A lateral gynandromorph in the bee genus Thyreus and the sting mechanism in the Melectini (Hymenoptera, Apidae)

2007·0.73 MB·English

by  Engel, Michael S

A tamerican museum
Novitates
PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY
CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024
Number 3553, 11 pp., 9 figures, 1 table March 8, 2007
A Lateral Gynandromorph in the Bee Genus Thyreus
and the Sting Mechanism in the Melectini
(Hymenoptera: Apidae)
MICHAEL S. ENGEL1
ABSTRACT
A lateral gynandromorph of Thyreus redactulusl Cockerell is described and figured, with
a particular emphasis on the genitalic sclerites. As such, the sting morphology and mechanism are
described for T. ramosus (Lepeletier de Saint Fargeau) to provide a comparative framework for
understanding the gynandromorph. The implications of the gynandromorph’s genitalic arrange¬
ments for intersexual homologies are explored.
INTRODUCTION 1929). More recently, Wcislo et al. (2004)
have partially summarized the variety of
Sex anomalies occur relatively frequently documented sex anomalies (omitting inter¬
among bees and may be of striking appear¬ sexes), and gynandromorphs have been impli¬
ance in species where the two sexes are cated in the development of male-like traits
markedly dissimilar in structure or color. in cleptoparasitic females (Cockerell, 1911;
Although sex anomalies appear to be more Wcislo, 1999).
common among the Megachilidae2, this is Most papers, particularly among the more
likely a result of the particular fascination with recent literature, have confined themselves to
the recognition and documentation of such consideration of the external characters, per¬
anomalies by the late Theodore B. Mitchell, haps owing to concern not to risk damage to
a specialist on this family (e.g., Mitchell, valuable specimens. However, as many docu-
1 Division of Invertebrate Zoology, American Museum of Natural History; Division of Entomology (Paleoentomology),
Natural History Museum, and Department of Ecology and Evolutionary Biology, 1501 Crestline Drive Suite 140,
University of Kansas, Lawrence, KS 66049-2811 ([email protected]).
2 Highlighting this fact, normal females of the former subgenus Androgynella (a synonym of Eutricharaea), when
originally proposed (originally as a separate genus before being placed in Megachile), were unknown—hence, its name.
Copyright © American Museum of Natural History 2007 ISSN 0003-0082
2 AMERICAN MUSEUM NOVITATES NO. 3553
merited sex anomalies have been, apparently, apical area and the little-exposed tergum VII
intersexes, the absence of information on forming part of the ventral surface of the
possible modifications of the genitalia is metasoma, the number of exposed sterna may
perhaps not serious. True gynandromorphs be greatly reduced). In females, six terga are
are, as Mitchell (1929) and Wcislo et al. (2004) usually exposed, terga VII (which retains its
document, of relatively rare occurrence among spiracular openings) and VIII being always
the bees, but a number have been more or less invaginated and dissociated into hemitergites
fully recorded. that are closely associated with the sting
Lateral gynandromorphs, where the sagittal mechanism proper. Ventrally, six sterna are
division of the insect into male and female usually exposed, the sixth frequently modified
halves may extend to the genitalia, are of to accommodate exsertion of the sting.
