1 Heredity 2006 Vol: 97(3):192-199. DOI: 10.1038/sj.hdy.6800863

Wing dimorphism in aphids

Many species of insects display dispersing and nondispersing morphs. Among these, aphids are one of the best examples of taxa that have evolved specialized morphs for dispersal versus reproduction. The dispersing morphs typically possess a full set of wings as well as a sensory and reproductive physiology that is adapted to flight and reproducing in a new location. In contrast, the nondispersing morphs are wingless and show adaptations to maximize fecundity. In this review, we provide an overview of the major features of the aphid wing dimorphism. We first provide a description of the dimorphism and an overview of its phylogenetic distribution. We then review what is known about the mechanisms underlying the dimorphism and end by discussing its evolutionary aspects.

Mentions
Figures
Figure 1: The female polyphenism (left) and male genetic polymorphism (right). In both cases, discrete alternative wingless (top) or winged (bottom) morphs are produced.
Altmetric
References
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    • . . . Other than one study reporting a negative result for ecdysterone (Applebaum et al, 1975), no other hormonal candidates for mediating the wing polyphenism have been investigated . . .
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    • . . . Different clones of the pea aphid, Acyrthosiphon pisum (Markkula, 1963; Lowe and Taylor, 1964; Weisser and Braendle, 2001; Hazell et al, 2005; Braendle et al, 2005b), and other species (MacGillivray and Anderson, 1958; Kvenberg and Jones, 1974; Blackman, 1979; Groeters, 1989) display variation in the propensity to produce winged females, even when exposed to the same environmental conditions . . .
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    • . . . Nonhost-alternating species are usually monophagous but may feed on a range of related host plants (Blackman and Eastop, 1994) . . .
    • . . . In host-alternating species, the morphs migrating between the primary and secondary hosts are always winged, whereas both winged and wingless females frequently occur during the parthenogenetic generations on the summer host for both host-alternating and nonhost-alternating species (Blackman and Eastop, 1994) . . .
    • . . . In most other taxa males are winged; for example, the males of all host-alternating aphidines are winged (Blackman and Eastop, 1994, 2000) . . .
    • . . . Winged and wingless males of the pea aphid are found both in the ancestral range of Europe and in introduced populations of North America (Meier, 1958; Müller, 1962; Cartier, 1963; Hille Ris Lambers, 1966; Blackman and Eastop, 1994, 2000) . . .
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    • . . . Increased aphid density triggers wing formation in many species and in some species a small increase in density is sufficient (Bonnemaison, 1951; Johnson, 1965; Lees, 1967; Sutherland, 1969a, 1969b; Shaw, 1970a) . . .
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    • . . . Different clones of the pea aphid, Acyrthosiphon pisum (Markkula, 1963; Lowe and Taylor, 1964; Weisser and Braendle, 2001; Hazell et al, 2005; Braendle et al, 2005b), and other species (MacGillivray and Anderson, 1958; Kvenberg and Jones, 1974; Blackman, 1979; Groeters, 1989) display variation in the propensity to produce winged females, even when exposed to the same environmental conditions . . .
    • . . . Some of this variation may be related to the host plant preferences of aphid clones (MacGillivray and Anderson, 1958; Weisser and Braendle, 2001), yet variation is also observed in clones collected from the same host plant species (Braendle et al, 2005b). . . .
    • . . . We have started to test this possibility by examining the wing-induction tendencies of the three possible api genotypes (Braendle et al, 2005b) . . .
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    • . . . Such offspring very frequently show an intermediate winged-wingless phenotype and wing development is inhibited in presumptive winged individuals (Johnson, 1958b, 1959; Christiansen-Weniger and Hardie, 1998, 2000). . . .
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    • . . . Such offspring very frequently show an intermediate winged-wingless phenotype and wing development is inhibited in presumptive winged individuals (Johnson, 1958b, 1959; Christiansen-Weniger and Hardie, 1998, 2000). . . .
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    • . . . Consistent with a predicted role for JH in mediating the aphid wing polyphenism, PII applied to mothers can induce the entire suite of characteristics found in the winged morph in her parthenogenetic offspring (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Rup and Sohal, 1989; Hardie et al, 1995, 1996; Gao and Hardie, 1996) . . .
    • . . . Although PII is able to induce winged progeny in several species, the majority of studies suggest that it fails to induce precocious development, the classic JH-mediated hallmark of precocenes (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Hardie et al, 1995, 1996) . . .
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    • . . . In Drepanosiphum dixoni, for example, all parthenogenetic females develop wings, yet some individuals lack indirect flight muscles and are therefore not capable of flight (Dixon, 1972) . . .
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    • . . . In contrast, the mere presence of particular natural enemies may elicit an increase in winged morph production in the pea aphid, Acyrthosiphon pisum (Dixon and Agarwala, 1999; Weisser et al, 1999; Sloggett and Weisser, 2002; Kunert and Weisser, 2003) (parasitization may also directly affect wing development, see below) . . .
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    • . . . Several studies showed that third- and fourth-instar nymphs without wing buds possess larger corpora allata, either by volume or nuclei diameter (White, 1965, 1968, 1971; Lamb and White, 1971; Elliot, 1975) . . .
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    • . . . The development of alternative phenotypes has been examined in several aphid species using histological methods (Shull, 1938; White, 1946; Kitzmiller, 1951; Johnson and Birks, 1960; Tsuji and Kawada, 1987a; Ganassi et al, 2005) . . .
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    • . . . Consistent with a predicted role for JH in mediating the aphid wing polyphenism, PII applied to mothers can induce the entire suite of characteristics found in the winged morph in her parthenogenetic offspring (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Rup and Sohal, 1989; Hardie et al, 1995, 1996; Gao and Hardie, 1996) . . .
    • . . . Consistent with this result, JH generally fails to reverse the winged morph-inducing effects of PII (Hardie, 1986; Hardie et al, 1995; Gao and Hardie, 1996) . . .
