alignment and homology of male terminalia in curculionoidea ...franz/weevilcourseresources/...male...

Introduction‘Chitinisation is often looked upon as the important thing whilst themembrane is disregarded, whereas the latter is the important part.’(Muir 1915: 150.)

Male genitalia and associated internal sclerotised plates havebeen recognised as a source of taxonomically important charac-ters in Coleoptera for some 200 years. During most of that timeit has been standard practice in beetle taxonomy to extract theaedeagus and attach it to a card near the mounted beetle. As aresult, our current view of genital structures is oversimplifiedbecause it has relied almost exclusively on the shape of thesclerotised aedeagus and has completely disregarded the trans-parent membranous structures and the connections betweensclerites. Muir (1915, 1918) apparently was the first to appreci-ate the relevance of genital membranes, and his ideas of thetwice-folded genital invagination developing during beetlemetamorphosis (Fig. 8b) were accepted without much dispute.Muir (1915, 1918) was also the first to describe the nature oftegminal lobes and the tegminal strut as secondary outgrowthsof the tegminal fold, and he suggested that all internal apodemesare ‘invaginations of the ectoderm’.

Apart from common usage of genital structures for speciesdiagnoses, several authors have attempted to employ them asbasic characters for family-level divisions of Coleoptera. Sharpand Muir (1912) pioneered the fundamental work on beetle gen-italia, and first recognised the affinities of the curculionoid andchrysomeloid aedeagus linking these groups in the seriesPhytophagoidea. They were followed by Crowson (1955, 1981),who characterised, and considered the most important, severalgeneral types of coleopteran aedeagus, including the ‘trilobe,

sheath, cucujoid, heteromeran and chrysomeline’ types. Thenomenclature, rather than the principles of division, was modi-fied by d’Hotman and Scholtz (1990), who recognised fourbasic types: trilobate, articulate, vaginate and annulate.Crowson (1955, 1981) treated the phytophagan aedeagus as abasically cucujoid type, although finally recognising it as a fifthmajor type in Coleoptera. It is distinct primarily in having acomplete tegmen, usually with a well-developed dorsal plate(variously called the tegminal plate, cap-piece, parameroidplate, or parameres), which is connected with the forked basalpiece (not forked and usually referred to as the phallobase in thenon-phytophagan beetles). The basal piece is provided with asingle apodeme (tegminal strut, manubrium). Crowson’s divi-sion of male genitalia in beetles was followed by that ofLawrence and Britton (1991), who treated the curculionoidtegmen as a modified cucujoid type, with a narrowed phallobaseand fused or absent parameral lobes, regardless of Crowson’s(1981) indirect questioning of the homology of cucujoid andcurculionoid parameres.

My studies on weevil male genital structures were initiated atthe end of the 1990s and were stimulated mainly by examinationof hundreds of large, primitive, New Caledonian apionids.These specimens provided many illustrative examples of thearrangement and structure of genital segments and revealednew, previously unrecognised characters related to inter-segmental membranes. Numerous authors have used most ofthese structures for apionid taxonomy (e.g. Alonso-Zarazaga1983, 1990; Kuschel 1995; Wanat 2001), but they also pointedto some important questions on the origin of male genital struc-

Invertebrate Systematics, 2007, 21, 147–171

10.1071/IS05055 1445-5226/07/020147© CSIRO 2007

Marek Wanat

Museum of Natural History, Wrocław University, Sienkiewicza 21, 50-335 Wrocław, Poland.Corresponding author. Email: [email protected]

Abstract. Male genitalia and associated internal sclerotised plates have been long recognised in beetle taxonomy, buttheir relative position in the connecting membrane and the genital membrane folding patterns have never been thoroughlyinvestigated. In this study, the structure of the genital chamber in weevils (Curculionoidea) and other Coleoptera has beeninvestigated in detail, focusing primarily on the alignment of the 9th abdominal segment and true genital plates.Three basic types of genital alignment are recognised based on the orientation of sclerotised plates and membrane folding:(1) a primitive eucinetid type (both 9th segment and tegmen non-inverted); (2) a derived phytophagan type (both 9thsegment and tegmen inverted) and (3) a cucujid type (9th segment non-inverted, tegmen inverted). A different origin ishere postulated for the parameroid plate in Curculionoidea, Chrysomeloidea and a part of the Cucujoidea (from the foldof the membrane linking tergite 9 with the tegmen) and for the true parameres in the remaining Coleoptera (from the foldof the membrane linking the tegmen with the aedeagus); hence these alignment types are considered non-homologous.The superfamily Cucujoidea was found to be heterogeneous with regard to genital alignment and considered polyphyletic.The proctiger and the paraprocts of the beetles are interpreted as belonging to the 9th abdominal segment and noextrategminal plates of the 10th segment were found in Coleoptera. Arguments for and against a hypothetical homologyof beetle genitalia with abdominal segments 10 and 11 are discussed.

Alignment and homology of male terminalia inCurculionoidea and other Coleoptera

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M. Wanat148 Invertebrate Systematics

tures in the weevils. I thus extended my studies to coverrepresentatives of all major weevil lineages, and further toseveral members of the Chrysomeloidea, sister group to theweevils. For comparative purposes, the same method was usedfor several representatives of nearly all beetle superfamilies,particularly the diverse Cucujoidea. The results, astonishing insome respects, provide a foundation for new hypotheses con-cerning the origin of weevil ‘parameres’, and the alignment andhomology of genital segments in beetles.

Materials and methodsEntire abdomens were separated from specimens that had beenrelaxed and cleared in hot KOH to remove soft tissues. Theywere then washed in distilled water and put into a drop of glyc-erol containing chlorazol black for a few minutes to stain mem-branous structures, then washed again in distilled water toremove excess stain. Internal (concealed) abdominal segmentswere then observed. If the features could not be clearly observedin situ, internal abdominal segments or plates (tergites, sternites,tegmen, aedeagus) were carefully separated from each other,together with membranes intact, in a drop of pure glycerol undera stereo-microscope. Smaller structures were studied using acompound microscope at 160× and 640× magnifications.Preparations are stored in glycerol, in polyethylene microvialspinned under specimens.

Genitalia of more than 100 species of all weevil families andsubfamilies recognised by Kuschel (1995) were examined inthis way, half of them representing the Apionidae. Additionally,48 representatives of 15 coleopteran superfamilies were studiedfor comparative purposes. A detailed list of species studied isgiven in Appendix 1.

The weevil species mentioned in this paper have beenassigned to families and subfamilies following Alonso-Zarazaga and Lyal (1999). For the sake of brevity, only genericnames are used later in the text (unless distinction between thespecies was necessary), but all species are referenced inAppendix 1.

