Polyphenetic development

Many insects will develop not only one phenotype but several at the same time or different pheno-types in a temporal sequence, phenomena known as polyphenisms. Obviously, when the same genotype develops different phenotypes, there must be developmental switches that are sensitive to environmental conditions. Therefore, polyphenetic development can be considered a prime case of phenotypic plasticity, also called discrete pheno-typic plasticity to differentiate it from the continuous phenotypic plasticity described by reaction norms. Functional genomic analysis should be able to reveal the expression programmes underlying development of alternative phenotypes.

Spectacular examples of polyphenisms are found in insects that can develop different morphotypes in different seasons or in response to changes in the diet. Several examples are discussed by Nijhout (2003a), including spring and summer forms of nymphalid butterflies, gregarious and non-gregarious phases of locusts, soldier and worker castes in ants, and hornless and horned mating types in dung beetles. In all cases investigated, polyphenetic switching of the developmental pathway is triggered by a hormonal signal. Development is canalized into two or more alternative pathways, through an altered hormone titre, an altered threshold sensitivity to the hormone, an altered timing of hormone secretion, or an altered timing of the hormone-sensitive period. Often the environmental signal triggering an alternative condition falls considerably before the actual developmental switch itself; when a decision on a specific pathway has been made, development usually becomes irreversible after some time and the animal is destined to become a specific morph.

Seasonal polyphenisms in Bicyclus butterflies (family Satyridae) have been investigated in detail. There are about 70 species in the genus Bicyclus, which inhabit a variety of habitats in Central Africa. Most species have a wet-season morph with brown-coloured wings, and conspicous eye-spots and bands, as well as a dry-season morph with dull colours and cryptic wing patterns. This seasonal diphenism can be understood as an adaptation to seasonal changes in the habitat, expressing camouflage against a background of dead vegetation in the dry season, when the butterflies are less active, and predator deflection using eyespots in the wet season, when butterflies are more active. The two morphs can be produced in laboratory cultures maintained at different temperatures (Fig. 5.19). However, it is not certain whether temperature alone is the most important environmental cue determing the morphs, since

Figure 5.19 Seasonal polyphenism in Bicyclus anyana (Lepidoptera, Satyridae) includes a wet-season morph (top) and a dry-season morph (bottom). Courtesy of P.M. Brakefield, University of Leiden.

temperature can be negatively correlated with humidity in one place and positively in another (Roskam and Brakefield 1999).

As Fig. 5.19 illustrates, a major difference between seasonal morphs lies in the eyespots on the wings. Butterfly eyespots are pattern elements composed of concentric rings of coloured scales. These rings develop around an organizing centre, a so-called developmental focus, which during metamorphosis induces the surrounding scale-building cells to produce a designated pigment (Brunetti et al. 2001; Beldade and Brakefield 2002; Carroll et al. 2005). Four stages can be recognized in the development of eyespots on butterfly wings. The first step already takes place in the imaginal disc of the last larval instar, when subdivisions (fields) of the wing are defined. In the second stage, foci are established within specific fields. The establishment of foci takes place in each field separately, which explains why mutants of butterflies with multiple eyespots on the wing can have one of the spots missing without any consequence to other spots (Monteiro et al. 2003). Specification of the eyespot focus is indicated by expression of a homeobox transcription factor, Distal-less (Dll), a Hox gene that has been cloned in Drosophila and many other species. Due to conservation of Hox genes throughout the animal kingdom, antibodies against the Drosophila Hox proteins also provide reactivity to the orthologous Hox proteins of other insects, which allows the expression of these developmental proteins to be localized in developing butterfly wings (Brunetti et al. 2001; Beldade et al. 2002). In the third stage, which takes place in the early pupa, a signal from the focus induces the surrounding cells to adopt a certain colour. The type of pigment that these cells adopt seems to depend on the sensitivity thresholds of the responding cells, whereas the strength of the signal determines the size of the eyespot. The fate determination around the focus uses the hedgehog signalling pathway, one of the major so-called toolkit genes of developmental genetics (Carroll et al. 2005). This pathway, like the insulin signalling pathway discussed in Section 5.2, translates the binding of an extracellular ligand into regulation of a transcription factor, which in this case is cubitus interruptus. Finally, the fourth phase of eyespot formation is the pigmentation itself, which takes place in the late pupal stage.

