bias may seriously affect our recon- structions of evolutionary patterns. For example, plants in the relatively derived orders Fagales, Rosales and Asterales appear to dominate lepi- dopteran host associations (our plant classifica- tion follows Cronquist [I9811 unless otherwise noted). But this may be in part an artifact of the predominance of these taxa in the Holarctic (e. g. Van Nieukerken 1986): Fagales and Rosales, at least, are much less conspicuous elements in the Southern Hemisphere flora.

A third problem is the rudimentary under- standing of phylogeny in most groups, particu- larly in the Ditrysia. Lacking detailed phyloge- nies, we may be tempted to assume that taxo-

nomically widespread or numerically predomi- nant habits represent the groundplan, a poten- tially misleading inference. Because uncertainty about phylogeny often can be traced to igno- rance about tropical and southern continent forms, inferences about ancestral feeding habits cannot be made with confidence. For example, the major obstacle to understanding of relation- ships within the Tortricoidea (Horak and Brown 1991) is insufficient knowledge of critical taxa from the Malayan-Papuan region and southern South America, areas for which we also have al- most no larval food data.

Phylogeny of Lepidopteran Feeding Habits: a Synopsis

Our review of major trends in the evolution of feeding habits emphasizes the basal lepidopteran grades and is not exhaustive; detailed accounts for individual groups are given elsewhere in this volume. With exceptions to be noted, we follow the phylogenetic arrangement and nomenclature of Nielsen (1989), as updated by Kristensen (1 -5). Phylogenetic uncertainties are discussed when these affect possible interpretations of feeding habit evolution. The synopsis below is mapped in summary form on a cladogram (Figs. 20.1, 2, 3) in hopes of facilitating critical discus- sion of evolutionary hypotheses.

Evolution of Larval Food Preferences in Lepidoptera

BASAL DlTRYSlANS typical larval

approx. no. feeding TINEOIDEA descr. spp. sitelhabitat typical larval hosts

Tineidae 2300 detritivory widespread, probably primitive - Eriocottidae 200 probably detritivorous Acrolophidae 250 detritivorous Psychidae 1000 feed inside case polyphagous on living plants; some

GRACILLARIOIOEA ~cavengers,lichenivores , Gracillariidae 1600 leaf miners >80 fam., esp. Fagac., Fabaceae

I Bucculatricidae 200 leaf miners >20 fam., esp. Asterac.. Fagales . Roeslerstammidae >PO miners; extern. Epacrid.,Proteac., Elaeoc., in later instars Fagac.; some polyphages

Douglasiidae 25 miners herbs., esp. Rosac., Borag., YPONOMEUTOIOEA Hydrophyll. ,. Acrolepiidae el00 facultat. leaf miners, 5 farn., esp. Aster., Solan.,Liliac.

skeletonizers . Argyresthiidae 160 leaf miners; later instars >13 farn.; 40% on conifers, 25% on in silken shelters Rosaceae ' Yponomeutidae 900 extern. foi~vores 50 fam., incl. ferns, gymnosp.

I Ochsenheimeriidae miners, borers monocots, esp. Poac. I Heliodinidae 50 facultat. miners diverse dicots.; 50 %on

Caryophyllales , Glyphipterigidae 400 stem & seed miners monocots, esp. Cyper., Junc.

Lyonetiidae 250 leaf mineis >27 fam.; a few polyphagous GELECHIOIDEA - Stenomatidae 1200 leaf tiers, 16 fam., mostly woody; esp. Myrt.

I ext. feeders (S. Hemisph. Fagales (Nearc). Ethmiidae 250 within or on flowers, Boraginales (8b%) -- buds, or leaves Depressariidae 600 hers, rollers, lvs, > 17 farn., esp . Apiac., Asterac.

J flowers, seeds Elachistidae s.s. 250 leaf or stem miners monocots (89%); primitive

1 genera on Asteridae t Agonoxenidae 95 borers, miners, Rosaceae,

webbers Arecaceae, others Xyiorictidae 500 leaf, bark feeders from >20 fam., esp. Proteac.. Myrt.

stem tunnels, tied leaves, etc.

I Scythrididae 370 ext. feeders, leaf 220 fam, esp. Aster., Cistac. J tiers, miners in Holarctic' some polyph.

Chimabachidae 6 tiers, rollers,lvs, flwrs [polyphagousj

A Oecophoridae 3000 case makers; most eat Myrtaceae in Australia dead lant material

Stathmopodidae 150 mncea& feeders, in plant refuse or on living plants Lecithoceridae 500 feed on leaf liner

Batrachedridae 125 live plants; scavengers diverse Coleophoridae 1400 leaf miners; from portable >30 fam., woody & herbac., incl.

case in later instars Aster., Betul., Rosac.. Juncac. Momphidae 60 miners, gallers Onagraceae (66%) Blastobasidae 300 mostly detr~tivorous Pterolonchidae 8 [root borer], , [Asteraceael Symmocidae 170 mostly detrltlvorous Peleopodidae 25 [leaf webber] [Verbenac., Malpighiac.,others] Cosmopterigidae 1200 miners, gallers. tiers, >35 farn., esp. Poac., Fabac.

scavengers Gelechiidae 4000 miners, borers, gallers, >80 fam., incl. Pinac., Myrt.,

ext. feeders & others monocots,mosses, ferns APODITRYSIA (Figure 3)

chief distribution

cosmop., mostly tropical Oriental. Ethiopian New World, mostly tropical cosmop.; 90% O.W.

cosmop.

cosrnop., 75% N. Hemisph. Palearc., Orlent., Aus.

mostly Holarctic

Holarc., Neotrop., Hawaii

mostly Holarctic

mostly Holarctic Palaearctic mostly New World

cosrnop., primarily tropical cosmop.

cosmop.; 90% Neotropical

cosmopolitan, esp. Neotrop

cosmopolitan

cosmop., esp. New World

cosmopolitan

Oriental, Australian

cosmop.; mostly Holarctic

Palaearctic

cosmop., esp. Australra

cosmop., esp. tropics most Austr., Oriental

cosmopolitan cosmop.; 82 % Holarctic

mostly Holarctic

cosmop., esp. New World Palaearctic; S. Africa cosmop., esp. Palaearctic cosmopolitan

COSmOpOlitan

cosmopolitan

Fig. 20.2. Phylogenetic synopsis of larval feeding habits in primitive Ditrysians. Sources for phylogenetic hypothe- ses in text. Sources for data in this and subsequent figure, when not referenced in text, include: Heppner 1991; Hodges 1974, 1978, 1-9; Munroe 1982; Powell 1980; Scoble 1992; Stehr 1987; M. A. Solis, pers. comm. Square brackets denote habits inferred from very few observations or species. Except as noted, hosts indicated to family only.

Editor's note: The names Zeugloptera, Aglossata and Heterobathmiina have purposely been retained in this chapter, though they are discarded in the preced- ing systematics accounts (1 -2, 1-3, 1-4).

CLADE ZEUGLOPTERA MICROPTERIGOIDEA. Micropterigidae live in humid forest floor habitats. Their distribution appears relictual, cosmopolitan with highest ge- neric and species diversity in the Palaearctic, western Pacific, and Australian regions (Hepp- ner 1991).

Traditionally micropterigid larvae have been characterized as specialists on bryophytes s. I. (e. g. Imms et al. 1957, Powell 1980, Tuskes and

Smith 1984). Recent reports, however, indicate restriction of the Sabutinca group to bryophytes but feeding on a wide range of foods in Micro- pterix, including herbaceous angiosperms, gras- ses, and plant detritus (Lorenz 1961, Carter and Dugdale 1982, Kristensen 1984, Davis 1987, Cornmon 1990, Nielsen and Common 1991). The adults eat pollen and spores (Nielsen and Com- mon 1991).

CLADE AGLOSSATA AGATHIPHAGOIDEA. Agathiphagids are known from just two species, in Queensland and islands of the southwest Pacific. The blind, apodous lar- vae develop within the seeds of Agathis (Araucar-

Evolution of Larval Food Preferences in Lepidoptera

caceae (Davis 1978; Powell 1980). The life cycle, timed around the early-spring availability of new leaf tissue for larval development, resembles that of heterobathmiids (Kristensen and Nielsen 1983).

ACANTHOPTEROCTETOIDEA. Acanthopteroc- tetidae consist of five species in western North America (Davis 1978), and Catapterix Zaguly- aev & Sinev (1988) in Crimea, which has been treated as a separate family (Scoble 1992) but should be assigned here (N. P. Kristensen pers. comm.). The larva of one Californian species has been described, a leaf miner in Ceunothus (Rhamnaceae) (Davis and Frack 1987).