The term ‘aedeagus’ is here restricted to the part commonlyknown as the median lobe, containing the internal sac and notincluding the tegmen. The letters S and T with consecutivenumbers denote sternites and tergites respectively. The mem-branes are ascribed to the preceding segmental plate, hence themembrane between S7 and S8 is called ‘membrane of S7’; thatbetween S8 and S9 is ‘membrane S8’, and so on. The positionof each internal abdominal segment, including the aedeagus,always refers to its position when retracted inside abdomen.While describing the orientation of particular segmentalmargins, the general body orientation is followed. Thus, themargin closer to the head is anterior, and that closer to the endof abdomen is posterior. Other terms, like distal v. proximal orbasal v. terminal or apical, are generally abandoned with regardto internal sterna, terga and the ventral part of the tegmen.However, these terms are retained in descriptions of theapodemes, dorsal tegminal plate and the aedeagus, where theiruse does not cause confusion. The apodeme base is alwayswhere it arises from the respective segment. The base of thetegminal plate is at its junction with the arms of the basal piece,whereas the lobes are apical. Analogously, the parts of theaedeagal pedon and tectum bordering the orifice through which

the internal sac is everted are called apical, whereas thosebearing apodemes are basal.

The diagrams of genital alignment are always sagittal sec-tions. The following abbreviations are used for description ofinternal abdominal structures on all photographs and diagram-matic figures:

aAE aedeagal apodemesAE aedeagus

aS8, aS9 sternal apodemesan anus

aTG tegminal apodemeBP basal piece

E endophallused ejaculatory ductF flagellum

op operculump process

pct proctigerPE aedeagal pedon

PM parameres/parameroid lobesppr paraproctpr pretegminal membrane (2nd connecting

membrane)ps post-tegminal membrane (1st connecting

membrane)ptg prostegium

R rectumS5, ..., S9 subsequent sternites

sc scleriteT6, ..., T9 subsequent tergites

TC aedeagal tectumTG tegmenTP tegminal plate

Following Wanat (2001), the term ‘pretegminal membrane’(membrane of T9 and S9) was found to be a more appropriatedescription for the part of the genital sheath between the 9thsegment and the tegmen, than the poorly informative term‘second connecting membrane’ used by Sharp and Muir (1912)and Lindroth and Palmén (1970). Analogously, the terminal partof the genital sheath linking the tegmen with the base of theaedeagus (the ‘first connecting membrane’by quoted authors) ishere termed ‘post-tegminal membrane’.

ResultsThe review of the male terminalia presented below is based pri-marily on weevils, although members of the related super-families Chrysomeloidea and Cucujoidea are often invoked forcomparative purposes. The order and structure of particulargenital plates and segments in weevils were earlier described andanalysed by many authors (for example Sharp and Muir 1912;Crowson 1955; Thompson 1992; Alonso-Zarazaga 1983, 1989;Wanat 2001), but the connecting membranes never attractedmuch attention, except for the primary folds of genital invagina-tion in beetle pupa (Muir 1915, 1918). The pupae of the weevildryophthorine Rhabdocnemis obscura (Boisduval) (currentlyRhabdoscelus obscurus) were studied by Muir (1915, 1918) forthe development of the genital sac, and his results were subse-quently accepted for all Coleoptera. Two primary folds associ-

Invertebrate Systematics 149

ated with the aedeagus and the tegmen were recognised in themale genital invagination, and the membranes connecting theseelements with each other and with the remaining abdominal seg-ments were numbered. The first connecting membrane was thatbetween the tegmen and aedeagus, and the second connectingmembrane connected the tegmen with the last tergite and stern-ite. It was usually T9 and S9, but in weevils and chrysomeloidsT9 is commonly missing, thus the 2nd membrane connectsdirectly to the pygidium (T8). In several other beetle groups thepresence of T10 (proctiger) is recorded; this is connected to thedorsal part of the tegmen by the 2nd membrane. The 9th abdom-inal segment, either forming a complete ring or devoid of T9,always rests inside the abdomen and is exposed only during theevertion of genitalia for copulation. The 8th abdominal segmentis invaginated in weevils and chrysomeloids, but a part of T8 isoften partly exposed to form a pygidium. Both T8 and S8 are notinvaginated and partly exposed in other beetle groups (exceptsome Cucujoidea). The membrane connecting terminal abdom-inal segments was never a subject of detailed studies, unless ithas some sclerites utilised for taxonomic diagnoses (such as insome primitive Apionidae). The course and folding of all thesemembranes, including those formerly recognised as the 1st and2nd connecting ones, and their mode of attachment to the inter-nal sclerotised plates, provided basic arguments for the newhypotheses presented in this paper.

Genital sheathThe male genital sheath forms a uniform membranous sac(genital chamber), in the wall of which all sclerotised elementsare incorporated. The sheath terminates at the base of the aedea-gal apodemes. The sheath’s membrane is two-layered, and in anyrigid element sclerotine is deposited between the layers. Whengenital elements are in repose, the variably long apical part ofthe tegminal plate and the body of the aedeagus lie free insidethe genital chamber, the sclerites of S8, S9, T9 and tegminalbasal piece are incorporated into the membranous wall of thegenital sheath, while all the apodemes are directed outside thechamber (Fig. 1, Cimberis; Nemonychidae).

The genital sheath is attached to the posterior edges of T8(pygidium) and S7 around the abdominal orifice. However, avariably broad basal margin of the membrane is more or lessheavily sclerotised and tightly adjoins the inner surfaces of T8and S7 along their posterior margins; thus the free membraneoriginates some distance from the margins of the abdominalopening, causing the attachment of the genital sheath to appearsubmarginal. In most examined weevil species this sclerotisedmargin is not fully connate and it can be separated from theinternal surface of at least S7 with a fine entomological pin. Insome others (for example, Liparus; Curculionidae) the conna-tion is full, ending with a transverse rib to which a true mem-brane is attached. Regarding the pygidium, the marginalsclerotisation of the membrane was particularly broad in somecerambycids (for example, Asemum and Dorcadion).

Since S8 lies withdrawn above S7, the S7 membrane is con-sistently folded towards the interior of the abdomen. A reversefold, directed towards the abdominal opening in repose, usuallyoccurs on the T8 membrane (Fig. 1b). Segment 8 is firmlyattached laterally to the pygidium or concealed T8, and mobilityof the latter is limited by the relatively short T7 membrane.

