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Selection on warning coloration by visually hunting predators is predicted to result in monomorphic aposematic prey3. Despite this, polymorphisms for aposematism exist4. These polymorphic phenotypes represent variations on a similar aposematic theme, rather than a difference between crypsis and conspicuousness. Changes from cryptic to aposematic morphs have been thought of as evolutionary change, not polymorphism, but phenotypic plasticity in coloration can allow this transition to occur within a single generation.

Some populations of juvenile S. emarginata in Texas feed mainly on Ptelea trifoliata (Rutaceae), despite the presence of other acceptable host plants5, causing nymphs to congregate there. S. emarginata nymphs from populations that feed on Ptelea exhibit a density-dependent colour polymorphism: typically, they are green at low rearing densities, and yellow and black at high rearing densities (Fig. 1a).

Figure 1: Avoidance of Schistocerca emarginata by Anolis carolinensis lizards.
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a, The green and yellow-and-black morphs of S. emarginata. b, Ptelea-conferred unpalatability. Adult A. carolinensis naive with respect to S. emarginata were controlled for motivational state and offered yellow-and-black S. emarginata nymphs reared on either Ptelea (n=19) or Rubus (n=19). Consumption without regurgitation was scored as acceptance. Attacking and releasing or regurgitation within 24 hours was scored as rejection. Each lizard was used once. c, Lizards discriminated against yellow-and-black in favour of green grasshoppers after experience with yellow-and-black Ptelea-reared grasshoppers. Lizards from the palatability assay were offered a simultaneous-choice test between a green Chortophaga viridifasciata nymph and a similar-sized yellow-and-black S. emarginata nymph. C. viridifasciata were used because it was not possible to rear green S. emarginata in sufficient numbers. Lizards eating both insects were omitted from the analysis.

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Juveniles from a Ptelea-feeding population were reared from hatching outdoors in screen cages as isolated individuals (n=28) or under crowded conditions in groups of ten (n=31). Increased rearing density significantly increased the melanized (black) proportion of the pronotum, wing, femur and abdomen of final-instar insects (P<0.0001, t-tests on arcsine-transformed data), as well as the frequency of yellow relative to green and yellow/green background coloration (P<0.0001, monte carlo contingency table). this polymorphism was independent of rearing diet5.

Yellow-and-black S. emarginata were unpalatable to insectivorous lizards (Anolis carolinensis) when reared on Ptelea, but not when reared on Rubus trivialis (Rosaceae) (P<0.0001, fisher's exact test) (Fig. 1b). Unpalatability was mediated by gut content and was rapidly lost when insects were fed a non-toxic plant. All 14 S. emarginata that were reared on Ptelea but fed Romaine lettuce for 24 hours were accepted by lizards (P<0.0001, fisher's exact test, comparison with Ptelea-only diet treatment in Fig. 1b). Lizards previously fed unpalatable yellow-and-black Ptelea-reared S. emarginata discriminated against yellow-and-black grasshoppers in favour of green grasshoppers significantly more often than lizards previously fed palatable yellow-and-black Rubus-reared S. emarginata(P<0.05, fisher's exact test; Fig. 1c). The yellow-and-black coloration of S. emarginata nymphs at high local densities can therefore function as a warning signal when the insects have been feeding on plants containing unpalatable chemicals.

The desert locust, S. gregaria, also exhibits a density-dependent nymphal colour polymorphism6, the biological role of which remains a mystery. My results indicate that the colour patterns of S. gregaria may be related to specific host plants. In non-outbreak populations, predation can be a strong mortality agent7. Nymphs eat plants containing compounds toxic to vertebrates8, and crowding on plants can facilitate colour change9. Density-dependent aposematism could reduce predation and population extinction rates in areas where insects feed on plants that make them unpalatable to predators, and could hasten the initial stages of population increase under favourable environmental conditions.

Phenotypic plasticity in coloration may have facilitated evolution of aposematism in insects. Density-dependent changes from cryptic to conspicuous phenotypes occur in several insect lineages10. Among organisms with the appropriate genotype, density-dependent colour polymorphism could reduce the initial cost of conspicuousness once unpalatability (or some form of unprofitability) has been achieved. The evolution of this trait would be influenced by many factors, including, but not limited to, prey population dynamics and local predator behaviour. Examples of density-dependent aposematism may represent snapshots of this evolutionary process in action.