Larval habits of Lophocoronidae and Neo- pseustidae are not known, but possession by these families of a piercing ovipositor, similar (especially in Lophocoronidae) to that of Eri- ocraniidae and Acanthopteroctetidae, suggests that they are endophagous (Common 1990, Davis 1975, Kristensen, 1-5).

CLADE EXOPORIA MNESARCHAEOIDEA. Mnesarchaeidae, one of two sister lineages making up the Exoporia, are

J known only from six New Zealand species found in the periphyton layer of moist forest floors

I characterized by mosses and liverworts. The lar- vae are unspecialized, exophagous feeders that appear to be generally phytophagous, feeding on fern sporangia, fungal spores, and algae in addi- tion to bryophytes (Gibbs 1979).

HEPIALOIDEA. Families in the other exoporian lineage, Hepialoidea, need redefinition (Scoble

I 1992), as there are several genera, mostly South-

! ern Hemisphere with unknown larval biologies, whose placement is unclear. The Hepialidae s. str. are the most diverse group of non-hetero- neurans, with more than 500 described species, distributed in all faunal regions. Australia, with more than 100 species, is the center of diversity (Common 1990). The larvae, at least in late in- stars, form tunnels in sod or in soil and feed ex- ternally on roots or surface vegetation, or tunnel

t into roots or trunks of woody plants. A few spe- cies appear to be specialists on mosses (Grehan and Patrick 1984), ferns (McCabe and Wagner 1989), grasses (Pinhey 1975) or woody plants such as conifers (Wagner et al. 1991) or Myrta- ceae (Common 1990), but these are exceptional. Although hepialid species have been recorded in older literature feeding on a wide variety of an- giosperms, recent detailed studies have led to the conclusion that most hepialids are generalists (Grehan 1984, 1989; Wagner 1989), and often detritivorous or mycophagous in early instars, graduating to roots or stems of vascular plants in later instars (Grehan 1981, 1987, 1989). Gen- eralist feeding probably is ancestral (Grehan 1989).

CLADE HETERONEURA The remaining superfamilies make up the Heter- oneura (Scoble 1992), relationships within which are not definitively settled. Basal members of the clade possess a piercing ovipositor by which the eggs are inserted into plant tissue, where endoph- agous larval feeding occurs, at least by early in- stars.

NEPTICULOIDEA. This superfamily consists of the sister families Opostegidae and Nepticulidae. Larvae of Nepticulidae typically are miners in mature leaves of woody angiosperms, though some are stem miners or petiole gall formers. The primitive Australian Pectinivalvinae, which feed on Myrtaceae (Common 1990), appear to be sis- ter group to the cosmopolitan remainder of the family (Van Nieukerken 1986). The latter are re- corded from over 40 angiosperm families, with a preponderance of records for Fagales and Ro- sales in the Holarctic (Powell 1980, Van Nieuker- ken 1986, Fig. 1). The larger genera are not asso- ciated with particular plant lineages, but several smaller subgenera are almost completely limited to one plant family, such as Anacardiaceae, Poly- gonaceae, Fabaceae, or Cistaceae (Van Nieuker- ken 1986).

A late Jurassic or early Cretaceous leaf mine on a fossil seed fern in Australia was interpreted by Rozefelds (1988) as lepidopteran and possibly nepticulid. The mine form is comparable to some modern Nepticulidae, but this fossil may actually be a dipteran rather than a lepidopteran; see also 1-2. Mid Cretaceous (97 mya) mines in leaves of Magnoliidae (Lauraceae), Hamamelidae (Platanaceae), and Rosidae have been identified as representatives of two extant genera of Nepti- culidae (Labandeira et al. 1994), and there are late Cretaceous nepticulid mines in Fagales (Skalski 1979, Van Nieukerken 1986).

The larvae of Opostegidae form subcutaneous mines, sometimes in bark, stems or fruit, on vari- ous angiosperms (Powell 1980, Davis 1987). The Chilean Notiopostega, proposed as sister group to the bulk of this cosmopolitan family, mines the cambium layer in trunks of Nothofagus (Carey et al. 1978, Davis 1989). Other genera mine leaves of Rutaceae (several Hawaiian spe- cies), and stems of Betulaceae, Saxifragaceae, Ranunculaceae and Polygonaceae in the Ho- larctic.

INCURVARIOIDEA. Relationships among the six families of this superfamily were proposed by Nielsen and Davis (1985). Foodplants are diverse and larval biologies vary. Later instars of some genera construct a portable case in which pupa- tion (Heliozelidae) and larval feeding (some In- curvariidae, Adelidae) take place. Strictly en- dophagous larvae that form no case (Cecidosi- dae, derived Prodoxidae) are believed to be de- rived (Nielsen and Davis 1985, Wagner and Pow- ell 1988).

Jerry A. Powell, Charles Mitter & Brian Farrell

Heliozelidae, with about 100 described and many described species, occur in all faunal re- gions. They are leafminers in at least 17 angio- sperm families, with numerical preponderance in Vitaceae and Cornaceae in the Holarctic and Myrtaceae in Australia (Common 1990; Powell 1980, unpublished data from Costa Rica).

Adelidae include 270 species (Heppner 1991). The basal dichotomy appears to lie between a mainly Southern Hemisphere Nematopogon group of genera, and the primarily Holarctic Ad- ela group, which are considered more derived (Nielsen 1980). In Adela, larvae feed at first in immature seeds, then in fallen leaves from a por- table case. Oviposition by each species is specific to one or two closely related plant genera (Pow- ell 1969). Hosts include at least 18 angiosperm families, with no strong numerical or geographi- cal emphasis on one or a few, although Cauchas, apparently the most basal lineage of the Adela group, specializes on Brassicaceae (Powell 1980). Nematopogon species evidently are non-specific in oviposition preferences and feed mainly on leaf litter, but the biologies are poorly known. The few host records for other members of the Nematopogon group are from Fabaceae in Africa and Australia (Janse 1945, Common 1990).

The single, European species constituting Cri- nopterygidae (Nielsen and Davis 1985) feeds on Cistaceae, mining from a portable case in the manner of coleophorid Gelechioidea (Petersen 1978).

Incurvariidae comprise a worldwide group of about 135 species, 80% Palaearctic and Austra- lian (Heppner 199 l). Some genera mine through- out larval life, while others leave the mine to feed in later instars on fallen leaves (Davis 1987, Common 1990). The basal, southern continent groups specialize on Myrtaceae and Proteaceae, while the more derived, Holarctic genera use about 10 unrelated angiosperm families. A few species are polyphagous (Nielsen 198 1, 1982, Nielsen and Davis 1981, Powell 1980, Scoble 1980).

Cecidosidae (including Ridiaschinidae, Niel- sen and Davis 1985) are southern South Ameri- can and southern African; the larvae cause galls on Anacardiaceae, in which the apodous larvae feed throughout growth (Powell 1980).

Prodoxidae are Holarctic, except for the southern South American Prodoxoides, which appears to be sister group to the rest of the fam- ily (Nielsen and Davis 1985). The biology of Pro- doxoides is unknown, but it is believed to be as- sociated with Myrtaceae. Basal genera of the Ho- larctic clade specialize on Rosaceae, Ericaceae, and Saxifragaceae (Davis et al. 1992). The more derived genera (yucca moths and allies = Pro- doxinae of Davis 1987) are entirely endophagous feeders on Agavaceae, the only non-ditrysians to adapt to monocots (Powell 1992). Molecular data indicate that this shift to monocots and the

correlated behavioral/morphological diversifica- tion of the prodoxine genera occurred over a brief interval during the Tertiary (Brown et al. 1994).

TISCHERIOIDEA. Tischeriidae are primarily Ho- larctic, with about 70 described species (1-6). The larvae make stout, silk-lined mines in which pupation occurs. They are reported on seven host plant families, primarily Fagaceae, Rosa- ceae and Asteraceae (Braun 1972; Powell 1980); a few species feed on annual herbs (Davis 1987).

PALAEPHATOIDEA. Palaephatidae consist of five genera in southern South America and one in Australia (Davis 1986; Nielsen 1987), totalling about 30 species. A single larva observed in Ar- gentina spun together the twigs of a verbena- ceous shrub (Davis 1986) and may have fed on dead leaves, while in Australia one larva was found between leaves of Proteaceae (Common 1 990).

