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subset of them is found in all multicellular animals. When this was realized it was agreed that this group of genes would be called the Hox genes, although both terms, homeotic and Hox, are still in use for the same group of genes. In many organisms these genes form a single cluster on one chromosome, although in Droso-phila they are organized into two clusters, an anteriorly expressed Antennapedia complex (Antp-C) and a posteriorly expressed Bithorax complex (Bx-C). The composition of these clusters in Drosophila is as follows (from anterior to posterior): (Antp-C) - labial {lab), proboscidea (pb), Deformed (Dfd), Sex combs reduced (Scr), Antennapedia (Antp); (Bx-C) - Ultrabithorax(Ubx), abdominal-A (abd-A), and Abdominal-B (Abd-B), as illustrated in the lower figure of a Drosophila embryo (after Carroll 1995; Purugganan 1998). The evolutionary conservation of the Hox genes is remarkable for not only are they conserved in their primary structure but they follow the same order on the chromosome, and their temporal order of expression and anterior border of expression along the body correspond to their chromosomal position. In the lower figure the anterior zone of expression of each gene and the zone of strongest expression is shown (for each gene there is a zone of weaker expression posteriorly); as each gene switches on, protein production from the gene anterior to it is repressed.

The zone of expression of a particular Hox gene may be morphologically very different in different organisms so it is evident that Hox gene activities demarcate relative positions but not particular morphological structures. A single Hox gene may regulate directly or indirectly many targets; for example, Ultrabithorax regulates some 85-170 genes. These downstream genes may operate at different times and also have multiple effects (pleiotropy); for example, wingless in Drosophila is involved successively in segmentation (embryo), Malpighian tubule formation (larva), and leg and wing development (larva-pupa).

Boundaries of transcription factor expression are important locations for the development of distinct morphological structures, such as limbs, tracheae, and salivary glands. Studies of the development of legs and wings have revealed something about the processes involved. Limbs arise at the intersection between expression of wingless, engrailed, and decapentaplegic (dpp), a protein that helps to inform cells of their position in the dorsal-ventral axis. Under the influence of the unique mosaic of gradients created by these gene products, limb primordial cells are stimulated to express the gene distal-less (Dll) required for proximodistal limb growth. As potential limb primordial cells (anlage) are present on all segments, as are limb-inducing protein gradients, prevention of limb growth on inappropriate segments (i.e. the Drosophila abdomen) must involve repression of Dll expression on such segments. In Lepidoptera, in which larval prolegs typically are found on the third to sixth abdominal segments, homeotic gene expression is fundamentally similar to that of Drosophila. In the early lepidopteran embryo Dll and Antp are expressed in the thorax, as in Drosophila, with abd-A expression dominant in abdominal segments including 3-6, which are prospective for proleg development. Then a dramatic change occurs, with abd-A protein repressed in the abdominal proleg cell anlagen, followed by activation of Dll and up-regulation of Antp expression as the anlagen enlarge. Two genes of the Bithorax complex (Bx-C), Ubx and abd-A, repress Dll expression (and hence prevent limb formation) in the abdomen of Drosophila. Therefore, expression of prolegs in the caterpillar abdomen results from repression of Bx-C proteins thus derepressing Dll and Antp and thereby permitting their expression in selected target cells with the result that prolegs develop.

A somewhat similar condition exists with respect to wings, in that the default condition is presence on all thoracic and abdominal segments with Hox gene repression reducing the number from this default condition. In the prothorax, the homeotic gene Scr has been shown to repress wing development. Other effects of Scr expression in the posterior head, labial segment, and prothorax appear homologous across many insects, including ventral migration and fusion of the labial lobes, specification of labial palps, and development of sex combs on male prothoracic legs. Experimental mutational damage to Scr expression leads, amongst other deformities, to appearance of wing primordia from a group of cells located just dorsal to the prothoracic leg base. These mutant prothoracic wing anlagen are situated very close to the site predicted by Kukalova-Peck from paleontological evidence (section 8.4, Fig. 8.4b). Furthermore, the apparent default condition (lack of repression of wing expression) would produce an insect resembling the hypothesized "proto-pterygote", with winglets present on all segments.

