The eye margin and compound-eye development in the cockroach: evidence against recruitment
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/. Embryo!, exp. Morph. Vol. 60, pp. 329-343, 1980 329
Printed in Great Britain © Company of Biologists Limited 1980
The eye margin and compound-eye
development in the cockroach: evidence
against recruitment
By MARK S. NOWEL 1 AND PETER M. J. SHELTON 1
From the Department of Zoology, University of Leicester
SUMMARY
The compound eye of the cockroach nymph grows from stadium to stadium by the
addition of new ommatidia to the growing edge of the eye. By a. series of transplant operations
on Periplaneta americana and from SEM studies on Gromphadorhina portentosa it is shown
that the proliferating region of the eye margin is a budding zone. There is no recruitment of
larval head-capsule epidermis into the eye.
INTRODUCTION
During development of the insect compound eye, new ommatidia are
continually added to one or more edges of the expanding structure. Thus the
youngest ommatidia are closest to the developing margin. The cells which are
incorporated into differentiating ommatidia are derived from a proliferating
zone lying just within the eye margin and next to the epidermis of the head
capsule. The proliferating zone is regarded by Bodenstein (1953) as a persistent
primitive portion of the original eye anlage already present in newly hatched
nymphs (Jorschke, 1914; Friza, 1928). The proliferating zone is thus an integral
part of the eye and is already determined to form eye. Bodenstein (1953) refers
to the proliferating zone as the budding zone, and his conclusion was based on
histological evidence. An alternative hypothesis is that the 'eye field' extends
beyond the eye margin into the epidermis which forms the head capsule. The
proliferating zone in that case would mark the position of an advancing front
at which cells are recruited into the eye margin where they subsequently divide
and differentiate to form ommatidia. This recruitment hypothesis is based on
the results of transplant experiments where marked grafts of retina or head-
capsule epidermis were exchanged between eye-colour mutants (White, 1961,
1963; Hyde, 1972; Egelhaaf, Berndt & Kuthe, 1975; Lawrence & Shelton, 1975;
Green & Lawrence, 1975; Nardi, 1977).
According to the first theory, 'there is no transformation of normal nymphal
1
Authors'' address; Department of Zoology, University of Leicester, Leicester LEI 7RH,
U.K.330 MARK S. NOWEL AND PETER M. J. SHELTON
ectoderm cells into sensory cells during postembryonic development' (Boden-
stein, 1953). The second theory proposes that epidermal cells which at one
stage secrete the cuticle of the head capsule are subsequently recruited and
transformed into eye cells. The object of this paper is to test both of the
theories, because to date none of the evidence is conclusive. On the one hand,
Bodenstein's observations were histological and did not test for recruitment.
On the other hand, the evidence for recruitment comes from transplant
experiments and is limited by the accuracy with which defined areas of tissue
can be excised and grafted.
In this paper, different types of grafting experiments on Periplaneta americana
are described which eliminate the ambiguities inherent in previous studies. The
results argue in favour of the budding-zone hypothesis. There is no evidence
for recruitment.
In another approach, using the scanning electron microscope (SEM), the
position of the eye margin with respect to identified bristles near to the eye
was examined at successive moults of the cockroach Gromphadorhina portentosa.
Some of these bristles are only one or two cells away from the eye margin, yet
over a period of considerable eye growth during two intermoult periods the
eye never approaches or envelopes the bristles. This provides a second line of
evidence in favour of the budding-zone hypothesis.
MATERIALS AND METHODS
Stocks of P. americana and G. portentosa were kept in standard laboratory
conditions. They were fed on rat pellets and water. Experimental animals were
kept in small gauze-topped sandwich boxes. For surgery, recently moulted
animals at larval stages 3-5 were anaesthetized in small glass vials cooled on
ice for 10-20 min. They were then placed on a bed of plasticine and held down
with narrow strips of plasticine. Cuts in the integument were made using a
razor-blade fragment (Gilette francais) supported in a pin vice. Sites were
prepared in host animals by removing cuticle and attached epidermis, and donor
fragments were cut to fit. They were transferred using tungsten needles or
watchmakers' forceps. The grafts were held in place using insect wax (Krogh
& Weis-Fogh, 1951) just above its melting point. Wild-type and lavender (Ross,
Cochran & Smyth, 1964) stocks of P. americana were used in graft exchanges.
