Coumarins and Caterpillars: a Case for Coevolution Author(S): M

Coumarins and Caterpillars: A Case for Coevolution Author(s): M. Berenbaum Source: Evolution, Vol. 37, No. 1 (Jan., 1983), pp. 163-179 Published by: Society for the Study of Evolution Stable URL: http://www.jstor.org/stable/2408184 Accessed: 03-04-2018 17:53 UTC

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This content downloaded from 165.230.49.193 on Tue, 03 Apr 2018 17:53:23 UTC All use subject to http://about.jstor.org/terms Evolution, 37(1), 1983, pp 163-179

COUMARINS AND CATERPILLARS: A CASE FOR COEVOLUTION

M. BERENBAUM' Department of Ecology and Systematics, Cornell University, Ithaca, New York 14853

Received December 4, 1981. Revised June 25, 1982

Ehrlich and Raven (1964) were among (1) Production of Novel Secondary the first to focus on coevolution as a dis- Substances by Mutation or tinct evolutionary process. In their for- Recombination mulation, insect-plant coevolution is a Natural products with a 2H-1-benzo- five-step sequence: 1. by mutation and re- pyran-2-one nucleus (Fig. 1), broadly combination, angiosperms produce novel called coumarins, are widespread in the secondary substances; 2. by chance, these plant kingdom. Various modifications of new secondary substances alter the suita- the benzopyran-2-one nucleus exist in na- bility of the plant as food for insects; 3. ture. By far, simple coumarins are the most the plants, released from the restraints im- common, characterized by the lack of ad- posed by herbivory, undergo evolutionary ditional fused ring systems. More than 30 radiation in a new adaptive zone; 4. by simple coumarins have been reported from mutation or recombination, insects evolve a total of 33 plant families (Hegnauer, mechanisms of resistance to the secondary 1964-1973; Gray and Waterman, 1978). substances; 5. able to exploit a plant re- Coumarins with an oxygen-containing source hitherto excluded from herbivores, substituent at the 7-position, such as um- the adapted insects enter a new adaptive belliferone (Fig. 1), appear to be biosyn- zone and undergo their own evolutionary thetically distinct from those, such as cou- radiation. marin, that lack such a function; This scenario was inspired by broad umbelliferone and related hydroxycou- patterns of hostplant utilization among marins are derived from p-coumaric acid families of butterflies (Rhopalocera). Al- whereas coumarin is derived from the un- though the schema gained widespread ac- substituted cis-cinnamic acid (Brown, ceptance, to date no specific example dem- 1960; Brown, 1970). Paracoumaric acid, onstrates most or all of the steps in the an intermediate in lignin biosynthesis, is sequence. This lack of empirical evidence widespread among angiosperm plants, oc- has been the subject of considerable crit- curring in at least 100 plant families; hy- icism (e.g., Jermy, 1976; Janzen, 1980). droxycoumarins are more restricted in dis- Recent experimental work on associations tribution, reported to occur in less than between various insects and plants con- three dozen plant families (Table 1). Hy- taining furanocoumarins and related com- droxycoumarins are known to possess bio- pounds (Berenbaum, 1978, 1980, 1981a, cidal properties and act as phytoalexins 1981b, 1981c), however, provides a case and germination inhibitors in many species study with either direct or circumstantial (Bose, 1958; Hughes and Swain, 1960; evidence for each part of the coevolution- Berrie et al., 1968; Jurd et al., 1973; Wil- ary process. liams and Hoagland, 1982). In many natural coumarins, a third ring is fused to the benzopyran-2-one nucleus,

1 Present address: Department of Entomology, 3 20 thus incorporating the 7-oxygen atom into Morrill Hall, University of Illinois at Urbana-Cham- a new heterocyclic ring. Incorporation into paign, Urbana, Illinois 61801. a 5-membered ring gives rise to furano-

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COUMARIN HYDROXYCOUMARIN

5,5 44 5.5 44 ZN^X 3,3 6,6 333

8,8 ~~~~~~~~~ H 8,8 1, a. Coumarin a. Umbelliferone (7-hydroxycoumarin) b. 2H- 1 -benzopyran-2-one b. 7-hydroxy-2H- 1 -benzopyran- 2-one

LINEAR FURANOCOUMARIN ANGULAR FURANOCOUMARIN 5,4 4,5 ~~~~~~~~~5,5 4.4 4',3 ~~~~3,66633

4 .9 5', 18, 1,8%

118 ~ ~ ~ 8 a. Psoralen a. Angelicin b. 7-Hi-furo [3,2-g]-1- b. 2-H-furo[2,3-H]-1- benzopyran-2-one benzopyran- 2-one

FIG. 1. Basic coumarin structural types with nomenclatural and numbering systems. (a) semi-rational nomenclature (first number at each position). (b) IUPAC nomenclature (second number at each position).

coumarins. All furanocoumarins share the ear furanocoumarins, occurring in only two precursor umbelliferone (7-hydroxycou- genera of Leguminosae and in less than marin). In contrast with hydroxycouma- ten genera in the Umbelliferae (Baskin et rins, furanocoumarins are restricted to eight al., 1967; Nielsen, 1970). families (Table 2) and occur with regular- Furanocoumarins have been found in ity and diversity in only two of those fam- all parts of plants, although roots and seeds ilies, the Umbelliferae and the Rutaceae. are the organs which have been investi- The two structural types of furanocou- gated most thoroughly (Karrer, 1958). marins-angular, with the furan ring at- Where furanocoumarins are reported in tached at the 7, 8 positions, and linear roots and seeds, they are frequently found furanocoumarins, with the furan ring at- in foliage as well after further investiga- tached at the 6, 7 positions (Fig. 1)-are tion, although foliar composition and con- biosynthetically distinct, although both centrations may differ from that of roots types derive from enzymatic prenylation (Fahmy et al., 1955; Steck, 1970). De- of umbelliferone. The enzymes that pren- pending on the taxon, fruits or roots ap- ylate umbelliferone appear to be site-spe- pear to be the primary storage sites for cific. Dimethylallylpyrophosphate: um- furanocoumarins. Concentrations in roots belliferone dimethylallytransferase, which can exceed 9%, calculated on a dry weight participates in the biosynthesis of linear basis (e.g., Heracleum canescens-Kumar furanocoumarins, attaches the prenyl unit et al., 1976). Yields from fruits vary de- to the 7-position only (Ellis and Brown, pending on the stage of maturity but most 1974). In that the enzyme is unable to often reach maximum concentrations of 1 % prenylate umbelliferone at the 8-position, to 5% while fully formed yet still green a separate enzyme is thought to mediate (Beyrich, 1966; Simsova and Blazek, 1967; the biosynthesis of angular furanocoumar- Balbaa et al., 1972; Stahl and Herting, ins (Ellis and Brown, 1974). Angular fur- 1976). Foliage typically contains far less anocoumarins are even more rare than lin- material, on the order of 0.1% to 1.0% dry

