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11 Endocrine Control of Insect Polyphenism 11 Endocrine Control of Insect Polyphenism K. Hartfelder Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil D.J. Emlen University of Montana, Missoula, MT, USA © 2012 Elsevier B.V. All Rights Reserved Summary the insulin-signaling pathway is now also emerging as a Polyphenism in insects is associated with some of the major player. We present an overview of current knowl- most striking and successful life histories. Insect poly- edge regarding wing length dimorphism in crickets, phenisms center around four major themes: wing the gradual phase shift from the solitary to gregarious length variation (including winglessness), differences syndrome in migrating locusts, the complex switch- in fertility or reproductive strategies, body and/or wing ing between wingless/winged forms and asexual/sexual coloration and exaggerated morphologies. Hormones, reproduction in aphids, wing and body color variants in especially juvenile hormone and ecdy steroids are butterflies, male horn dimorphism in beetles, and caste important factors underlying the generation of dis- polyphenism occurring in the hemimetabolous termites tinct morphologies and reproductive strategies, and and holometabolous hymenopterans. 11.1. Polyphenism and Polymorphism: Discontinuity in the Variation of Insects 464 11.2. Polyphenism in the Hemimetabola 465 11.2.1. Hemiptera/Homoptera Wing Polyphenism 465 11.2.2. Orthoptera 470 11.2.3. “Isoptera” (Termites) — Caste Polyphenism in the Hemimetabola 476 11.3. Polyphenism in the Holometabola 479 11.3.1. Lepidoptera 479 11.3.2. Coleoptera — Male Dimorphism for Weaponry 484 11.3.3. Hymenoptera — Caste Polyphenism and Division of Labor 487 11.4. Synthesis and Perspectives 501 11.1. Polyphenism and Polymorphism: Discontinuity in the Variation of Insects focus on relatively discrete or discontinuous variation in Historically, the terms polymorphism and polyphen- phenotype expression. Polyphenic mechanisms can be ism have the same meaning, namely intraspecific varia- described at two levels: (1) cues that serve as proximate tion in sets of characters. !is phenomenon is seen as triggers of developmental alternatives and (2) endogenous an adaptive response that allows genotypes to track response cascades that drive the developmental responses. short-term cycles of environmental variation and, at Triggering stimuli may consist of external environmental the same time, maintain cohesiveness of adapted gene factors (e.g., photoperiod, crowding), internal genetic fac- complexes. With recent advances in population genetics, tors (e.g., alleles at polymorphic loci), or a mixture of the enzymology, genomics, and proteomics the term poly- two. Endogenous response cascades involve a series of sys- morphism has now gained a much wider meaning. It tems that relay, synchronize, and coordinate differentiated has come to denote variation in nucleotide sequences processes in target systems. in general. !is genetic variation may or may not have !e most common form of polyphenism in animals is consequences for phenotypic character states, depending sexual dimorphism. !is, in most cases, is triggered by on whether it occurs in coding regions, promoter and genetic factors that generate distinct phenotypes that regulatory regions, or in selectively neutral DNA, such then act at the tissue level through a series of endocrine as microsatellites. response cascades. Even though sexual polyphenism In this chapter we use the term polyphenism to occurs to some degree in all insects, we consider it only describe, in a more narrow sense, the occurrence of peripherally in this chapter. Rather, and following the tra- intraspecific variation in phenotypes. Specifically, we dition already set forward in the review on this subject DOI: 10.1016/B978-0-12-384749-2.10011-1 11: Endocrine Control of Insect Polyphenism 465 by Hardie and Lees (1985), and building on our prior changed dramatically is the proportion of the population version of this review (Hartfelder and Emlen, 2005), we expressing wings: derived populations (on the new host) focus on distinct phenotypes (in either or both sexes) that have significantly fewer winged animals than ancestral are triggered by environmental or other exogenous fac- populations. tors. When reviewing recent studies on this subject and Dingle and Winchell (1997) demonstrated that this comparing these to insights already presented in the 2005 polyphenism is regulated by a threshold mechanism, and version of this chapter, it became clear that considerable that this threshold behaves like a polygenic character with progress has been made in the elucidation of endogenous high levels of additive genetic variance. Manipulations response cascades underlying polyphenic trait expres- of the amount of nymphal food