Experimental animals were photographed using a Zeiss Tessovar Photomacro-
graphic Zoom system. For the SEM, either newly cast exuviae or heads prepared
by immersion in liquid nitrogen followed by freeze-drying were mounted on
aluminium stubs, coated with a 1-3 nm layer of gold using an ISI sputter
coating unit, and examined with an ISI-60 SEM.Cockroach eye development 331
Fig. 1. Several types of operations exchanging grafts of eye margin and head
epidermis between wild-type and lavender P. americana nymphs were performed to
distinguish whether the shape of the vertex epidermis or merely the extent of eye
margin determines the shape of the graft-derived retinal material in the resulting
mosaic eye. Following triangular grafts (a), a process of recruitment of vertex
epidermis into the growing eye would be detected by widely diverging lateral
graft/host borders. If the eye expands through the proliferation of cells in the
budding zone of the eye margin, mosaic eyes resulting from triangular grafts would
be indistinguishable from those resulting from rectangular grafts (b).
RESULTS
Transplantation experiments
(a) Triangular grafts
The grafts in this series of experiments had the shape of an isosceles triangle
with an apical angle of 80-90°. The apex of the triangle included a small
amount of eye margin tissue; the rest of the grafted tissue was vertex epidermis
from the right side of the head (Fig. 1 a). An implant site was prepared by
excising a triangle from the corresponding position in the host animal. Of 50
operations, 37 animals showed patches of eye tissue derived from the graft.
According to the mode of eye growth, two different results are expected.
Assuming that the eye grows by recruitment of vertex epidermis, the triangular
graft tissue would be progressively transformed into eye. During post-operative
eye growth, the shape of the graft-derived retina would be similar to the shape
of the original implant. Tf the eye grows without recruiting epidermis cells, the
shape of the graft-derived eye tissue would not be dependent upon the shape
of the implanted vertex tissue. Its shape would depend upon the rate of cell
division within the implanted eye margin only, and on the subsequent growth
of the ommatidia.
The shapes of the graft-derived tissue were examined in each of the 37 mosaic
eyes. The pattern of eye growth revealed was somewhat variable, but in no case
provided support for the recruitment hypothesis. In some cases the pheno-
typically donor eye tissue appears as an elongated narrow strip often with the
oldest graft/host border retaining the original angular profile (Fig. 2). The long
edges of such grafts are more or less parallel (Fig. 3). In some cases the long
edges do diverge as they approach the eye margin (Fig. 4), but in these cases the
included angle is much less than the angle of the original graft.332 MARK S. NOWEL AND PETER M. J. SHELTON
Cockroach eye development 333
If no recruitment occurs, similar results would be obtained whatever the
shape of the vertex component of the graft. Consequently, the results of the
triangular graft experiments were compared with the results of experiments in
which the graft was rectangular in shape.
(b) Rectangular grafts
Of 12 nymphs receiving rectangular implants of donor material (Fig. 1 b),
10 were successful. The shapes of the patches of graft-derived ommatidia were
essentially the same as those described above for triangular grafts. That is, they
had near-parallel long edges which occasionally diverged slightly as they
approached the eye margin (Fig. 5). It is concluded that the shape of the vertex
component of the graft does not affect the shape of the graft-derived eye tissue.
That must depend upon the length of eye margin originally implanted.
(c) Transplants of eye margin material only
In these experiments involving 20 animals, a length of eye margin material
only (Fig. 6) was removed and replaced by a similar genetically marked graft
from a suitable donor. (The stocks used were wild type and lavender, as before.)
Particular care was taken to ensure that no vertex tissue was included in the
graft. The transplanted tissue measured approximately 0-04 by 0-4 mm in a
representative animal where the graft was measured. A graft of this size
represented approximately one half of the eye margin along the dorsal border
of the retina. Because of the size of the graft, this type of transplant is on the
limits of technical feasibility and only one was successful. In this animal, the
graft-derived tissue extended right up to the eye margin (Fig. 8). If recruitment
of head-capsule epidermis had occurred, the graft-derived ommatidia would
have been isolated from the eye margin by ommatidia derived from host tissue.