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TABLE 1. Plant families containing hydroxycou- TABLE 2. Plant families and genera with furano- marins (from Hegnauer, 1964-1973). coumarins. Data from Hegnauer (1964-1973); Niel- sen, 1970; Gonzalez et al., (1976); Gray and Water- Apocynaceae Moraceae man (1978). Araliaceae Nepenthaceae Caprifoliaceae Oleaceae Number of Number of genera Caryophyllaceae Passifloraceae genera with furano- Compositae Pittosporaceae Family in family coumarins Convolvulaceae Ranunculaceae Umbelliferae 200 23 Ebenaceae Rosaceae Rutaceae 140 19 Euphorbiaceae Rubiaceae Leguminosae 550 2 Fouquieriaceae Rutaceae Moraceae 73 1 Hippocastaneaceae Sapindaceae Solanaceae 85 1 Labiatae Saxifragaceae Pittosporaceae 9 1 Leguminosae Solanaceae Thymelaeaceae 40 1 Loganiacae Sterculiaceae Compositae 950 1 Magnoliacae Theaceae Meliaceae Thymelaeaceae Umbelliferae

nus Citrus, furanocoumarins are localized in oil glands in the peel (Fisher and Tra- weight (Beyrich, 1965a, 1965b, 1966; ma, 1979); and in the seeds of Umbellifer- Steck, 1970). Linear furanocoumarins in- ae, Ladygina et al. (1970) found furano- variably make up the greatest proportion coumarins primarily in the segmented of total furanocoumarin content, irrespec- secretory ducts overlying the seed coat, tive of botanical source. When angular fu- where they form small needle-like crys- ranocoumarins are present, they generally tals. In shoots of Heracleum lanatum occur at levels ranging from .001% to .15% (Umbelliferae), furanocoumarins occur in dry weight (Steck and Bailey, 1969; Ku- oil channels associated with each vascular mar et al., 1976) and thus comprise, on bundle in the petioles of unexpanded leaves average, less than 10% of the total furano- (Camm et al., 1976), and in roots of Pas- coumarin content of plant tissue (Spaeth tinaca sativa (Umbelliferae), Beyrich (1966) and Simon, 1936; Hata and Kozawa, 1961; found that furanocoumarins occur only in Nielsen and Lemmich, 1964; Ignat'eva and the outer cylinder. Localization of second- Nikonov, 1966). ary substances in special organs has been According to Beyrich (1967), the site of suggested as a mechanism for avoiding storage or accumulation of furanocouma- autotoxicity in plants (McKey, 1979), and rins is also the site of synthesis; reciprocal thus is often associated with allelochemic, root graft studies with Levisticum offici- as opposed to internal physiological, ac- nale and Pastinaca sativa demonstrated a tivity (Whittaker and Feeny, 1971). fundamental inability to translocate furanocoumarins away from the site of syn- (2) New Secondary Substances Alter the thesis. Brown and Steck (1973), however, Suitability of Plants as Food established that skimmin, the glucoside for Insects precursor of furanocoumarin biosynthesis, Linear furanocoumarins are more toxic can be translocated from petiole cut ends to polyphagous insects than their hydro- to leaf blades, where biosynthesis is coumarin precursors by virtue of a double thought to take place. bond in the furan ring that allows ultra- Irrespective of taxon, furanocoumarins violet light to inactivate DNA (see refer- occur in special organs. In seeds of Psora- ences in Berenbaum, 1978). Spodoptera lea subaucalis, a legume, furanocouma- eridania, the southern armyworm (Lepi- rins are restricted to the seed coat and are doptera: Noctuidae), readily eats plants or completely absent from the endosperm artificial diets containing hydroxycouma- (Baskin et al., 1967); in the rutaceous ge- rins; this caterpillar cannot consume fu-

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TABLE 3. Coumarin chemistry and number of species not cause great mortality in the absence of of plant genera in the umbelliferae. From Willis, 1966; ultraviolet light (Berenbaum, 1978); tox- genera according to Drude, 1898; chemical datafrom icity dependent upon UV light is consis- Gonzalez et al., 1973. tent with the mechanism of phototoxicity