    • . . . Moreover, although the inhibition of winged morph production caused by PIII is accompanied by precocious development and destruction of the corpus allatum (Hales and Mittler, 1981; Kambhampati et al, 1984; Hardie, 1986; Hardie et al, 1995, 1996), the application of JH is capable of rescuing precocious development without reversing the inhibition of winged morphs (Gao and Hardie, 1996) . . .
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    • . . . Consistent with this idea, species feeding on large or perennial host plants may exhibit a lower incidence of winged morph production (Groeters, 1989) . . .
    • . . . Different clones of the pea aphid, Acyrthosiphon pisum (Markkula, 1963; Lowe and Taylor, 1964; Weisser and Braendle, 2001; Hazell et al, 2005; Braendle et al, 2005b), and other species (MacGillivray and Anderson, 1958; Kvenberg and Jones, 1974; Blackman, 1979; Groeters, 1989) display variation in the propensity to produce winged females, even when exposed to the same environmental conditions . . .
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    • . . . The failure to unequivocally induce or correlate winglessness with JH led to the proposal that the use of anti-JH compounds or experimental destruction of the corpus allatum might break the experimental impasse (Hales, 1976) . . .
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    • . . . Moreover, although the inhibition of winged morph production caused by PIII is accompanied by precocious development and destruction of the corpus allatum (Hales and Mittler, 1981; Kambhampati et al, 1984; Hardie, 1986; Hardie et al, 1995, 1996), the application of JH is capable of rescuing precocious development without reversing the inhibition of winged morphs (Gao and Hardie, 1996) . . .
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    • . . . Both long days and natural JHs administered to first- and early second-instar nymphs of these individuals cause them to develop as wingless morphs (Hardie, 1980, 1981) . . .
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    • . . . Both long days and natural JHs administered to first- and early second-instar nymphs of these individuals cause them to develop as wingless morphs (Hardie, 1980, 1981) . . .
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    • . . . Consistent with a predicted role for JH in mediating the aphid wing polyphenism, PII applied to mothers can induce the entire suite of characteristics found in the winged morph in her parthenogenetic offspring (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Rup and Sohal, 1989; Hardie et al, 1995, 1996; Gao and Hardie, 1996) . . .
    • . . . Although PII is able to induce winged progeny in several species, the majority of studies suggest that it fails to induce precocious development, the classic JH-mediated hallmark of precocenes (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Hardie et al, 1995, 1996) . . .
    • . . . Consistent with this result, JH generally fails to reverse the winged morph-inducing effects of PII (Hardie, 1986; Hardie et al, 1995; Gao and Hardie, 1996) . . .
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    • . . . Attempts to measure JH directly have detected JH III at very low levels in Megoura viciae (Hardie et al, 1985), but no study has successfully correlated JH titers with the production of wingless morphs. . . .
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    • . . . Consistent with a predicted role for JH in mediating the aphid wing polyphenism, PII applied to mothers can induce the entire suite of characteristics found in the winged morph in her parthenogenetic offspring (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Rup and Sohal, 1989; Hardie et al, 1995, 1996; Gao and Hardie . . .
    • . . . Although PII is able to induce winged progeny in several species, the majority of studies suggest that it fails to induce precocious development, the classic JH-mediated hallmark of precocenes (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Hardie et al, 1995, 1996) . . .
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    • . . . Consistent with a predicted role for JH in mediating the aphid wing polyphenism, PII applied to mothers can induce the entire suite of characteristics found in the winged morph in her parthenogenetic offspring (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Rup and Sohal, 1989; Hardie et al, 1995, 1996; Gao and Hardie, 1996) . . .
    • . . . However, PIII is capable of inhibiting the production of winged morphs, at least in the pea aphid (Hardie et al, 1995; Gao and Hardie, 1996). . . .
    • . . . Although PII is able to induce winged progeny in several species, the majority of studies suggest that it fails to induce precocious development, the classic JH-mediated hallmark of precocenes (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Hardie et al, 1995, 1996) . . .
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    • . . . These studies have yielded disparate and sometimes conflicting results (Hardie and Lees, 1985), in part due to mistaking mere juvenilization by JH for authentic apterization (Lees, 1977), but also because of differences in species, dosages, means of administration, and experimental design . . .
    • . . . In at least one other species, however, this correlation does not hold (Leckstein and Llewellyn, 1975; Leckstein, 1976) and the working assumption that volume or nuclei diameter are suitable proxies for either corpus allatum secretory activity or JH titer may be invalid (Hardie and Lees, 1985) . . .
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    • . . . Consistent with this theme, winged forms are also more resistant to starvation (Tsuji and Kawada, 1987b; Hazell et al, 2005). . . .
    • . . . Different clones of the pea aphid, Acyrthosiphon pisum (Markkula, 1963; Lowe and Taylor, 1964; Weisser and Braendle, 2001; Hazell et al, 2005; Braendle et al, 2005b), and other species (MacGillivray and Anderson, 1958; Kvenberg and Jones, 1974; Blackman, 1979; Groeters, 1989) display variation in the propensity to produce winged females, even when exposed to the same environmental conditions . . .
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    • . . . Many species of the more primitive taxa, such as the Calaphidinae, produce only winged parthenogenetic females (Hille Ris Lambers, 1947, 1966; Heie, 1982) . . .
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    • . . . In some of these species, however, some winged females may differ in their flight capability or colonies may display variation in wing length (Hille Ris Lambers and van den Bosch, 1964; Hille Ris Lambers, 1966; Dixon, 1972; Heie, 1982; Heikinheimo, 1987) . . .
    • . . . In other calaphidine species (eg, Symydobius oblongus) the parthenogenetic females show consistent differences in wing length, and the short-winged females do not fly (Heikinheimo, 1987) . . .