Although it would not be worth reporting this single observation by itself, the
fact that it is consistent with the other results lends support to the budding-
zone hypothesis.
FIGURES 2-5
Figs. 2-4. Mosaic eyes of P. americana generated following transplantations of
triangular grafts as in Fig. 1 a. The angular profile at the base of the graft-derived
ommatidia (g) in Fig. 2 is suggestive of the original apex angle (80-90°) of the
grafted integument. The parallel (Figs. 2, 3) or near-parallel (Fig. 4) sides of the
graft-derived retina implies that the non-eye-margin portion (i.e. the head-epidermis
portion) of the graft did not become retina.
Fig. 5. Mosaic eye of P. americana generated following transplantation of rectangular
grafts as in Fig. 1 (b). The shape of the graft-derived retina is essentially the same
as that in mosaic eyes following triangular graft implantations (Figs. 2-4). A,
anterior; D, dorsal; h, host ommatidia. Bars represent 0-25 mm.
EMB 60334 MARK S. NOWEL AND PETER M. J. SHELTON
Fig. 6. Portions of the eye margin material only were exchanged between lavender
and wild-type nymphs to determine whether the eye margin acts as an organ for
recruiting adjacent head-capsule epidermis or as a budding zone in the production
of new ommatidia.
{d) Implants of eye tissue into the eye region after retinectomy
One eye was removed from each of 20 newly moulted lavender animals.
Great care was taken to excise completely all eye tissue including the eye margin.
After one or two moults, the animals were examined for signs of eye regeneration.
No regeneration was observed. Exchange transplants were subsequently per-
formed using these retinectomized lavender nymphs and wild-type donors. A
section of the wild-type eye was removed and placed in a site on the retinec-
tomized lavender host in the position normally occupied by the eye. The graft
was carefully excised with regard to shape and tissue composition. Most of it
was taken from the area of mature ommatidia, but a small portion of the eye
margin and head-capsule epidermis was included (Fig. 7). Thus, host head-
capsule epidennis was contiguous with mature retina and eye margin of the
graft. Twelve animals survived the operations and metamorphosed into adults.
Of these, six showed signs of the grafted eye tissue. Thus they had one normal
unoperated lavender eye and one small graft-derived eye. The experimental eye
always consisted entirely of wild-type tissue. Sometimes the graft formed a
jmound of wild-type ommatidia which showed no increase in numbers of
ommatidia with successive moults. In three animals this structure's attachment
to the host's head became progressively constricted in subsequent moults, and
one was eventually sloughed off. However, in the three other cases the graft
formed a growing diminutive eye with a distinct eye margin extending along theCockroach eye development 335 Fig. 7. The retina of a lavender P. americana nymph was completely removed. After one or two post-operative moults, a piece of regenerated integument from the head capsule was exchanged with a graft of retina and head epidermis from a wild-type nymph. The purpose of these experiments is to test for recruitment by confronting wild-type head epidermis, eye margin and mature retina with lavender head epidermis. If head epidermis can be recruited to form retinal tissue, lavender ommatidia will be generated. dorsal, anterior and ventral borders (Fig. 10). In this type of experiment, lavender ommatidia were never observed in the experimental eye. This means that the regenerated eye margin must have formed from the wild-type graft tissue only, and that no head-capsule epidermis was recruited into the eye. (e) Implantation of regenerated head-capsule epidermis into the eye As a further test, regenerated head epidermis from the 12 retinectomized animals obtained above was implanted into the site left after removal of tissue from the wild-type eye (Fig. 7). These operations caused obvious disruptions in the shape of the growing host retina. The host eye grew around the implanted
336 MARK S. NOWEL AND PETER M. J. SHELTON
ȣ
Fig. 8. Mosaic eye of P. americana resulting from the implantation of a lavender
eye margin only into a wild-type host (as in Fig. 6). Note that no wild-type (i.e.
host-specific) ommatidia (h) appear subsequent to the establishment of the lavender
tissue in the region of the implant, as would be expected if the eye margin acts to
recruit the head epidermis.