Number Number via furanocoumarin-induced inactivation of of of DNA. Genera species Genera species Angular furanocoumarins are toxic to Without furanocoumarins or with dihydrofurano- oligophagous insects that are able to ingest coumarins only (*) and tolerate linear furanocoumarins (Ber- Echinophora 10 Capnophyllum 4 enbaum and Feeny, 1981). Fecundity of Anisosciadium 2 Dorema 16 Dicyclophora 1 Leptotaenia* 16 the black swallowtail (Papilio polyxenes), Pycnocycla 10 Lomatium* 80 an umbellifer-feeding specialist that is ca- Scandix 15-20 Zozimia* 10 pable of ingesting and assimilating linear Myrrhis 2 Guillonea 1 furanocoumarins, is drastically reduced by Molospermum 1 Laserpitium 35 Astrodaucus 4 Thapsia 6 angelicin in an artificial diet. These ob- Torilis 15 Melanoselinum 7 servations suggest that the change of con- Zizia* 3 Exoacantha 2 figuration of the furan ring from the linear Cryptotaenia 4 Artedia 1 to the angular position affects the prop- Carum 1 Ammodaucus 1 erties of furanocoumarins. In the angular Athamanta* 15 Daucus 60 Pteryxia 2 position, the furan ring double bond is in- capable of photobinding with DNA (see Average number of species per genus = 12.1 ? 3.6. references in Berenbaum and Feeny, 1981) With linear furanocoumarins only so phototoxicity is theoretically an impos- Chaerophyllum 40 Agasyllis 1 sibility; some other mode of action must Coriandrum 2 Cymopterus 18 be responsible for the adverse response Cachrys 22 Levisticum 35 Conium 4 Phellopterus 5 noted in swallowtails. Hippomarathrum 12 Ferula 133 Prangos 30 Ferulago 50 (3) Plants Undergo Evolutionary Apium 1 Xanthogalum 3 Radiation in a New Adaptive Zone Cicuta 10 Malabaila 10 Petroselinum 5 Laser 3 That plants underwent evolutionary ra- Anethum 1 Siler 1 diation as a result of producing linear and Cnidium 20 angular furanocoumarins is suggested by Foeniculum 5 patterns of species diversification and Libanotis endemism within the Umbelliferae. With Sphenosciadium 1 its 1,950 species, the Apioideae, the only Average number of species per genus = 17.4 + 5.8. group in the family containing any type of With linear and angular furanocoumarins coumarin, far outnumbers the plants in Ammi 10 Angelica 80 the subfamilies Hydrocotyloideae (320 Bupleurum 150 Archangelica 2 species) and Saniculoideae (250 species). Pimpinella 150 Pastinaca 15 Ligusticum 60 Peucedanum 120 Within the Apioideae, the vast majority Selinum 3 Heracleum 70 of monotypic genera and genera with ex- Seseli 80 tremely restricted geographic distributions

Average number of species per genus = 67.3 + 16.8. are those that produce no furanocoumarins (Table 3). At the opposite extreme, * Plants containing dihydrofuranocoumarins. the majority of holarctic genera in the family (Bupleurum, Ligusticum, Angelica, ranocoumarins or grow on plants contain- Pastinaca, and Heracleum) are plants ing them (Soo Hoo and Fraenkel, 1966; containing both linear and angular fur- Berenbaum, 1978). Toxic effects are at- anocoumarins; monotypic genera are the tributable to the furan ring. Artificial diet exception in this group of plants. containing levels of furanocoumarins le- As for the new "adaptive zone" that thal in the presence of ultraviolet light does plants producing furanocoumarins pre-

This content downloaded from 165.230.49.193 on Tue, 03 Apr 2018 17:53:23 UTC All use subject to http://about.jstor.org/terms CATERPILLAR COUMARINS 167 sumably entered, there is little direct evi- TABLE 4. Coumarin chemistry of hostplants of de- dence that such exists. However, it can be pressariinae (Lepidoptera: Oecophoridae) in North argued that furanocoumarins facilitated America (Hodges, 1974). the colonization and expansion of the Um- TRIBE AMPHISBATINI belliferae into progressively drier habitats Machimia, Eupragia, Psilocorsis (Mathias, 1965). Root elongation in sev- Ulmaceae* Salicaceae* eral species of Umbelliferae is reduced by Juglandaceae* Rosaceae? ultraviolet light, and, in these species, Fagaceae* Cornaceae* synthesis of flavonoid pigments that ab- Betulaceae* Aceraceae* sorb ultraviolet light and screen the plants Tiliaceae? Oleaceae? from its harmful effects is stimulated by TRIBE DEPRESSARIINI light (Wellman, 1976). Enzymes in phe- Himmacia, Nites, and Bibarrambla nylpropanoid metabolism (and thus fur- Juglandaceae,* Fagaceae,* Betulaceae,* Acera- anocoumarin metabolism) are similarly in- ceae,* Salicaceae* duced by light (Heller et al., 1979). Since Apachea and Semioscopis furanocoumarins are highly UV-absorb- Betulaceae,* Rosaceae,' Rutaceaet ing, they may also act as screens for dam- Martyrhilda aging sunlight and may thus have facili- Betulaceae,* Malvaceae,* Salicaceae,* Composi- tated establishment and growth in open taet# habitats. After establishment plants may Agonopterix have experienced reduced herbivory as Juglandaceae,* Myricaceae,* Lythraceae,* Salica- well due to the phototoxic properties of ceae,* Rosaceae,' Leguminosae,t Guttiferae,?# furanocoumarins. Rutaceae,t Umbelliferae t Araliaceae,? Boragi- naceae,* Compositaet#

(4a) Insects Evolve Physical Resistance Depressaria to Novel Secondary Substances Umbelliferae,t Compositaet#

Polyphagous lepidopteran herbivores * Families containing p-coumaric acid. cannot digest or detoxify furanocoumarins Families containing hydroxycoumarins. t Families containing furanocoumarins. (Yajima et al., 1977; Berenbaum, 1978; # Families containing phototoxins other than furanocoumarins Gebreyesus, 1980), yet caterpillars of species adapted to feeding on umbelliferous plants are immune to the effects of positae and Umbelliferae contain photoac- some furanocoumarins. This immunity can tive secondary substances. Hypericum be conferred by physiological mecha- species in the Guttiferae, hosts for A. hy- nisms, as in Papilio polyxenes (discussed perella, A. lythrella and A. nubiferella, above); it can also be enhanced by behav- contain hypericin, a dimeric quinone that ioral adaptations. In the case of leaf-roll- acts as a primary photosensitizer in mam- ing oecophorids that feed exclusively on mals (Pathak, 1974; Galitzer and Oehme, Umbelliferae, resistance to the chemicals 1978). In the Leguminosae, Psoralea spp., may simply be the result of the leaf-rolling hosts for A. psoraliella and A. posticella, habit. Rolled leaves shield the caterpillar contain phototoxic furanocoumarins (Bas- from ultraviolet light and thereby from kin et al., 1967). The composite host plants UV-induced phototoxicity (Berenbaum, Antennaria, Artemisia, Eupatorium, Co- 1978). reopsis, Bidens, Senecio and Erigeron Leaf-rolling is by no means restricted to contain several polyacetylenic substances, caterpillars that feed on phototoxic plants. notably tridecapentayene, thiophene de- However, a remarkable number of host- rivatives such as a-terthienyl, and matri- plants for the oecophorid genera Depres- caria ester, with antibiotic and phototoxic saria and Agonopterix contain photoactive properties (Towers et al., 1977). In the case secondary substances (Table 4). Of the of a-terthienyl and derivatives, phototox- families reported as hosts for Agonopterix icity to nematodes, fungi and insects de- species, Guttiferae, Leguminosae, Com- pends on the presence of longwave ultra-