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    • . . . Many species of the more primitive taxa, such as the Calaphidinae, produce only winged parthenogenetic females (Hille Ris Lambers, 1947, 1966; Heie, 1982) . . .
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    • . . . In some of these species, however, some winged females may differ in their flight capability or colonies may display variation in wing length (Hille Ris Lambers and van den Bosch, 1964; Hille Ris Lambers, 1966; Dixon, 1972; Heie, 1982; Heikinheimo, 1987) . . .
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    • . . . Many species of the more primitive taxa, such as the Calaphidinae, produce only winged parthenogenetic females (Hille Ris Lambers, 1947, 1966; Heie, 1982) . . .
    • . . . In some of these species, however, some winged females may differ in their flight capability or colonies may display variation in wing length (Hille Ris Lambers and van den Bosch, 1964; Hille Ris Lambers, 1966; Dixon, 1972; Heie, 1982; Heikinheimo, 1987) . . .
    • . . . In the few species that have been examined in detail, this dimorphism is apparently caused by a genetic polymorphism (Hille Ris Lambers, 1966; Müller, 1969; Smith and MacKay, 1989). . . .
    • . . . The environmental conditions affecting the production of winged versus wingless morphs have been studied intensively (Hille Ris Lambers, 1966; Lees, 1966; Mittler and Sutherland, 1969; Kunkel and Kloft, 1974; Müller et al, 2001) . . .
    • . . . Winged and wingless males of the pea aphid are found both in the ancestral range of Europe and in introduced populations of North America (Meier, 1958; Müller, 1962; Cartier, 1963; Hille Ris Lambers, 1966; Blackman and Eastop, 1994, 2000) . . .
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    • . . . In this species, wing anlagen first appear as hypodermal thickenings shortly before the embryonic moult (Johnson, 1958a), which takes place about one day before birth . . .
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    • . . . Such offspring very frequently show an intermediate winged-wingless phenotype and wing development is inhibited in presumptive winged individuals (Johnson, 1958b, 1959; Christiansen-Weniger and Hardie, 1998, 2000). . . .
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    • . . . Such offspring very frequently show an intermediate winged-wingless phenotype and wing development is inhibited in presumptive winged individuals (Johnson, 1958b, 1959; Christiansen-Weniger and Hardie, 1998, 2000). . . .
    • . . . The observation that wingless adults and nymphs are morphologically similar led early workers to suggest that high titers of juvenile hormone (JH) induce the wingless state by promoting the retention of juvenile features in adults (Lamb, 1956; Johnson, 1959; Kennedy and Stroyan, 1959) . . .
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    • . . . Increased aphid density triggers wing formation in many species and in some species a small increase in density is sufficient (Bonnemaison, 1951; Johnson, 1965; Lees, 1967; Sutherland, 1969a, 1969b; Shaw, 1970a) . . .
    • . . . The proximate mechanism mediating these environmental conditions appears to be increased tactile stimulation between individual aphids (Johnson, 1965) . . .
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    • . . . Several other factors, in particular temperature, may influence wing production either directly or indirectly via the host plant (White, 1946; Kenten, 1955; Johnson and Birks, 1960; Schaefers and Judge, 1971; Liu, 1994) . . .
    • . . . The development of alternative phenotypes has been examined in several aphid species using histological methods (Shull, 1938; White, 1946; Kitzmiller, 1951; Johnson and Birks, 1960; Tsuji and Kawada, 1987a; Ganassi et al, 2005) . . .
    • . . . For example, Johnson and Birks (1960) examined a large number of fully developed embryos and first instar nymphs of Aphis craccivora and found wing anlagen in all of them, irrespective of whether or not they were destined to develop into winged adults . . .
    • . . . This suggests that signals either from the brain or the corpus allatum of the mother are likely to induce winged characteristics and not to suppress them as the JH model suggests (Johnson and Birks, 1960; Lees, 1966). . . .
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    • . . . Besides having wings and functional flight muscles, the fully winged morph exhibits heavier sclerotization of head and thorax, more fully developed compound eyes, ocelli, longer antennae, more rhinaria, and sometimes larger siphunculi and cauda (Kalmus, 1945; Kring, 1977; Kawada, 1987; Miyazaki, 1987) . . .
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    • . . . Moreover, although the inhibition of winged morph production caused by PIII is accompanied by precocious development and destruction of the corpus allatum (Hales and Mittler, 1981; Kambhampati et al, 1984; Hardie, 1986; Hardie et al, 1995, 1996), the application of JH is capable of rescuing precocious development without reversing the inhibition of winged morphs (Gao and Hardie, 1996) . . .
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    • . . . Besides having wings and functional flight muscles, the fully winged morph exhibits heavier sclerotization of head and thorax, more fully developed compound eyes, ocelli, longer antennae, more rhinaria, and sometimes larger siphunculi and cauda (Kalmus, 1945; Kring, 1977; Kawada, 1987; Miyazaki, 1987) . . .
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    • . . . The observation that wingless adults and nymphs are morphologically similar led early workers to suggest that high titers of juvenile hormone (JH) induce the wingless state by promoting the retention of juvenile features in adults (Lamb, 1956; Johnson, 1959; Kennedy and Stroyan, 1959) . . .
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    • . . . Several other factors, in particular temperature, may influence wing production either directly or indirectly via the host plant (White, 1946; Kenten, 1955; Johnson and Birks, 1960; Schaefers and Judge, 1971; Liu, 1994) . . .
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    • . . . The development of alternative phenotypes has been examined in several aphid species using histological methods (Shull, 1938; White, 1946; Kitzmiller, 1951; Johnson and Birks, 1960; Tsuji and Kawada, 1987a; Ganassi et al, 2005) . . .
  49. Kleinjan JE, Mittler TE. A chemical influence of ants on wing development in aphids. Entomol Exp Applicata 18: 384-388 , (1975) .