DITRYSIAN CLADE Phylogenetic relationships within Ditrysia, which includes 98% of the described Lepidoptera spe- cies, are not well resolved. Following Nielsen (1989), and with exceptions to be noted, we adopt the definitions of families, superfamilies and several more inclusive groups proposed or accepted by Minet (1986, 1990, 1991). The most inclusive of these clades is the Apoditrysia (1-2), and within it, the Obtectomera (Fig. 3), consisting of those apoditrysians with both a non-motile pupa at eclosion and a modified pul- villus. While this scheme is tentative, there seems little doubt that the non-apoditrysian groups, Ti- neoidea, Gracillarioidea, Yponomeutoidea, and Gelechioidea, are the most primitive (Fig. 20.2); our arrangement of these follows Kristensen (1 -2). Because of the enormous diversity of Dit- rysia, we attempt only a brief overview, particu- larly in Apoditrysia, with focus on a few groups in which recent phylogenetic studies alter the pic- ture of feeding habit evolution, since Powell (1980).

PRIMITIVE (NON-APODITRYSIAN) SUPERFAMlLIES TINEOIDEA. We follow recent restrictions on the definition of tineoids, including removal of Lyo- netiidae (s. s.) and Ochsenheimeriidae to Ypono- meutoidea (Kyrki 1984, 1990), and proposal of the superfamily Gracillarioidea for the leaf-min- ing gracillariid-bucculatricid set of families (Davis 1988, cited in Nielsen 1989; Robinson 1988; Minet 1991). Relationships shown among the remaining families (Fig. 20.2) follow Robin- son (1988) and Robinson & Nielsen (1993).

Evolution of Larval Food Preferences in Lepidoptera

Tineidae include some 3,500 described species, mostly tropical (Heppner 1991. Robinson and Nielsen 1993). Feeding habits vary considerably among the 15 subfamilies recognized by Robin- son and Nielsen (1993), but generalized fun- givores/detritivores occur in all the major sub- families and probably represent the ancestral condition (Robinson and Nielsen 1993). As sum- marized by Robinson and Nielsen, Powell (1980), and Davis (1987), Tineinae tend to be as- sociated with mammals or social insects, and their larvae are often keratophagous or coproph- agous, although many are detritivores, and some consume ant brood (Pierce 1995); Nemapogoni- nae and Scardiinae mostly specialize on wood- rot fungi, especially Polyporaceae (Lawrence and Powell 1969); many or most Meessiinae prefer lichens; Setomorphinae tend to feed on dead plant matter; Hieroxestinae feed mostly on fungi or dead plant materials but sometimes on living plants, while members of one genus are coproph- agous in caves (Robinson 1980, Zimmermann 1978); and many Myrmecozelinae are detriti- vores and live in grass turf (Zagulyaev 1971), caves, or mammal burrows (Davis et al. 1986, Robinson 1980).

Larvae of Eriocottidae, a family of about 200 primarily Oriental and Ethiopian described spe- cies (Heppner 1991), are thought to be detriti- vores, perhaps endophagous in decaying wood or leaf litter (Common 1990, Davis 1990 citing Zagulyaev, Nielsen 1978).

There are 250 -t described species of Acro- lophidae in a single New World, mostly tropical genus. The few known larvae are detritivorous, feeding from tunnels in grass turf and sugarcane, or in polypore fungi (Davis 1990); one species is coprohagous and detritivorous in tortoise bur- rows (Davis and Milstrey 1988).

Psychidae are cosmopolitan (90% Old World), numbering about 800 described species (1-7). Many species in the more primitive subfamily Taleporiinae feed on lichens, some live in ant nests where they are presumed to be scavengers, and others are polyphagous on trees and shrubs. Most Psychinae evidently are generalist herbi- vores, some moving from initial herb feeding to shrubs or trees in later instars (Common 1990, Davis 1987, Powell 1980).

GRACILLARIOIDEA. Gracillariidae make up the most species rich family of predominantly leaf mining Lepidoptera: the 1,600 described spe- cies undoubtedly represent fewer than half the total. Most are specialists on one or a few closely related plant species, usually woody angio- sperms, and at least 80 families of hosts are re- corded (Common 1990, Powell 1980). There is no strong preference for particular plant taxa by any of the three subfamilies. On a world basis, Fagaceae and Fabaceae are most often recorded (Powell 1980), but records are generally lacking

for tropical regions. Larval mines identified as phyllocnistine Gracillariidae have been described from mid Cretaceous (97 mya) Magnoliidae of three genera representing two families (Laban- deira et al. 1994). This is by far the earliest re- corded instance of ditrysian leaf mining.

Bucculatricidae are a monogeneric leaf mining family with about 175 described species (1-7), occurring in all geographical regions, 75% in the Northern Hemisphere (Heppner 1991). Host- plant records that were summarized with Lyo- netiidae (Powell 1980) represent one gymno- sperm and 20 angiosperm families, predomi- nantly Asteraceae (45%) and Fagales (23%), do- minated by Nearctic records.

Roeslerstammiidae (= Amphitheridae) are found in the Palaearctic, Oriental and Australian regions. The larvae mine in leaves in early in- stars, then feed externally from a slight web or fully exposed, on Epacridaceae, Proteaceae, Elaeocarpaceae and Fagaceae (Common 1990). Roeslerstammiu in Europe is polyphagous (Kyrki 1983 a).

Douglasiidae comprise about 25 Holarctic species plus one each in the Orient and Australia (Heppner 1991). We follow Davis (1988) and Mi- net (1991) in treating them as Gracillarioidea; ti- neoid, yponomeutoid and other affinities also have been proposed. The larvae mine herbaceous angiosperms, primarily Rosaceae and Boragina- ceae -~ydro~h~ l l aceae (Powell 1980, Scoble 1992).

YPONOMEUTOIDEA. This superfamily has been redefined recently. Kyrki (1983 b, 1984) recog- nized lineages, though not defining families, that represent Acrolepiidae, Argyresthiidae, Lyonetii- dae (s. s.), Heliodinidae, Yponomeutidae (includ- ing Plutellidae), and Ochsenheimeriidae. Minet (1986) added to this list Glyphipterigidae (in- cluding Orthotelidae, Kyrki and Itamies 1986), which had been placed in Copromorphoidea, but subordinated Acrolepiidae and Argyresthiidae to Yponomeutidae. Kyrki (1990) again revised the taxonomic status of the groups (1-B), but the characters employed in his cladistic analysis need reevaluation; the separation of Ypsolophidae from Plutellidae in particular seems unwar- ranted.

Acrolepiidae are a mostly Holarctic group of 80 + species, also occurring in the Neotropical region and in Hawaii (Gaedike 1984, Heppner 1987, 1991, Zimmerman 1978). The larvae are facultative leafminers or skeletonize the leaf sur- face from slight webs, using plants of five un- related families, with 30% of the records from Asteraceae (Europe), 26'1/0 Solanaceae (Neotropi- cal and endemic species in Hawaii), and 30%) Liliaceae (Holarctic) (Gaedike 1984, records in- cluded in Yponomeutidae by Powell 1980, Zim- merman 1978).

Jerry A. Powell, Charles Mitter & Brian Farrell

Argyresthiidae (Yponomeutidae, Argyresthii- nae, 1-8) include about 160 species, primarily Holarctic. The larvae are leafminers in early in- stars, usually leaving the mines to form silken shelters in new foliage. Some conifer-feeding spe- cies remain in the mines until maturity. At least 13 gymnosperm and dicot families are used by monophagous or oligophagous species of Argyr- esthia; more than 40% of recorded species use conifers, 26% Cupressaceae, the highest propor- tional adaptation to conifers by any moth family. Nearly 25% specialize on Rosaceae in the Pa- laearctic (Moriuti 1977, Powell 1980).

Heliodinidae are mostly New World moths; there are 75 + described species, more than half Neotropical, with a few from other tropical areas and Australia, and a considerably larger fauna is likely (Common 1990, Heppner 1991, Y.-F. Hsu unpubl. data, Powell 1991). The larvae often feed on thick-leaved plants such as Abronia (Nyctagi- naceae) in facultative mines. Knowledge of food- plants has been increased greatly during recent studies by Y.-F. Hsu. There are larval food re- cords for 32 mainly Holarctic and American sub- tropical species, from several unrelated dicotyle- donous families, with pronounced specialization on Caryophyllales (kzoaceae, Chenopodiaceae, Nyctaginaceae, Portulacaceae) (Powell 1980, 1991, Hsu and Powell unpubl. data).