This content downloaded from 165.230.49.193 on Tue, 03 Apr 2018 17:53:23 UTC All use subject to http://about.jstor.org/terms 168 M. BERENBAUM violet radiation (Gommers and Geerligs, (4b) Insects Evolve Biochemical 1973; Wat et al., 1981), as does the pho- Resistance to New Plant totoxicity of phenylheptatryene (Wat et al., Secondary Substances 1979). Wavelengths below 400 nm are necessary for the photoactivation of fur- Comparisons between polyphagous and anocoumarins in such Agonopterix hosts oligophagous species provide the best evi- as Angelica, Cicuta, Heracleum, and Pas- dence of biochemical adaptation by insects tinaca in the Umbelliferae, Ptelea and to furanocoumarins. Black swallowtail Xanthoxylum in the Rutaceae, and Pso- caterpillars (Papilio polyxenes-Lepidop- ralea in the Leguminosae. tera: Papilionidae), which feed exclusively The proportion of phototoxic species on the family Umbelliferae (Tietz, 1972; among the foodplants of Agonopterix cat- Tyler, 1975) appear to be unaffected either erpillars is higher than among other groups behaviorally or physiologically by dietary within the family Oecophoridae. The Oec- levels of xanthotoxin (a linear furanocou- ophorini, the largest tribe in the family, marin) ten times greater than those that feed almost exclusively on detritus, par- kill 100% of the polyphagous Spodoptera ticularly on fungus under bark (Hodges, eridania. In fact, growth is actually en- 1974); Hofmannophila feeds on hides and hanced in the presence of the chemical Martyringa and Endrosis feed on stored (Berenbaum, 1981c). The physiological grain, flesh and wool. Members of the tribe mechanism of resistance to furanocou- Amphisbatini feed primarily on tree species marins in these oligophagous insects is un- in the families Fagaceae, Rosaceae, Be- known. Papilio polyxenes caterpillars feed tulaceae and Juglandaceae; there are no externally on plants, fully exposed to nat- species known to be photoactive in these ural levels of ultraviolet light, yet manifest families. no short-term physiological symptoms of Specialization on plants containing pho- phototoxicity. High concentrations of fu- totoxic substances may have developed as ranocoumarins in artificial diet are excret- a consequence of the leaf-rolling habit of ed in the feces (pers. observ.), but metab- oecophorids feeding on material with low olism or uptake of these chemicals has not water content. For tree feeders, low water been established. content is often a factor limiting to larval Indirect evidence suggests adaptation to growth (Scriber, 1977, 1979). For detritus angular furanocoumarins by oligophagous feeders such as the Oecophorini, low water insect herbivores of umbellifers. While the content is even more of a problem (Hodges, black swallowtail (P. polyxenes) suffers 1974). The water content of most species reduced fecundity from naturally occur- of hostplants for genera in the Depressa- ring levels of angular furanocoumarins in riini other than Agonopterix and Depres- its diet (Berenbaum and Feeny, 1981), the saria is considerably lower than the water short-tailed swallowtail (P. brevicauda), content of hosts of Agonopterix and De- feeds almost exclusively on plants contain- pressaria (Berenbaum, 1980); leaf-rolling ing angular furanocoumarins, which are acts to minimize water loss by maintaining generally avoided by P. polyxenes. Of 24 high humidity and, in fact, enhances the genera recorded as hosts of P. polyxenes, rate of transpiration (O'Toole et al., 1979). only two genera (Angelica, Pastinaca) Though undoubtedly biochemical and contain angular furanocoumarins; of six physiological adaptation has taken place genera reported as hosts of P. brevicauda, within Agonopterix and Depressaria to four (Heracleum, Angelica, Ligusticum and furanocoumarin-containing plants, leaf- Pastinaca) contain angular furanocou- rolling, a vestige of the tree-feeding habits marins (Tietz, 1972; Tyler, 1975; Jackson, of their evolutionary predecessors, may 1979). Moreover, Depressaria pastinacel- well have facilitated the adoption of pho- la, the parsnip webworm (Lepidoptera: totoxic plants as hosts. Oecophoridae), feeds entirely on those few