    • . . . The presence of ants (which provide some protection for aphids against predators) seems to inhibit the production of winged individuals (El-Ziady and Kennedy, 1956; Kleinjan and Mittler, 1975) . . .
  50. Kring JB. Structure of the eyes of the pea aphid, Acyrthosiphon pisum. Ann Entomol Soc Am 70: 855-860 , (1977) .
    • . . . Besides having wings and functional flight muscles, the fully winged morph exhibits heavier sclerotization of head and thorax, more fully developed compound eyes, ocelli, longer antennae, more rhinaria, and sometimes larger siphunculi and cauda (Kalmus, 1945; Kring, 1977; Kawada, 1987; Miyazaki, 1987) . . .
  51. Kunert G, Otto S, Rose SR, Gershenzon J, Weisser WW. Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecol Lett 8: 596-603 , (2005) .
    • . . . The induction of winged morphs seems to result from increased tactile stimulation triggered by either predator avoidance behavior or from the release of aphid alarm pheromone (Kunert et al, 2005) . . .
  52. Kunert G, Weisser WW. The interplay between density- and trait-mediate effects in predator-prey interactions: a case study in aphid wing polymorphism. Oecologia 135: 304-312 , (2003) .
    • . . . In contrast, the mere presence of particular natural enemies may elicit an increase in winged morph production in the pea aphid, Acyrthosiphon pisum (Dixon and Agarwala, 1999; Weisser et al, 1999; Sloggett and Weisser, 2002; Kunert and Weisser, 2003) (parasitization may also directly affect wing development, see below) . . .
  53. Kunert G, Weisser WW. The importance of antennae for pea aphid wing induction in the presence of natural enemies. Bull Entomol Res 95: 125-131 , (2005) .
    • . . . However, it is possible that chemical cues play an additional minor role (Kunert and Weisser, 2005) . . .
  54. Kunkel H, Kloft W. Polymorphismus bei Blattläusen. In: Schmidt GH (ed) Sozialpolymorphismus bei Insekten. Wissenschaftliche Verlagsgesellschaft: Stuttgart. pp 152-201 , (1974) .
    • . . . The environmental conditions affecting the production of winged versus wingless morphs have been studied intensively (Hille Ris Lambers, 1966; Lees, 1966; Mittler and Sutherland, 1969; Kunkel and Kloft, 1974; Müller et al, 2001) . . .
  55. Kvenberg JE, Jones PA. Comparison of alate offspring produced by two biotypes of the greenbug. Env Entomol 3: 407-408 , (1974) .
    • . . . Different clones of the pea aphid, Acyrthosiphon pisum (Markkula, 1963; Lowe and Taylor, 1964; Weisser and Braendle, 2001; Hazell et al, 2005; Braendle et al, 2005b), and other species (MacGillivray and Anderson, 1958; Kvenberg and Jones, 1974; Blackman, 1979; Groeters, 1989) display variation in the propensity to produce winged females, even when exposed to the same environmental conditions . . .
  56. Lamb KP. Physiological Relations Between Aphids and Their Host Plants, pp. Cambridge University: Cambridge, England , (1956) .
    • . . . The observation that wingless adults and nymphs are morphologically similar led early workers to suggest that high titers of juvenile hormone (JH) induce the wingless state by promoting the retention of juvenile features in adults (Lamb, 1956; Johnson, 1959; Kennedy and Stroyan, 1959) . . .
  57. Lamb RJ, MacKay PA. Acyrthosiphon kondoi influences alata production by the pea aphid A. pisum. Entomol Exp Applicata 45: 195-204 , (1987) .
    • . . . Interactions among different aphid species that aggregate on the same host plant can cause increased production of winged individuals (Lamb and MacKay, 1987), but this is likely to reflect a density-dependent response . . .
  58. Lamb KP, White DF. Endocrine aspects of alary polymorphism in Brevicoryne brassicae (L.). Endocrinol Exp 5: 19-22 , (1971) .
    • . . . Several studies showed that third- and fourth-instar nymphs without wing buds possess larger corpora allata, either by volume or nuclei diameter (White, 1965, 1968, 1971; Lamb and White, 1971; Elliot, 1975) . . .
  59. Leckstein PM. The role of the corpus allatum in prenatal wing determination in Megoura viciae. J Insect Physiol 22: 1117-1121 , (1976) .
    • . . . In at least one other species, however, this correlation does not hold (Leckstein and Llewellyn, 1975; Leckstein, 1976) and the working assumption that volume or nuclei diameter are suitable proxies for either corpus allatum secretory activity or JH titer may be invalid (Hardie and Lees, 1985) . . .
  60. Leckstein PM, Llewellyn M. Corpus allatum activity and wing determination in Megoura viciae. Nature 258: 714-715 , (1975) .
    • . . . In at least one other species, however, this correlation does not hold (Leckstein and Llewellyn, 1975; Leckstein, 1976) and the working assumption that volume or nuclei diameter are suitable proxies for either corpus allatum secretory activity or JH titer may be invalid (Hardie and Lees, 1985) . . .
  61. Lees AD. Clonal polymorphism in aphids. In: Kennedy JS (ed) Insect Polymorphism. Royal Entomological Society: London. pp 68-79 , (1961) .
    • . . . In many species where wing determination occurs prenatally (in parthenogenetic embryos carried within adults), winged adults rarely or never produce winged offspring (Lees, 1961; Sutherland, 1970) . . .
  62. Lees AD. The control of polymorphism in aphids. Adv Insect Physiol 3: 207-277 , (1966) .
    • . . . The environmental conditions affecting the production of winged versus wingless morphs have been studied intensively (Hille Ris Lambers, 1966; Lees, 1966; Mittler and Sutherland, 1969; Kunkel and Kloft, 1974; Müller et al, 2001) . . .