Figs. 9, 10. Compound eyes of adult P. americana following operations as shown
in Fig. 7, to confront lavender head epidermis with mature ommatidia and eye
margins of wild-type animals. Figure 9 shows an adult eye after six post-operative
moults following implantation of a graft of lavender head epidermis (g) into a
wild-type host. The host eye has grown around the lavender epidermis but has not
recruited it, as is demonstrated by the lack of any lavender ommatidia. Figure 10
shows a dorsal view of an adult P. americana after six post-operative moults.
Following implantation of a graft of wild-type retina into a unilaterally retinec-
tomized lavender host, the donor eye (g) has grown considerably in the host, but
not by recruiting adjacent lavender head epidermis, as shown by the lack of any
lavender ommatidia. A, anterior; D, dorsal; a, antenna; g, graft-derived tissue; h,
host ommatidia. Bars represent 0-25 mm.Cockroach eye development 337
epidermis which could often be distinguished from the host epidermis by its
colour. However, in none of the 12 animals did any lavender tissue form
ommatidia (Fig. 9).
In these last two experiments (Wand e), head-capsule epidermis was confronted
with mature and differentiating regions of the eye, including the eye margin. If
recruitment of head-capsule epidermis (by the adjacent retina or eye margin)
had occurred, then lavender ommatidia should have formed.
(/) Scanning electron microscopy of the compound eye/head capsule border in G.
portentosa
In cockroaches, the head epidermis lying medial to the developing dorsal
eye margin contains a small number of bristles. Some are close to the eye
margin. It is possible to count the number of epidermal cells between a bristle
and the eye margin by examining the cuticle surface, because the microsculpture
of the surface shows a pattern of polygons each representing the area of cuticle
secreted by a single epidermal cell (Hinton & Gibbs, 1971). For this part of the
study, the cockroach Gromphadorhina portentosa was chosen because the poly-
gonal pattern on the surface is much clearer than in P. americana. Since the
same bristles persist from moult to moult (Wigglesworth, 1939; Lees &
Waddington, 1942), they can be used as markers to investigate the question of
whether epidermal cells adjacent to the eye are recruited into it. Thirty newly
moulted G. portentosa and their exuviae (cuticles I) were collected from a
crowded stock culture. The head region of each cast exoskeleton was removed
and mounted for examination by the SEM. The number of cells between
suitable bristles and the eye margin was then counted. These 30 animals were
placed in separate containers and kept until they moulted once more. A second
series of exuviae (cuticles 2) was then prepared as before. The animals themselves
were killed at this stage by immersion in liquid nitrogen. Their heads were
freeze-dried and prepared for SEM examination. Thus for each animal it is
possible to examine the surface at three stages of growth: in cuticles 1 and 2
and in the fixed head (cuticle 3). However, most cockroaches consume the shed
exuviae shortly after ecdysis, and for this reason, cuticle 2 was sometimes lost.
Bristles near to the eye margin in cuticle 1 which were recognizable in
cuticles 2 and 3 were labelled in each series (Fig. 11). Fifty-six bristles in the
nine cleanest series were examined in this way. Eighteen bristles (averaging
4-2 cells from the eye margin in cuticle 1) show an increase in cell number
between the marker bristle and the eye, with an average increase of 1-3 cells
over the two intermoult periods. Six bristles show a decrease during the period
(averaging a loss of 1-2 cells from the 5-0 cells separating the bristle from the
eye in cuticle 1). Thirty-two bristles separated from the eye by an average of
4-1 cells show no change during the three stadia examined. A significant
observation is that in 16 cases, bristles were separated from the eye by only
one or two cells in cuticle 1 and that this distance was stably maintained in
cuticles 2 and 3. These data are summarized in Table 1.338 MARK S. NOWEL AND PETER M. J. SHELTON
(a)
m ^
**
(b)
Fig. 11. These montages of scanning electron micrographs of a compound eye (ce)
of a G. portentosa nymph show that the eye margin does not recruit epidermal
cells to supply the growing retina. To show the relationship between the eye margin
and the head-capsule epidermis (e) of the growing cockroach, the head cuticle was
examined at three succeeding stadia. The surface of the retina and the head epidermis
(containing bristles) can be seen in cuticle \{a) and cuticle 3(6), nymphal stadia
separated by two moults. Individual bristles (A-E) are recognizable in these two
preparations by their relative positions. The distance between the eye and the
bristles is maintained over the three stadia examined. Bars represent 50/*m.