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North American umbelliferous genera that TABLE 5. Diversity of insect taxa and hostplant contain angular furanocoumarins (Ange- chemistry. lica, Pastinaca, Heracleum), and occurs A. Depressariini (Oecophoridae)' with statistically greater frequency within Hostplant chemistry Number of a Pastinaca sativa (wild parsnip) popula- Genus (# host families) species tion plants containing angular furanocou- Depressaria LFC, AFC, HC (2) 100 marins (Berenbaum, 1981a). Agonopterix LFC, HC (12) 125 Martyrhilda HC (4) 38 (5) Adapted Insects Can Enter a New Semioscopis HC (3) 12 Adaptive Zone and Undergo an Apachea LFC, HC (1) 1 Bibarrambla NC (5) 1 Evolutionary Radiation Nites NC (5?) 5 "Adaptive zone" has been an ill-defined Himmacia NC (5?) 3 concept as used by Ehrlich and Raven B. Genus Papilio (Papilionidae)2 Hostplant chemistry Number of (1964). If number of species can be used Section (# host families) species as a measure of evolutionary diversifica- Section II LFC, AFC, HC (9) 139 tion, then, at least in the two major her- Section IV LFC, HC (5) 34 bivore groups associated with furanocou- Section V HC (2) 18 marin-containing plants, the Oecophoridae Section I HC (2) 9 and the Papilionidae (Table 5), there has Section III HC (13) 8 been considerably more speciation in ' North American species only (Hodges, 1974). 2 From Scriber (1973). NC = no coumarins. HC = with hydroxy- groups of feeding on plants containing fu- coumarins. LFC= with linear furanocoumarins. AFC= with an- ranocoumarins than there has been in those gular furanocoumarins. groups most closely related to them on hosts lacking furanocoumarins. pastinacella feed on leaves and seeds of (6) Parallel Evolution of Insects Pastinaca sativa, respectively. Leaves Adapted to Particular Noxious contain only linear furanocoumarins Phytochemicals whereas seeds of some individuals contain According to Ehrlich and Raven (1964), angular furanocoumarins as well as linear similar coevolutionary pressures along dif- furanocoumarins [Berenbaum, 1981a]). ferent phylogenetic lines should generate Among the taxa associated with Um- parallel evolutionary series. Such series belliferae, there are several striking ex- have been dismissed as rare (Jermy, 1976), amples of convergence in hostplant usage but these series may escape detection for patterns. These patterns are consistent at least two reasons. First, phylogenet- with patterns of coumarin chemistry and ically distinct plant species can share sim- could well be construed to be parallel se- ilar chemistry. For example, Ficus in the ries arising independently through the Moraceae shares a biosynthetic pathway process of coevolution. for furanocoumarin production that is identical in all respects to that of the Um- (6a) Lepidoptera belliferae and Rutaceae (Caporale et al., The greatest biomass, numerical abun- 1970; Caporale et al., 1972), despite the dance and species diversity of herbivores lack of any close taxonomic affinity. Sec- associated with Umbelliferae are lepidop- ond, closely related insect species may feed terous larvae. In the Oecophoridae, the on the same plant species but heteroge- genera Agonopterix and Depressaria, in neity in production and distribution of addition to feeding on furanocoumarin- secondary substances may create a situa- containing Umbelliferae, Leguminosae tion in which insects, by feeding on dif- (Psoralea), and Rutaceae (Ptelea and ferent plant parts, actually encounter dif- Xanthoxylum), are found on plants in the ferent secondary chemicals (e.g., Guttiferae, Rosaceae, Leguminosae, Ar- Agonopterix clemensella and Depressaria aliacae, and Compositae, all families con-

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TABLE 6. Hostplants of the genus Papilio (Scriber, the section feed on Leguminosae, Meli- 1973). aceae, Sapindaceae, Araliaceae, Labiatae and Rubiaceae-all families that contain A. Sections of the genus in North America (Munroe, hydroxycoumarins (the single exception 1960) being a single record on Verbenaceae). Section II, machaon complex Sections I, IV and V of the genus, thought Rutaceae,t Umbelliferae,t Compositaet to be less advanced phylogenetically than Section III Section II, feed on Magnoliaceae and Lau- Lauraceae, Magnoliaceae, Platanaceae,* Ulma- raceae, primitive plants that nonetheless ceae,* Juglandaceae,* Betulaceae,* Tili- possess hydroxycoumarins; Section III aceae,? Salicaceae,* Rosaceae,? Rhamna- ceae,* Aceraceae,* Rutaceae,t Oleaceae? species fed on virtually the same plants as do genera in the tribe Amphisbatini in the Section IV Oecophoridae, plants in families contain- Lauraceae,? Rutaceae,t Piperaceae, Nyssaceae, Salicaceae* ing either hydroxycoumarins or p-coumaric acid. B. Sections of the genus outside North America The family Noctuidae, known for its Section I many highly polyphagous species (e.g., Magnoliaceae,? Lauraceae? Spodoptera), nevertheless contains several Section II, excluding machaon complex species that are restricted as caterpillars to Leguminosae,t Meliaceae,t Rutaceae,t Sapin- plants in the family Umbelliferae (Table daceae,? Araliaceae,? Umbelliferae,t Verben- 7). Papaipema marginidens and P. harrisi aceae,* Labiatae,? Rutaceaet are both stem borers of furanocoumarin- Section, IV containing umbelliferous genera. The ma- Magnoliaceae,? Lauraceae? jority of Papaipema species feed on plants * Families containing p-coumaric acid. containing hydroxycoumarins (Oleaceae, Families containing hydroxycoumarins t Families containing furanocoumarins. Ranunculaceae, Compositae) or furanocoumarins; of the two leguminous genera reported as hosts for Papaipema, one, taining hydroxycoumarins. The remain- Psoralea, is one of only two genera in the der of host families for Agonopterix, while family producing furanocoumarins. The lacking coumarins per se, almost univer- remainder of host families, with the ex- sally contain p-coumaric acid, the biosyn- ception of Polypodiaceae and Tiliaceae, thetic precursor of umbelliferone (Brown, contain p-coumaric acid. In the genus 1960). While p-coumaric acid has an ex- Platysenta, P. sutor is recorded as feeding tremely broad distribution among plant on celery (Apium); its congeners all feed families (Hegnauer, 1964-1973) and thus exclusively on Compositae, a family known is hardly suggestive of a coevolutionary to contain both hydroxy- and furanocou- relationship, it nonetheless is a prerequi- marins. site for coumarin synthesis and its presence, in lieu of ferulic, sinapic, or cinnam- (6b) Diptera ic acid, indicates the phytochemical Two genera of Diptera in separate fam- relationship of the plant taxon to couma- ilies mine leaves of Umbelliferae (Table 8). rin-producing forms. Euleiafratria is a blotch miner associated The host plants of the genus Papilio are primarily with plants in the Umbelliferae much the same as Agonopterix and De- and incidentally with plants in the Com- pressaria (Table 6). The section of the ge- positae. Both of these plant families are nus most closely associated with the Um- reported to contain furanocoumarins as belliferae is Section II of Munroe (1960). well as hydroxycoumarins. The genus Outside the machaon complex, which feeds Phytomyza, an enormous and poorly exclusively on the furanocoumarin-con- understood genus in the Agromyzidae taining families Umbelliferae, Rutaceae (Griffiths, 1973), contains a number of and Compositae,. other Papilio species in species that feed exclusively (e.g., P. an-

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TABLE 7. Genera of Noctuidae containing at least TABLE 7. Continued. one Umbellifer specialist (from Crumb, 1956; Tietz, 1972). POLYGONACEAE-Rumex, GRAMINEAE-Zea

