Entomology 3rd edition - C.Gillott - Chapter 20 ppt

Formation and Growth of Germ Band The next stage is blastoderm differentiation, giving rise to the embryonic primordiuman area of closely packed columnar cells from which the future embr

in the egg, carried to an extreme in certain parasitic Hymenoptera and viviparous Diptera(Cecidomyiidae), whose eggs are yolkless and receive nutrients from their surroundings, hassome important consequences Broadly speaking, the eggs of endopterygotes are smaller(size measured in relation to the body size of the laying insect) and develop more rapidlythan those of exopterygotes The increased quantity of cytoplasm leads to the more rapidformation of more and larger cells at the yolk surface that facilitates the formation of a largerembryonic area from which development can take place Compared with that of exoptery-gotes, development of endopterygotes is streamlined and simplified There has been, asAnderson (1972b, p 229) put it, “reduction or elimination of ancestral irrelevancies,” whichwhen taken to an extreme, seen in the apocritan Hymenoptera and cyclorrhaph Diptera, re-sults in the formation of a structurally simple larva that hatches within a short time of egglaying However, superimposed on this process of short-circuiting may be developmentalspecializations associated with an increasing dissimilarity of juvenile and adult habits.

2 Cleavage and Blastoderm Formation

As it moves toward the center of an egg after fusion, the zygote nucleus gins to divide mitotically The first division occurs at a predetermined site, the cleav-age center (Figure 20.1), located in the future head region, which cannot be recognizedmorphologically but which appears to become activated either when sperm enter an egg orwhen an egg is laid Early divisions are synchronous, and as nuclei are formed and migrate

be-597

CHAPTER 20

FIGURE 20.1. Positions of cleavage center, activation center, and

differen-tiation center in eggs of Platycnemis (Odonata) [After D Bodenstein, 1953, Embryonic development, in: Insect Physiology (K D Roeder, ed.) Copy-

right @ 1953, John Wiley and Sons, Inc Reprinted by permission of John Wiley and Sons, Inc.]

through the yolk toward the periplasm, each becomes surrounded by an island of cytoplasm(Figure 20.2A) Each nucleus and its surrounding cytoplasm are known as a cleavage en-ergid In eggs of endopterygotes and possibly exopterygotes, but not those of apterygotes,the energids remain interconnected by means of fine cytoplasmic bridges

The rate at which nuclei migrate to the yolk surface and the method of colonization arevaried In eggs of some species nuclei appear in the periplasm as early as the 64-energidstate (after six divisions); in others, nuclei are not seen in the periplasm until the 1024-energid stage In eggs of most endopterygotes and in those of paleopteran and hemipteroidexopterygotes, the periplasm is invaded uniformly by the energids However, in eggs oforthopteroid insects the periplasm at the posterior pole of the egg receives energids first,after which there is progressive colonization of the more anterior regions

In eggs of most insects not all cleavage energids migrate to the periphery but continue

to divide within the yolk to form primary vitellophages, so-called because in most speciesthey become phagocytic cells whose function is to digest the yolk (Figure 20.2B) In eggs ofLepidoptera, Diptera, and some orthopteroid insects, however, all of the energids migrate tothe periplasm and only later do some of their progeny move back into the yolk as secondaryvitellophages (Figure 20.2F) Secondary vitellophages are also produced in eggs of otherinsects to supplement the number of primary vitellophages So-called tertiary vitellophagesare produced in eggs of some cyclorrhaph Diptera and apocritan Hymenoptera from theanterior and posterior midgut rudiments

After their arrival at the periplasm, the energids continue to divide, often synchronously,until the nuclei become closely packed (the syncytial blastoderm stage), after which cellmembranes form by radial infolding, then tangential expansion of the original egg plas-malemma (the uniform blastoderm stage) (Figure 20.2C–F) From the resulting monolayer

of cells develop all of the cells of the larval body, except in a few species where vitellophages

or yolk cells contribute to the formation of the midgut (Section 7.4)

3 Formation and Growth of Germ Band

The next stage is blastoderm differentiation, giving rise to the embryonic primordium(an area of closely packed columnar cells from which the future embryo forms) and the

EMBRYONIC DEVELOPMENT

FIGURE 20.2. Stages in cleavage and blastoderm formation in egg of Dacus tryoni (Diptera) (A) Frontal

section through anterior end during 6th division; (B) transverse section after 8th division; (C) transverse section

after 12th division; (D) transverse section during 13th division; (E) transverse section at syncytial blastoderm

stage; and (F) frontal section through posterior end after formation of uniform cellular blastoderm [After D T.