    • . . . Photoperiod may be responsible for wing induction of parthenogenetic females in clones that do not undergo sexual reproduction (Lees, 1966). . . .
    • . . . This suggests that signals either from the brain or the corpus allatum of the mother are likely to induce winged characteristics and not to suppress them as the JH model suggests (Johnson and Birks, 1960; Lees, 1966). . . .
  63. Lees AD. The production of the apterous and alate forms in the aphid Megoura viciae Buckton, with special reference to the role of crowding. J Insect Physiol 13: 289-318 , (1967) .
    • . . . Increased aphid density triggers wing formation in many species and in some species a small increase in density is sufficient (Bonnemaison, 1951; Johnson, 1965; Lees, 1967; Sutherland, 1969a, 1969b; Shaw, 1970a) . . .
  64. Lees AD. Action of juvenile hormone mimics on the regulation of larval-adult and alary polymorphisms in aphids. Nature 267: 46-48 , (1977) .
    • . . . These studies have yielded disparate and sometimes conflicting results (Hardie and Lees, 1985), in part due to mistaking mere juvenilization by JH for authentic apterization (Lees, 1977), but also because of differences in species, dosages, means of administration, and experimental design . . .
  65. Leonardo TE, Mondor EB. Symbiont modifies host life-history traits that affect gene flow. Proc R Soc B-Biol Sci 273: 1079-1084 , (2006) .
    • . . . Aphid or plant pathogens (eg, fungi or viruses) and the facultative aphid endosymbionts may also affect wing induction (Müller et al, 2001; Leonardo and Mondor, 2006). . . .
  66. Liu S-S. Production of alatae in response to low temperature in aphids: a trait of seasonal adaptation. In: Danks HV (ed) Insect Life-Cycle Polymorphism: Theory, Evolution, and Ecological Consequences for Seasonality and Diapause Control. Kluwer Academic Publishers: Dordrecht. pp 245-261 , (1994) .
    • . . . Several other factors, in particular temperature, may influence wing production either directly or indirectly via the host plant (White, 1946; Kenten, 1955; Johnson and Birks, 1960; Schaefers and Judge, 1971; Liu, 1994) . . .
  67. Lowe HJB, Taylor LR. Population parameters, wing production and behaviour in red and green Acyrthosiphon pisum (Harris) (Homoptera: Aphididae). Entomol Exp Applicata 7: 287-295 , (1964) .
    • . . . Different clones of the pea aphid, Acyrthosiphon pisum (Markkula, 1963; Lowe and Taylor, 1964; Weisser and Braendle, 2001; Hazell et al, 2005; Braendle et al, 2005b), and other species (MacGillivray and Anderson, 1958; Kvenberg and Jones, 1974; Blackman, 1979; Groeters, 1989) display variation in the propensity to produce winged females, even when exposed to the same environmental conditions . . .
  68. MacGillivray ME, Anderson GB. Production of apterous and alate progeny by apterous and alate viviparae of Macrosiphum solanifolii (Ashm.) (Homoptera: Aphididae). Can Entomol 90: 241-245 , (1958) .
    • . . . Different clones of the pea aphid, Acyrthosiphon pisum (Markkula, 1963; Lowe and Taylor, 1964; Weisser and Braendle, 2001; Hazell et al, 2005; Braendle et al, 2005b), and other species (MacGillivray and Anderson, 1958; Kvenberg and Jones, 1974; Blackman, 1979; Groeters, 1989) display variation in the propensity to produce winged females, even when exposed to the same environmental conditions . . .
  69. Mackauer M, Nair KK, Unnithan GC. Effect of precocene II on alate production in the pea aphid, Acyrthosiphon pisum. Can J Zool 57: 856-859 , (1979) .
    • . . . Consistent with a predicted role for JH in mediating the aphid wing polyphenism, PII applied to mothers can induce the entire suite of characteristics found in the winged morph in her parthenogenetic offspring (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Rup and Sohal, 1989; Hardie et al, 1995, 1996; Gao and Hardie, 1996) . . .
    • . . . Although PII is able to induce winged progeny in several species, the majority of studies suggest that it fails to induce precocious development, the classic JH-mediated hallmark of precocenes (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Hardie et al, 1995, 1996) . . .
  70. MacKay PA, Lamb RJ. Migratory tendency in aging populations of the pea aphid, Acyrthosiphon pisum. Oecologia 39: 301-308 , (1979) .
    • . . . In contrast, early born (wingless) progeny derived from wingless mothers respond strongly to wing-inducing stimuli (Mackay and Wellington, 1977; MacKay and Lamb, 1979) . . .
  71. MacKay PA, Reeleder DJ, Lamb RJ. Sexual morph production by apterous and alate viviparous Acyrthosiphon pisum (Harris) (Homoptera: Aphididae). Can J Zool 61: 952-957 , (1983) .
    • . . . In addition, in response to shortened photoperiod, winged females tend to produce mainly sexual females whereas wingless females produce both sexual females and males (MacKay et al, 1983; Nunes and Hardie, 1996). . . .
  72. MacKay PA, Wellington WG. A comparison of the reproductive patterns of apterous and alate virginoparous Acyrthosiphon pisum (Homoptera: Aphididae). Can Entomol 107: 1161-1166 , (1975) .
    • . . . In general, the winged phenotype differs from the wingless phenotype by showing longer nymphal development, longer pre-reproductive adult period, longer reproductive period, lower offspring production, and prolonged longevity (Noda, 1960; MacKay and Wellington, 1975; Campbell and Mackauer, 1977; Tsuji and Kawada, 1987b; Tsumuki et al, 1990) . . .
  73. Mackay PA, Wellington WG. Maternal age as a source of variation in the ability of an aphid to produce dispersing forms. Res Popul Ecol 18: 195-209 , (1977) .
    • . . . Similarly, early born progeny descended from winged mothers exhibit a decreased production of winged morphs (Mackay and Wellington, 1977) . . .