particular interest as a potential source of Among genitalic structures proper I have
information on homologies between the struc¬ generally followed the terminology of earlier
tures contributing to the male and female authors, although I have employed the term
genitalia. From the Anthophila, examples furcula (as used by many authors: e.g., Packer,
have been described and figured by Bischoff 2003; Rightmyer, 2004) for the dorsal, wish¬
and Ulrich (1929: for Chalicodoma) and by bone-shaped, or merrythought-shaped struc¬
Popov (1937: for Halictus). The present paper ture arising from the convergence and fusion
deals with a lateral gynandromoph of an of the structures referred to by Michener
Indian species of Thyreus (Melectini), and, (1944) as the apodemes of the stylet. The
since the study of this specimen necessitated structure usually termed the gonostylus and
investigation of the structure and mechanics of also variously known, in the Hymenoptera, as
the sting in normal female Thyreus, with the the third valvula, ovipositor sheath, sting
latter subject also. In general, the genitalic palpus, or dorsal or lateral valve (or accessory
morphology in Melectini has not been in¬ lobe) of the second valvifer, is homologous
vestigated outside of the usual taxonomic neither with the styli (distal processes of the
description of the male terminalia. Among coxopodites) of the Zygentoma and some
melectines, the sting morphology has been Pterygota nor with the first and second
adequately described only for a single species valvulae (Snodgrass, 1935). Neither of the
of Thyreomelecta (Rightmyer and Engel, terms gonostylus nor third valvula, therefore,
2003). is morphologically correct. Recognizing the
possible confusion in terms of homology
TERMINOLOGY across broader groups, Scudder (1961, 1971)
proposed the term gonoplac3 for this structure.
It may be recapitulated that in the Apoidea, For the Apoidea, however, where the structure
like all Apocrita, the first abdominal segment in question is most often styliform and where
forms part of the mesosoma. For this reason, I no other structure is referred to as a stylus, the
have numbered the segments throughout this term gonostylus has continued in use and, if
paper based on their metasomal rather than employed in strictly a descriptive sense, poses
abdominal count. In other words, the “sixth no confusion. Similarly, the first valvifer of
sternum” referred to herein is that of the Hymenoptera has been lost and is replaced by
metasoma, or the seventh abdominal sternum the gonangulum4, a basal differentiation of the
(= sixth metasomal sternum). In males there second valvifer that articulates with the ninth
are therefore nine metasomal segments (ab¬ abdominal tergum (eighth metasomal tergum
dominal segments 2-10). Seven terga are
usually exposed, tergum VIII being invaginat-
3It should be noted that the term “gonoplac” is perhaps
ed, weakly sclerotized, and closely applied to
malformed in Greek. It is presumably derived from yovf) +
the inner surface of tergum VII. A lesser nXatL If so, its forms in third declension TtkaKog and gives
number of sterna are usually exposed, sterna in Latin third declension plax, placis (i.e., gonoplax).
VII and VIII being invaginated (in the 4It should be noted that the term “gonangulum” is
a hybrid of Greek and Latin. Perhaps a more linguistically
Megachilidae, where tergum VI commonly
favorable term would be gonogonium (Greek) or, perhaps,
forms the apparent apex of the metasoma, its something like semiangulum (Latin).
2007 ENGEL: THYREUS GYNANDROMORPH (APIDAE) 3
in Apocrita), the second valvifer, and the first segment, with both of which they are loosely
valvulae in Dicondylia (Scudder, 1961, 1964; connected (cf. figs. 1, 2). The hemitergites of
Grimaldi and Engel, 2005). Despite this, many the eighth segment are relatively large, weakly
melittologists persist in referring to this sclerotic, and broadly united with their equally
structure as the first valvifer (or gonocoxa) large, scaphoid apodemes. Dorsally, each
or “triangular plate”. Terminologies should hemitergite becomes membranous and is
ideally, of course, be valid both morphologi¬ applied to the outer surface of the apical half
cally and descriptively. In practice this is of the second valvifer; postero-ventrally, it
rarely achieved, owing, on the one hand to articulates with the small, strongly sclerotic
changing morphological concepts and, on the gonangulum. The second valvifer consists of
other, to the difficulty of finding terms that a rigid, well sclerotized anterior costa, which
are both sufficiently elastic to accommodate articulates laterally with an angular projection
all the forms in which a given morphological of the gonangulum and is prolonged dorso-
unit may be expressed and sufficiently distinc¬ apically in the distinct, terminally hamate
tive to obviate confusion with all other terms costal process (where the proctiger connects)
in use. It seems probably that descriptive and a broad, membranous limb from which
terminologies will long be required to supple¬ arises, dorso-apically, adjacent to the costal
ment morphological terminologies. Nonetheless, process, the gonoplac. The gonoplac consists
herein I depart from melittological tradition of a simple basal article (or stylifer) and
and employ the terms gonoplac and gonangu- a distinct, more strongly sclerotized, setigerous
lum. apical article (or ortho stylus). The gonangu¬
As some of the structures referred to in this lum and second valvifers give rise ventrally to
paper he in an inverted and reversed position the first and second valvulae. The rami of the
when the sting is retracted, it is necessary to valvulae are slender, elongate, and in contact
note that such terms as dorsal and basal and throughout their length—that of the second
their opposites are used, unqualified, in valvula supports the ventral margin of the
a morphological sense. limb of the second valvifer. The sting (com¬
prising the lancets of the first valvulae and the
DESCRIPTIONS stylet of the dorsally fused second valvulae) is
long and heavy and occupies the whole length
Thyreus Sting Morphology of the sixth sternum. The furcula is broad,
Thy reus ramosus (Lepeletier de Saint Fargeau) subcordate, and apically appendiculate, and
figures 1-3, 9 its two arms are closely but freely articulated
at the sides of the bulb of the stylet basally (cf.