Glyphipterigidae include nearly 400 described species distributed in all faunal regions, primar- ily at lower latitudes (Heppner 1982, 1991, Com- mon 1990). The larvae of most species feed in stems and seeds of Cyperaceae, Juncaceae and other monocots (Heppner 1985, Powell 1980), though a few use herbaceous Asteraceae.

Yponomeutidae (including Plutellidae and Yp- solophidae of Kyrki 1990, 1-8) as defined by Minet (1986) number nearly 900 species, and oc- cur in all geographical regions. The larvae are external feeders on leaves, living communally in some genera. Plants in at least 50 families are used, including a fern (Cyathaceae) and a gym- nosperm (Podocarpaceae) in New Zealand, other gymnosperms (Ephedraceae, Cupressaceae, Pi- naceae) in the Holarctic, monocots (Cyperaceae, Poaceae), and Proteaceae and Myrtaceae in the Indo-Australian region. There is a predominance of records from Brassicaceae, Cupressaceae, Fa- gaceae, Celastraceae, and Rosaceae, especially the last two, in the Holarctic (Moriuti 1977, Powell 1980).

Lyonetiidae s. str. (1 -8) are widely distributed and include about 250 described species (Com- mon 1990, Heppner 1991). The larvae are leaf- miners in at least 27 families of angiosperms, with no concentration on any one or a few re- lated families. A few species use monocots; a few in the Holarctic are polyphagous (Common 1990, lyonetiid records other than Phyllocnistis and Bucculutrix from Powell 1980). About 17'!40

of 75 records are Fabaceae, mainly in the western Palaearctic, India, and Japan.

GELECHIOIDEA. This is the largest superfamily of lower Ditrysia by far, and the species numbers may rival those of Noctuidae and Pyralidae be- cause vast numbers of species remain unde- scribed. In better known temperate faunas (Aus- tralia, Europe, and probably the Nearctic), Gel- echioidea are more species rich than any other superfamily. Although there is agreement on the phylogenetic integrity of the superfamily (Com- mon 1990; Hodges 1978 and 1-9, Minet 1986, 1990, 1991), there have been wide differences of opinion on the number and composition of in- cluded families and their relationships (e. g. Kuz- netsov and Stekol'nikov 1979, Minet 1990, 1-9). As a result, analysis of gelechioid larval substrate evolution is tentative. Recent studies have begun to agree on major lineages. Minet (1990) distin- guished a clade consisting of Oecophoridae s. str. and allies, and an unresolved residual assem- blage including Elachistidae, Gelechiidae and others, while Hodges (1-9) proposes a broader oecophorid assemblage and a more restricted elachistid assemblage. Our nomenclature follows Minet (1990), except that we retain family status 1 for several biologically distinctive groups in- cluded as subfamilies in Elachistidae, Xyloricti- dae, or Coleophoridae by Minet or Hodges, such 1 as Stenomatidae, Ethmiidae, Agonoxenidae, Scythrididae, and Blastobasidae. Our arrange-

1 1

ment (Fig. 20.2) follows Hodges (1-9). 1 In the subset of the oecophorid clade con-

sisting of Oecophoridae s. str. and its nearest rel- atives (Fig. 20.2), detritivory is predominant among the basal lineages and is possibly primi- tive. Oecophoridae s. str. are a dominant group in Australia (ca. 1,850 described species in 250 + genera, Common 1994), a radiation that Com- mon (1990) attributes to exploitation of the highly diverse Myrtaceae flora, particularly the persistent leaf litter; 95% of the larval food re- cords are for living (28%) or fallen leaves of Myrtaceae (Common 1990, 1994; Australian re- cords in Powell 1980 from Common pers. comm.). Elsewhere, at least 25 dicot families are eaten, but nearly half the records represent det- ritivory, on bark or wood of dead trees, plant refuse, wood-rot fungi, ground litter, or stored products (Powell 1980). Larvae of Stathmopodi- nae live in fallen leaves, fruit or other decaying vegetable matter, on living plants, usually in cat- kins (including Araucariaceae), galls, fruits, seed heads, bark, or as predators of scale insects (Common 1990, Powell 1980). Lecithoceridae in Australia resemble Oecophoridae in feeding on leaf litter beneath Myrtaceae and grass tussocks (Common 1990). Blastobasidae (Coleophoridae, Blastobasinae, 1-9) and Symmocidae (Autos- tichidae, Symmocinae, 1-9) as well as the re- maining Autostichidae sensu Hodges (1-9) are

Evolution of Larval Food Preferences in Lepidoptera

also mostly detritivorous (Adamski 1989, Powell 1976a, 19801, though some prey on scale insects (Pierce 1995).

The remaining gelechioids, including the rest of the oecophorid clade and the elachistid assem- blage (Elachistidae of Hodges, 1 -9), are primar- ily living plant feeders. Scythrididae (Xyloricti- dae, Scythridinae, 1-9) include 370 described species mostly from the western Palaearctic, and probably 400 + undescribed species in the Nearc- tic (Landry 1991). Larvae of only a small frac- tion of species are known, but at least 20 families of angiosperms are used. Cistaceae and Astera- ceae dominate Palaearctic records; a few species use Poaceae, lichens, or mosses (Bengtsson 1984; Landry 1991; Powell 1980). Polyphagy may be more prevalent than the scattered records indi- cate (Powell 1976 b). The cosmopolitan Coleoph- oridae (Coleophorinae, 1 -9), with about 1,400 described species, 82% in the Holarctic (Heppner 199 1 ), and 500 + undescribed Nearctic species (J.-F. Landry, pers. comm.), feed on more than 30 families of angiosperms. The major host taxa are shared with those of the more primitive leaf mining moths, especially Betulaceae, Rosaceae, and Asteraceae. Many coleophorines use Junca- ceae (Powell 1980), and some feed on scale in- sects (Pierce 1995).

Gelechiidae, with more than 4,000 described species (Heppner 1991) and probably at least as many more known that are undescribed, feed on an extremely diverse array of plants, with more than 80 families recorded, especially Fabaceae and Asteraceae, with appreciable numbers using Pinaceae, Myrtaceae, monocots, and a few on mosses and ferns (Powell 1980).

Stenomatidae (Elachistidae, Stenomatinae, 1-9) are richest in the Neotropical Region (90% of 1,200 described species; Heppner 1991), and foodplants are therefore poorly documented, but larvae been recorded on at least 16 angiosperm families, predominantly Myrtaceae (Southern Hemisphere) and Fagales (Nearctic).

Lesser clades within Gelechioidea, probably derived, specialize on derived kinds of angio- sperms. Examples include Elachistidae (Elachis- tinae, 1-9) on monocots (89%); Cosmopterigi- dae (Cosmopteriginae, 1-9) on monocots; Momphidae (Coleophoridae, Momphinae, 1-9) on Onagraceae (70% +); and Ethmiidae (Elachi- stidae, Ethmiinae, 1-9) on Boraginales (Hydro- phyllaceae, Ehretiaceae, Boraginaceae) (80°/0) (Powell 1980, 1983, Janzen and Powell, unpubl. data from USA and Costa Rica). Momphidae and Cosmopterigidae also contain several preda- tors of scale insects (Pierce 1995).

APODITRYSIAN CLADE (1-2; Fig. 20.3) Primitive (non-obtectomeran) apoditrysians are nearly all living plant feeders. Many have adopted leaf tying or other forms of partial con-

cealment, but there are also clades of both borers and external leaf feeders (Fig. 20.3). We com- ment only on selected major groups.

COSSOIDEA. Cossidae, often regarded as rela- tively primitive, number about 670 described spe- cies and are cosmopolitan but predominantly tropical. Few life histories are known because the larvae are borers in root crowns and stems, but cossids appear to have broad host preferences. More than 20% are known to be polyphagous, and many others recorded from only one or two hosts probably are generalists too. Recorded hosts of specialist species span 17 families, in- cluding one monocot, with woody legumes ac- counting for 25% of recorded species (Common 1990; Powell 1980).

