Mimicry 633 a directional fl ight across Gatun Lake in the Panama Canal. Clock- Further Reading shift experiments resulted in changes in the direction of orientation that were consistent with a sun compass, even though there was also Brower , L. P. , and Malcolm , S. B. ( 1991 ) . Animal migrations: Endangered phenomena . Am. Zool. 31 , 232 – 242 . a component imposed by wind drift. The sophisticated orientation Dingle , H. ( 1996 ) . “ Migration: The Biology of Life on the Move . ” Oxford mechanisms of honey bees, ants, and certain other insects incorpo- University Press , New York . rating a sun compass, imply that orientation is probably widespread. Dingle , H. ( 2001 ) . The evolution of migratory syndromes in insects . In The future will undoubtedly reveal the presence of a sun compass in “ Insect Movement: Mechanisms and Consequences ” ( I. Woiwood , and other migrants, as well as the presence of other mechanisms, espe- D. R. Reynolds , eds. ) , pp. 159 – 181 . CAB International , London, U.K. cially in nocturnal migrants. Radar observations indicate that the Johnson , C. G. ( 1969 ) . “ Migration and Dispersal of Insects by Flight . ” passage of many species of nocturnal migrants is specifi c to winds Methuen , London, U.K. of a certain direction, but the means by which this preference is Kennedy, J. S. (1985). Migration: Behavioral and ecological. In “ Migration: enforced are unknown. Mechanisms and Adaptive Signifi cance ” (M. A. Rankin, ed.). Contr. Mar. Sci. 27 (suppl.), 5 – 26. p2700 In addition to behavioral and physiological characters, migration Oliveira , E. G. , Srygley , R. B. , and Dudley , R. ( 1998 ) . Do Neotropical migrant syndromes often include life history traits such as the age at fi rst butterfl ies navigate using a solar compass? J. Exp. Biol. 201 , 3317 – 3331 . reproduction and fecundity, particularly in many wing-polymorphic Rankin , M. A. ( 1991 ) . Endocrine effects on migration . Am. Zool. 31 , insects. Typically, in these species the short-winged or wingless forms 217 – 230 . reproduce earlier and display higher fecundities than their long- Rankin , M. A. , and Burchsted , J. C. A. ( 1992 ) . The cost of migration in winged counterparts. This dichotomy is at least in part because of insects . Annu. Rev. Entomol. 37 , 533 – 559 . trade-offs between fl ight and reproduction. The metabolically active Zera , A. J. , and Denno , R. F. ( 1997 ) . Physiology and ecology of dispersal poly- fl ight muscles that accompany long wings and migration are costly morphisms in insects . Annu. Rev. Entomol. 42 , 207 – 231 . to maintain, requiring considerably more maintenance energy than the thoracic musculature of wingless or short-winged individuals. In contrast, the later reproducing individuals, with lower egg produc- tion, are often longer lived. p2710 Migration syndromes that include life history traits are the result of underlying genetic mechanisms, as revealed in artifi cial experiments c9080 Mimicry using the large milkweed bug. Like all fl ying insects, this migrant can be induced to fl y by removing substrate contact. Bugs that are glued Mathieu Joron at the prothorax to a tether will fl y if contact with the tarsi is removed. Musé um National d’Histoire Naturelle, France An individual in the migratory state can fl y on the tether for several hours, and the duration of fl ight can be used as an index of migra- M tion. Artifi cial selection can be used to increase the proportion of imicry is the adaptive resemblance in signal between sev- p10470 individuals making long (or short) fl ights, with the duration of fl ights eral species in a locality. The most spectacular and intrigu- also affected. Selection was used to both increase and decrease the ing cases are those of accurate resemblance between M proportion of bugs undertaking long fl ights. In addition to fl ight, wing distantly related animals, such as spiders mimicking ants. Closely length and fecundity responded to this selective regime. The bugs of related species can also benefi t from mutual resemblance, in which the line with a higher proportion of long fl ights also had longer wings case mimicry results from selection against signal divergence. on average, and the females of this line produced more eggs during The vast majority of the hundreds of thousands of insect spe- p10480 the fi rst 5 days of reproductive life. This means that the genes infl u- cies are described and identifi able on the basis of morphological encing fl ight also infl uenced wing length and fecundity, most likely characters. This bewildering diversity is, however, ordered because via pleiotropic effects. Longer term selection experiments on wing species share characters with their relatives — and one of the taxono- length, which also resulted in higher fecundities