Comments: Tergites VII and VIII are fig. 9).
dissociated into lateral, sclerotized hemiter-
gites, their medial, dorsal areas becoming
membranous and elastic to accommodate the
Thyreus Sting Mechanism
movements of the sting and associated struc¬
tures during exsertion. Although completely The sting and its associated structures in
invaginated within the genito-anal atrium, the Thyreus (including, in a wider sense, the sixth
seventh hemitergite retains its spiracular open¬ sternum, the hemitergites of the seventh and
ings; in the eighth hemitergites, they are lost. eighth segments, and the gonangula and
The hemiterigites of the seventh metasomal second valvifers) are typical of those of the
(last spiracular) segment are small and weakly parasitic Apinae. The sting is enlarged, and
sclerotic. They occupy a lateral position the metasoma has correspondingly undergone
between the lateral processes of the sixth modification in two complementary directions
sternum (with which they are loosely articu¬ to house the retracted sting (which may extend
lated, this articulation forming the pivot on basad beyond the apical margin of the second
which the sting mechanism rotates when the sternum; cf. fig. 1) and to accommodate the
sting is exserted) and the basal extremities of extended range of movements necessary for its
the apodemes of the hemitergites of the eighth full exsertion.
4 AMERICAN MUSEUM NOYITATES NO. 3553
Fig. 1. Thyreus ramosus (Lepeletier de Saint Fargeau), dorsal view of female metasoma depicting
genitalia in situ. Scale bar = 1 mm.
The sixth sternum, which forms the floor of The Retracted Sting
the sting atrium, is large, elongate, and
trough-shaped. Postmedially, it carries a pair
When the sting is retracted (fig. 2), the
of angular lateral processes that are indirectly hemitergites of the seventh metasomal seg¬
connected (through loose intermediate con¬ ment are inverted, and the hemitergites of the
nections with the hemitergites of the seventh eighth segment, with the gonangula and
segment ventrally) with the apodemes of the second valvifers, are inverted and displaced
hemitergites of the eighth segment basally to basad, as the result of rotation (in an anti¬
provide an axis about which the sting and its clockwise sense as seen from the right side)
more intimately associated structures (the about the lateral processes of the sixth
hemitergites of the eighth segment and the sternum. The costal processes of the second
gonangula and second valvifers) may rotate valvifers and the gonostyli are accordingly
on exsertion or retraction. Apically it is displaced ventrad and directed apicad and are
narrowed, and its sides are more strongly located with the stylet in the trough of the
reflexed and incurved to form a semi-tubular sixth sternum. The rami of the first and second
sting guide. valvulae are located dorsally and directed
The other structures associated with the basad and ventrad to a point above the
sting have already been described (vide supra). membranous anterior margin of the sixth
2007 ENGEL: THYREUS GYNANDROMORPH (APIDAE) 5
1-1
Figs. 2, 3. Thyreus ramosus (Lepeletier de Saint Fargeau), female, lateral view of genitalia, setae omitted;
seventh hemitergite not shaded or stippled; eighth hemitergite densely shaded; gonangulum solid black;
second valvifer stippled; furcula, sting, and sixth sternum (except anterior weakly sclerotized area) densely
stippled. 2. Position of sclerites with sting retracted. 3. Position of sclerites with sting exserted (the sting is
shown drawn away from the sting guide to make the relative positions of the furcula and the rami of the
valvulae clearer). Scale bars = 1 mm.