TORTRICOIDEA. Tortricidae, which constitute the largest non-obtectomeran, apoditrysian su- perfamily, exhibit a great range of larval habits (Horak and Brown 1991, Powell 1980), and an- cestral detritivory is possible. The family con- tains more than 6,600 described species, and is well represented in both temperate and tropical regions (Heppner 1991). Phylogenetic relation- ships among the three subfamilies are uncertain, but the Tortricinae, probably not monophyletic, appear to contain the most primitive tortricids. Larval feeding in the Indo-Australian tortricine tribe Epitymbiini is almost entirely restricted to leaf litter, especially of Myrtaceae (Common 1990). Based on the Epitymbiini and unpub- lished observations of other unrelated but primi- tive species, Horak and Brown (1991) postulated that detritus or mycelium feeding by a free-living larva was the ancestral tortricid trait. However, extant members of the morphologically primitive tortricine tribes Phricanthini and Schoenotenini are phytophagous (Powell and Common 1985), as are nearly all Tortricini (Razowski 1966). No Tortricini are known to be detritivores, but some African species related to Accra, considered by Razowski (1966, 1981) to be primitive, feed on scale insects (Lamborn 19 14, Ghesquiere 1940). Hence, this hypothesis awaits rigorous phylo- genetic testing.

Among phytophagous tortricids (the great majority), external feeding probably is primitive, with independent origin of root, stem, cone and seed borers in at least three tribes in all three subfamilies (Horak and Brown 1991). Among external feeders there appears to be a trend to- ward polyphagy, correlated with a transforma- tion series in oviposition behavior (Powell 1964, Powell and Common 1985). In Phricanthini, Schoenotenini, Tortricini, and Cochylini, the eggs are laid singly and most species are special- ized feeders. The Phricanthini are recorded only from Dilleniaceae, and in Tortricini and Cochyl- ini only 17%) and 11%1 of species, respectively, use hosts in two or more plant orders (data from Common 1990, Horak and Brown 1991, Powell

Jerry A. Powell, Charles Mitter & Brian Farrell

1980, Powell and Common 1985). In contrast, in tribes that are believed to be more derived, eggs are laid in imbricate masses, and larvae are more often polyphagous. Thus, analysis of larval foods for about 900 species of Tortricinae (Brown and Powell 1991; Common 1990; Powell 1980, 1985, unpubl. data) reveals that polyphagy is common in Sparganothidini (70%) + others recorded only once) and Archipini (36%); Atteriini are proba- bly also generalists, as species in three genera have been reared on synthetic diet, which nor- mally is not accepted by host-specific tortricids. The proportions of generalists in these three tribes are far greater than in any other phytopha- gous non-obtectomeran Ditrysia.

Apart from Phricanthini and Epitymbiini, all tortricid tribes use a wide diversity of angio- sperms and gymnosperms (Horak and Brown 1991; Powell 1980; Powell and Common 1985), with no predilection for one plant subclass or order shown by any tribe or any species rich genus.

OBTECTOMERAN CLADE Within Obtectomera, we follow Minet's (1991) provisional recognition of the clade Macrolepi- doptera, following Scott (1986). The non-macro- lepidopteran obtectomerans are primarily con- cealed feeders in living plants. However, there is extensive detritivory in the largest superfamily, Pyraloidea.

PYRALOIDEA. Division of Pyralidae in the traditional sense into Pyralidae and Crambidae (Minet 1982, 1983, following Munroe 1972) has been widely accepted. The Crambidae essentially all feed on living plants, with diverse specializa- tions among the 16 subfamilies, including for ex- ample monocots (Crambinae), aquatic monocots (Schoenobiinae), aquatic plants more generally (Nymphulinae), mosses (Scopariinae), and Bras- sicaceae (Evergestiinae) (Munroe and Solis 1-14). Although there are a few scavengers and lichen feeders, e. g. some glaphyriines, no major lineage is primarily detritivorous. By contrast, detritivorous habits are widespread in the Pyrali- dae s. str., concentrated especially in the Pyrali- nae, Galleriinae, and Phycitinae. Phycitine habits are especially diverse, including genera that feed on foliage, bore into the cortex of succulents, stems of cacti, conifer cones, or angiosperm seed pods, even in an ascomycete fungus, while a series of genera specialize on dry seeds, grain, or nuts; some of these are detritivorous (Heinrich 1956, Powell 1967) and several genera contain species predaceous on scale insects (Pierce 1995). Further resolution is needed, but the current hy- pothesis of subfamily relationships (Solis and Mitter 1992) allows the possibility that feeding on fallen or dead plant material is primitive for the family.

MACROLEPIDOPTERAN CLADE (Scoble 1992; 1-2) Caterpillars of Macrolepidoptera, which consti- tute about half the described lepidopteran spe- cies, are typically exposed feeders on foliage. However, various forms of concealed feeding, reminiscent of microlepidopterans, occur in sev- eral groups, probably secondarily. Mimallonidae (Bombycoidea s. I.), for example, construct por- table cases, and Hesperioidea are typically leaf- tiers or borers. Among Noctuidae (Godfrey 1987), Apameini are often stem borers and include an example of early-instar leaf mining, Heliothinae often bore into reproductive structures; and leaf- tying occurs within several subfamilies. A similar array of concealed habits occurs in larentiine Geometridae (Scoble 1992).

Although the great majority of Macrolepidop- tera feed on living higher plants, adoption of non-phytophagous habits has occurred repeat- edly. Consumption of lower plants and/or detri- tus has arisen in several groups, most notably Noctuoidea. Thus, the lithosiine Arctiidae feed on lichens and algae, while detritivory/mycoph- agy is dominant in Herminiinae and recurs spo- radically in other noctuid subfamilies (Rawlins 1984). Lichenivores also occur in Lycaenidae and Geometridae (Scoble 1992).

As in microlepidopterans, derived members of several macrolepidopteran families have become facultative or obligate carnivores, again largely of scale insects (Pierce 1995). Notable examples occur in Noctuidae, and one group of larentiine geometrids captures flies (Montgomery 1982). Predation is especially well developed in Lycaeni- dae, many of which feed on the ants and/or ho- mopterans with which they are associated (Sco- ble 1992; Pierce 1995).

In phytophagous Macrolepidoptera, as in non-ditrysians, the predominant and probably ancestral hosts are woody dicots, but there have been multiple radiations onto herbaceous plants. Within Noctuoidea, for example, arboreal feed- ing is probably primitive, being dominant in the oldest lineages (Notodontidae s, I.), in Lymantri- idae, and in most "quadrifine" and some "trifine" subfamilies of Noctuidae s. 1. (see Kitching and Rawlins, 1-19). Among the trifines, Holloway (1989) postulated a trend from tree feeding in the basal groups, especially in tropical lowland habitats, toward herb feeding, especially in open habitats at higher elevations and latitudes, in de- rived groups such as noctuine cutworms. Diver- sification of the latter might have paralleled the proliferation of herbaceous plant taxa as regions of temperate climate expanded during the Terti- ary, a hypothesis that needs testing. There have been independent major radiation of herb-feed- ing taxa in the Arctiidae, and within other super- families (e. g. Geometridae).

Some of the most prominent departures from arboreal feeding occur in the Rhopalocera, the

Evolution of Larval Food Preferences in Lepidoptera

habits of which have been intensively studied (e. g. Ehrlich and Raven 1964; Ackery 1988; Vane-Wright and Ackery 1984). Hesperioidea and essentially all families of Papilionoidea con- tain major elements associated with plant fami- lies which are characteristically herbs (especially in temperate regions), lianas, or shrubs. Selected examples include: in the Pieridae, Pierinae on CapparidaceaeIBrassicaceae; in Papilionidae, Troidini and Parnassiinae on Aristolochiaceae; and in Nymphalidae, Satyrinae, Arnathusiini and Brassolini on monocots, Acraeini on Passiflora- ceae and Urticaceae, Danainae on Apocynaceael Asclepiadaceae and Solanaceae. The contrast be- tween such butterflies and more typical, tree- feeding Macrolepidoptera has figured in the de- velopment of theories relating plant growth and defense to insect host choice and associated life history traits including diurnality and aposema- tism. We return to this topic below.

Discussion

In light of the foregoing review, we can address the questions posed in the introduction.

Origins of higher-plant feeding

Several groups scattered through the primitive lepidopteran lineages show habits reminiscent of the panorpoid groundplan, living on the ground and feeding on detritus, non-vascular plants or fungi. Although further information is needed, such habits appear to be primitive within Zeug- loptera, Exoporia, Tineoidea, possibly the puta- tive oecophoric clade of Gelechioidea, and possi- bly, though doubtfully, in Tortricidae. This raises a question introduced by Grehan (1989): Might such generalized habits have persisted through the early history of Lepidoptera, giving rise multiple times to specialized higher-plant feeding?