Therefore, the complete sclerotised ring of S8+T8 is barely ornot extrudable, and folds of both S7 and T8 intersegmentalmembranes apparently remain permanent, that is, the membraneremains folded even when the aedeagus is everted to itsmaximum range for copulation. Permanence of the fold may beadditionally reinforced by the presence of weak sclerotisationon the fold margin of the T8 membrane in some studied weevilspecies (such as Liparus), and by the development of apodemeor membranous processes exactly on the margin of the S7 mem-brane fold (see sections below). In the further course of thegenital sheath the S8 membrane is again permanently folded onthe posterior margin of S8, and runs horizontally above S8towards S9. Ventrally, the unfolded membrane next links S9with the posterior edge of the forked basal piece of the tegmen.The respective dorsal portion of genital sheath runs unfoldedtowards T9 (reduced in a vast majority of Curculionoidea), thenconnects at various levels to the dorsal tegmen plate (see therespective section). Therefore, continuity of the membranoustube of the weevil genital chamber (the sclerites of S9 are eitherabsent, or they constitute small ‘islands’ surrounded by a softmembrane), is interrupted by a complete ring of tegmen, unlessthe dorsal tegminal plate is completely reduced, as in manygonatocerous groups such as Dryophthorinae, Cossoninae,Scolytinae, Entiminae (for example Entimus, after Thompson1992), Cryptorhynchinae (for example Cryptorhynchus) orConoderinae (for example Coryssomerus). What precedes thistegminal ring is called here the ‘pretegminal membrane’,morphologically referring to the membrane of T9 and S9respective to the dorsal and ventral parts of the weevil tegmen.Consequently, the membrane behind the tegminal ring (the onelinking the tegmen with the base of aedeagus) should be con-sidered a post-tegminal membrane.

Since the tegmen and aedeagus are telescopic and movablerelative to each other, and as a whole unit against the 9thsegment, this allows the aedeagus to extrude out of abdomen.Thus, the membrane of the genital sheath is folded in repose.The distances between rigid elements within the membrane arenot similar on the dorsal and ventral sides of genital sheath,hence the folds are usually irregular, do not form completerings, and do not exactly correspond to each other. Some ofthese folds are sharp and constantly positioned, remaining trace-able even when the membrane is maximally stretched. In amajority of weevils and other beetles such semi-permanentfolds are fringed with fine filamentous processes calledpennons (Wanat 2001), visible with chlorazol black.

The membrane of the genital sheath limits movability ofgenital parts when everted or retracted during copulation. Therange of movement of the aedeagus against the tegmen islimited by the length of the post-tegminal membrane, and isusually relatively short. A notable exception among weevils isIthycerus (Ithyceridae), in which both pre- and post-tegminalportions of genital sheath are very long and, by extensive tele-scoping, they allow long distance movements of both aedeagusagainst tegmen, and tegmen + aedeagus against the 9th segment.

The appearance of various secondary sclerotisations in thegenital sheath seems generally underestimated. They mayapparently develop easily and more frequently than expected,especially on the membranous working sectors or folds. Suchplates may reinforce the weakest points of the membrane when

Homology of male terminalia in Curculionoidea


it is in tension, or they serve as parts of secondary lockingdevices, or prevent the sticking of soft membranous edgeswithin the abdominal opening.

Anal outlet

The rectum is confluent with the genital chamber and opens dor-sally through the pretegminal membrane between T9 and thetegmen. Thus, the genital chamber receives the rectum before itopens outside, forming a kind of cloaca, with the true anusslightly displaced inwards in weevils. This is clearly seen in theNemonychidae, where the rectal opening is situated closebehind the sclerite(s) of T9 (Figs 1a, 2a). A similar condition isfound in the chrysomeloids Donacia and Orsodacne. Theremainder of Curculionoidea, and in the majority of Chryso-meloidea and Cucujoidea, the sclerites of T9 are completely

reduced, so the position of the anus is less obvious, lyingbetween T8 (pygidium) and the dorsal tegminal plate.Frequently in these beetles the sternal part of the membrane ofsegment 8 is much longer than its respective tergal part, whichcauses displacement of S9 farther away from S8 than the anus isfrom T8. This was misleading to some authors, who placed theanal outlet in adult weevils between the 8th and 9th abdominalsegments, which is discordant with the larval anus alwaysopening behind the 9th abdominal segment.

8th tergite (pygidium)

Either exposed or concealed in repose, T8 is the last tergite inthe non-invaginated part of the weevil abdomen, and forms thepygidium (in the Anthribinae the fully exposed pygidium con-stitutes T7). Tergite 8 forms a capsule, often with a tucked down

F

Eps BPaTG

aAE

AE

aS9

pr

pr

R

aS8

S8

T9

S9

ps

(a)

(b)

T6

T7

T8

T9

R

PMTP

TC

EPE

BP

S9

S7

S6

S8

S5

pr

ps

ps

pr

ed

TP

an

aS8aS9

Fig. 1. Genital chamber of Cimberis (Curculionoidea:Nemonychidae), lateral view: (a) photographed(T8 removed); (b) diagrammatic (original inversion of genitalia omitted to show generalised weevil con-dition). [Abbreviations explained on p. 148.]


lateral and/or posterior margin, which receives the T7 mem-brane at its anterior edge. This membrane is usually simple inweevils, but in eurhynchids and some primitive apionids (forexample Rhadinocybinae, Myrmacicelinae, Cybebinae,Rhinorhynchidius) it is provided with a variably developed,sometimes melanised median pouch of unknown function,which is invaginated towards the interior of the abdomen (Wanat2001). Another interesting structure found in several orthocer-ous weevils, particularly in the brentoid family complex, is asemi-circular or tongue-like process developed from the poste-rior margin of T8 on its inner side (Fig. 2b). It originates fromthe T8 membrane fold, which is attached to the margin of theprocess, thus being displaced from the top margin of T8. Thefunction of this tongue-like process is not clear, it may simplyreinforce the junction of the pygidium with the membrane in thearea where the hard genital plates pass during their eversion andretraction, but in several brentoid groups (Brentinae, Eurhynch-idae, apionid Antliarhininae, Tanainae, Myrmacicelinae, andZelapterus) with a corresponding median sclerite in the S8membrane, it may possibly serve a locking device for theabdominal orifice (Wanat 2001).

8th sternite

In most weevils S8 is totally concealed in repose and only partlyextrudable, if any, during copulation. A notable exception isAustralian amycterine Phalidura, in which S8 is largely exposedand modified to form the so called ‘forceps’ (Thompson 1992;Zimmerman 1993). An extensive review of S8 over majorgroups of Curculionoidea has been done by Thompson (1992).It is either composed of two hemisternites separated by a mem-brane, or a uniform, but nearly always bilobed plate. Thesestates are not evident in many cases, depending on a variouslyexpressed range and extent of sclerotisation in the middle of theplate, thus the value of this character for considerations ofhigher weevil phylogeny seems to be overestimated. Unlike trueanthribids, S8 is completely reduced to a simple membrane inthe Urodontinae.

The apodeme (false spiculum by Muir 1918; spiculum relic-tum by Thompson 1992), if present, is either separate(Nemonychidae, Anthribidae, Caridae, Belidae) or connate withthe sternum (Ithyceridae, Eurhynchidae, Brachycerinae,Nanophyidae?). The apodeme is attached exactly to the fold


Fig. 2. (a) The 9th abdominal segment of Nemonyx (Curculionoidea:Nemonychidae), showing position of the anus, lateral view; (b) male pygidium with atongue-like process, Myrmacicelus sp. (Curculionoidea:Apionidae), SEM micrograph, ventral view; (c) genital chamber of Rhynchites(Curculionoidea:Rhynchitidae), showing false ‘T9’ sclerites behind the anus, lateral view; (d) genital chamber of Bruchela rufipes(Curculionoidea:Anthribidae:Urodontinae), showing secondary sclerite in the position of S9, lateral view.


margin of the S7 intersegmental membrane and directed almosthorizontally anterad. An exception is Anthribus, in which theapodeme is short and distant from the S8 hemisternites, and it isdirected obliquely posteriad in repose. In several weevil genera(Notaris, Chlorophanus, Otiorhynchus, Metacinops and Apsis,for example) the fold of the S7 membrane is provided with amedian forked process (two simple processes in Crypto-rhynchus), that are either fully membranous or sclerotised distally.Whether this structure is homologous with the apodeme of prim-itive orthocerous weevils is open to question (Thompson 1992).