Which developmental switches are made to produce the alternative seasonal morphs of butterflies like Bicyclus is not known precisely. Given the knowledge about eyespot formation summarized above, it is likely that the switch will involve regulation of developmental genes such as Distal-less, or one of the genes in the hedgehog signalling pathway. The involvement of ecdysteroid hormones in seasonal polyphenisms has been demonstrated for several butterfly species, so it seems reasonable to assume that the upstream part of the regulation consists of an endocrine signal, which in some way or another is sensitive to an environmental cue. Seasonal polyphenism represents a fascinating area of research where genomics, through developmental genetics, can meet ecology and evolution in a fruitful manner.

Another well-known case of polyphenism is represented by the castes of many social insects (termites, ants, wasps, and bees). The best-investigated caste system is that of the worker/ queen polyphenism in the honey bee, Apis mellifera. Experiments have shown convincingly that the development of a larva into a worker or a queen is completely under environmental control, rather than reflecting a genetic predisposition of some larvae to follow a distinct developmental pathway. Larvae are induced to develop into queens when fed a rich mixture of food throughout development, including royal jelly, a secretion from the mandibular gland of nursing workers which contains a higher concentration of sugar than worker jelly. As a consequence, queen larvae develop faster, grow larger, and have larger corpora allata, the source of juvenile hormone, which controls the differentiation of oocyctes and the production of vitellogenic proteins by the fat body. Levels of juvenile hormone are considerably higher in queen larvae than in worker larvae, especially in the fifth instar, the stage just before pupation. Up to the fourth instar (2.5-3.5 days old) the queen developmental pathway is reversible, but after entry into the fifth stage a change of feeding regime has no further influence on the phenotype appearing after pupation. Obviously, the alternative developmental pathways are regulated by larval nutrition, mediated by endocrine signals, which in some way are translated into gene expressions.

Are the castes of honey bees characterized by specific expression signatures? In an early study, Evans and Wheeler (1999) looked at differential gene expression between queen and worker larvae of Apis mellifera using an SSH protocol (see Section 2.1.2, Fig. 2.4); this was followed later by macroarray expression profiling using 144 cDNAs from enriched libraries (Evans and Wheeler 2000, 2001). Gene expressions were compared between early fourth instar (bipotential) larvae and fifth instar larvae destined to workers or queens. Several loci were confirmed to be differentially expressed and, interestingly, many of these were downregulated in queen larvae and the data showed that workers resemble the bipotential young larvae more than queens. So the suggestion is that the worker programme is the default pathway, which must be altered actively to produce a queen programme, and this latter programme includes switching off many genes and turning on a limited set of queen genes.

Fig. 5.20 provides a summary of differential gene expression in honey bee castes. Young larvae (Y in Fig 5.20) overexpressed two heat-shock proteins and several proteins related to RNA processing. Among the genes specifically upregulated in worker larvae (W) is hexamerin 2, a member of a group of hexameric storage proteins, which serve as a source of energy during metamorphosis and adult life. Such hexameres also accumulate in the haemolymph of insects preparing for diapause (Denlinger 2002). A cytochrome P450 was also upregulated consistently in workers and this was also found in another bee species, Melipona quadrifasciata (Judice et al. 2004). The expression profile of queen larvae (Q) shows overexpression of ATP synthase and cytochrome oxidase I. This is consistent with earlier work by Corona et al. (1999) who, using differential display, identified three mitochondrial proteins, mitochondrial translation-iniation factor, cytochrome oxidase subunit 1, and cytochrome c, that were upregulated consistently in queen larvae compared with worker larvae.

LIFE-HISTORY PATTERNS 199 RNA helicase Hsp70 RNA binding Hsp90 Elongation factor 2

LIFE-HISTORY PATTERNS 199 RNA helicase Hsp70 RNA binding Hsp90 Elongation factor 2

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