"Mapping" of the alternative conditions, "re- striction to vascular plants" vs. "other habits", on the cladograms of Figures 20.1-3 argues against this idea. That is, if we allow that larval phytophagy on higher plants might be a homolo- gous trait, the most parsimonious hypothesis of ancestral conditions is evolution of all Lepidop- tera except Micropterigoidea from a higher plant-feeding common ancestor. Similar reason- ing suggests that all Lepidoptera except Micro- pterigoidea and Agathiphagoidea derive from an angiosperm-feeding common ancestor. These hypotheses require independent reversion to non-phytophagy in basal Exoporia and Ti- neoidea, as well as within many more advanced ditrysian groups. Conversely, a scenario of an- cestral detritivory/fungivory in basal lineages up

through the common ancestor of Ditrysia re- quires independent origins of higher plant phy- tophagy in an additional seven or more lineages (Fig. l), i. e., Agathiphagoidea, Heterobathmi- oidea, Eriocranioidea, Acanthopteroctetidae, Neopseustoidea, Lophocoronidae, Tischerioidea andlor Palaephatoidea, and basal non-tineoid Ditrysia. Most of these groups, including Neo- pseustidae and Lophocoronidae, whose habits are inferred from the piercing ovipositor (1-5), share a particular form of phytophagy, arboreal leaf mining, although ovipositor forrn/function and larval morphology vary markedly among them.

Several problems are raised, however, by the hypothesis that endophagous phytophagy origi- nated only once, or twice (in Agathiphagoidea and in Heterobathmioidea + Glossata), very early in lepidopteran evolution (e. g. late Jurassic or early Cretaceous). Why are there no extant non-ditrysian lineages associated with pterido- phytes, gymnosperms (other than agathipha- gids), or primitive angiosperms (but see Laban- deira et al. 1994)? An Upper Jurassic lepidop- teran fossil (Kozlov 1989), inferred to have a well developed maxillary siphon and large, three-seg- mented labial palpi is provisionally assigned to the Ditrysia (Labandeira et al. 1994). If the age and morphology are correctly interpreted, the major clades including Ditrysia must have devel- oped prior to radiation of the angiosperms. Was the larva of this Jurassic moth an exophagous generalist with habits analogous to extant Micro- pterigidae and Mnesarchaeidae, a detritivore similar to modern tineids, or a specialist herbi- vore on a primitive plant, an association that dis- appeared following the radiation of the angio- sperms? Labandeira et al. (1994) suggest that an- giosperms in the Cretaceous offered a new food resource to existing herbivores, but if so, what did such herbivores eat and why did none of the pre-angiosperm glossatan host associations sur- vive?

The alternative hypothesis, that phytophagy and endophagy arose in several lepidopteran lin- eages independently during the early diversifica- tion of the angiosperms, avoids these dificulties. It also avoids the need to postulate the loss, in both Exoporia and Tineoidea, of morphological and behavioral specializations associated with angiosperm leaf-mining. Although this alterna- tive appears less parsimonious on the cladogram, it should not be ruled out.

Whatever one's view of the earliest history of phytophagy, secondary shifts to detritivory (and thence often in stages to mycophagy, Rawlins 1984), are a recurrent feature of higher lepidop- teran evolution, characterizing subgroups, for example, of Pyralidae, Noctuoidea, Tortricoidea, and Gelechioidea. Hypotheses of the selective pressures favoring such shifts, including resource

Jerry A. Powell, Charles Mitter & Brian Farrell

availability (Rawlins 1984; Common 1990), war- phagy, and could have significant evolutionary rant rigorous test. consequences. Disadvantages to endophagy

How did typical, host-specific, higher plant might include limits on body size and voltinism, feeding initially arise in Lepidoptera? One model and in leafminers, vulnerability to excision. En- is suggested by possible stepwise evolution dophagy might also limit the ability to colonize within several detritivorous/fungivorous lin- alternative hosts (Gaston et al. 1992) and habi- eages. For example, in Hepialidae, early instars tats, and thereby restrict the potential for specia- appear to be detritivorous or mycophagous, tion. Exophagy may be resisted by strong evolu- while later instars feed externally on the roots tionary barriers among Holometabola (South- of, or bore into, living plants and typically are wood 1973), and is found in relatively few holo- polyphagous. However, a few species, possibly metabolous phytophage lineages (Mitter et al. more derived, seem to be specific in their host- 1988). but may promote the evolutionary success plant selection (Grehan 1989). A sequence from of groups adopting it. This hypothesis needs detritivory to generalized and thence to specific testing. phytophagy can similarly be envisioned in Ti- neoidea (some Psychidae are host specific), sug- gesting that lepidopteran phytophagy originally Parallel diversfiration with hostplants?

arose in this way several times. However, the cla- If the predilection for a particular plant taxon distic evidence for primitive moths suggests an were faithfully passed from ancestral to descen- abrupt transition to arboreal, host-specific endo- dant species, lepidopteran clades should remain phagy; there are no phytophagous lineages that associated with particular host clades over long are polyphagous among Agathiphagoidea, Het- time spans, and might undergo divergence in erobathmioidea, or basal glossatans. Indeed, parallel with those hosts. Such a history should among strictly phytophagous clades, polyphagy be detectable by correspondence between lepi- is relatively rare, seems clearly derived in many dopteran and hostplant phylogenies, unless ex- instances, and is most prevalent among external tinction or within-species host switch obscure feeders (Gaston et al. 1992). It may also be of early host associations. Different evolutionary relevance that the carnivorous lepidopterans are models predict different degrees of cladogram often, if not invariably, in groups that also con- match (Mitter and Farrell 1991), but the exis- tain detrivorous species (Pierce 1995). tence of any such pattern for a lepidopteran

The current hypothesis of phylogeny (1-2) group would suggest that its present-day host use suggests a trend among phytophagous Lepidop- reflects long-term history, and that there has tera from internal to external feeding (Figs. 20.1, been significant opportunity for reciprocal evo- 2,3; Scoble 1992) that is stronger than any corre- lutionary influence between these insects and lation with host plant phylogeny. Although their hosts. much further analysis is needed, the cladogram From comparison of host use among the basal (Fig. 20.1, 2) suggests there have been a number lineages, earlier reviews found little support for of transformations through intermediate condi- parallel diversification between Lepidoptera as a tions leading to external feeding. (Evolution in whole and their hostplants (Powell 1980; Mitter the reverse direction may have occurred in some and Brooks 1983). The question warrants re-ex- groups, e. g. Tortricidae; Horak and Brown amination, however, in light of new information 1991.) Construction of a portable case from on phylogeny and host use, and development of which larvae feed either externally (Incurvari- quantitative measures of cladogram correspon- oidea) or by mining (Coleophoridae) has proba- dence. To re-assess possible parallel cladogenesis bly arisen several times (e. g. Incurvarioidea, Ti- for the non-ditrysian lineages, we prune the cla- neoidea, Gelechioidea, Pyraloidea). Among in- dogram of Figure 20.1, leaving only phytopha- curvarioids there is a trend toward earlier con- gous lineages whose host associations can rea- struction of the case, from just before pupation sonably be characterized to the plant family or (Heliozelidae), to an exophagous function after ordinal level. While our analysis is thus limited one or more endophagous instars (Adelidae, In- by lack of phyletic resolution for groups with di- curvariidae). In several leaf mining groups, par- verse hosts, its bias toward low-diversity and titularly among lower Ditrysia, there are transi- biogeographically relictual taxa should maximize tions from leaf mining to various forms of exter- the chance of detecting relictual host associa- nal feeding. Such adaptations occur within indi- tions. This pruned tree, together with a recent vidual ontogenies, with exophagous instars phylogeny estimate for the hostplants, is shown either concealed, as in Argyresthiidae and Grac- in Figure 20.4. For evaluation of cladogram con- illariidae, or exposed, as in Bucculatricidae and cordance, we used component analysis (Nelson Epermeniidae. Feeding exposed on foliage has and Platnick 1981) as implemented by Page arisen a number of times, but it is most prevalent (1990). in Macrolepidoptera. If bryophytes are treated as the ancestral and

Transition to exophagy might be viewed as an primary hosts of Micropterigoidea, the overall adaptive "escape" from the constraints of endo- concordance of lepidopteran and hostplant phy-

Evolution of Larval Food Preferences in Lepidoptera 41 5

Micropterigidae Agathiphagidae Heterobathmiidae Eriocraniidae

Acanthop- teroctetidae

Crinopter~g~dae Cecidosidae Nepticulidae: Pectinivalvinae

Opostegidae: Notiopostega

??Liverworts Coniferales Nothofagus Fagaceae, Betulaceae Rharnnaceae Cistaceae Anacardiacea Myrtaceae