9th tergiteNemonychidae are the only weevils with T9 retained as a com-plete or broken sclerotised arc forming a ring with S9 to consti-tute abdominal segment 9, and preceding the anus in the courseof abdominal invagination (Fig. 2a). Although paired scleritesresembling T9 can be occasionally found in other weevil groups(for example, Rhynchites (Fig. 2c), Byctiscus, Grypus andDesmidophorus), the sclerites are always situated between theanus and the tegmen, and hence considered secondary scleroti-sations. In some cases the sclerites are situated dorso-laterally asextensions of the arms of the spiculum gastrale, and may repre-sent displaced fragments derived from S9.

Regarding the position in the membrane of the genital sheath,T9 is simply incorporated between the layers of two-layeredmembrane, and no folds are associated. Thus, the membrane ofT8 joins the posterior margin of T9, whilst the pretegminal mem-brane leaves the anterior margin of T9. The same situation isfound in Donacia and Orsodacne, and is likely to be the case inthe Palophaginae, another possessor of T9 among chrysomeloids(Kuschel and May 1996). Tergite 9 is absent from all ceram-bycids, nitidulids and the cryptophagid Antherophagus exam-ined. A completely different condition of T9 exists in theremaining Cucujoidea and all other examined superfamilies, andthis is discussed in the section on genital alignment.

9th sternite (spiculum gastrale)The basal part of S9, forming a uniform, bilobed or V-like plate,is always incorporated into the membrane of the genital sheath.Similar to the situation with T9 in nemonychids and mentionedchrysomeloids, the membrane of the genital sheath is straightand unfolded on S9. Thus, the membrane running from S8adjoins the posterior margin of S9, and the pretegminal mem-brane rises from the anterior margin of S9.

Typically, S9 has a single basal plate or fork with a singleapodeme, both situated ventrally. Departures from this standardcondition have been found in Apsis and in members ofDryophthorinae, Cossoninae, Scolytinae and Platypodinae. InApsis, two apodemes of approximately the same length occur,and the basal plate is almost completely divided into two lobes.In Sphenophorus and other dryophthorines the base of thisapodeme is displaced to a more or less lateral position and thebasal plate of S9 is totally obscured, forming a ring of scleroti-sation around the unusually thickened genital sheath (Sharp andMuir 1912; Zimmerman 1993). In Cossonus and the scolytinesthe basal plate is attached to the genital membrane in its normal,ventral position. However, the fork is largely asymmetrical, withone arm vestigial, and the other long and strictly an extension ofa long apodeme directed laterad. In Platypus S9 is absent, butreplaced with a large, rectangular evagination of the genitalsheath’s membrane, provided with latero-terminal, plate-likepennons.

A peculiar S9 occurs in the Urodontinae. In Bruchela S9comprises an obsolescent fork with a long apodeme, that is dis-placed almost to the position of the reduced S8. Additionally,midway on the ventral pretegminal membrane a small partlysclerotised process bearing pennons (B. suturalis) or a crescen-tic sclerite (B. rufipes, Fig. 2d) occurs. The presence of anormal, double fold of genital membrane between S7 and S9clearly identifies the latter, while the additional plate-likeprocess or sclerite is a secondary development.

Genital segmentsTwo major segments of genitalia are considered here separatelyas the tegmen and aedeagus, and this is the condition in weevils,since both these segments are connected by a long post-tegmi-nal membrane and are largely movable against each other, atleast in the orthocerous groups. The situation is different inmany other beetle groups with ‘trilobe’ or ‘sheath’ type of gen-italia, where both the basal piece (phallobase) bearingparameres, and the so called median lobe are often firmly unitedand work as a single element called by many authors ‘the aede-agus’ (for example, Crowson 1955, 1981; Lindroth and Palmén1970; Lawrence and Britton 1991).

In a vast majority of the weevils and chrysomeloids, the gen-italia are oriented in such a way that the tegminal plate andaedeagal tectum are dorsal, while the basal piece and aedeagalpedon lie on the ventral side of the genital chamber. The aede-

Fig. 3. Inverted genitalia, lateral view: (a) Cucujus (Cucujoidea); (b) Donacia sp. (Chrysomelidae:Donaciinae).


agus in these groups is curved dorsad and its ostium is on thedorsal side. The same orientation of genital segments is found innitidulids and the cryptophagid Antherophagus. According toCrowson (1981) such genitalia orientation is probably ancestralin beetles, reflecting a standard copulatory position, with themale on the back of the female. A variant copulatory position isknown for the Cucujidae and some related families, in whichboth mating partners rest on the substratum facing in oppositedirections, and are joined only by their terminalia (Crowson1981). This results in a subsequent rotation of the genitaliathrough 180°, as seen in Cucujus (Fig. 3a). Evans (1961)described inverted genitalia in the cryptophagid Atomaria,while Wilson (1930) recorded a 90° twisted genitalia inCryptophagus. Such an inverted cucujid type of genitalia alsooccurs in some chrysomelids, as well as in some groups of prim-itive weevils. This is seen in the chrysomelid Donacia, whichcan have genitalia half- or fully rotated, depending on thespecies (Fig. 3b). Torsion of the genitalia was recorded also inGalerucella by Verma (1958). Among basal weevil groups, theNemonychidae (Fig. 1a), Oxycoryninae and Aglycyderinae, allexhibit genitalia rotation. Twisting around the long body-axisalways involves the entire genitalia, wherein the tegminal plateremains above the aedeagal tectum, and the basal piece abovethe aedeagal pedon. Considering the structure of the genitalchamber in these groups, all having a long pretegminal mem-brane unfolded and uninterrupted by sclerotisations, such atorsion appears a relatively simple evolutionary change, suscep-tible to selection based on the mode of life and matingbehaviour, as illustrated by various species of Donacia(Konstantinov 2004). The niches occupied by the weevils pos-sessing rotated genitalia resemble those of cucujids, that is,narrow crevices under bark or under scales of gymnospermcones, where such departure from the ordinary copulation modeis advantageous.