Anderson, 1972b, The development of holometabolous insects, in: Developmental Systems: Insects, Vol I (S J.V

Counce and C H Waddington, eds.) By permission of Academic Press Ltd., and the author.]

extra-embryonic ectoderm from which the extra-embryonic membranes later differentiate

(Figure 20.3) For more than a century, attempts have been made to explain how the body

pattern of an insect is determined Following the classic experiments of the German

embry-ologist Seidel in the late 1920s, it was widely believed that differentiation was controlled

by two centers (Counce, 1973; Heming, 2003) As energids move toward the posterior end

of the egg, they interact with a so-called “activation center” (Figure 20.1), and

differen-tiation subsequently occurs Seidel’s experiments showed that neither an energid nor the

activation center alone could stimulate differentiation It was presumed that the center is

caused to release an unidentified chemical that diffuses anteriorly This diffusion is seen

morphologically as a clearing and slight contraction of the yolk As the chemical reaches

CHAPTER 20

FIGURE 20.3. Diagrammatic transverse (A) and sagittal (B) sections of egg of Pontania (Hymenoptera) to

show differentiation of blastoderm into embryonic primordium and extra-embryonic ectoderm Note also the germ (pole) cells at the posterior end [After D T Anderson, 1972b, The development of holometabolous insects,

in: Developmental Systems: Insects, Vol I (S J Counce and C H Waddington, eds.) By permission of AcademicV Press Ltd., and the author.]

the future prothoracic region of the embryo (the “differentiation center”) (Figure 20.1), theblastoderm in this region gives a sharp twitch and becomes slightly invaginated Blastodermcells aggregate within this invagination and differentiate into the embryonic primordium.(Later in embryogenesis, other processes, for example, mesoderm formation and segmen-tation, begin at the differentiation center and spread anteriorly and posteriorly from it.)

An alternate view for the cause of embryonic differentiation is the “gradient hypothesis,”which had its origins at the end of the 19th century but then fell out of favor after Seidel’spioneering work (Sander, 1984, 1997; Lawrence, 1992) Essentially, the hypothesis proposesthat a chemical produced at each end of an egg diffuses throughout the egg, producing twogradients of concentration (Figure 20.4) Cells within the egg then “recognize” their positionwithin the egg by the relative concentrations of the chemical and differentiate accordingly.Initial support for the existence of chemical gradients in eggs came from experiments inwhich eggs either were ligatured at various distances along their length and at varied timesafter embryonic development began or were centrifuged, thereby disrupting the proposedgradient Recently, the application of genetic and molecular techniques to the study of

pattern development in Drosophila has given further support to the idea of gradients Thus,

a modern interpretation of Seidel’s differentiation center is that it is a “commitment center”;that is, it is the point at which blastoderm cells are committed to following a particular path

of differentiation by virtue of their position within the gradients (Heming, 2003)

FIGURE 20.4. Diagrammatic representation of the gradient hypothesis A chemical produced at each end of

an egg diffuses lengthwise, forming two gradients of concentration At any point along the length of the egg, the relative concentration of the two chemicals provides positional information to cells.

EMBRYONIC DEVELOPMENT

FIGURE 20.5. Form and position of embryonic primordium in exopterygotes (A) Periplaneta; (B) Platycnemis;

(C) Zootermopsis; and (D) Notonecta [After D T Anderson, 1972a, The development of hemimetabolous insects,

in: Developmental Systems: Insects, Vol I (S J Counce and C H Waddington, eds.) By permission of AcademicV

Press Ltd., and the author.]