sternum (between the basal extremities of its metasoma, the hemitergites of the seventh and
apodemes), where they are abruptly flexed eighth segments rotate clockwise around the
apicad immediately before the origin of the lateral processes of the sixth sternum—the
sting. The furcula is directed dorsad and former through about 140°, when their spira¬
apicad, with its appendix located in the cles regain a normal, dorsal position; the latter
conjunctiva between the bases of the valvifers through about 160°, bringing their points of
and gonangula. articulation with the gonangula into a ventral
position near the base of the sting guide. The
gonangula and second valvifers are now erect
The Exserted Sting
(with the costal processes of the latter and the
When the sting is exserted (fig. 3), by means gonostyli separated from the sting and di¬
of forces generated in the anterior part of the rected dorsad and basad), the rami of the first
6 AMERICAN MUSEUM NOVITATES NO. 3553
and second valvulae are directed apicad and the specimen. Deposited in the Division of
located in the sting guide, and the base of the Entomology, University of Kansas Natural
sting lies near the apex of the guide. History Museum. The specimen is almost
Concurrently with the rotation of the hemi- assuredly an individual of T. redactulus.
tergites, the furcula hinges clockwise on its Nonetheless, I have been slightly hesitant with
articulations with the base of the sting and, as the identification, as noted by the interogative
the sting travels back through the sting guide, mark after the epithet, given the distortion of
describes an angle of about 150% coming to genitalic structures.
rest in a plane a little above that of the rami of Comments: The gynandromorph is on the
the valvulae, where it functions as a strut left side, male; on the right side, female. The
between the base of the sting (above the left antenna is that of the normal male (i.e.,
insertion of the rami of the valvulae) and the with 13 antennal articles), the right that of the
region of the inter-valvifer articulations. These normal female (i.e., with 12 antennal articles).
movements may be readily demonstrated in Structural differences between the two sides of
preparations from dried material. the head, mesosoma, and first through fifth
Simultaneously with these movements with¬ metasomal segments are otherwise unremark¬
in the sting atrium, the sixth sternum (which able (e.g., figs. 4-6). The legs show a mixture
externally is largely enveloped by the latero- of male and female characters, and on the
ventral lobes of the sixth tergum) is itself male side the modifications of the metafemora
partially exserted. This movement, and the and metatibiae characteristic of species of the
upward probing or stinging movements of the takaonis group are not developed. The condi¬
apical segments of the metasoma repeatedly tion of the apical segments of the metasoma
observed in living material, are presumably and of the genitalia is more complex.
enabled by the great development of the The metasoma is modified by the apparent
sternal apodemes (cf. fig. 1). While in dried loss of the eighth segment on the male side and
material the sting, when exserted, is not on the female side by a retrogressive, in-
usually exposed beyond about the middle of tersegmental transfer of characters that results
the bulb (and then issues from the apex of the in the appearance of a supernumerary exposed
sting guide), in a few instances it may be found segment and in a corresponding decrease in
fully exserted and directed upward through the number of concealed terga, which reduce
the dorsal commissure of the guide. The to one. The principal effect of these modifica¬
gonoplacs are not exserted but remain within tions is the bringing together in one segment
the sting atrium: having no capacity for
(the seventh) of the male and female halves of
movement independent of that of the second the genitalia, the genitalia of the normal male
valvifers, they become (as mentioned) sepa¬ being located between the eighth tergum and
rated from the sting with the rotation of the
the eighth sternum, invaginated within the
gonangula and valvifers. Although the apices
seventh segment, and those of the female
may just protrude from the opening of the
within the sixth segment between the hemi-
sting guide when the sting is retracted or only
tergites of the seventh and eighth segments
slightly exserted, and consequently the apices
(which are displaced laterad and modified to
may be presumed to retain a limited sensory
form part of the sting mechanism). There are,
function, it is apparent that their usefulness as
therefore, seven exposed terga and six exposed
“sting palpi”, to revert to an older term, has
sterna.
become sensibly diminished.