Nothofagus

Fig. 20.4. Phylogeny of primitive moths (non-ditry- sians) (left), from Figure 1, excluding taxa not associ- ated primarily with a single plant order, contrasted to recent estimate of relationships among their host fami- lies (right), based on rbcL gene sequences (Chase et al. 1993). Positions of Cistaceae, Myrtaceae, not studied by Chase et a]., inferred from those of confamilial or con-ordinal species according to Cronquist (1981). Cladogram concordance assessed using component analysis under Assumption 1, as implemented in Com- ponent 1.5 (Page 1990). For all taxa, items of error (IOE) = 46, p. = 0.01 under Markovian null distribu- tion of host phylogenies (1000 replications). With Micropterigidae deleted, IOE = 46, p = 0.08; with Agathiphagidae also deleted, IOE = 46, p > 0.50. AI- ternative plant phylogeny of Hufford (1992) yields very similar conclusions.

logenies is significantly greater than random (Fig. 20.4). However, it is questionable whether bryophyte feeding is primitive within micropteri- gids. Even if it were, the habit is more likely to reflect a retained, ancestral amphiesmenopteran habitat preference (N. P. Kristensen, unpub- lished) than plant phylogeny. That is, it seems far-fetched to postulate that Micropterigidae fed ancestrally on bryophytes because vascular plants, host to nearly all subsequent lepidopteran lineages and dominant since the Carboniferous or before, were not yet available.

If Micropterigoidea are excluded, cladogram concordance still approaches statistical signifi- cance, due to the basal split between the conifer- feeding Aglossata and the remaining lineages, which primarily eat angiosperms. Whether or not agathiphagids represent an independent ori- gin of phytophagy, this is plausibly interpretable as paralleling host phylogeny, perhaps the only such instance in Lepidoptera (Scoble 1992); that is, Aglossata may well retain an association established before angiosperms or their more im- mediate ancestors became available as hosts.

For the angiosperm-feeding lineages alone, in contrast, there is no hint of concordance with any recent host phylogeny estimate. It would not be surprising for comparison across the major non-ditrysian lineages to show no correspon- dence to angiosperm phylogeny, if the suggestion is accurate that divergence of these lineages pre- ceded that of angiosperms. Match to host phy- logeny might in that case be more apparent upon detailed studies within the larger lineages. How-

ever, strikingly few species within any non-ditry- sian group (Powell 1980) are associated with hosts identified as early-diverging by recent cla- distic analyses, such as the orders of Magnolii- dae, "lower" Hamamelidae, or (primitive) mono- cots (Chase et al. 1993; Hufford 1992). Even No- thofagus and other Fagales, hosts for the two oldest angiosperm-feeding lineages, appear rela- tively derived in cladistic position, despite a long fossil record. This association, ostensibly homol- ogous between Heterobathmioidea and Eri- ocranioidea, must be independently derived if these lineages are both older than angiosperms. This suggests that extinction and host transfer may have obliterated most traces of early co-di- versification with angiosperms if it occurred. (An alternative explanation would be that lepidopter- ans did not start feeding on angiosperms until these plants were extensively diversified). The possibility that primitive angiosperms were in fact important hosts for early non-ditrysians is supported by discovery in fossil magnoliid and lower hamamelid (platanoid) leaves of mid Cre- taceous age of mines attributed to two modern nepticulid genera (Labandeira et al. 1994).

A conserved habit that merits further analysis is the prevalent restriction of non-ditrysian lin- eages to woody host plants. Association with herbs, particularly those taxa that have prolifer- ated in the Tertiary, occurs among non-ditrysians only in some presumably derived clades, such as Prodoxidae (Davis et al. 1992, Wagner & Powell 1988), a few nepticulid lineages (Van Nieukerken 1986), and Tischeriidae (Davis 1987). In con- trast, the Ditrysia, including non-apoditrysian groups, contain many lineages that appear to have radiated on modern herbaceous host taxa.

Explicit phylogeny comparisons for lower level lepidopteran taxa, e. g. genera or families, and their hosts, have been few and mostly pre- liminary. However, cladogram concordance be- tween Lepidoptera and their host plants seems rare at this level also (reviews in Miller 1987, Mitter and Farrell 1991). The best candidate for parallel cladogenesis is the subfamily Heliconii- nae (Nymphalidae), which at the species level provides evidence for coevolution in the sense of reciprocal counter-adaptation with its passiflora- ceous hosts (Gilbert 1984). However, even this example is disputed (Benson et al. 1975; Mitter and Brooks 1983; Mickevich and Weller 1990; B. A. B. Venables, unpublished). Detailed study of this and other intimate lepidopteran-host plant associations is needed to determine whether parallel phylogenesis, which is uncom- mon but known in other phytophagous groups (e. g. Chrysomeloidea; Farrell et al. 1992), can be ruled out entirely in Lepidoptera.

The persistence of ancestral host associations in Lepidoptera appears intermediate in compari- son with that in two other recently-reviewed phy- tophagous insect clades of comparable age. The

Fulgoroidea (19 families), which date from the lower Cretaceous or earlier, show no convincing instances of parallel phylogenesis with their host- plants at any taxonomic level, despite prevailing host specificity (Wilson et al. 1993). The only trend reminiscent of Lepidoptera is a progression from concealed (mostly underground) to ex- posed sites of feeding.

In contrast, trends inferrable from morpholog- ical classifications of the chrysomeloid Coleo- ptera (Chrysomelidae + Cerambycidae), sup- ported by recent molecular studies (B. D. Farrell, in prep.), suggest several parallels to Lepidoptera in the evolution of host associations. In chrysomeloids, which date from the upper Juras- sic (Crowson 1981), saprophagy (dead wood feeding) appears ancestral, and subsequent phy- tophages have given rise to secondary detritivory (Crowson 198 I), though apparently much less often than in Lepidoptera. Four morphologically isolated, primitive, and species-poor subfamilies of chrysomeloids are restricted to cycads or coni- fers. An example is the Palophaginae (Chryso- melidae), which consists of two monotypic gen- era, one each in Chile and Australia, that feed on Araucaria cones (Kuschel and May 1990), analogous to Agathiphagidae. In the chrysomel- oid sister group Curculionoidea, in which phy- tophagy has arisen independently one or more times (Anderson 1993), there are likewise several small, Southern Hemisphere groups restricted to gymnosperms, in the primitive families Nemo- nychidae (Kuschel 1983), Brentidae and Belidae.

Chrysomeloid subfamilies of intermediate morphological advancement feed characteristi- cally either on monocots (e. g. Donaciinae; Askevold 1991) or, like basal glossatans, on woody Hamamelidae, Rosidae and Dilleniidae. The most derived subfamilies, having the most numerous generic radiations, feed on recent, mostly herbaceous plant families, especially the subclass Asteridae (Jolivet 1988). A further chrysomeloid parallel to Lepidoptera is predomi- nant and ancestral concealed feeding, which has given rise multiple times to external larval herbi- vory.

While similar trends are apparent, ancestral host affiliations appear to be much better pre- served in Chrysomeloidea than in Lepidoptera, as reflected for example in the extent of the prim- itive, gymnosperm-feeding element. Further- more, two genera of advanced, herb-feeding chrysomeloids provide the strongest examples known of herbivorelplant cladogram correspon- dence (Farrell and Mitter 1990; Farrell et al. 1992). Greater evolutionary lability of larval food choice in Lepidoptera than in Chrysomel- oidea is also indicated by the apparently much more frequent origin of non-phytophagous hab- its in lepidopterans. Apart from the basal wood- feeding clades, departures from live-plant feed- ing in chrysomeloids occur only in the case-bear-

Jerry A. Powell, Chatles Mitter & Brian Farrell

ing clade of Chrysomelidae, which consists of Lamprosomatinae, Chlamisinae, Cryptocephali- nae and Clytrinae (Suzuki 1988). Chlamisinae and Cryptocephalinae include some species with detritivorous larvae, while Clytrinae are invaria- bly myrmecophilic, and larvae may feed on ant brood as well as detritus (Jolivet 1988), parallel- ing some Lycaenidae (Pierce 1995).

This difference in evolutionary lability needs explanation. Perhaps shifts of food preference in living plant-feeding chrysomeloids are disc6ur- aged in part by the similar specificity of feeding requirements between larvae and ovipositing adults, both of which, particularly in Chrysomel- idae, typically chew somatic tissue of the same host plant. In contrast, adult Lepidoptera take liquid food and usually are nutritionally inde- pendent of the larval host. This presumably pro- vides greater opportunity for host shifts through oviposition on novel host plants (Chew and Rob- bins 1984).