A. Papaipema P. furcata OLEACEAE-Fraxinus, P. marginidens ACERACEAE-Acer UMBELLIFERAE-Cicuta

P. harrisi B. Platysenta UMBELLIFERAE-Angelica P. sutor P. cerina UMBELLIFERAE-Apium LILIACEAE-Lilium, P. apameioides BERBERIDACEAE-Podophyllum COMPOSITAE-Bidens P. cataphracta P. vecors GENERALIST COMPOSITAE-Lactuca P. duovata P. discitriga COMPOSITAE-Solidago COMPOSITAE-Chrysothamnus P. pterisii P. videns POLYPODIACEAE-Pteris COMPOSITAE-Aster, Solidago P. lysimache PRIMULACEAE-Lysimachia P. nebris GENERALIST gelicae, pastinacae, chaerophylli, sii, ci- P. polymniae cutae, etc.) or incidentally (P. albiceps, COMPOSITAE-Polymnia fallociosa, obscurella) on the Umbellifer- P. circumlucens ae. In addition to Umbelliferae, these in- LEGUMINOSAE-Psoralea, COMPOSITAE-Senecio?, sects feed on Compositae, Leguminosae, Vernonia, APOCYNACEAE Caprifoliaceae, and Ranunculaceae, all P. insulidens families that contain hydroxycoumarins COMPOSITAE-Senecio (the single exception to the pattern is P. P. pertincta obscurella, which feeds on Aquifoliaceae COMPOSITAE-Petasites, and Crassulaceae in addition to five fam- LEGUMINOSAE-Lupinus ilies containing coumarins). P. beeriana COMPOSITAE-Liatris (6c) Coleoptera P. eupatorii COMPOSITAE-Eupatorium The only beetle eating the foliage of P. impecuniosa Umbelliferae to any great extent in eastern COMPOSITAE-Aster, Helenium North America is Apion, a curculionid. P. arctivorens Host records for foliage-feeding Apion COMPOSITAE-Cirsium, Arctium species (Table 9) are far from complete, DIPSACACEAE-Dipsacus but all recorded hosts (with the single ex- P. nelita ception of Arctostaphylos in the Ericaceae) COMPOSITAE-Rudbeckia for Apion species north of Mexico are P. frigida RANUNCULACEAE-Thalictrum species of plants in families with hydroxy- P. sciatra coumarins. In fact, Apion feeds on mem- SCROPHULARIACEAE-Veronica bers of three families that are reported to P. maritima contain furanocoumarins-several genera COMPOSITAE-Helianthus in the Umbelliferae, Psoralea in the Le- P. cerussata guminosae and Xanthoxylum in the Ru- COMPOSITAE-Vernonia taceae. P. merrickata BERBERIDACEAE-Podophyllum (7) Overview and Case in Point (Emboloecia) sauzalitae There is not a single example of an in- COMPOSITAE, SCROPHULARIACEAE-Castilleja, sect in eastern North America feeding exclusively on furanocoumarin-containing

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TABLE 8. Hostplants of North American Diptera occurring on Umbelliferae. a

Euleiafratria (=Acidia heraclei) (Tephritidae) UMBELLIFERAE-Angelica, Apium, Cryptotaenia, Heracleum, Levisticum, Pastinaca, Petroselinum, Sium COMPOSITAE-Arctium, Artemisia, Carduus, Chrysanthemum, Cirsium, Cnicus, Helianthus, Onopor- dum, Prenanthes

Phytomyza albiceps (Agromyzidae) UMBELLIFERAE-Heracleum, Pastinaca, Pimpinella COMPOSITAE-Arctium, Artemisia, Aster, Bidens, Centaurea, Chrysanthemum, Cirsiu, Erechtites, Eu- patorium, Onopordum, Senecio, Solidago, Sonchus, Tanacetum, Taraxacum LEGUMINOSAE-Lathyrus, Melilotus, Pisum CAPRIFOLIACEAE-Sambucus, Symphoricarpos

Phytomyza angelica (Agromyzidae) UMBELLIFERAE-Angelica, Heracleum, Laserpitium

Phytomyza archangelicae UMBELLIFERAE-Angelica

Phytomyza brunnipes UMBELLIFERAE-Sanicula

Phytomyza chaerophylli

UMBELLIFERAE-Anthriscus, Chaerophyllum, Selinum, Torilis

Phytomyza chrysanthemi UMBELLIFERAE-Daucus carota, Pastinaca sativa COMPOSITAE-Ambrosia, Antennaria, Bidens, Chrysanthemum, Eupatorium, Gazania, Helianthus, Senecio, Solidago, Tanacetum, Taraxacum

Phytomyza cicutae UMBELLIFERAE-Cicuta

Phytomyza fallaciosa UMBELLIFERAE-Heracleum, Pastinaca, Peucedanum COMPOSITAE-Arctium, Eupatorium, Lapsana BORAGINACEAE-Symphytum RANUNCULACEAE-Ranunculus

Phytomyzafascialis UMBELLIFERAE-Bupleurum

Phytomyza helosciadii UMBELLIFERAE-Helosciadium

Phytomyza latifolii UMBELLIFERAE-Laserpitium

Phytomyza marginella

UMBELLIFERAE-Peucedanum (Lomatium)

Phytomyza melana UMBELLIFERAE-Pimpinella

Phytomyza nigra UMBELLIFERAE-Helosciadium, Heracleum COMPOSITAE-Arctium RANUNCULACEAE-Aquilegia

Phytomyza obscurella UMBELLIFERAE-Aegopodium, Anthiscus, Chaerophyllum, Daucus, Pimpinella, Selinum COMPOSITAE-Chrysanthemum

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TABLE 8. Continued.