The sixth segment has the appearance of
a normal intermediate metasomal segment.
On the right, the special characters of the
Thyreus Gynandromorph
normal female sixth tergum, in particular the
Thyreus redactulusl Cockerell
pygidial process, are entirely suppressed.
figures 4-8
The tergum of the seventh segment is
Material: South India, Coimbatore, 30.iii. irregularly developed and, particularly later¬
1950, P. S. Nathan. Genitalia dissected and ally, only weakly sclerotized. The left half
permanently set in slide mount associated with tends to the form shown in a normal male, the
2007 ENGEL: THYREUS GYNANDROMORPH (APIDAE) 7
Figs. 4-6. Thyreus redactulusl Cockerell, gynandromorph. 4. Lateral aspect. 5. Facial aspect. 6.
Dorsal aspect.
AMERICAN MUSEUM NOVITATES NO. 3553
right half to that shown by the preceding
tergum in a normal female, the normal
condition, that of a small, wholly invaginated
and laterally located hemitergite, being entire¬
ly lost. The tergum is fimbriate apically, but
a pygidial plate is not developed. The appar¬
ent sternum of the same segment is a broad,
weakly sclerotized plate, closely adapted on
the left to the anteroventral surface of the
gonobase and on the right underlying the
female genitalia basally. On the female side,
neither this sternum (which, with that of the
eighth segment, is not present as a separate
sclerite in the normal female) nor that of the
preceding (sixth) segment shows any tendency
toward the highly distinctive form of the sixth
sternum in a normal female.
The eighth segment, on the male side, is
either entirely lost or, at least, not represented
by a separate sclerite; on the female side, the Fig. 7. Photomicrograph of dissected genitalia
hemitergite approaches the normal form, of Thyreus redactulusl Cockerell gynandromorph.
particularly in the apodeme, but is only
weakly sclerotized. DISCUSSION
The genitalia (figs. 7-8) are, on the left side,
A study of the terminalic sclerites and their
substantially normal male; on the right,
articulations in the present gynandromorph
abnormal female with male tendencies. The
(fig. 8: a normal female in similar orientation
hemitergite of the eighth segment, the second
is depicted in fig. 9) suggests the intersexual
valvifer, the gonoplac, and the rami of the
homologies outlined in table 1. The principal
valvulae are relatively little altered and imme¬
homologies indicated stand in full agreement
diately recognizable, the most noticeable
with those suggested by the gynandromorphs
modifications lying in the contraction and
of Chalicodoma and Halictus recorded by
strengthening of the costal process of the
Bischoff and Ulrich (1929) and by Popov
second valvifer and in the expansion of the
(1937), and with the conclusions arrived at by
gonoplac. The second valvula forms an
Michener (1944) following a general review of
imperfect and twice geniculate stylet ending
the question of homologies between the male
in a distinct, pointed bulb, which does not,
and female genitalia in bees. Some potential
however, represent the bulb of a normal sting
refinements of the previously established
but a contraction of the apical part of the homologies are, however, supported by the
stylet. The bulb bears a single, strong seta. The development and articulation of sclerites in
strong, erect, laminar basal process (fig. 8), the present gynandromorph. In particular,
suggestive of the highly developed sternal that the apodemes of the penis valve corre¬
apodemes found in Thyreus (cf. fig. 1), does spond with a basal prolongation of the side of
apparently represent the right side of the bulb the bulb of the stylet, and not with either
of a normal sting. The equally strongly a development of the ramus of the second
sclerotized structure (fig. 8), articulated at valvula or an arm of the furcula (“apodeme
the base of the sting laterally, is clearly the of the stylet”), is abundantly clear from the
right half of the furcula. Its presence in manner of entry of the ramus and the joint
addition to the apodeme-like process of the presence of both the apodeme-like structure
sting, and its free articulation with the base of (fig. 8) and the entirely separate half-furcula
the bulb, render suspect earlier identifications (fig. 8). Similarly, it is tempting to see in the
of the furcula as the “apodeme of the stylet” furcula, as a common dorsal structure lying
(and, accordingly, such terminology). above and closely associated with the bulb of
2007 ENGEL: THYREUS GYNANDROMORPH (APIDAE) 9
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10 AMERICAN MUSEUM NOVITATES NO. 3553
TABLE 1
Intersexual Homologies Suggested by Present Gynandromorph
Male Female
Gonobase
| Second valvifer3
Gonocoxa
inner apical process of gonocoxa costal process of second valvifer?