  74. Markkula M. Studies on the pea aphid, Acyrthosiphon pisum Harris (Hom., Aphididae), with special reference to the differences in the biology of the green and red forms. Ann Agriculturae Fenniae 2: 1-30 , (1963) .
    • . . . Although all three possible api genotypes may occur on the same host plant species, several studies suggest that male morph production may correlate with host plant range and persistence (Meier, 1958; Müller, 1962; Markkula, 1963; Eastop, 1971) . . .
    • . . . Different clones of the pea aphid, Acyrthosiphon pisum (Markkula, 1963; Lowe and Taylor, 1964; Weisser and Braendle, 2001; Hazell et al, 2005; Braendle et al, 2005b), and other species (MacGillivray and Anderson, 1958; Kvenberg and Jones, 1974; Blackman, 1979; Groeters, 1989) display variation in the propensity to produce winged females, even when exposed to the same environmental conditions . . .
  75. Meier W. Beiträge zur Kenntnis der auf Papilionaceen lebenden Acyrthosiphon-Arten (Hemipt. Aphid). Mitteilungen der Schweizerischen Entomologischen Gesellschaft 31: 291-312 , (1958) .
    • . . . Winged and wingless males of the pea aphid are found both in the ancestral range of Europe and in introduced populations of North America (Meier, 1958; Müller, 1962; Cartier, 1963; Hille Ris Lambers, 1966; Blackman and Eastop, 1994, 2000) . . .
    • . . . Although all three possible api genotypes may occur on the same host plant species, several studies suggest that male morph production may correlate with host plant range and persistence (Meier, 1958; Müller, 1962; Markkula, 1963; Eastop, 1971) . . .
  76. Mittler TE, Sutherland ORW. Dietary influences on aphid polymorphism. Entomol Exp Applicata 12: 703-713 , (1969) .
    • . . . The environmental conditions affecting the production of winged versus wingless morphs have been studied intensively (Hille Ris Lambers, 1966; Lees, 1966; Mittler and Sutherland, 1969; Kunkel and Kloft, 1974; Müller et al, 2001) . . .
  77. Miyazaki M. Forms and morphs of aphids. In: Minks AK and Harrewijn P (ed) Aphids, Their Biology, Natural Enemies and Control. Elsevier: Amsterdam. pp 163-195 , (1987) .
    • . . . Besides having wings and functional flight muscles, the fully winged morph exhibits heavier sclerotization of head and thorax, more fully developed compound eyes, ocelli, longer antennae, more rhinaria, and sometimes larger siphunculi and cauda (Kalmus, 1945; Kring, 1977; Kawada, 1987; Miyazaki, 1987) . . .
  78. Moran NA. The evolutionary maintenance of alternative phenotypes. Am Natural 139: 971-989 , (1992) .
    • . . . Environmental control of alternative phenotypes can therefore evolve in organisms living in spatially or temporally variable environments in which cues can be used to reliably predict the future selective environment (Moran, 1992) . . .
  79. Müller CB, Williams IS, Hardie J. The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecol Entomol 26: 330-340 , (2001) .
    • . . . The environmental conditions affecting the production of winged versus wingless morphs have been studied intensively (Hille Ris Lambers, 1966; Lees, 1966; Mittler and Sutherland, 1969; Kunkel and Kloft, 1974; Müller et al, 2001) . . .
    • . . . However, a review by Müller et al (2001) showed that more than half of 38 examined studies in 12 different aphid species did not confirm the hypothesis that poor nutrition is responsible for an increase in winged morph production . . .
    • . . . In many of the earlier studies, the reported host plant effect on winged morph production was likely due to the effect of the host plant on the number of physical contacts between aphids (Müller et al, 2001) . . .
    • . . . Aphid or plant pathogens (eg, fungi or viruses) and the facultative aphid endosymbionts may also affect wing induction (Müller et al, 2001; Leonardo and Mondor, 2006). . . .
    • . . . Most studies have reported a decline in winged morph production as temperature increases (Müller et al, 2001) . . .
  80. Müller FP. Biotypen und Unterarten der 'Erbsenlaus' Acyrthosiphon pisum (Harris). Z Pflanzenkrankheiten Pflanzenschutz 69: 129-136 , (1962) .
    • . . . Winged and wingless males of the pea aphid are found both in the ancestral range of Europe and in introduced populations of North America (Meier, 1958; Müller, 1962; Cartier, 1963; Hille Ris Lambers, 1966; Blackman and Eastop, 1994, 2000) . . .
    • . . . Although all three possible api genotypes may occur on the same host plant species, several studies suggest that male morph production may correlate with host plant range and persistence (Meier, 1958; Müller, 1962; Markkula, 1963; Eastop, 1971) . . .
  81. Müller FP. Bastardierungsversuche zur Feststellung von Isolierungsmechanismen zwischen nahe verwandten Formen in der Gattung Myzus Passerini (Homoptera: Aphididae). Biol Zentralblatt 88: 147-164 , (1969) .
    • . . . In the few species that have been examined in detail, this dimorphism is apparently caused by a genetic polymorphism (Hille Ris Lambers, 1966; Müller, 1969; Smith and MacKay, 1989). . . .
  82. Noda I. The emergence of winged viviparous female in aphid. - VI. Difference in rate of development between the winged and unwinged forms. Jap J Appl Entomol Zool 10: 97-102 , (1960) .
    • . . . In general, the winged phenotype differs from the wingless phenotype by showing longer nymphal development, longer pre-reproductive adult period, longer reproductive period, lower offspring production, and prolonged longevity (Noda, 1960; MacKay and Wellington, 1975; Campbell and Mackauer, 1977; Tsuji and Kawada, 1987b; Tsumuki et al, 1990) . . .