LEGUMINOSAE-Lupinus CAPRIFOLIACEAE-Diervilla, Lonicera, Sambucus, Symphoricarpus RANUNCULACEAE-Actaea, Aquilegia AQUIFOLIACEAE-Ilex CRASSULACEAE-Sedum

Phytomyza pastinacae UMBELLIFERAE-Pastinaca, Heracleum, Angelica

Phytomyza pauli-loewii UMBELLIFERAE-Peucedanum, Pimpinella

Phytomyza sphondylii UMBELLIFERAE-Heracleum, Pastinaca

Phytomyza tlingitica UMBELLIFERAE-Heracleum

a Hostplant records from Frost (1924) and Griffiths (1973). -a plant species with more than a single record constitutes a major hostplant.

plants (Berenbaum, 198 lb) that is not also ciprocal change in the array of species ex- closely related to species that feed on plants erting the initial selective pressure. Such containing hydroxycoumarins. Given the appears to be the case in at least three taxa limited distribution of coumarins in na- of insects (Coleoptera, Diptera and Lepi- ture, it is difficult to believe that hydroxy- doptera). Insects that feed on plants con- coumarin-feeding insects are related to taining furanocoumarins almost invari- furanocoumarin-feeding insects by phylo- ably feed also on plants containing genetic accident. The genus Psoralea, for hydroxycoumarins or are closely related to example, is the only North American ge- species that feed on plants containing hy- nus in the Leguminosae reported to con- droxycoumarins. Synthesis of hydroxy- tain furanocoumarins (Baskin et al., 1967) coumarins is a necessary prerequisite for and is at the same time a hostplant of formation of furanocoumarins; thus, it Apion, Agonopterix, Papaipema and is the seems eminently reasonable that insects sole leguminous host recorded for the ge- that feed on plants containing hydroxy- nus Papilio (Scriber, 1973)-all genera coumarins are most likely over evolution- with strong associations with furanocou- ary time to encounter plants containing marin-containing umbellifers. At best, it furanocoumarins and are thus most likely is unconvincing to invoke coincidence as to evolve resistance to them. Similarly, an explanation for the pattern; considering since angular furanocoumarins are not the vastly differing ecologies of the insect commonly produced in the absence of lin- genera, no other consistent explanation ear furanocoumarins, insects that feed on comes to mind except that these insect plants with linear furanocoumarins are genera have independently evolved resis- most likely to encounter angular furano- tance to furanocoumarins from progeni- coumarins and are most likely to evolve tors adapted to plants containing hydroxy- resistance to them. That these particular coumarins. insects are capable of generating sufficient It is difficult, if not impossible, to prove selective pressure to effect evolutionary coevolution-indeed, it has even proved changes in plant chemistry is suggested by difficult simply to define it (Janzen, 1980). the work of Hendrix (1979), who observed Janzen (1980) defines coevolution as an that Depressaria pastinacella is capable of evolutionary change in a trait of an array reducing seed set of Pastinaca sativa by of populations or species, followed by re- half, a substantial reduction in fitness.

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TABLE 9. Hostplants of Apion (Curculionidae) North TABLE 9. Continued. of Mexico (Kissinger, 1968). A. metallicum COMPOSITAE-Ambrosia, Aster, Dahlia, He- SUBGENUS FALLAPION lenium, Xanthocephalum A. anceps A. troglodytes COMPOSITAE COMPOSITAE-Artemisia A. ellipticum A. commodum UMBELLIFERAE-Chaerophyllum LEGUMINOSAE-Psoralea A. erraticum A. patruele COMPOSITAE-Chrysothamnus LEGUMINOSAE-Apios A. impunctistriatum A. perforicolle COMPOSITAE-Ambrosia, Heterotheca, Rud- LEGUMINOSAE-Amorpha, Tephrosia beckia A. procatum A. melanarium LEGUMINOSAE-Robinia COMPOSITAE-Bidens A. roseae A. minutum LEGUMINOSAE-Desmodium? UMBELLIFERAE-Ptilimnium A. cribicolle A. occidentale LEGUMINOSAE-Lotus COMPOSITAE-Helianthus A. tenuirostrum A. pennsylvanicum LEGUMINOSAE-Krameria, Petalostemum UMBELLIFERAE-Cicuta A. robustum COMPOSITAE-Xanthium? A. coracellumI (8) A Scenario of Coumarin-Insect UMBELLIFERAE-Cicuta, Sium, Angelica Coevolution

SUBGENUS IXIAS Host records and experiments with A. xanthoxyli bioassays of relative toxicity and resis- RUTACEAE-Xanthoxylum tance suggest the following scenario in the A. frosti evolution of coumarin chemistry: 1. P- CAPRIFOLIACEAE-Viburnum coumaric acid, an important intermediate A. heraculanum in lignin biosynthesis in many angiosperm CAPRIFOLIACEAE-Viburnum plant families, is the evolutionary precur- A. idiastes sor of hydroxycoumarins found in approx- CAPRIFOLIACEAE-Viburnum imately three dozen plant families. 2. Um- A. umboniferum CAPRIFOLIACEAE-Viburnum belliferone and related hydroxycoumarins possess toxic properties lacking in their p- SUBGENUS TRICHAPION coumaric acid precursors (Jurd et al., 1973; A. proclive LEGUMINOSAE-Lupinus Williams and Hoagland, 1982). 3. Plants producing hydroxycoumarins are freed A. simile BETULACEAE-Betula from constraints imposed by certain ene- A. glyphium mies (e.g., fungi, bacteria and plant com- LEGUMINOSAE-Diphysa petitors). 4. By mutation or recombina- A. cordatum tion, several groups of insects evolve LEGUMINOSAE-Psoralea mechanisms of resistance to hydroxycou- ERICACEAE-Arctostaphylos marins. This mechanism may be a gener- A. dolosum alized detoxication response present in po- LEGUMINOSAE-Robinia lyphagous species such as Spodoptera A. rostrum LEGUMINOSAE-Baptisia eridania (Lepidoptera: Noctuidae) (Scri- A. griseum ber, 1981). 5. As a result of adaptation to LEGUMINOSAE-Phaseolus feeding on plants containing hydroxycou- A. oriotes marins, insects can specialize on these LEGUMINOSAE-Phaseolus plants (tribe Amphisbatini in Oecophori- A. sayi dae; Section II Papilio excluding machaon LEGUMINOSAE-Strophostyles complex). 6. In response to selective pres-