Gonoplac (=“Gonostylus”) Gonoplacb
Penis valve Second valvula
apodeme of penis valve bulb of stylet (in part)
bridge of penis valve furcula?
aThe gonobase is developmentally a basal, secondary division of the gonocoxae; thus, the gonobase and gonocoxae are
together homologs of the second valvifer.
bThe female gonoplac clearly shows an intermediate condition, including a shift of sclerotization toward the apices of
the orthostylus.
the stylet, the homolog of the bridge of the extensive modifications of the apical segments
penis valves (table 1), a structure that is well of the metasoma in the present gynandro¬
developed in many bee lineages, including the morph (affecting both halves of the sixth,
Melectini, and that occupies a similar position. seventh, and eighth metasomal segments)
While the genitalia of the present gynan¬ suggest, in fact, an overriding requirement
dromorph thus provide direct confirmation of for the approximation of the male and female
established homologies, the conditions shown half-genitalia, and therefore a strong morpho¬
by the apical segments of the metasoma are logical and ontogenetic connection between
likewise of some interest. Certainly, the them. The present gynandromorph, and
appendicular origin of male genitalic sclerites others like it, is one more, small element of
in certain pterygotes, particularly some support for the view that the male and female
Holometabola, is of some debate. As has genitalia of the Hymenoptera are essentially
been noted by previous authors, however, if homologous structures (those of the female
the male and female genitalia of Hymenoptera including certain additional elements). That
were of entirely independent origin, the one the female genitalia are of appendicular origin
a phallic structure borne within the eighth is of little question given the elegant trans¬
metasomal segment (or, more exactly, be¬ formation series extending back to the prim¬
tween the tergum and sternum of the eighth itive “gonangular” condition seen in Zygen-
segment invaginated within the seventh seg¬ toma (a.k.a., the “lepismatoid” ovipositor)
ment) and the other a derivative of the coxal and from there into the even more primitive
or sternal appendages of the seventh and Archaeognatha. Certainly, male structures
eighth metasomal (eighth and ninth abdomi¬ across Pterygota are remarkably challenging
nal) somites of the primitive insect (borne in to homologize, and some have argued that in
the sixth metasomal segment between the at least a few lineages these sclerites are of
dissociated and laterally displaced hemiter- sternal, rather than appendicular, origin and
gites of the seventh and eighth metasomal thereby independently evolved and not homo¬
segments), the expected condition in lateral logs of female genitalia. If the tight homology
gynandromorphs would be that of the in¬ between male and female genitalia observed
dependent appearance of the male and female here is correct, then for at least the
half-genitalia in the segments appropriate to Hymenoptera the interpretation of a common
each sex. The condition that is found, on the origin of external genitalic sclerites in both
contrary, is one of the closest associations of sexes continues to be well grounded (as in
these structures in a single, intermediate Archaeognatha and Zygentoma), as is gener¬
metasomal segment (i.e., the seventh). The ally believed by most hymenopterists.