View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Current Biology 21, R738–R749, September 27, 2011 ª2011 Elsevier Ltd All rights reserved DOI 10.1016/j.cub.2011.06.006 Polyphenism in Insects Review Stephen J. Simpson1, Gregory A. Sword2, and Nathan Lo1 cues. Until publication of Mayr’s 1963 book, however, envi- ronmentally induced phenotypic plasticity suffered the taint of Lamarckism and was largely ignored in favour of Polyphenism is the phenomenon where two or more the more respectable, or to use Mayr’s words, ‘‘more useful distinct phenotypes are produced by the same genotype. and precise’’ study of genetic polymorphisms, in which Examples of polyphenism provide some of the most phenotypic variants are produced by different rather than compelling systems for the study of epigenetics. Poly- the same genotypes [5]. phenisms are a major reason for the success of the Mayr’s definition of polyphenism was broadly inclusive of all insects, allowing them to partition life history stages manner of discontinuous and continuous phenotypes. Other (with larvae dedicated to feeding and growth, and adults definitions have been more restrictive. As pointed out by dedicated to reproduction and dispersal), to adopt Canfield and Greene [5], however, it is somewhat arbitrary different phenotypes that best suit predictable environ- to impose limits such as whether plastic phenotypes are mental changes (seasonal morphs), to cope with tempo- discrete or continuous [6], present within or between develop- rally heterogeneous environments (dispersal morphs), mental stages [7] or seasons [8], fixed rather than reversible and to partition labour within social groups (the castes of [9], or demonstrably adaptive rather than apparently offering eusocial insects). We survey the status of research no selective advantage. We are inclined to endorse Mayr’s on some of the best known examples of insect polyphen- more inclusive definition, especially given that what is ism, in each case considering the environmental cues known of the controlling mechanisms of polyphenisms does that trigger shifts in phenotype, the neurochemical and not support more restrictive definitional boundaries. As we hormonal pathways that mediate the transformation, the describe below, this is exemplified by the involvement of molecular genetic and epigenetic mechanisms involved the same developmental hormones that control insect in initiating and maintaining the polyphenism, and the metamorphosis in various environmentally induced poly- adaptive and life-history significance of the phenomenon. phenisms, including examples that are continuous or discrete We conclude by highlighting some of the common fea- in nature. Regardless of the definition used, the insects offer tures of these examples and consider future avenues for a marvellous array of examples of poylphenisms [10]. research on polyphenism. Where Does Polyphenism Occur among the Insects? Introduction Everywhere is the brief answer. The developmental stages of insects offer some of the most extraordinary examples, as seen in the transition from larva to pupa to adult in holome- ‘‘In order to make the term ‘polymorphism’ more useful tabolous (discontinuously developing) insects such as the and precise, there is now a tendency to restrict it Lepidoptera (moths and butterflies), Coleoptera (beetles), to genetic polymorphism. Since this would leave nonge- Hymenoptera (ants, bees and wasps) and Diptera (true flies). netic variation of the phenotype without a designation, Additionally, there are seasonal morphs (exemplified by the the term ‘polyphenism’ is here proposed for it. Poly- aphids and Lepidoptera), density-dependent phenotypes phenism is discontinuous when definite castes are (the defining feature of the group of grasshopper species present (certain social insects) or definite stages in the known as locusts), plastic sexually selected phenotypes life cycle (larvae vs. adults; sexual vs. parthenogenetic) (for example, in horned beetles), and diet-mediated pheno- or definite seasonal forms (dry vs. wet; spring vs. types (as seen in some caterpillar morphs and in the castes summer). Polyphenism may be continuous, as in the of social insects), to mention only a selection [10]. cyclomorphosis of fresh-water organisms and some Indeed, polyphenisms are a major reason for the success other seasonal variation.’’ of the insects. They offer the opportunity for insects to deploy — Ernst Mayr [1] the same genome to partition life history stages (feeding larval stages versus reproducing, dispersing adults), to With this statement in 1963, Ernst Mayr helped return the adopt phenotypes that best suit predictable environmental study of phenotypic plasticity to respectability [1]. During changes (seasonal morphs) or what might be termed the late 1800s, August Weismann in Freiburg and Edward ‘predictably unpredictable’ environmental shifts such as Poulton at Oxford had shown the power of environmental the transformation of desert environments after unpredict- cues to change the phenotype in moths and butterflies able rain or the degradation of an environment by overcrowd- [2,3]. Later, working on helmet length (cyclomorphosis) in ing. Insects have even recruited polyphenism to partition clones of Daphnia, Leipzig biologist Richard Woltereck [4] labour within social groups, leading to some of the most introduced the term ‘reaktionsnorm’ (reaction norm) to successful animals on the planet, the eusocial insects. describe how the phenotype of an individual depends on Here we will leave aside insect developmental stages, the interaction between its genotype and environmental and instead focus upon some of the archetypal examples of environmentally induced polyphenisms. In discussing each case we will consider first the nature of the polyphenism, 1School of Biological Sciences, The University of Sydney, NSW 2006, then the sensory cues that trigger shifts in phenotype, the Australia. 2Department of Entomology, Interdisciplinary Faculty of neurochemical and hormonal pathways that mediate the Ecology and Evolutionary Biology, Texas A&M University, College transformation, and finally, the molecular genetic and epige- Station, TX 77843-2475, USA. netic mechanisms involved in initiating and maintaining the E-mail: [email protected] polyphenism. Additionally, where it is known, we will discuss Special Issue R739 Figure 1. The catkin (left) and twig (right) morphs in caterpillars of the moth Nemoria arizonaria (photo courtesy of Erik Greene). the adaptive significance and popula- tion-level consequences of the phenomenon. As we shall show, no single example is known exhaustively in all of these respects, but each system nevertheless illustrates important aspects of the general phenomenon. Seasonal and Diet-Induced Morphs in Lepidoptera Since the work of Poulton and Weis- man, the Lepidoptera have provided an abundant source of examples for polyphenism research [11]. Here we will consider two notable examples, the first concerning a remarkable larval polyphenism and the second involving adult butterflies. The genus Nemoria contains over 130 species of geome- however, is associated with the timing of development trid moths, all of which are found in the New World and rather than temperature per se. The key hormonal signals many of which are superb mimics of their host plants are circulating levels of ecdysteroids, whereas juvenile as caterpillars. The species N. arizonaria is a host-plant hormone (JH) appears not to be involved [14]. An abrupt specialist restricted to oak. The moth has two generations shift in the timing of peak concentrations of ecdysteroids each year, one in spring and the other in summer. Caterpil- in the haemolymph of the pupa occurs at larval develop- lars from the spring generation emerge when the oaks are mental temperatures between 21 and 23C. At 21C and in flower. They feed upon and develop into perfect physical below, the peak occurs later during pupal development mimics of oak flowers (catkins). The summer generation, (at 40% of pupal development) than it does at larval rearing by contrast, emerges onto oaks that are no longer in flower temperatures of 23C and higher (30% of pupal develop- and instead feed upon leaves. These caterpillars grow to ment). Hence, ecdysteroid release translates a continuous look like oak twigs. Adding to the effectiveness of this twig environmental cue (temperature) into a threshold phenotypic mimicry, when resting they anchor their hind ends and trait [14]. project their bodies outwards at an appropriately twig-like Experiments involving gene expression studies, use of angle (Figure 1). mutants, and surgical manipulations have uncovered the Greene and colleagues [12,13] showed that the catkin and mechanisms of eye-spot formation (reviewed in [11] and twig morphs are produced as a result of larval diet: young [15]). The initial formation of an eye-spot occurs by activation caterpillars fed catkins grow to be catkin mimics, whereas of a focal region of cells, which signal surrounding epidermal those fed leaves become twig mimics. Other environmental cells to seed the synthesis of pigment, leading to formation cues, such as day length, temperature, humidity and back- of an eye spot. The gene distal-less (Dll) is involved in stipu- ground colour, have no effect. Which aspect of food lation of a focal region [16]. Expression of genes such as chemistry is responsible for the developmental switch Dll appears to be regulated via levels of circulating