It is clear from these results that while there is some fluctuation in the width
of the band of cells separating the eye margin from the bristle markers, there
is no trend of a steady decrease in numbers of intervening cells. This trend
would be expected if the eye margin were recruiting the adjacent head epidermis.
DISCUSSION
The preceding results conclusively show that recruitment of non-eye tissue
does not occur in the postembryonic development of the cockroach eye. Like
Bodenstein (1950, 1953) we regard the eye margin as a persistent primitive
portion of the embryonic eye anlage.
Similar conclusions can be drawn from an earlier study. Lew (1933) hasCockroach eye development 339
Table 1. Number of epidermal cells between bristle and eye margin
in different stadia
Cuticle Cuticle Cuticle Cuticle
Retina Bristle 1 3 Change Retina Bristle 1 3 Change
A right a 8 8 0 e 2 3 +
b 2 2 0 f 6 6 0
c 2 2 0 g 6 6 0
d 2 3 +
h 2 2 0 Rleft a 2 2 0
i 3 3 0 b 3 3 0
j 3 2 - c 10 10 0
k 1 2 + e 5 5 0
f 2 3 +
E left a 7 8 +
b 2 3 + R right a 3 3 0
c 10 11 + b 2 3 +
d 4 2 — c 5 5 0
e 4 4 0 d 10 10 0
f 4 4 0 e 2 4 +
f 4 4 0
M right a 4 4 0
b 9 8 — Wleft a 2 3 +
c 3 3 0 b 4 4 0
d 5 5 0 c 4 3 —
e 3 4 + d 4 5 +
e 7 6 —
Oleft a 4 8 + f 3 3 0
b 3 4 + g 3 2 —
c 3 3 0 h 2 2 0
d 8 9 + i 12 13 +
e 3 3 0
W right b 3 4 +
Qleft a 3 3 0 c 9 9 0
b 2 2 0 d 3 3 0
c 6 8 + e 6 6 0
d 2 2 0 g 2 2 0
examined the growing dragonfly eye and its relationship with the adjacent head-
capsule epidermis. He made tiny wounds in the retina and head capsule of the
dragonfly by pricking them with a fine needle. After each moult he compared
the resulting marks on the exuviae with the scars on the emerged animal and
found that wounds made outside the eye boundary (marked by the budding
zone) never appear in the eye.
The recruitment hypothesis was introduced by Hyde (1972), and results of
later experiments (Lawrence & Shelton, 1975; Green & Lawrence, 1975) were
interpreted according to her hypothesis. In these later studies, grafts were
exchanged between wild-type and mutant animals with a distinctive eye
pigmentation. Typically, a rectangular piece of head epidermis from one340 MARK S. NOWEL AND PETER M. J. SHELTON animal was placed in the epidermis of a young host in a site close to the developing and growing eye margin after a similar piece of epidermis had been excised from the host. According to Hyde's original (1972) experiments, the implant was located at a considerable distance from the eye margin and eventually after several moults it was recruited into the eye where it was recognizable by its distinctive eye pigmentation. Hyde (1972) also reported that prothoracic epidermis could be recruited into the eye to form ommatidia. Neither of these claims has been substantiated by subsequent work (Shelton, 1976; Shelton, Anderson & Eley, 1977). The latter workers found that very few eyes incorporate graft material even when the grafts were made very close to the eye margin (success rate: 3/50). It occurred to us that this low success rate would be consistent with the occasional inclusion of donor eye margin in the graft. A similar explanation could also account for the results of experiments on Oncopeltus fasciatus (Shelton & Lawrence, 1974; Lawrence & Shelton, 1975; Green & Lawrence, 1975). Here the animal is so small at the time of the operation that accuracy in excluding donor eye margin from the graft is even more difficult than in P. americana. Repeating experiments of this sort is of little value. Negative results would not necessarily show that epidermal cells are not recruited for a variety of reasons. For instance, the graft could be damaged or rejected at the time of the operation with subsequent migration of epidermal cells into the wound (see Wigglesworth, 1937, 1939). If any cells were subsequently recruited from the site of the implant, they would have the host phenotype and recruitment would be undetected. Also if the 'eye field' extends only a short distance beyond the eye margin, it is possible that the donor material does not contain any cells with the competence to form eye if no eye-field cells are included in the graft. In addition, positive results could always be explained in terms of accidental inclusion of eye-margin tissue in the graft. The present series of transplant experiments described in this paper avoids these ambiguities because eye-margin tissue is intentionally included in the graft. In conjunction