  83. Nunes MV, Hardie J. Differential photoperiodic responses in genetically identical winged and wingless pea aphid, Acyrthosiphon pisum, and the effect of day length on wing development. Physiol Entomol 21: 339-343 , (1996) .
    • . . . In addition, in response to shortened photoperiod, winged females tend to produce mainly sexual females whereas wingless females produce both sexual females and males (MacKay et al, 1983; Nunes and Hardie, 1996). . . .
  84. Ohta T, Bowers WS. Synthesis of insect antijuvenile hormones. Chem Pharm 25: 2788-2789 , (1977) .
    • . . . Cells of the corpus allatum are selectively destroyed by the plant-derived precocenes, Precocene I (PI) and Precocene II (PII), as well as the more potent synthetic precocene, Precocene III (PIII) (Ohta and Bowers, 1977) . . .
  85. Rup BJ, Sohal SK. Morphogenetic effects of precocene II on Lipaphis erysimi (Homoptera, Aphididae). Acta Entomol Bohemoslov 86: 172-178 , (1989) .
    • . . . Consistent with a predicted role for JH in mediating the aphid wing polyphenism, PII applied to mothers can induce the entire suite of characteristics found in the winged morph in her parthenogenetic offspring (Mackauer et al, 1979; Delisle et al, 1983; Hardie, 1986; Rup and Sohal, 1989; Hardie et al, 1995, 1996; Gao and Hardie, 1996) . . .
  86. Schaefers GA, Judge FD. Effects of temperature, photoperiod, and host plant on alary polymorphism in the aphid, Chaetosiphon fragaefolii. J Insect Physiol 17: 365-379 , (1971) .
    • . . . Several other factors, in particular temperature, may influence wing production either directly or indirectly via the host plant (White, 1946; Kenten, 1955; Johnson and Birks, 1960; Schaefers and Judge, 1971; Liu, 1994) . . .
  87. Shaw MJP (1970a). Effect of population density on alienocolae of Aphis fabae Scop. I. The effect of crowding on the production of alatae in the laboratory. Ann Appl Biol 65: 191-196 , .
    • . . . Increased aphid density triggers wing formation in many species and in some species a small increase in density is sufficient (Bonnemaison, 1951; Johnson, 1965; Lees, 1967; Sutherland, 1969a, 1969b; Shaw, 1970a) . . .
  88. Shaw MJP (1970b). Effect of population density on alienocolae of Aphis fabae Scop. III. The effect of isolation on the development of form and behaviour of alatae in a laboratory clone. Ann Appl Biol 65: 205-212 , .
    • . . . In the case of Aphis fabae and other species, these intermediates can be induced when wing-inducing stimuli are removed at different time points of nymphal development (Shaw, 1970b) . . .
  89. Shull AF. Time of determination and time of differentiation of aphid wings. Am Natural 72: 170-179 , (1938) .
    • . . . The development of alternative phenotypes has been examined in several aphid species using histological methods (Shull, 1938; White, 1946; Kitzmiller, 1951; Johnson and Birks, 1960; Tsuji and Kawada, 1987a; Ganassi et al, 2005) . . .
  90. Sloggett JJ, Weisser WW. Parasitoids induce production of the dispersal morph of the pea aphid, Acyrthosiphon pisum. Oikos 98: 323-333 , (2002) .
    • . . . In contrast, the mere presence of particular natural enemies may elicit an increase in winged morph production in the pea aphid, Acyrthosiphon pisum (Dixon and Agarwala, 1999; Weisser et al, 1999; Sloggett and Weisser, 2002; Kunert and Weisser, 2003) (parasitization may also directly affect wing development, see below) . . .
  91. Smith MAH, MacKay PA. Genetic variation in male alary dimorphism in populations of pea aphid, Acyrthosiphon pisum. Entomol Exp Appl 51: 125-132 , (1989) .
    • . . . In about 10% of European species, however, both winged and wingless males have been recorded (Smith and MacKay, 1989) . . .
    • . . . In the few species that have been examined in detail, this dimorphism is apparently caused by a genetic polymorphism (Hille Ris Lambers, 1966; Müller, 1969; Smith and MacKay, 1989). . . .
    • . . . The male polymorphism is controlled by a single locus on the X chromosome called aphicarus (api) (Smith and MacKay, 1989; Caillaud et al, 2002; Braendle et al, 2005a) . . .
  92. Sutherland ORW (1969a). The role of crowding in the production of winged forms by two strains of the pea aphid, Acyrthosiphon pisum. J Insect Physiol 15: 1385-1410 , .
    • . . . Increased aphid density triggers wing formation in many species and in some species a small increase in density is sufficient (Bonnemaison, 1951; Johnson, 1965; Lees, 1967; Sutherland, 1969a, 1969b; Shaw, 1970a) . . .
  93. Sutherland ORW (1969b). The role of the host plant in the production of winged forms by two strains of the pea aphid, Acyrthosiphon pisum. J Insect Physiol 15: 2179-2201 , .
    • . . . Increased aphid density triggers wing formation in many species and in some species a small increase in density is sufficient (Bonnemaison, 1951; Johnson, 1965; Lees, 1967; Sutherland, 1969a, 1969b; Shaw, 1970a) . . .
    • . . . For a given aphid clone, variation in winged morph production correlates with variation in host plant species (Vereschagina and Shaposhnikov, 1998) and with changes in host plant quality or host plant age (Sutherland, 1969b) . . .
  94. Sutherland ORW. An intrinsic factor influencing the alate production by two strains of the pea aphid, Acyrthosiphon pisum. J Insect Physiol 16: 1349-1354 , (1970) .
    • . . . In many species where wing determination occurs prenatally (in parthenogenetic embryos carried within adults), winged adults rarely or never produce winged offspring (Lees, 1961; Sutherland, 1970) . . .
  95. Tsuji H, Kawada K (1987a). Development and degeneration of wing buds and indirect flight muscles in the pea aphid (Acyrtosiphon pisum (Harris)). Jap J Appl Entomol Zool 31: 247-252 , .