The orientation of internal structures related to the genitalchamber may be correlated with the shape of the larval anus,and more precisely with the position and orientation of therespective cell mass, one of the so called imaginal discs, situatedbetween the 9th sternum and the ventral anal lobe, and givingrise to genital invagination during the metamorphosis (Richardsand Davies 1977). Muir (1915, 1918) localised this in a medianpoint between S9 and S10 in the early pupa of Rhabdocnemisobscura (Curculionidae: Dryophthorinae), where the cell massis connected by a Y-shaped thread with the testes. The anus isusually X-shaped (4-lobed) in the weevil larvae, and the respec-tive imaginal disc must be situated near the ventral anal lobe.Only this placement could result in a final displacement of theanus to the dorsal wall, so called the ‘ceiling’ of the genitalchamber in the adult weevil. Notable exceptions include belids,the larvae of which are distinct in having a T- or Y-shaped(3-lobed) anus (Lawrence 1991b; May 1993). In adult males ofAglycyderes and Oxycraspedus the genitalia do not lie horizon-tally, but they are twisted laterad, while the rectum is twisted inthe other direction and its opening to the genital chamber isdorso-lateral, not dorsal as in other weevils (Fig. 9b). This maybe due to the asymmetrical position of the respective imaginaldiscs in their larvae.

Two basic types of weevil genitalia are recognised, primitiveand derived, often named ‘orthocerous’ and ‘gonatocerous’

respectively, following the major division of the weevils intoprimitive groups with straight antennae, and derived ones withgeniculate antennae. Differences concern the dorsal plate of thetegmen, which is well developed, sclerotised and diversifiedinto different sectors in primitive weevil families. The advancedcurculionids usually have much smaller, simple and transparentmembranous lobes attached to a thin ring surrounding the baseof the aedeagus. Another relevant character pertinent to primi-tive weevils is a division of the aedeagus into two movableplates, the tectum and the pedon (Fig. 4d), while in derived cur-culionids the tectum is totally reduced (Fig. 4e). Such a divisionworks well with derived weevils, but turns out slightly dubiousin regard to some basal groups of gonatocerous curculionids.While Brachycerus and Desmidophorus undoubtedly haveorthocerous tegmina, in true erirhinines (Notaris, Grypus) thetegmen is doubtfully orthocerous, with the dorsal plate undif-ferentiated, often not prominent beyond the junction with thearms of the basal piece, and with the pretegminal membraneattached closely to the basal margin of the plate. Only the sizeof the tegminal plate is comparable to that in orthocerousgroups, but examples of equally large tegminal plates are pro-vided by some derived weevils, for example the conoderineEuryommatus (Fig. 4a). Moreover, in some erirhinines (forexample Echinocnemus) a total reduction of the tegminal plateoccurs (Zimmerman 1993).

TegmenThis part of weevil genitalia consists of a flattened and usuallybilobed tegminal plate, V-shaped basal piece and an apodeme.The plate may be connate, subarticulated or fully articulated tothe arms of the basal piece in orthocerous families, while inderived weevils the tegmen is always connate, unless its dorsalpart is totally reduced. In orthocerous families the tegminalplate may be diversified into distinctive sectors, highly diverseand species-specific. By far the greatest structural diversity ofthe tegminal plate is expressed by the Apionidae, hence, in thisweevil group its particular parts or sectors have gained their ownterms (Fig. 4b, c) explained in detail by Wanat (2001). Theexamination of large apionid and eurhynchid tegmina revealedthat the plate evidently consists of two horizontal layers, ventraland dorsal, which are connate to each other only at their outermargins and incorporate different parts of those recognised andnamed in Fig. 4b, c. The layers are derived from invagination ofthe pretegminal membrane toward the genital chamber, whichhas become secondarily sclerotised. As a rule, the dorsal layer isshortened, thus leaving the basal part of the ventral layer uncov-ered, and its arched anterior (basal) margin is contiguous withthe soft pretegminal membrane derived from the T9 sector. If thefenestrae and/or subfenestral sclerites are absent (for example inNemonychidae, Rhynchitidae, Nanophyidae, Caridae and somearchaic Apionidae), the unsclerotised basal margin of the dorsallayer is not positioned. The dorsal membrane then becomesloose towards the apex of the tegminal plate, and forms amovable fold. The more apically the dorsal membrane isattached, the smaller the part of the tegminal plate that projectsfreely into the genital chamber. The components of the tegminalplate shown in Fig. 4b, c constitute subsequent sectors of thesclerotised fold, and they can be ordered as follows (d, dorsallayer; v, ventral layer; dv, both): subfenestral plate, d; fenestrae,



Fig. 4. (a) tegmen and aedeagus of Euryommatus (Curculionidae:Conoderinae), dorsal view; (b, c) division of apionid tegminal plate, based onApionocybus nigricollis Heller (Curculionoidea:Apionidae): (b) dorsal and (c) lateral view [aml, apical membranous lobes; pl, parameroid lobes; mn, mediannotch; spf, suprafenestral sclerites; fn, fenestrae; sbf, subfenestral sclerites; prf, fold of pretegminal membrane; ptg, prostegium]; (d, e) aedeagi, dorsal view:(d) orthocerous type, Eurhynchus (Curculionoidea:Eurhynchidae), gonatocerous type, Otiorhynchus (Curculionidae:Entiminae); (f) aedeagus of Alissapion(Curculionoidea:Apionidae), showing extraordinary long flagellum, lateral view; (g, h) endophallus with flagellum: (g) Glischrochilus (Cucujo-idea:Nitidulidae), (h) Orsodacne (Chrysomeloidea:Orsodacnidae).


d (or dv, if corresponding desclerotised windows are developedin the ventral layer as well); suprafenestral sclerites, d;parameroid lobes (including apical membranous lobes), dv;prostegium, v. The post-tegminal membrane originates at theopposite end of the dorsal tegminal fold, and is confluent withthe prostegium (Figs 1b; 7a). Also, the arms of the basal pieceare attached to the prostegium at its lateral margins. Kuschel(1989) adopted the term ‘supraannular sclerite’ for the proste-gium in nemonychids.

Contrary to the tegminal plate, a typically V-shaped basalpiece is simply incorporated into the unfolded genital sheath,hence this sclerotised fork receives pretegminal membrane atone (posterior) edge, and the post-tegminal membrane leaves itat the opposite (anterior) edge to join the base of the aedeagus.Occasionally, in species having the tegminal plate enlarged lat-erally and enveloping the aedeagus (for example numerousApionidae), the basal piece may be diminutive, bar-like, or thefork may be filled and sclerotised to a varying degree. Theapodeme usually constitutes a simple, variably long sclerotisedrod forming a Y- or T- shape with the basal piece. Numerousapionid groups, particularly the Rhadinocybinae, have the distalend of the apodeme strongly expanded to form a triangular orfoot-like plate, that is sometimes even wider than the dorsaltegminal plate (see Wanat 2001 for examples).