This content downloaded from 165.230.49.193 on Tue, 03 Apr 2018 17:53:23 UTC All use subject to http://about.jstor.org/terms CATERPILLAR COUMARINS 175 sure of herbivores adapted to hydroxy- cases where experimental evidence is coumarins, plants in three dozen plant available, the generality of the test results families proliferate possessing an enzyme has not been demonstrated (e.g., steps 4, prenylating umbelliferone at the 7-position 6 and 11). Nonetheless, the scheme pro- and leading to formation of linear furano- vides at least a partial explanation for ob- coumarins. Due to the acquisition of a served patterns of insect herbivory and furan ring, linear furanocoumarins pos- plant resistance. Moreover, it can be used sess toxic properties lacking in their hy- to facilitate qualitative prediction within droxycoumarin precursors, i.e., photo- the system. The genus Artemisia in the toxicity (Berenbaum, 1978). 7. Plants Compositae, for example, is a hostplant producing linear furanocoumarins are for Phytomyza, Euleia, Apion, Agonop- freed from constraints imposed by cer- terix, Depressaria and is the only Com- tain enemies adapted to feeding on hy- positae host known for the genus Papi- droxycoumarins. 8. Insects feeding on lio-all genera with strong associations plants containing hydroxycoumarins en- with furanocoumarin-containing plants. counter linear furanocoumarins; some de- Artemisia, already known to contain hy- velop mechanisms of tolerating furano- droxycoumarins (Hegnauer, 1964), may coumarins (machaon complex in the genus well prove to be a rich source of furano- Papilio (Berenbaum, 1981c); genus Ago- coumarins. nopterix in the Oecophoridae). Those species that do not develop such a mechanism DISCUSSION either drop furanocoumarin-containing This study adds to the growing body of plants from their diets or become extinct. information the chemistry of insect-plant 9. As a result of adaptation to feeding on interaction, reinforcing and clarifying pat- plants containing linear furanocoumarins, terns observed in other systems (e.g., glu- insects can specialize on these plants. 10. cosinolates-Feeny, 1977; Rodman and In response to herbivory of specialist her- Chew, 1980). Despite its limitations in bivores, plants in two families proliferate scope, this system-coumarin-containing that possess an enzyme that prenylates plants and associated herbivores-can umbelliferone at the 8-position, leading serve as a paradigm for similar systems, to the formation of angular furanocou- i.e., plants containing "qualitative" toxins marins. 11. Angular furanocoumarins (sensu Feeny, 1976) and their associated possess toxic properties to herbivores lack- specialized herbivores. Insofar as taxono- ing in linear furanocoumarins produced in my reflects chemistry, insect-plant coevo- the same plants (e.g., Papilio polyxenes) lution often appears to follow consistently. (Berenbaum and Feeny, 1981). 12. Insects Yet there are many examples of hostplants feeding on plants containing linear fu- perceived as anomalies in hostplant usage ranocoumarins encounter angular furan- patterns because they do not follow along ocoumarins; some develop mechanisms of taxonomic lines. These anomalies may well tolerating the toxicity of angular furano- be resolved with greater understanding of coumarins. Those species that do not de- the biochemistry of the "aberrant" host- velop such a mechanism either drop these plants; taxonomic inconsistency may ob- plants from their diets or become extinct. scure independent evolution of biosyn- 13. Insects adapted to feeding on plants thetic pathways in disparate groups of containing angular furanocoumarins be- plants. Preadaptation on the part of the gin to specialize on these plants (genus De- insect with subsequent specialization could pressaria in Oecophoridae, P. brevicauda generate such anomalous usage patterns. in Papilio machaon complex?) (Beren- Coumarins provide a case in point. Sec- baum, 1981a). tion II of the genus Papilio is associated This scenario is speculative; many of the primarily with the furanocoumarin-con- proposed steps (e.g., 12) have yet to be taining Rutaceae and, within the ma- tested experimentally and even in those chaon, demolion and demoleus groups,

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Umbelliferae. Within the demoleus group lacking coumarins (e.g., Umbelliferae), and there is a species restricted to the genus insect groups associated with coumarin- Psoralea in the Leguminosae (J. M. Scri- containing plants are more diverse than ber, unpubl.). This pattern is anomalous related groups on plants without couma- taxonomically-yet is compatible with host rins (e.g., Oecophoridae and Papilioni- chemistry, Psoralea being one of only two dae). This is consistent with the idea that leguminous genera that synthesize furan- reciprocal evolutionary interactions, fo- ocoumarins. Taxonomically anomalous cusing on secondary plant chemistry, hostplant "omissions" can be accounted for greatly augment the organic diversity of by chemical coevolution as well. The ab- both herbivorous insects and plants. sence of hostplant records for the machaon group on Araliaceae, a family with some ACKNOWLEDGMENTS herbaceous representatives sympatric with This work was supported by an N.S.F. and closely related to Umbelliferae (Hey- predoctoral fellowship and by National wood, 1971), is understandable in that the Science Foundation research grants DEB family is chemically distinct from the Um- 7620114 and DEB 7922130 to Paul Feeny. belliferae, lacking flavones and furano- I thank members of my thesis committee, coumarins altogether (Hegnauer, 1964- Thomas Eisner and David Bates, for com- 19 7 3; Heywood, 19 7 1). Similar patterns of ments on relevant portions of my disser- omissions or inclusions in other herbivore- tation, Mark Rausher for discussion, and plant systems may be resolved with a clos- my advisor Paul Feeny for his insight, ex- er examination of the underlying biosyn- pertise and general good nature. Frances thetic relationships among the plants. By Chew and Douglas Futuyma made helpful the same token, the documentation of par- suggestions and Don Strong did a breath- allel series of herbivorous groups across takingly thorough and much appreciated broad phyletic lines may provide insights job of reviewing the manuscript. into hitherto unsuspected chemical simi- larities among plants. LITERATURE CITED

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There will be a joint meeting of

Society for the Study of Evolution Genetics Society of America American Society of Naturalists Stadler Symposium

June 12-16, 1983 Washington University St. Louis, Missouri

Symposia will be held on Molecular Evolution, Plant Genetics, Immunogenetics, Mass Extinctions, Chromatin Structure, Genetic Epidemiology, and Human Evolu- tion, and there will be contributed paper sessions and a poster session. Additional information can be obtained from:

The Organizing Committee Evolution 83 Department of Botany Washington University St. Louis, Missouri 63130

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