A final point of comparison between the Chrysomeloidea and the Lepidoptera concerns the evolution of carnivory. Feeding on ant brood by species of Clytrinae is the only apparent de- parture from phytophagous habits in Chryso- meloidea, and it parallels lycaenid habits (Pierce 1995). Thus the Lepidoptera seem much more labile overall in the evolution of non-phytopha- gous habits, and prey items are typically insects frequently encountered in the larval environ- ment.

Evolutionary Patterns of Host Shift

Although parallel cladogenesis with host lineages is evidently rare in Lepidoptera, the evolution of lepidopteran host plant affiliations is not ran- dom. It has long been noted, for example, that in some groups, related species tend to feed on related plants (e. g. Brues 1920). The prevalence of this tendency across the order as a whole has not been rigorously assessed. The preferred ap- proach (Van Nieukerken 1986) would be to re- construct the history of host shifts on clado- grams inferred from other characters. Seven lepi- dopteran groups, representing one macrolepi- dopteran and three microlepidopteran superfam- ilies, were included in a recent compilation of species-level cladograms for phytophagous in- sects (Mitter and Farrell 1991). The mean ratio of host family shifts to speciation events inferred from the lepidopteran cladograms was about 0.22, close to the value for all insect groups col- lectively. This small sample can hardly character- ize the order, but does illustrate the great varia- tion among groups in the propensity for taxo- nomically radical host shifts. For example, the seven species in Yponorneuta "group A" (Ypono- meutidae) have shifted among four host families, with essentially all species using different host genera (Menken 1982). In contrast, the -ten

Evolution of Larval Food Preferences in Lepidoptera

congeneric species of Heterobathmioidea share a single host genus, as do most of the -70 species of the Heliconius group (Nymphalidae). The at- tempt to classify and explain such heterogeneity in host-use evolution has only begun. In the re- mainder of this chapter we sketch several current research directions, but a thorough treatment is beyond our scope. Relevant recent reviews in- clude Thompson and Pellmyr (1991), Stamp and Casey (1993) and Renwick and Chew (1994).

Advances in lepidopteran and angiosperm phylogenetics are increasing the detectability of host use patterns reflecting plant relatedness above the family level. Ehrlich and Raven (1964) pointed out examples including papilionoid groups broadly associated with monocots, with the subclass Magnoliidae (Magnoliales, Laurales etc.) and with Violales (Violaceae, Passifloraceae etc.); Miller (1992) has described parallels in No- todontidae. The disparate-seeming hosts of a number of apoditrysian clades (e. g., Ackery 1988; Mitter and Farrell 1991) are united by membership in an expanded concept of the sub- class Asteridae (Asteridae of Cronquist 198 1, plus Apiales, Cornales, Ericales and several oth- ers), monophyly of which is supported by recent molecular studies (Olmstead et al. 1993).

Chemical similarities between host plants probably underlie such conserved host-taxon as- sociations, though the mechanisms are still poorly understood. Lepidopteran host recogni- tion is complex (Renwick and Chew 1994), and host shift patterns no doubt reflect multivariate similarity. In some groups, however, diet evolu- tion appears strongly influenced by particular secondary-chemical or other putatively defensive plant attributes, which may even be "tracked" across unrelated plant lineages (Ehrlich and Ra- ven 1964). Recently-documented syndromes in- clude associations with plants possessing com- plex coumarins (Berenbaum 1983), and with those containing iridoid glycosides (Bowers 1988). Iridoids are characteristic of, though not universal in, Asteridae, and may in part account for affiliations with that subclass. For example, the host families of epiplemine Uraniidae as compiled by Lees and Smith (1991) are Rubia- ceae (Rubiales), Caprifoliaceae (Dipsacales), Oleaceae and Bignoniaceae (both Scophulari- ales), Verbenaceae (Lamiales), and Daphniphyl- laceae. All but the last are iridoid-bearing Asteri- dae; Daphniphyllaceae (subclass Hamamelidae) are one of the few non-asterid groups to contain iridoids (Olmstead et al. 1993).

Numerous lepidopteran and other insect clades have shifted among hosts, often unrelated and chemically dissimilar, which have secretory canals containing latex or resin (Peigler 1986; Farrell and Mitter 1993). These repeatedly evolved structures discourage herbivory by dis- charging viscous, often toxic fluids when severed. Caterpillars in a number of families overcome

this barrier by means such as severing the canal and lowering its fluid pressure before feeding dis- tal to the cut (Dussourd 1993). Canal-plant pat- terns are best documented in Macrolepidoptera. For example, the main hosts of danaine Nymph- alidae are Asclepiadaceae/Apocynaceae; the most reliable other records (Ackery and Vane- Wright 1984) are from Moraceae, Convolvula- ceae, Caricaceae, Euphorbiaceae and Rubiaceae. All but the last bear latex. Euteliine Noctuidae most commonly feed on Anacardiaceae; promi- nent among their other hosts are Burseraceae, Dipterocarpaceae, Moraceae and altingioid Ha- mamelidaceae, all likewise canal-bearing (Hollo- way 1985; Forbes 1954; Peigler 1986). The prob- able euteliine sister group, Stictopterinae, is asso- ciated primarily with Dipterocarpaceae and Gut- tiferae (= Clusiaceae) (1 - 19), which also bear secretory canals. Further examples occur in epi- paschiine Pyralidae (Solis 1993), aganaine Noc- tuidae (Holloway 1988), Uraniidae (Lees and Smith 1991), Saturniidae (Peigler 1986) and doubtless many others.

The canal-plant syndrome, like that for com- plex coumarins (Berenbaum 1983), illustrates a way in which Lepidoptera may participate in "diffuse" coevolution between plants and herbi- vores. Canals seem to have evolved as broad- spectrum defenses against herbivores and patho- gens, presumably including lepidopterans, and canal-bearing plant clades show consistently ele- vated diversity as compared to their sister groups (Farrell et al. 1991), as predicted by Ehrlich and Raven's (1964) coevolutionary model. The mod- el's converse prediction, that radiation should be correspondingly accelerated in lepidopteran clades able to colonize these or other sets of plants bearing distinctive defenses, has yet to be tested. Like that of other phytophagous insects, lepidopteran diversity is elevated in comparison to their sister group, Trichoptera (Mitter et al. 1988); but the question of whether this results from radiation onto different plant resources, however defined, is unexplored.

Several authors (e. g., Janzen 1984; Holloway 1987; Feeny 1991 b; Miller 1992) have contrasted lepidopterans feeding on plants bearing distinc- tive, "qualitative" or "mobile" secondary com- pounds (Feeny 1991 a), typically toxic or repel- lent to vertebrates as well as to non-adapted in- sects, to species whose hosts typically lack such features. Lepidoptera associated with "toxic" plants often show marked specificity and conser- vatism of host choice, an example being troidine Papilionidae, restricted to Aristolochiaceae (Feeny 1991 b). Such conservatism has been at- tributed in part to herbivore dependence on dis- tinctive chemistry for host finding and accep- tance, and possibly for defense as well: toxic plant lepidopterans are often aposematic day-fli- ers, and some sequester host toxins in the larval stage for use in their own defense.

Jerry A. Powell, Charles Mitter & Brian Farrell

In contrast, plant in some taxonomic or eco- logical assemblages may be less chemically dis- tinctive, lowering the barriers to host transfer. Thus, temperate deciduous forests are dominated by tanniferous angiosperms in which resistance to herbivores is manifested mainly by toughness and low nutritional content of mature foliage. Among Lepidoptera that eat these plants the in- cidence of polyphagy is elevated, at least in Macrolepidoptera (Futuyma 1976). Even conge- neric species in host-specific groups often have adapted to unrelated hosts (Powell 1980); exam- ples include Yponomeuta, cited above, all the larger genera of non-obtectomeran ditrysians and of Geometridae, and many genera of arbo- real Noctuoidea (Miller 1992, Mitter and Farrell 1991). In such groups, feeding site and habitat preference, particularly if these require special adaptations, may be conserved more often than associations with plant taxa.

Correlations of larval diet evolution with other life history traits and with plant chemistry and ecology have only begun to be documented, and will prove much more complex than our coarse dichotomy would suggest (see e. g. Janzen 1984). Phylogenetic study of such patterns is a promising avenue toward better understanding of the evolution of lepidopteran diet.

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