    • . . . The development of alternative phenotypes has been examined in several aphid species using histological methods (Shull, 1938; White, 1946; Kitzmiller, 1951; Johnson and Birks, 1960; Tsuji and Kawada, 1987a; Ganassi et al, 2005) . . .
    • . . . A similar scenario has been described in the pea aphid where all embryos, first-instar nymphs and second-instar nymphs exhibit wing buds, which subsequently degenerate in the developing wingless morph (Tsuji and Kawada, 1987a). . . .
  96. Tsuji H, Kawada K (1987b). Effects of starvation on life span and embryo development of four morphs of pea aphid (Acyrthosiphon pisum (Harris)). Jap J Appl Entomol Zool 31: 36-40 , .
    • . . . Consistent with this theme, winged forms are also more resistant to starvation (Tsuji and Kawada, 1987b; Hazell et al, 2005). . . .
    • . . . In general, the winged phenotype differs from the wingless phenotype by showing longer nymphal development, longer pre-reproductive adult period, longer reproductive period, lower offspring production, and prolonged longevity (Noda, 1960; MacKay and Wellington, 1975; Campbell and Mackauer, 1977; Tsuji and Kawada, 1987b; Tsumuki et al, 1990) . . .
  97. Tsumuki H, Nagatsuka H, Kawada K, Kanehisa K. Comparison of nutrient reservation in apterous and alate pea aphids, Acyrthosiphon pisum (Harris). 1. Developmental time and sugar content. Appl Entomol Zool 25: 215-221 , (1990) .
    • . . . In general, the winged phenotype differs from the wingless phenotype by showing longer nymphal development, longer pre-reproductive adult period, longer reproductive period, lower offspring production, and prolonged longevity (Noda, 1960; MacKay and Wellington, 1975; Campbell and Mackauer, 1977; Tsuji and Kawada, 1987b; Tsumuki et al, 1990) . . .
  98. Vereschagina AB, Shaposhnikov GC. Influence of crowding and host-plant on development of winged and apterous aphids. In: Nieto Nafrio JM and Dixon AFG (ed) Aphids in Natural and Managed Ecosystems. Universidad de Leon: Leon, Spain , (1998) .
    • . . . For a given aphid clone, variation in winged morph production correlates with variation in host plant species (Vereschagina and Shaposhnikov, 1998) and with changes in host plant quality or host plant age (Sutherland, 1969b) . . .
  99. Waloff N. Absence of wing polymorphism in the arboreal, phytophagous species of some taxa of temperate Hemiptera - A hypothesis. Ecol Entomol 8: 229-232 , (1983) .
    • . . . An exception are tree-dwelling aphid species, which often produce exclusively winged females compared to species feeding on herbaceous plants, possibly because flight allows aphids to find a suitable feeding location in architecturally complex trees (Waloff, 1983). . . .
  100. Weisser WW, Braendle C. Body colour and genetic variation in winged morph production in the pea aphid. Entomol Exp Applicata 99: 217-223 , (2001) .
    • . . . Different clones of the pea aphid, Acyrthosiphon pisum (Markkula, 1963; Lowe and Taylor, 1964; Weisser and Braendle, 2001; Hazell et al, 2005; Braendle et al, 2005b), and other species (MacGillivray and Anderson, 1958; Kvenberg and Jones, 1974; Blackman, 1979; Groeters, 1989) display variation in the propensity to produce winged females, even when exposed to the same environmental conditions . . .
  101. Weisser WW, Braendle C, Minoretti N. Predator-induced morphological shift in the pea aphid. Proc R Soc Lond B 266: 1175-1181 , (1999) .
    • . . . In contrast, the mere presence of particular natural enemies may elicit an increase in winged morph production in the pea aphid, Acyrthosiphon pisum (Dixon and Agarwala, 1999; Weisser et al, 1999; Sloggett and Weisser, 2002; Kunert and Weisser, 2003) (parasitization may also directly affect wing development, see below) . . .
  102. West-Eberhard MJ. Developmental Plasticity and Evolution. Oxford University Press: Oxford , (2003) .
    • . . . It is possible that polyphenisms originated as polymorphisms that accumulated environmental influences (West-Eberhard, 2003) . . .
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    • . . . Several studies showed that third- and fourth-instar nymphs without wing buds possess larger corpora allata, either by volume or nuclei diameter (White, 1965, 1968, 1971; Lamb and White, 1971; Elliot, 1975) . . .
  104. White DF. Cabbage aphid - effect of isolation on form and on endocrine activity. Science 159: 218-219 , (1968) .
    • . . . Several studies showed that third- and fourth-instar nymphs without wing buds possess larger corpora allata, either by volume or nuclei diameter (White, 1965, 1968, 1971; Lamb and White, 1971; Elliot, 1975) . . .
  105. White DF. Corpus allatum activity associated with development of wingbuds in cabbage aphid embryos and larvae. J Insect Physiol 17: 761-773 , (1971) .
    • . . . Several studies showed that third- and fourth-instar nymphs without wing buds possess larger corpora allata, either by volume or nuclei diameter (White, 1965, 1968, 1971; Lamb and White . . .
  106. White WS. The environmental conditions affecting the genetic mechanism of wing production in the chrysanthemum aphid. Am Natural 80: 245-270 , (1946) .
    • . . . Several other factors, in particular temperature, may influence wing production either directly or indirectly via the host plant (White, 1946; Kenten, 1955; Johnson and Birks, 1960; Schaefers and Judge, 1971; Liu, 1994) . . .
    • . . . The development of alternative phenotypes has been examined in several aphid species using histological methods (Shull, 1938; White, 1946; Kitzmiller, 1951; Johnson and Birks, 1960; Tsuji and Kawada, 1987a; Ganassi et al, 2005) . . .
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