with the observations on bristle position, the present results unequivocally demonstrate that the eye margin is a budding zone and that no recruitment occurs. Since this conclusion contradicts Hyde's (1972) findings, an examination of her experimental approach is necessary. Hyde's decision to graft between either wild-type or lavender and pearl P. americana partly explains her incorrect conclusions. The pearl mutation results in an unpigmented white eye (Ross et al. 1964). However, pearl eyes can synthesize wild-type pigment when in contact with wild-type or lavender eye- tissue (Hyde, 1972; Shelton et al. 1977). Hyde's criterion that recruitment had occurred was the appearance of dark pigmentation within the host pearl eye margin. However, darkening of the pearl retina can be due to factors other than the synthesis of wild-type eye pigments. If damage occurs to eye tissue, as inevitably happens following some of the experimental procedures adopted by
Cockroach eye development 341 Hyde, there would be an influx of haemocytes to the site of damage (Ries, 1933; Wigglesworth, 1937; Ermin, 1939). It has previously been pointed out that pigmentation in the pearl eye could be due to haemocyte-based melanization (Shelton, 1976). It has also been shown that pearl animals injected with wild- type haemolymph can show a darkening of wounded eyes (Nowel, 1979). For these reasons, the appearance of pigment in a. pearl retina does not necessarily mean that they are eye pigments. Although recruitment does not occur in the postembryonic development of compound eyes in hemimetabolous insects, there is a process not unlike recruitment which has been described for eye development in many holo- metabolous forms. Here the main stages in eye formation occur in the pupa within a short period of time. In all such forms, retinal differentiation begins on one side of the prospective eye region (Umbach, 1934; Meinertzhagen, 1973). This region has been called the differentiation centre, and if it is destroyed by cautery, eye development does not continue (Wolsky, 1949, 1956; White, 1963; Wachmann, 1965). In normal development, a wave of developmental events spreads out from the differentiation centre in an organizational front which passes across the prospective eye region. In Ephestia ktihnielfa, for example, a furrow and two waves of mitosis sweep across the prospective eye region from the differentiation centre (Egelhaaf et ah 1975; Nardi, 1977). Similar events take place in the eye discs of Drosophila melanogaster (Ready, Hanson & Benzer, 1976). Transplants between eye-colour mutants of E. kiihniella strongly support the notion that the developmental front does actually pass across the prospective eye region like a travelling wave. The alternative would be that the developmental front behaves like a standing wave. According to this latter hypothesis, the movement of the wave would be due to the production and expansion of ommatidia on one side of the furrow. The results of transplant experiments are subject to all the limitations described above, and before it is concluded that the organizational front really does pass across the prospective eye region additional evidence is required. In Drosophila there is one piece of evidence which would be consistent with a developmental front passing across the eye disc. This is that clones generated late in development can cross the eye-head-capsule border (Morata & Lawrence, 1979). If the eye is formed by the standing wave model, then clones should be restricted to either the eye or the head capsule. Nevertheless, the mechanism in eye development in holometabolous insects should not be described as recruitment. Recruitment implies that cells which at one time could form head capsule could later be redetermined to form eye. In the case of eye development in holometabolous forms, the front would be passing across tissue which is destined to form eye. To that extent at least, there is no cell transformation and no recruitment. M.S.N. was supported in part by a Fulbright-Hays Scholarship. P.M.J.S. is grateful to The Science Research Council for financial support. We thank Dr Ross for supplying our cultures of lavender and pearl P. americana, and Mr G. McTurk for valuable technical assistance with the SEM.
342 MARK S. NOWEL AND PETER M. J. SHELTON
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{Received 12 March 1980, revised 19 May 1980)You can also read