As a result of the differing amounts of yolk that exopterygote and endopterygote eggs

contain, important differences occur in the formation of the embryonic primordium In

exopterygote eggs where there is initially little cytoplasm, the embryonic primordium is

normally relatively small, and its formation depends on the aggregation and, to some extent,

proliferation of cells In these eggs it usually occupies a posterior midventral position (Figure

20.5A–D) In contrast, in endopterygote eggs with their greater quantity of cytoplasm, the

primordium forms as a broad monolayer of columnar cells that occupies much of the ventral

surface of the yolk (Figure 20.6A,B) In other words, the primordium in endopterygote eggs

does not require to undergo much increase in size, as is necessary in eggs of exopterygotes,

so that tissue differentiation can occur directly and embryonic growth more rapidly At its

extreme, seen in eggs of some Diptera and Hymenoptera, the primordium occupies both

ventral and lateral areas of the egg, with the extra-embryonic ectoderm covering only the

dorsal surface (Figure 20.6C)

The shape of the primordium is varied, though in most insects the anterior region is

expanded laterally as a pair of head lobes (= protocephalon), behind which is a region of

varied length, the protocorm (postantennal region) (Figure 20.5) In eggs of Paleoptera,

hemipteroid insects, and some orthopteroid species, the protocorm is semilong and at its

formation includes the mouthpart-bearing segments, the thoracic segments, and a posterior

growth region from which the abdominal segments arise In eggs of other orthopteroid

insects the postantennal region consists initially of only the growth zone Though the

proto-corm in most endopterygote embryos is long, it also includes a posterior growth zone from

which rudimentary abdominal segments proliferate As the embryonic primordium

elon-gates and begins to differentiate, it becomes known as the germ band During elongation

and differentiation, the abdomen grows around the posterior end and forward over the dorsal

surface of the egg (Figure 20.7) In eggs of some higher endopterygotes

(Hymenoptera-Apocrita and Diptera-Muscomorpha), there is no posterior growth zone and the abdominal

segments arise directly from the primordium

CHAPTER 20

FIGURE 20.6. Form and position of embryonic primordium in endopterygotes (A) Tenebrio; (B) Sialis; and (C) Pimpla [After D T Anderson, 1972a,b, The development of hemimetabolous insects, and The development

of holometabolous insects, in: Developmental Systems: Insects, Vol I (S J Counce and C H Waddington, eds.).V

By permission of Academic Press Ltd., and the author.]

It is during the differentiation and elongation of the germ band that the primordialgerm cells first become noticeable in most endopterygote eggs, though in those of someColeoptera they are distinguishable even as the syncytial blastoderm is forming They arelargish, rounded cells in a distinct group at the posterior pole of the yolk, and accordingly arereferred to as pole cells (Figure 20.3) In eggs of Dermaptera, Psocoptera, Thysanoptera, andhomopterans also, the germ cells differentiate early at the posterior end of the primordium

In those of most exopterygotes, however, they are not apparent until gastrulation or somiteformation has occurred

As the germ band elongates and becomes broader, segmentation and limb-bud formationappear externally and are accompanied internally by mesoderm and somite formation.Growth of the germ band may occur either on the surface of the yolk (superficial growth) asseen in eggs of Dictyoptera, Dermaptera, Isoptera, some other orthopteroid insects, and allendopterygotes (Figure 20.7), or by immersion into the yolk (immersed growth) as occurs

in eggs of Paleoptera, most Orthoptera, and hemipteroid insects (Figure 20.8) Immersion ofthe germ band (anatrepsis) forms the first of a series of embryonic movements, collectivelyknown as blastokinesis The reverse movement (katatrepsis), which brings the embryoback to the surface of the yolk, occurs later (see Section 6) Anatrepsis has developedsecondarily (i.e., superficial growth is the more primitive method) and convergently amongthose exopterygotes in which it occurs Its functional significance is, however, not clear(Anderson, 1972a; Heming, 2003)

4 Gastrulation, Somite Formation, and Segmentation

As the embryonic primordium begins to increase in length, its midventral cells sinkinward to form a transient, longitudinal gastral groove (Figure 20.9A) The invaginated

EMBRYONIC DEVELOPMENT

FIGURE 20.7. Stages in elongation and segmentation of germ band in Zootermopsis (Isoptera) (A–C) and

Bruchidius (Coleoptera) (D–F) [After D T Anderson, 1972a,b, The development of hemimetabolous insects,

and the development of holometabolous insects, in: Developmental Systems: Insects, Vol I (S J Counce andV

C H Waddington, eds.) By permission of Academic Press Ltd., and the author.]

