Mr. Berenbaum et Ar. Zangerl, FURANOCOUMARIN METABOLISM IN PAPILIO-POLYXENES - BIOCHEMISTRY, GENETIC-VARIABILITY, AND ECOLOGICAL SIGNIFICANCE, Oecologia, 95(3), 1993, pp. 370-375
The ubiquitous occurrence of series of biosynthetically related plant
secondary compounds within individual species has given rise to the su
ggestion that such multiplicity is adaptive; one possible mechanism th
at would serve to maintain such within-plant diversity is analog syner
gism. In a series of experiments, we provide evidence that synergism m
ay account for the presence of multiple structurally related furanocou
marins in apiaceous plants. The black swallowtail, Papilio polyxenes,
feeds exclusively on plant species containing furanocoumarins. Growth
of larvae fed parsley leaves treated with both xanthotoxin and angelic
in, two furanocoumarins that co-occur widely in swallowtail hostplants
, was significantly slower than that of larvae fed leaves with an equi
molar concentration of either xanthotoxin or angelicin. A multivariate
combination of growth, food consumption and frass excretion differed
significantly between larvae fed leaves treated with both xanthotoxin
and angelicin and larvae fed leaves treated with angelicin alone. In a
ddition, we measured rates of in vitro cytochrome P450-mediated metabo
lism of three furanocoumarins - bergapten, xanthotoxin, and angelicin.
While bergapten and xanthotoxin, both linear furanocoumarins, were me
tabolized at similar rates (8.07 and 9.86 nmoles/min/g fw caterpillar,
respectively), angelicin, an angular furanocoumarin, was metabolized
more slowly (2.76 nmoles/min/g fw caterpillar). When all three furanoc
oumarins were assayed together, overall rates of metabolism were signi
ficantly reduced, suggesting substrate inhibition. Thus, the pattern o
f growth of larvae is consistent with the pattern of in vitro metaboli
sm and is evidence in support of analog synergism. In a separate exper
iment, metabolism of xanthotoxin and angelicin individually and togeth
er were compared in six maternal families. Again, angelicin was metabo
lized more slowly than xanthotoxin and each furanocoumarin inhibited m
etabolism of the other. That significant family effects were found for
rates of metabolism and for the ratio of moles of angelicin metaboliz
ed for each mole of xanthotoxin metabolized raises the possibility tha
t genetic variation exists for the rate and specificity of metabolism
and suggests that insect herbivores may be able to adapt to analog syn
ergism.