and increased fl ight mist’s tasks is indeed to recognize, among the shared and divergent as wing length increased, suggested that linkage disequilibrium is characters, a sign of the relatedness of the taxa. Nevertheless, some unlikely. Parallel selection experiments on a population that did not distantly related species may share a common morphology. Such migrate failed to reveal genetic correlations among wing length, fl ight, resemblance may be the result of evolutionary convergence, that is, and fecundity, indicating that the genetically based syndrome of cor- parallel lifestyles leading to the selection of similar morphological relations among these traits is unique to migratory populations. The structures; in this case, resemblance per se is not under selection. selection experiments reveal that natural selection has produced an On the contrary, when a character is taken as a signal between indi- adaptive migratory syndrome that includes wing length and fecundity. viduals, one species may benefi t from bearing the same signal as the Interestingly, the age at fi rst reproduction is unaffected by selection. one already used by another species; then selection acts directly to favor increased resemblance. p2720 The conclusion from the brief survey of insect migration is that this behavior involves more than simply extended movement to escape to a new habitat. Rather, migration is a trait of considerable AN INTERACTION BETWEEN THREE s9620 complexity, requiring knowledge of behavior, development, ecology, PROTAGONISTS physiology, and genetics to provide a full understanding of its evolu- tion and function. The Discovery of Mimicry and the s9630 Development of Evolutionary Hypotheses Mimicry in insects has been a puzzle for entomologists long p10490 s1020 See Also the Following Articles before the Darwinian concept of natural selection, but the expla- p2730 Aphids ■ Juvenile Hormone ■ Locusts ■ Magnetic Sense ■ Monarchs nations for mimicry are tightly linked to the development of evolu- ■ Orientation tionary thinking. While he was traveling in the Amazon with Alfred CARDE 978-0-12-374144-8 00012 CH012.indd 633 3/18/2009 7:46:46 AM 634 Mimicry Russel Wallace in 1842, British entomologist Henry Walter Bates noted that distantly related butterfl y species bore the same wing color pattern. Moreover, these communities of species changed their shared pattern in concert across localities. Among these species were the very abundant Ithomiinae (called Danaoid Heliconiidae then, now a subfamily in the Nymphalidae) and rarer Dismorphiinae (called Leptalidae then, now a subfamily in the Pieridae). Bates, as a pioneer evolutionist (but after Darwin published his On the Origin of Species ), developed an adaptive explanation for the resemblance. Hypothesizing that ithomiines were inedible to most predators, he proposed that the edible pierids would benefi t from being mis- taken for their defended counterparts and would thus be selected to resemble them. Edward B. Poulton later named this kind of mimicry after him as Batesian mimicry, when an edible species mimics a dis- FIGURE 1 Conditioned predators and signaling prey. Predators f0290 tasteful one. are known to generalize their knowledge of distasteful prey to other p10500 Bates also realized that some apparently inedible ithomiine resembling prey. Therefore, once predators recognize one prey as species in the genus Napeogenes seemed to mimic other inedible distasteful (prey A), other prey may gain from mimicry, whatever Ithomiinae. He proposed that, in fact, rare species, whatever their be their palatability (prey B and C). If the prey is palatable (prey palatability, should benefi t from resembling defended common spe- C), its mimetic gain becomes limited by its abundance in the local- cies. It was, however, more diffi cult to understand the resemblance ity. Finally, a conspicuous prey with a (nonmimetic) pattern new to of abundant and distasteful Melinaea , Mechanitis (Ithomiinae), the predator should suffer higher mortality, making the evolution of Lycorea (Danainae), and some Heliconius (Heliconiinae) from Peru diversity in warning color and mimicry a puzzle. and Colombia, so he assumed the resemblance was the result of some inorganic or environmental factors. In 1879, German naturalist Fritz M ü ller was the fi rst to develop a mathematical demonstration prey is thus fooled by the predator via its own conspecifi c signal. that two unpalatable prey could benefi t from mutual resemblance. The two senders can also be the same species. This is sometimes the He understood that, if the community of predators had to kill a cer- case in chemical-sequestering phytophagous insects when unpalat- tain (fi xed) number of prey to learn to avoid them, two indistinguish- ability varies among individuals