cells soon separate from the outer layer, which closes to obliterate the groove It is from

the anterior and posterior points of closure of the gastral groove that the stomodeum and

proctodeum, respectively, develop The outer layer can now be distinguished as the

em-bryonic ectoderm The invaginated cells, which proliferate and spread laterally, form the

mesoderm (Figure 20.9B,C) except adjacent to the developing stomodeum and proctodeum

where they become the anterior and posterior midgut rudiments, respectively The

meso-dermal cells become concentrated into paired longitudinal tracts which soon separate into

CHAPTER 20

FIGURE 20.8. Early embryonic development in Calopteryx to show anatrepsis and katatrepsis [A–E, after O A Johannsen and F H Butt, 1941, Embryology of Insects and Myriapods By permission of McGraw-Hill Book Co., Inc F, After R F Chapman, 1971, The Insects: Structure and Function By permission of Elsevier/North-Holland,

Inc., and the author.]

segmental blocks, leaving only a thin longitudinal strip, the median mesoderm, from whichhemocytes later differentiate From these segmental blocks, paired hollow somites usuallyarise (Figure 20.9E) Somite formation is initiated and occurs more or less simultaneously

in the gnathal and thoracic segments, spreading anteriorly and posteriorly after gastrulationtakes place Formation of the coelom (the cavity within a somite) may occur in one of twoways, by internal splitting of a somite or by median folding of the lateral part of each somite

EMBRYONIC DEVELOPMENT

FIGURE 20.9. Formation of gastral groove, somites, and embryonic membranes [After D T Anderson, 1972a,

The development of hemimetabolous insects, in Developmental Systems: Insects, Vol I (S J Counce and C H.V

Waddington, eds.) By permission of Academic Press Ltd., and the author.]

In embryos of a given species, one or both methods may be seen in different segments For

example, internal splitting of the somites occurs in all segments of embryos of Phasmida,

most hemipteroid insects, and most endopterygotes, and in the abdominal segments of

Locusta embryos Median folding is the method used in all segments in embryos of Odonata,

Dictyoptera, and Mallophaga, and in the gnathal and thoracic segments of those of Locusta,

and some Coleoptera, Lepidoptera, and Megaloptera In exopterygote embryos, all somites

usually develop a central cavity, though this may be only temporary Among endopterygotes,

members of more primitive orders retain a full complement of somites in their embryos and

the latter usually develop a coelom In embryos of some species, however, cavities may not

form, and somite formation may be suppressed in the head segments In embryos of Diptera

and Hymenoptera, no distinct head somites appear, and in those of some Muscomorpha

and Apocrita, somite formation is entirely suppressed, so that mesodermal derivatives are

produced directly from a single midventral mass

5 Formation of Extra-Embryonic Membranes

Simultaneously with gastrulation and somite formation, two extra-embryonic

mem-branes, the amnion and serosa, develop from the extra-embryonic ectoderm (Figure 20.9)

Cells at the edge of the germ band proliferate and the tissue formed on each side folds

ventrally to give rise to the amniotic folds These meet and fuse in the ventral midline to

form inner and outer membranes, the amnion and serosa, respectively, the former enclosing

a central fluid-filled amniotic cavity Many authors have suggested that such a cavity would

CHAPTER 20 son (1972a) considered, however, that these functions are redundant and that the cavity

must have an as yet unidentified function Another possibility is that the amnion and itscavity are used to store wastes, which are thus kept separate from the yolk The generalmethod of amnion and serosa formation outlined above is found in all insect embryos (withsome modification where immersion of the germ band into the yolk occurs) except those

of Muscomorpha and Apocrita, in which, it will be recalled, the embryonic primordiumcovers most of the yolk surface In these, embryonic membranes are greatly reduced orlost In embryos of Apocrita the extra-embryonic ectoderm separates from the edge of theprimordium and grows ventrally to form the serosa; that is, amniotic folds are not formed Inembryos of Muscomorpha neither an amnion nor a serosa forms, and the extra-embryonicectoderm covers the yolk until definitive dorsal closure occurs (see below)

After the embryonic membranes form, the serosa in most insect eggs secretes a cuticlethat is often as thick as the chorion For several species, production of the serosal cuticle isclosely synchronized with a peak of molting hormone in the egg (see Section 9)