The function of the weevil tegmen is primarily mechanical intwo respects. First, the tegmen limits the range of eversion of theaedeagus and serves as a point of attachment for the post-tegmi-nal membrane. Second, it assists with eversion and retraction ofthe genitalia through the action of the muscles attached to theapodeme. Normally, no part of the male tegmen enters thefemale genital tract, although a remarkable exception is knownfrom the apionid genus Myrmacyba, where connate tegminallobes may be extended into a long, ribbon-like filament that isintroduced deeply into female’s bursa copulatrix along with theendophallus and serves as a kind of external stiffener. A sensoryfunction of the dorsal tegminal plate lobes is indicated by thepresence of various setae, pores and/or sensillae in primitiveweevil groups. This function loses importance and is apparentlytaken over by sensory organs on the apex of the aedeagus inderived weevils, in which the tegminal plate becomes dimin-ished or rudimentary. The reduction of the tegminal plate, likethat of the whole tegmen, is generally correlated with a tubularshape and stronger sclerotisation of the aedeagus, followed byshortening of the internal sac. Taken together, these modifi-cations facilitate deeper penetration of the vagina and bursacopulatrix by a rigid aedeagus. This deep penetration probablymakes copulation faster, safer (easier to stop when matingbeetles are disturbed), provides better protection against com-peting males, and makes multiple attempts easier. Perhaps forthese reasons parallel changes in the structure of the male geni-talia and the mechanism of copulation evolved independently inboth Curculionoidea and Chrysomeloidea.

AedeagusThe weevil aedeagus is a sclerotised tubular organ containing amembranous eversible endophallus (internal sac) and is con-nected to the tegmen by the post-tegminal membrane. The mem-brane is attached to the base of the aedeagal tube, and at thesame place paired lateral projections of the tube (actually sclero-

tised evaginations of the membrane) are developed to formaedeagal apodemes (called ‘temones’ by Alonso-Zarazaga1989, 1990; Gønget 1997). A similar structure is characteristicof the aedeagus in chrysomeloids, while in nitidulids theapodemes are commonly confluent to form a single rod. Theweevil aedeagal tube may be divided into two movable parts: thedorsal tectum and ventral pedon, consisting of a ventral pedonwith upfolded margins and the dorsal part of the tube membra-nous, or the tube is evenly sclerotised both ventrally and dor-sally along most of its length. The pedon gives shape to theaedeagus and its apex and sides are always heavily sclerotised.The pedon’s venter may be either entirely sclerotised, bearing anotch filled by a simple membrane, or largely desclerotised ven-trally giving the aedeagus a frame-like shape. A broader extentof ventral desclerotisation seems to be correlated with theenlarged size of the endophallus and its armature.

A widely accepted belief maintains that the most primitivecondition of the aedeagus in Curculionoidea is a well preservedand plate-like, sclerotised tectum, separated from the pedon bylateral membranes along its whole length (Fig. 4d). This is char-acteristic of nearly all orthocerous weevils, including thearchaic Nemonychidae, Anthribidae and Belinae, as well as ofsome gonatocerous groups considered phylogenetically mostbasal. In most orthocerous families the tectum has a tendency toreduction and the aedeagus tends to become tube-like, similar tothat seen in the Curculionidae. However, a reduction of thetectum in weevils may be accomplished in two dramatically dif-ferent ways. In all orthocerous families (Nemonychidae,Anthribidae, Belidae, Attelabidae, Brentidae and Apionidae) thetectum becomes narrowed from sides to mid-line, to form a rib-like median strip in extreme cases, while the membrane con-necting it with the pedon becomes expanded. A clearlycontinuous connection of the tectum with the apodemes is thenretained in most instances (unless secondarily broken, forexample in nemonychids). The same condition occurs with theapodemal connection to the pedon, except there is a secondaryarticulation in the Apionidae, Nanophyidae, Cyladinae andDesmidophorus. Hence, each apodeme is bifurcate basally for avariable distance to produce a dorsal branch confluent with thetectum and a ventral one confluent with the pedon. Apart fromthe orthocerous weevil groups (including Ithycerus), this type ofaedeagus is found in Brachycerus, Notaris, Grypus, and, accord-ing to Thompson (1992) and Kuschel (1995), also inRaymondionyminae, Ocladiinae and Cryptolarynginae (notstudied by me). A different path to reduction seems universal forthe remaining Curculionidae. The sclerotisation of the tectumvanishes from the middle, leaving a broad, simple membrane,and its sclerotised margins become fused to the pedon togetherforming a sclerotised upfolded margin of the aedeagal tube(Fig. 4e). In this aedeagal type the apodemes are not clearlybifurcate basally and, since the fusion is usually complete, theyare confluent with the pedon. An example of this kind of trans-formation is seen in the Dryophthorinae, which retained a suturebetween the connate lateral margins of the tectum and pedon.Other evidence comes from the entimine Apsis, where basaldichotomy of the apodemes can be recognised, which branch tothe dorsal and ventral margins of the side walls of the aedeagus.Among the primitive weevils the fusion of the tectum and pedonhas been reported from the belid subfamilies Oxycoryninae and



Aglycyderinae by Kuschel (1995). Fusion has not been con-firmed in Rhopalotria, which has a typically orthocerous aede-agus with the tectum completely separated from the pedon, andthe apodemes disconnected with the pedon. However, in bothOxycraspedus and Aglycyderes the tectum and pedon areequally broad and subequal in size, leaving very narrow lateralmembranous ‘sutures’ in the basal part of the aedeagus (absentfrom a specimen of Aglycyderes from Tenerife), resembling thedryophthorine condition.

Endophallus (the internal sac)The membranous sac enclosed within the aedeagus constitutesthe intromittent organ proper. In many weevils the internal sacis the only part of the male genitalia that penetrates the femalevagina and bursa copulatrix during copulation. The endophallusmembrane is attached to the margin of the aedeagal apical (withrespect to the pedon rather subapical) orifice (the ostium) and,in repose, extends inside the aedeagus towards its basalforamen. In numerous weevils the retracted endophallus ismuch longer than the pedon, or even the apodemes. (An extremeexample is seen in Ulomascus, which has an endophallusseveral times longer than the whole beetle body.) The endophal-lus has a gonopore near the terminal end, where the ejaculatoryduct is attached (exceptionally among studied beetles, the cer-ambycid Dorcadion has the ejaculatory duct reduced and pairedvasa deferentia are attached to the end of the endophallus). Theendophallus is exposed through the ostium when fully evertedfor copulation, becoming then a terminal extension of thesclerotised aedeagus, with the gonopore situated apically orsubapically, and the ejaculatory duct running inside the evertedsac. Therefore, the endophallus could be considered a terminalpart of the abdominal invagination, although it is usually treatedas ‘a specialised and widened apical part of the ejaculatory duct’(Crowson 1981).

The endophallus membrane often has various sclerotisedoutgrowths forming variably shaped sclerites, larger teeth,spinules or miniplates, and usually becomes outwardly promi-nent when the endophallus is extruded. Special kinds ofendophallic sclerites are the frena, which are always paired,have a comma- or hook-like shape with enlarged, roundedbases, and they are situated sub-basally in the evertedendophallus, as illustrated for the apionid Myrmacicelus(Wanat 2001). Since the frena are regularly present in archaicweevil groups, their presence was recognised as a primitivefeature by Kuschel (1995).