predictably affected the sion in some insect polyphenisms, and these now truly percent of winged offspring, as did topical applications of represent model systems. Major progress in the field can methoprene (Dingle and Winchell, 1997). In laboratory be attributed to genomic resources and high throughput animals sampled from an ancestral population, increases platforms for both transcriptome and proteome analy- in the amount of food decreased the percent develop- ses. !ese were championed for the honey bee, which ing with wings. Similarly, experimental augmentation of became the first polyphenic (social) insect to have its juvenile hormone (JH) levels at the beginning of the final genome sequenced (!e Honey Bee Genome Sequencing nymphal instar also decreased the proportion of winged Consortium, 2006). Next came the genome of the pea animals, suggesting that high levels of JH result in a aphid Acyrthosiphon pisum, which has recently been con- reduction of the relative amount of wing growth (Dingle cluded and published (International Aphid Genomics, and Winchell, 1997). 2010) and the road has been paved for several other !ere is no information regarding the sensitivity of genomes. animals to JH during the penultimate or earlier instars, nor of the relative levels of ecdysteroids. Nevertheless, 11.2. Polyphenism in the results available at this time show striking similarities Hemimetabola with the polyphenic mechanism described for crickets (Section 11.2.2.1.). !e timing of the sensitive period, Wing length is the most predominant form of polyphen- the implicated role for JH, and the direction of the effect ism in hemimetabolous insects. It involves differential of JH all agree with the basic model for cricket wing investment in wings and wing muscles, and appears to polyphenism. reflect an ecophysiological trade-off in resource allocation between dispersal and reproduction. It is observed in spe- 11.2.1.2. Planthoppers Planthoppers often occur in cies that colonize and/or exploit ephemeral resources, and both winged and wingless forms (Denno and Perfect, 1994; may be integrated into life histories of considerable com- Kisimoto, 1965; Morooka et al., 1988), and dimorphism plexity, such as seen in locust and aphid phase polyphen- in these species results from a threshold mechanism with ism and in termite caste polyphenism. In the following heritable variation for the threshold (Denno et al., 1986, sections, we will review the current status of endocrine 1996; Matsumara, 1996; Morooka and Tojo, 1992; Peterson regulation of wing, phase, and caste polyphenism encoun- and Denno, 1997). Where studied, the environmental factor tered in the Hemimetabola. most relevant to wing expression appears to be population density, or crowding, and as with the wing polyphenism already described, the physiological response to nymphal 11.2.1. Hemiptera/Homoptera Wing crowding appears to be mediated by levels of JH. Polyphenism To date, the endocrine regulation of wing polyphen- 11.2.1.1. Soapberry bugs A number of hemipteran ism has been best studied in the brown planthopper, species have polyphenic wing expression (Dingle Nilaparvata lugens (Homoptera: Delphacidae). !e and Winchell, 1997; Tanaka and Wolda, 1987). !e default developmental pathway appears to involve wing hemipteran Jadera haemotoloma (the soapberry bug) production, but Iwanaga and Tojo (1986) showed that exhibits a wing polymorphism as four morphs: three both exposure to solitary (low density) conditions and winged forms, one that always has viable flight muscle, topical applications of JH could suppress wing devel- one that histolyzes flight muscles part way through the opment and result in a greater proportion of wingless adult stage, and a winged form that never produces viable individuals. !ey identified sensitive periods in the pre- flight musculature, as well as a completely wingless form penultimate (third) and penultimate (fourth) instars that also has inviable flight musculature (Dingle and (Iwanaga and Tojo, 1986). !e timing of these sensitive Winchell, 1997). Jadera haemotoloma has undergone periods and the effect of JH were corroborated by Ayoade rapid recent evolution following a host-shift that occurred et al. (1999), who induced wingless morphs in a strain within the past 50 years (Carroll and Boyd, 1992; Carroll of planthoppers that had been selected to be entirely et al., 1997, 2001), and one characteristic that has winged. 466 11: Endocrine Control of Insect Polyphenism Bertuso et al. (2002) then induced expression of wings or host plant preference). !e large variation in species- in a line selected to be entirely wingless by applying preco- specific aphid life cycles stems from the fact that these cene to animals at these same sensitive periods. Dai et al. elements of polyphenism can
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