6 Dorsal Closure and Katatrepsis

When germ band elongation and segmentation are complete, limb buds develop, theembryonic ectoderm grows dorsolaterally over the yolk mass, and internally organogenesisbegins This phase of growth is ended abruptly as the extra-embryonic membranes fuseand rupture and the germ band reverts to its original (pre-anatreptic) position (in mostexopterygotes) or shortens (endopterygotes)

In embryos of most insects, the amnion and serosa fuse in the vicinity of the head, andthe combined tissue then splits to expose the head and rolls back dorsally over the yolk(Figure 20.10A) As a result, the serosa is reduced to a small mass of cells, the secondarydorsal organ, and the amnion becomes stretched over the yolk, forming the provisionaldorsal closure (Figure 20.10B) In some endopterygote embryos, variations of this processcan be seen In those of Nematocera (Diptera) and Symphyta (Hymenoptera), for example,

it is the amnion that ruptures and is reduced, leaving the serosa intact As noted above, ineggs of Apocrita only a serosa is formed, and this persists until definitive dorsal closureoccurs, and in those of Muscomorpha no extra-embryonic membranes develop, and the yolkremains covered by the extra-embryonic ectoderm until definitive dorsal closure

Except in dictyopteran embryos where the germ band remains superficial and ventralduring elongation, extensive movement of the germ band now occurs in exopterygote eggswhich serves (1) to bring an immersed germ band back to the surface of the yolk and (2) torestore the germ band to its pre-anatreptic orientation, that is, on the ventral surface of theyolk with the head end facing the anterior pole of the egg This movement, the reverse ofanatrepsis, is known as katatrepsis (Figure 20.8)

At the beginning of provisional dorsal closure, the germ band of most endopterygotes

is quite long so that, although its anterior end is ventral, its posterior component passesround the posterior tip of the yolk and forward along the dorsal side (Figure 20.7F) Duringclosure, the germ band shortens and broadens rapidly so that its posterior end now comes

to lie near the posterior end of the egg (Figure 20.11A)

Definitive dorsal closure, that is, the enclosing of the yolk within the embryo, thenoccurs It is achieved in all insect embryos by a lateral growth of the embryonic ectoderm,which gradually replaces the amnion or, rarely, the serosa (Figures 20.10C and 20.11B)

EMBRYONIC DEVELOPMENT

FIGURE 20.10. Diagrammatic representation of dorsal closure (A) Initial fusion of amnion and serosa and

beginning of rolling back; (B) provisional dorsal closure with amnion covering yolk; and (C) definitive dorsal

closure with yolk enclosed within embryonic ectoderm.

7 Tissue and Organ Development

7.1 Appendages

Paired segmental evaginations of the embryonic ectoderm appear on the thoracic,

antennal, and gnathal segments while the abdominal part of the germ band is still forming

(see Figure 20.7) Their subsequent growth results from proliferation of the ectoderm

as a single layer of cells and of mesodermal cells within The cephalic and thoracic

limbs ultimately differentiate into their specific form, except in eggs of secondarily apodous

species where they soon shorten or become reduced to epidermal thickenings In embryos

of Muscomorpha, the thoracic appendages never develop beyond the epidermal thickening

stage

CHAPTER 20

FIGURE 20.11. (A) Five-day embryo of Bruchidius (Coleoptera) after shortening of germ band Compare this figure with Figure 20.7F; and (B) embryo of Bruchidius at hatching stage (9 days) [After D T Anderson, 1972b, The development of holometabolous insects in: Developmental Systems: Insects, Vol I (S J Counce and C H.V Waddington, eds.) By permission of Academic Press Ltd., and the author.]

In Paleoptera and orthopteroid insects, 11 pairs of abdominal appendages evaginate fore provisional dorsal closure In most hemipteroid embryos, no sign of abdominal limbs

be-is evident, though in those of Hemiptera and Thysanoptera appendages develop on thefirst and last abdominal segments Ten pairs of abdominal evaginations develop in most en-dopterygote embryos The fate of the abdominal appendages varies, and some or all of themmay disappear before embryonic development is completed The first (most anterior) pairdisappears after blastokinesis in embryos of Paleoptera and some orthopteroid insects, butremains as glandular pleuropodia in those of Dictyoptera, Phasmida, Orthoptera, Hemiptera,and some Coleoptera and Lepidoptera The function of the pleuropodia is uncertain, thoughsome authors have suggested that in orthopteran embryos they secrete chitinase that bringsabout dissolution of the serosal cuticle The pleuropodia are resorbed or discarded before orshortly after hatching The appendages of the second through seventh abdominal segmentsare resorbed, except in some endopterygotes where they persist as larval prolegs Pairs 8–10may differentiate into the external genitalia or disappear, while the last pair either persists