A different kind of endophallic sclerotisation is the flagel-lum, which is always derived from the ejaculatory duct. Mostoften the flagellum is a uniform tubular structure formed byprojection and subsequent sclerotisation of either the endophal-lic wall surrounding the gonopore (as illustrated by Lawrenceand Britton 1991), or the wall of the ejaculatory duct, to theinside of endophallus (defined as a ‘sclerotized terminal pro-longation of the ejaculatory duct’ by Lindroth and Palmén(1970)). In the former case, the outer membrane is derived fromthe endophallus, while the inner one is derived from the ejacu-latory duct. In the latter case both outer and inner membranesare derived from the evaginated ejaculatory duct. The ejacula-tory duct thus either passes through the flagellum, or it consti-tutes its lining. Both variants, as well as their combinations, can

be found in weevils and other taxa possessing flagella, but dis-tinguishing between these types is practically impossiblebecause the ejaculatory duct is confluent with the endophallus,and the membranes of both look the same when stained withchlorazol black. Regardless of the origin of its walls, the flag-ellum formed in this way becomes one more eversible sclero-tised element of the weevil genital duct, a kind of secondfunctional ‘aedeagus’ inside the true aedeagus, for which themembrane of the endophallus plays a role analogous to that ofthe post-tegminal membrane for the true aedeagus. An exces-sively developed flagellum of this kind is the coccinellid sipho.Good illustrations of the way in which flagella are formed areprovided by Glischrochilus (Fig. 4g) and Orsodacne (Fig. 4h);in the latter the invagination of the tip of the endophallus iseven double.

A different type of flagellum is found in the apionid genusNanomyrmacyba (Wanat 2001), which has the form of a sclero-tised internal rod or a pair of rods placed inside the ejaculatoryduct, close to, but evidently outside the endophallus in repose.This kind of flagellum is non-eversible when the endophallus isbeing evaginated.

Typically the flagellum is long and filiform, as in Ithycerus,carids, nanophyids and several Australo-Pacific apionid genera,for example Alissapion (Fig. 4f), but may vary considerably inform and shape. Numerous examples exist of great infragenericvariation in this structure, from the typical and apparently prim-itive filiform shape, to short and bottle-like rudiments or com-plete reductions (for example in the apionid Pterapion andTetrapion). In some very speciose apionid genera (Myrmacybaand Apionocybus) the flagellum was found only in a singlespecies, suggesting the possibility of convergence. Occasionally(for example in the Apionidae and Rhynchitidae) the flagellumdevelops into a larger, sclerotised and complicated structurecalled a ‘complex apparatus’ (also named a ‘transfer apparatus’,for example by Riedel 1999, 2001).

The presence of a flagellum is primarily characteristic ofprimitive weevil groups, and this was usually considered a ple-siotypic character, for example by Alonso-Zarazaga (1989) andWanat (2001). Among apionids a flagellum has never beenobserved in the members of the derived subfamily Apioninae,comprising a vast majority of the world fauna. However, whenthe origin of this genital structure is considered, the phylo-genetic value of this character probably should be re-evaluated.The presence of flagellum-like structures may well be apomor-phic and probably a highly homoplastic character in some oldlineages, while its universal reduction or under-development inderived weevils is probably related to the more tubular aedeagalshape followed by a shortening of the endophallus. Thesechanges in aedeagal shape may allow precise sperm depositionclose to the opening of the female’s spermathecal duct; hencethe basic function of the flagellum (according to Evans (1961))is fulfilled in another way. Although a primitive character, thepresence of a flagellum may have evolved independently manytimes in the weevils, and its secondary reduction in many groupsseems even more frequent. Like many other weevil features, thepresence v. absence of the flagellum appears to be an equivocalcharacter, which may be stable and well applicable for thefamily level diagnoses in some groups, but suitable for onlyspecies distinction in others.


Alignment of the genital chamber

Family groups within Curculionoidea all share the same genitalchamber alignment (Figs 5a, 6a, in both the retracted andeverted positions). Other beetle superfamilies, namely Tene-brionoidea, Cleroidea, Lymexyloidea, Dascilloidea, Bostri-choidea, Byrrhoidea, Eucinetoidea, Elateroidea, Cantharoidea,Hydrophiloidea, Staphylinoidea and Caraboidea (Figs 5b, 6b)exhibit notable differences, particularly in the everted stage.Although the number and order of sclerotised plates are the

same, the course of the genital sheath membrane is different forthe 9th segment and the tegmen. In the ‘standard’ condition per-tinent to most polyphagan superfamilies (Figs 5b, 6b) the mem-brane of segment 8 extends to the anterior margin of thewell-developed capsule of segment 9. In weevils both T9 and S9are inverted dorso-ventrally, and receive the respective mem-branes of T8 and S8 on their posterior margins (Figs 1b, 2a, 5a,6a). Moreover, in weevils a similar inversion occurs with thetegmen, which receives the pretegminal membrane at the poste-


(a)

(c)

(b)

Fig. 5. Diagram of genital alignment, retracted: (a) phytophagan type; (b) eucinetid type; (c) cucujid type.


rior end (apical, when the orientation of the dorsal tegminalplate is considered, and the parameroid fold is disregarded) asseen in Fig. 7a in Eurhynchus. This is the anterior margin (basalrelative to the phallobase with parameres) receiving thepretegminal membrane in other beetle superfamilies listedabove, as seen in the lycid Lygistopterus. In the latter example,the tegmen resembles in structure that of many cucujoids havinga large, even slightly bilobed, dorsal plate and bifurcate basalpiece (phallobase). However, in Lygistopterus the pretegminal

membrane joins the anterior (not posterior as in cucujoids)margin of this tegminal plate. Furthermore, the post-tegminalmembrane originates from the posterior margin of the plate andruns cephalad along the ventral side towards the base of theaedeagus (Fig. 7b).

The Chrysomeloidea all have the same genital chamberalignment as weevils, but the Cucujoidea are problematic. InNitidulidae and Cryptophagidae the sclerotised plates of T9 aretotally reduced, while S9 is present, nearly adjoining S8 and

(a)

(c)

(b)

Fig. 6. Diagram of genital alignment, everted: (a) phytophagan type; (b) eucinetid type; (c) cucujid type.


usually bearing a single apodeme (Glischrochilus, Kateretes,Antherophagus and the New Caledonian Carpophilus), or it isoccasionally replaced with paired membranous projections(Soronia). Therefore, the position of S9 and associated mem-branes resembles that in the weevils, and both pre- and post-tegminal membranes are attached similarly, hence the nitidulidand cryptophagid tegminal plate is inverted. In coccinellids(best seen in Henosepilachna) the alignment is ‘standard’: thecomplete and well developed segment 9 is telescoped withinsegment 8, and the pretegminal membrane joins the anterior(basal) margin of the tegminal ring, while the post-tegminalmembrane arises from the distal end and runs adpressinglyalong the inner side of the parameres towards the aedeagus base.Interestingly, in Cucujus and Byturus an intermediate conditionwas found; the plates of segment 9 were well developed, notinverted and normally telescoped within segment 8, while thegenitalia looked exactly as in weevils, chrysomeloids, nitidulidsand the cryptophagid Antherophagus, all having inverted tegmi-nal plates (Figs 5c, 6c).