Regarding the variations in wing expression seen in the pterygotes, Ubx activity differs in Drosophila between the meso- and metathoracic imaginal discs; the anterior produces a wing, the posterior a haltere. Ubx is unexpressed in the wing (mesothoracic) imaginal disc but is strongly expressed in the metathoracic disc, where its activity suppresses wing and enhances haltere formation. However, in some studied non-dipterans Ubx is expressed as in Drosophila - not in the fore-wing but strongly in the hind-wing imaginal disc - despite the elaboration of a complete hind wing as in butterflies or beetles. Thus, very different wing morphologies seem to result from variation in "downstream" response to wing-pattern genes regulated by Ubx rather than from homeotic control.

Clearly, much is yet to be learnt concerning the multiplicity of morphological outcomes from the interaction between Hox genes and their downstream interactions with a wide range of genes. It is tempting to relate major variation in Hox pathways with morphological disparities associated with high-level taxonomic rank (e.g. animal classes), more subtle changes in Hox regulation with intermediate taxonomic levels (e.g. orders/suborders), and changes in downstream regulatory/functional genes perhaps with suborder/ family rank. Notwithstanding some progress in the case of the Strepsiptera (q.v.), such simplistic relationships between a few well-understood major developmental features and taxonomic radiations may not lead to great insight into insect macroevolution in the immediate future. Estimated phylogenies from other sources of data will be necessary to help interpret the evolutionary significance of homeotic changes for some time to come.

Fig. 6.6 Examples of larval types. Polypod larvae: (a) Lepidoptera: Sphingidae; (b) Lepidoptera: Geometridae; (c) Hymenoptera: Diprionidae. Oligopod larvae: (d) Neuroptera: Osmylidae; (e) Coleoptera: Carabidae; (f) Coleoptera: Scarabaeidae. Apod larvae: (g) Coleoptera: Scolytidae; (h) Diptera: Calliphoridae; (i) Hymenoptera: Vespidae. ((a,e-g) After Chu 1949; (b,c) after Borror et al. 1989; (h) after Ferrar 1987; (i) after CSIRO 1970.)

Fig. 6.6 Examples of larval types. Polypod larvae: (a) Lepidoptera: Sphingidae; (b) Lepidoptera: Geometridae; (c) Hymenoptera: Diprionidae. Oligopod larvae: (d) Neuroptera: Osmylidae; (e) Coleoptera: Carabidae; (f) Coleoptera: Scarabaeidae. Apod larvae: (g) Coleoptera: Scolytidae; (h) Diptera: Calliphoridae; (i) Hymenoptera: Vespidae. ((a,e-g) After Chu 1949; (b,c) after Borror et al. 1989; (h) after Ferrar 1987; (i) after CSIRO 1970.)

Strepsiptera. Apod larvae (Fig. 6.6g-i) lack true legs and are usually worm-like or maggot-like, living in soil, mud, dung, decaying plant or animal matter, or within the bodies of other organisms as parasitoids (Chapter 13). The Siphonaptera, aculeate Hymenoptera, nema-toceran Diptera, and many Coleoptera typically have apod larvae with a well-developed head, whereas in the maggots of higher Diptera the mouth hooks may be the only obvious evidence of the cephalic region. The grub-like apod larvae of some parasitic and gall-inducing wasps and flies are greatly reduced in external structure and are difficult to identify to order level even by a specialist entomologist. Furthermore, the early-instar larvae of some parasitic wasps resemble a naked embryo but change into typical apod larvae in later instars.

A major change in form during the larval phase, such as different larval types in different instars, is called larval heteromorphosis (or hypermetamor-phosis). In the Strepsiptera and certain beetles this involves an active first-instar larva, or triungulin, followed by several grub-like, inactive, sometimes legless, later-instar larvae. This developmental phenomenon occurs most commonly in parasitic insects in which a mobile first instar is necessary for host location and entry. Larval heteromorphosis and diverse larval types are typical of many parasitic wasps, as mentioned above.

6.2.3 Metamorphosis

All pterygote insects undergo varying degrees of transformation from the immature to the adult phase of their life history. Some exopterygotes, such as cockroaches, show only slight morphological changes during post-embryonic development, whereas the body is largely reconstructed at metamorphosis in many endoptery-gotes. Only the Holometabola (= Endopterygota) have a metamorphosis involving a pupal stadium, during which adult structures are elaborated from larval structures. Alterations in body shape, which are the essence of metamorphosis, are brought about by differential growth of various body parts. Organs that will function in the adult but that were undeveloped in the larva grow at a faster rate than the body average. The accelerated growth of wing pads is the most obvious example, but legs, genitalia, gonads, and other internal organs may increase in size and complexity to a considerable extent.

