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Wing Dimorphism in Aphids Heredity (2006) 97, 192–199 & 2006 Nature Publishing Group All rights reserved 0018-067X/06 $30.00 www.nature.com/hdy SHORT REVIEW Wing dimorphism in aphids C Braendle1, GK Davis2, JA Brisson2 and DL Stern2 1Institut Jacques Monod, CNRS, Universite´s Paris 6 and 7, Tour 43, 2 place Jussieu, 75251 Paris cedex 05, France; 2Department of Ecology & Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA Many species of insects display dispersing and nondispers- fecundity. In this review, we provide an overview of the major ing morphs. Among these, aphids are one of the best features of the aphid wing dimorphism. We first provide a examples of taxa that have evolved specialized morphs for description of the dimorphism and an overview of its dispersal versus reproduction. The dispersing morphs phylogenetic distribution. We then review what is known typically possess a full set of wings as well as a sensory about the mechanisms underlying the dimorphism and end and reproductive physiology that is adapted to flight and by discussing its evolutionary aspects. reproducing in a new location. In contrast, the nondispersing Heredity (2006) 97, 192–199. doi:10.1038/sj.hdy.6800863; morphs are wingless and show adaptations to maximize published online 5 July 2006 Keywords: alternative phenotypes; aphids; phenotypic plasticity; wing polyphenism; wing polymorphism Aphid biology Differences between winged and wingless Aphids are small, soft-bodied insects of the order aphid morphs Hemiptera that feed on the fluid in plant phloem. The winged and wingless phenotypes in aphids differ Aphids exhibit complex life cycles. Approximately 10% in a range of morphological, physiological, life history of species alternate between a primary (usually woody) and behavioural features. Besides having wings and host plant and a secondary (herbaceous) host plant. functional flight muscles, the fully winged morph Nonhost-alternating species are usually monophagous exhibits heavier sclerotization of head and thorax, more but may feed on a range of related host plants (Blackman fully developed compound eyes, ocelli, longer antennae, and Eastop, 1994). Aphids display a high reproductive more rhinaria, and sometimes larger siphunculi and rate due to three peculiarities of their reproductive cauda (Kalmus, 1945; Kring, 1977; Kawada, 1987; biology. First, during the spring and summer months, Miyazaki, 1987). Most of these differences reflect female aphids reproduce parthenogenetically, obviating the different life styles of the two phenotypes, as the the need for males. Second, during these parthenogenetic winged morphs are equipped with an elaborate sensory generations, the embryos initiate development immedi- system for flight and host plant location. Consistent ately after the budding of the oocyte from the germarium with this theme, winged forms are also more resistant and are born as fully developed first-instar nymphs (ie, to starvation (Tsuji and Kawada, 1987b; Hazell et al, they are viviparous). Finally, the oldest embryos also 2005). contain embryos, so that adult parthenogenetic aphids The morphological differences between winged and carry not only their daughters but also some of their wingless phenotypes usually correlate with differences granddaughters within them. During the fall, declining in life history. In general, the winged phenotype differs daily photoperiod and temperature induce the develop- from the wingless phenotype by showing longer nym- ment of sexual females and males. These sexual aphids phal development, longer pre-reproductive adult period, mate and females produce yolk-rich eggs that undergo longer reproductive period, lower offspring production, diapause to survive the winter (ie, they are oviparous). and prolonged longevity (Noda, 1960; MacKay and Different species of aphid may exhibit wing dimorph- Wellington, 1975; Campbell and Mackauer, 1977; Tsuji ism at various stages of the life cycle. Here, we and Kawada, 1987b; Tsumuki et al, 1990). In addition, in distinguish between environmentally induced dimor- response to shortened photoperiod, winged females tend phism, known as polyphenism, and genetically determined to produce mainly sexual females whereas wingless dimorphism, known as polymorphism. Wing polyphen- females produce both sexual females and males (MacKay ism occurs primarily among parthenogenetic females, et al, 1983; Nunes and Hardie, 1996). while wing polymorphism has been found only in males. While the bulk of the discussion that follows concerns the female polyphenism, we end with a consideration of Phylogenetic distribution of wing dimorphisms its relationship to the male polymorphism (Figure 1). Phylogenetic evidence indicates that the wingless form in aphids has been secondarily derived, as