as cerci or disappears

7.2 Integument and Ectodermal Derivatives

Soon after definitive dorsal closure, the outer embryonic ectoderm differentiates intoepidermis, which in embryos of most insects then secretes the first instar larval cuticle Insome insects, however, one or more embryonic cuticles are produced which may be shedbefore or at hatching As in larvae, production of the cuticles in embryos appears to beregulated by molting hormone (Section 9)

External sensilla generally develop from a dividing precursor epidermal cell, whosedaughter cells then differentiate to form the sensory neuron and accessory cells (Chapter 12).The axon of the sensory neuron finds the appropriate interneurons within the central nervous

EMBRYONIC DEVELOPMENT

system by growing along the surface of pioneer neurons (Section 7.3) or neurons of

previ-ously formed sensilla (Heming, 2003) Similarly, both compound and simple eyes develop

from groups of epidermal cells, each of which divides and differentiates to form the

pho-toreceptive and accessory components of the light-sensitive structures

Imaginal discs and histoblasts, from which many adult tissues are derived at

metamor-phosis in higher Diptera and Hymenoptera (Chapter 21, Section 4.2), can be recognized

soon after germ-band formation They are groups of cells that separate from the ectoderm

in characteristic numbers, sizes and shapes, at specific sites in the body (Heming, 2003)

Concurrently with the formation of abdominal appendages a number of ectodermal

invaginations develop, from which differentiate endoskeletal components, various glands,

the tracheal system, and certain parts of the reproductive tract (for the latter, see Section

7.6) From ventrolateral invaginations at the junctions of the antennal/mandibular segments

and the mandibular/maxillary segments are derived the anterior and posterior arms of the

tentorium Paired mandibular apodemes differentiate from invaginations near the bases of

the mandibles The apodemes of the trunk region arise from intersegmental invaginations

in the thorax and abdomen

Salivary glands develop from a pair of invaginations near the bases of the labial

ap-pendages When the appendages fuse the invaginations merge to form a common salivary

duct that opens midventrally on the hypopharynx

The corpora allata develop from a pair of ventrolateral invaginations at the junction

of the mandibular/maxillary segments Initially, they exist as hollow vesicles, though these

fill in as they move dorsally to their final position adjacent to the stomodeum The molt

glands also originate as paired ventral ectodermal invaginations, usually on the prothoracic

segment Although the endocrine glands arise before katatrepsis, at this time they are

non-secretory, and maternally derived hormones (especially ecdysteroids) stored in the egg are

used in embryonic endocrine regulation (Section 9) Other invaginations on the head may

give rise to specialized exocrine glands on the mandibles or maxillae

Elements of the tracheal system can be seen first as paired lateral invaginations on

each segment from the second thoracic to the eighth (ninth in a few Thysanura) abdominal

However, not all of these invaginations develop completely into tracheae Those that do,

bifurcate and anastomose with branches from adjacent segments and from their opposite

partner of the same segment The cells differentiate as tracheal epithelium and then secrete a

cuticular lining After cuticle secretion but before hatching, gas is secreted into the tracheal

system Some of the invaginated ectodermal cells differentiate into oenocytes These may

remain closely associated with the tracheal system, form definite clusters in specific body

regions, or become embedded as single cells in the fat body

7.3 Central Nervous System

Soon after somite formation has commenced, specialized ectodermal cells on each

side of the midventral line, the neuroblasts (Figure 20.9E), begin to proliferate, resulting

in the formation of paired longitudinal neural ridges separated by a neural groove As

proliferation occurs, the cells move slightly inward so that they become separated from

the ectoderm They then begin to divide vertically, unequally and repeatedly, the small

daughter cells eventually developing into ganglion cells from which both neurons and glial

cells differentiate (Figure 20.12) Remarkably, the number and arrangement of neuroblasts

is highly conserved across the Insecta: each half-ganglion has 30 or 31 neuroblasts from

which all neurons are produced (Thomas et al., 1984) However, the number of neurons in