The onset of metamorphosis generally is associated with the attainment of a certain body size, which is thought to program the brain for metamorphosis, resulting in altered hormone levels. Metamorphosis in most studied beetles, however, shows considerable independence from the influence of the brain, especially during the pupal instar. In most insects, a reduction in the amount of circulating juvenile hormone (as a result of reduction of corpora allata activity) is essential to the initiation of metamorphosis. (The physiological events are described in section 6.3.)

The molt into the pupal instar is called pupation, or the larval-pupal molt. Many insects survive conditions unfavorable for development in the "resting", non-feeding pupal stage, but often what appears to be a pupa is actually a fully developed adult within the pupal cuticle, referred to as a pharate (cloaked) adult. Typically, a protective cell or cocoon surrounds the pupa and then, prior to emergence, the pharate adult; only certain Coleoptera, Diptera, Lepidoptera, and Hymenoptera have unprotected pupae.

Several pupal types (Fig. 6.7) are recognized and these appear to have arisen convergently in different orders. Most pupae are exarate (Fig. 6.7a-d) - their appendages (e.g. legs, wings, mouthparts, and antennae) are not closely appressed to the body (see Plate 3.2, facing p. 14); the remaining pupae are obtect (Fig. 6.7g-j) - their appendages are cemented to the body and the cuticle is often heavily sclerotized (as in almost all Lepidoptera). Exarate pupae can have articulated mandibles (decticous), that the pharate adult uses to cut through the cocoon, or the mandibles can be non-articulated (adecticous), in which case the adult usually first sheds the pupal cuticle and then uses its mandibles and legs to escape the cocoon or cell. In some cyclorrhaphous Diptera (the Schizophora) the adectic-ous exarate pupa is enclosed in a puparium (Fig. 6.7e,f) - the sclerotized cuticle of the last larval instar. Escape from the puparium is facilitated by eversion of a membranous sac on the head of the emerging adult, the ptilinum. Insects with obtect pupae may lack a cocoon, as in coccinellid beetles and most nemato-cerous and orthorrhaphous Diptera. If a cocoon is present, as in most Lepidoptera, emergence from the cocoon is either by the pupa using backwardly directed abdominal spines or a projection on the head, or an adult emerges from the pupal cuticle before escaping the cocoon, sometimes helped by a fluid that dissolves the silk.

6.2.4 Imaginal or adult phase

Except for the mayflies, insects do not molt again once the adult phase is reached. The adult, or imaginal, stage has a reproductive role and is often the dispersive stage in insects with relatively sedentary larvae. After the imago emerges from the cuticle of the previous instar (eclosion), it may be reproductively competent almost immediately or there may be a period of maturation in readiness for sperm transfer or oviposition. Depending on species and food availability, there are from one to several reproductive cycles in the adult stadium. The adults of certain species, such as some mayflies, midges, and male scale insects, are very short-lived. These insects have reduced or no mouthparts and fly for only a few hours or at the most a day or two - they simply mate and die. Most adult insects live at least a few weeks, often a few months and sometimes for several years; termite reproductives and queen ants and bees are particularly long-lived.

Adult life begins at eclosion from the pupal cuticle. Metamorphosis, however, may have been complete for some hours, days, or weeks previously and the pharate

Fig. 6.7 Examples of pupal types. Exarate decticous pupae: (a) Megaloptera: Sialidae; (b) Mecoptera: Bittacidae. Exarate adecticous pupae: (c) Coleoptera: Dermestidae; (d) Hymenoptera: Vespidae; (e,f) Diptera: Calliphoridae, puparium and pupa within. Obtect adecticous pupae: (g) Lepidoptera: Cossidae; (h) Lepidoptera: Saturniidae; (i) Lepidoptera: Papilionidae, chrysalis; (j) Coleoptera: Coccinellidae. ((a) After Evans 1978; (b,c,e,g) after CSIRO 1970; (d) after Chu 1949; (h) after Common 1990; (i) after Common & Waterhouse 1972; (j) after Palmer 1914.)