in most other Correspondence: C Braendle, Institut Jacques Monod, CNRS, Universite´s insects. Within the Aphididae – comprising more than Paris 6 and 7, Tour 43, 2 place Jussieu, 75251 Paris cedex 05, France. E-mail: [email protected] 95% of all 4400 extant aphid species – there is extensive Received 9 January 2006; accepted 1 June 2006; published online 5 variation in the occurrence of winged and wingless July 2006 morphs at different stages of the life cycle. Many species Wing dimorphism in aphids C Braendle et al 193 Figure 1 The female polyphenism (left) and male genetic polymorphism (right). In both cases, discrete alternative wingless (top) or winged (bottom) morphs are produced. of the more primitive taxa, such as the Calaphidinae, dwelling aphid species, which often produce exclusively produce only winged parthenogenetic females (Hille winged females compared to species feeding on herbace- Ris Lambers, 1947, 1966; Heie, 1982). In some of these ous plants, possibly because flight allows aphids to find a species, however, some winged females may differ in suitable feeding location in architecturally complex trees their flight capability or colonies may display variation in (Waloff, 1983). wing length (Hille Ris Lambers and van den Bosch, 1964; In most species the sexual females are wingless, with Hille Ris Lambers, 1966; Dixon, 1972; Heie, 1982; exceptions in more primitive taxa. Sexual males of Heikinheimo, 1987). In Drepanosiphum dixoni, for exam- Eriosomatinae, Anoeciinae, Hormaphidinae, and some ple, all parthenogenetic females develop wings, yet some Lachninae are wingless. In most other taxa males are individuals lack indirect flight muscles and are therefore winged; for example, the males of all host-alternating not capable of flight (Dixon, 1972). In other calaphidine aphidines are winged (Blackman and Eastop, 1994, 2000). species (eg, Symydobius oblongus) the parthenogenetic In about 10% of European species, however, both winged females show consistent differences in wing length, and and wingless males have been recorded (Smith and the short-winged females do not fly (Heikinheimo, 1987). MacKay, 1989). In the few species that have been Most species of the Aphididae, however, produce both examined in detail, this dimorphism is apparently fully winged and completely wingless parthenogenetic caused by a genetic polymorphism (Hille Ris Lambers, females. 1966; Mu¨ ller, 1969; Smith and MacKay, 1989). The diverse dispersal strategies of aphids appear to have evolved in association with two dominant ecologi- cal factors: host plant alternation and type of host Mechanisms plant. In host-alternating species, the morphs migrating between the primary and secondary hosts are always Environmental cues winged, whereas both winged and wingless females The environmental conditions affecting the production of frequently occur during the parthenogenetic generations winged versus wingless morphs have been studied on the summer host for both host-alternating and intensively (Hille Ris Lambers, 1966; Lees, 1966; Mittler nonhost-alternating species (Blackman and Eastop, and Sutherland, 1969; Kunkel and Kloft, 1974; Mu¨ ller 1994). Certain host plant characteristics, such as host et al, 2001). Here, we briefly summarize the conditions plant persistence, may also correlate with the propensity known to cue production of the winged morph, focusing to produce predominantly winged or wingless parthe- on parthenogenetic females. nogenetic females. Ephemeral host plants, including annual herbaceous hosts, can be exploited only tempora- Density (tactile stimulation): Density-dependent regula- rily and dispersal to new or more persistent hosts must tion of alternative dispersal phenotypes is common in take place at some point during the life cycle. Consistent aphids and other insects. Increased aphid density with this idea, species feeding on large or perennial host triggers wing formation in many species and in plants may exhibit a lower incidence of winged morph some species a small increase in density is suffi- production (Groeters, 1989). An exception are tree- cient (Bonnemaison, 1951; Johnson, 1965; Lees, 1967; Heredity Wing dimorphism in aphids C Braendle et al 194 Sutherland, 1969a, b; Shaw, 1970a). The proximate carried within adults), winged adults rarely or never mechanism mediating these environmental conditions produce winged offspring (Lees, 1961; Sutherland, 1970). appears to be increased tactile stimulation between Similarly, early born progeny descended from winged individual aphids (Johnson, 1965). However, it is mothers exhibit a decreased production of winged possible that chemical cues play an additional minor morphs (Mackay and Wellington, 1977). In contrast, role (Kunert and Weisser, 2005). While the location of
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