Fig. 6.7 Examples of pupal types. Exarate decticous pupae: (a) Megaloptera: Sialidae; (b) Mecoptera: Bittacidae. Exarate adecticous pupae: (c) Coleoptera: Dermestidae; (d) Hymenoptera: Vespidae; (e,f) Diptera: Calliphoridae, puparium and pupa within. Obtect adecticous pupae: (g) Lepidoptera: Cossidae; (h) Lepidoptera: Saturniidae; (i) Lepidoptera: Papilionidae, chrysalis; (j) Coleoptera: Coccinellidae. ((a) After Evans 1978; (b,c,e,g) after CSIRO 1970; (d) after Chu 1949; (h) after Common 1990; (i) after Common & Waterhouse 1972; (j) after Palmer 1914.)

adult may have rested in the pupal cuticle until the appropriate environmental trigger for emergence. Changes in temperature or light and perhaps chemical signals may synchronize adult emergence in most species.

Hormonal control of emergence has been studied most comprehensively in Lepidoptera, especially in the tobacco hornworm, Manduca sexta (Lepidoptera: Sphingidae), notably by James Truman, Lynn Riddiford, and colleagues. The description of the following events at eclosion are based largely on M. sexta but are believed to be similar in other insects and at other molts. At least five hormones are involved in eclosion

(see also section 6.3). A few days prior to eclosion the ecdysteroid level declines, and a series of physiological and behavioral events are initiated in preparation for ecdysis, including the release of two neuropeptides. Ecdysis triggering hormone (ETH), from epitracheal glands called Inka cells, and eclosion hormone (EH), from neurosecretory cells in the brain, act in concert to trigger pre-eclosion behavior, such as seeking a site suitable for ecdysis and movements to aid later extrication from the old cuticle. ETH is released first and ETH and EH stimulate each other's release, forming a positive feedback loop. The build-up of EH also releases crustacean cardioactive peptide (CCAP) from cells

Fig. 6.8 The nymphal-imaginal molt of a male dragonfly of Aeshna cyanea (Odonata: Aeshnidae). The final-instar nymph climbs out of the water prior to the shedding of its cuticle. The old cuticle splits mid-dorsally, the teneral adult frees itself, swallows air and must wait many hours for its wings to expand and dry. (After Blaney 1976.)

Fig. 6.8 The nymphal-imaginal molt of a male dragonfly of Aeshna cyanea (Odonata: Aeshnidae). The final-instar nymph climbs out of the water prior to the shedding of its cuticle. The old cuticle splits mid-dorsally, the teneral adult frees itself, swallows air and must wait many hours for its wings to expand and dry. (After Blaney 1976.)

in the ventral nerve cord. CCAP switches off pre-eclosion behavior and switches on eclosion behavior, such as abdominal contraction and wing-base movements, and accelerates heartbeat. EH appears also to permit the release of further neurohormones - bursi-con and cardiopeptides - that are involved in wing expansion after ecdysis. The cardiopeptides stimulate the heart, facilitating movement of hemolymph into the thorax and thus into the wings. Bursicon induces a brief increase in cuticle plasticity to permit wing expansion, followed by sclerotization of the cuticle in its expanded form.

The newly emerged, or teneral, adult has soft cuticle, which permits expansion of the body surface by swallowing air, by taking air into the tracheal sacs, and by locally increasing hemolymph pressure by muscular activity. The wings normally hang down (Fig. 6.8; see also Plate 3.4), which aids their inflation. Pigment deposition in the cuticle and epidermal cells occurs just before or after emergence and is either linked to, or followed by, sclerotization of the body cuticle under the influence of the neurohormone bursicon.

Following emergence from the pupal cuticle, many holometabolous insects void a fecal fluid called the meconium. This represents the metabolic wastes that have accumulated during the pupal stadium. Sometimes the teneral adult retains the meconium in the rectum until sclerotization is complete, thus aiding increase in body size.

Reproduction is the main function of adult life and the length of the imaginal stadium, at least in the female, is related to the duration of egg production. Reproduction is discussed in detail in Chapter 5. Senescence correlates with termination of reproduction and death may be predetermined in the ontogeny of an insect. Females may die after egg deposition and males may die after mating. An extended post-reproductive life is important in distasteful, aposematic insects to allow predators to learn the distastefulness of the prey at a developmental period when prey individuals are expendable (section 14.4).

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