Because of obvious symmetry in the everted state (Fig. 6b),referring to abdominal segmentation, and its common occur-rence in beetles, including the basalmost polyphagan groupslike Eucinetoidea or Hydrophiloidea, the ‘standard’ alignmentillustrated in Figs 5b, 6b should be considered plesiotypic.Moreover, although in the Adephaga the tegminal basal piece isabsent resulting in the parameres loosely adjoining the base ofthe aedeagus and largely movable laterad, the respective mem-brane fold is retained and the alignment is similar to that foundin the basal Polyphaga. This arrangement of the genital sheath isreferred to as the eucinetid type of alignment further in the text,because of the relatively legible course of all the membranes inEucinetus (perhaps even more clearly seen in Dascillus) and thevery basal position of this group in the suborder Polyphaga. Theeucinetid alignment resembles the scheme seen in thecoleopteran abdomen (Lindroth and Palmén 1970), except thatthe position of the membranes attached to T9 and S9 waswrongly illustrated by those authors, implying a rotation ofsclerotised and often firmly connected plates during terminaliaeversion. The phytophagan type of alignment (called as suchlater in the text), possessed by Curculionoidea, Chrysomeloidea

and a part of Cucujoidea (Nitidulidae, Antherophagus), wouldbe apomorphic, while the condition of the genital chamber inCucujus and Byturus (the cucujid alignment) is plesiomorphicwith regard to segment 9, and apomorphic with regard to thetegmen.

Regarding segment 9, the difference between basic types ofalignment could be best explained by the development of sclero-tised plates of T9 and S9 in either a non-invaginated (eucinetidand cucujid alignment) or invaginated (phytophagan alignment)apex of the abdomen. The abdominal foramen margin is actuallya fold of invaginated membrane, so when the range of invagina-tion increases to exceed the 9th segment, primitively telescopedwithin the 8th one, both T9 and S9 are displaced from the outerto the inner side of the fold, being rotated at the same time. Therange of the invaginated part of the abdomen must be estab-lished before sclerotisation takes place during metamorphosis,and indeed Muir (1915) reported the late appearance of a sclero-tised spiculum gastrale (S9) during development of the genitalinvagination in the pupa of Rhabdocnemis obscura(Curculionidae: Dryophthorinae), at least contemporaneouslywith development of the remaining aedeagal and tegminalapodemes. A further consequence of such internalisation androtation of T9 is a displacement of the anus to the inside of thegenital chamber, while in the eucinetid and cucujid genitalalignment the anus is closer to the end of the abdomen, hencethe digestive tract is more widely separated from the reproduc-tive tract.

The hypothetical evolutionary change required for transfor-mation from the eucinetid to the cucujid and phytophagantegmen is relatively simple. The inverted and non-inverted states


Fig. 7. Tegmina, showing alignment of pretegminal membrane, lateral view: (a) Eurhynchus (Curculionoidea:Eurhynchidae); (b) Lygistopterus(Cantharoidea : Lycidae).

TG

AE

AE

TG

E

ed

TG

AE

AE

TG

E

ed

(a) (b)

Fig. 8. Diagram of genital invagination: (a) eucinetid type; (b) phyto-phagan type (after Muir 1915, modified).


of tegminal plates could be easily derived from the tegminalfold. This fold is formed during the development of genitalinvagination during metamorphosis, as described by Muir(1915), and different layers of this fold may become sclerotised.If the sclerotisations develop on the inner membrane of thetegminal fold, we would have a eucinetid type of genitalia(Fig. 8a). Displacement of the sclerotisations to the outer mem-brane of the fold (possibly caused simply by shallowing of theinvagination between the tegminal fold and pregenital tube)would lead exactly to the model illustrated by Muir (1915),referring to the phytophagan and cucujid condition (Fig. 8b).

Different folding patterns of the tegminal sector of thegenital sheath in the phytophagan/cucujid and eucinetid types ofalignment result in different paramere origins. In the groupshaving eucinetid alignment (Figs 5b, 6b), the parameres developfrom the fold of the membrane linking the tegminal basal piece(phallobase) with the aedeagus, and thus from the post-tegminalmembrane. In weevils, chrysomeloids and cucujoids with aphytophagan or cucujid alignment of genitalia, the ‘parameres’(the lobes of tegminal plate) develop from the fold of the mem-brane linking the T9 sector with the tegminal plate, and thusfrom the pretegminal membrane (Figs 5a, 6a). In the eucinetidalignment, the arrangement is fully symmetrical and the fold isring-like, thereby allowing for equally easy development of theparameres from every sector of the fold. Therefore, develop-ment is simple for trilobed or sheath-type genitalia, with theaedeagus completely surrounded by the parameres, even if theyare multiplied or excessively developed and diversified (like theparameres and whole tegmina of some coccinellids). Moreover,since in this eucinetid type of alignment it is unnecessary for theaedeagus to pass over the tegmen during eversion, both thesegenital segments often become more or less firmly united andeither act as a single sclerotised organ, or are modified as asingle functional unit, which frequently leads to reduction orover-development of one part in relation to another. A remark-able example is the ‘bilobate aedeagus’ of advancedscarabaeoids, with the so-called median lobe completelyreduced (d’Hotman and Scholtz 1990). The modification andreduction of some parts of scarabaeoid male genitalia oftencause problems in resolving the course of pre- and post-tegmi-nal membranes, and the true homologies of segmental junctionsin the more derived forms.

The potential for structural diversity is much lower in thepossessors of the phytophagan or cucujid type of genitalia,which have one fold less at each side of the primary genitalinvagination for development of secondary structures.Moreover, the existing fold of pretegminal membrane is alwaysincomplete; it is not ring-like but limited only to the dorsal orventral side of the genital chamber, depending on where the‘parameres’ develop. Another structural limitation comes froma distinct functional division of the phytophagan/cucujidtegmen into the bilobed plate provided with sensory organs(the ‘parameres’), and the ring-like part bearing a strongapodeme that takes part in mechanical movement of the geni-talia. Such functional division is much less evident in theeucinetid type of genitalia, where no distinct, rod-likeapodemes associated with the basal piece are present, and thismechanical function is performed mainly by the pairedapodemes of abdominal segment 9.

Because of the basic differences in folding and origin of theparameres, the hypothetical development of the ‘cucujoid aede-agus’ from the primitive ‘trilobe aedeagus’ through four inter-mediate stages, as suggested by Crowson (1955), could not takeplace. For the same reasons, the ‘heteromeroid’ aedeagus is notderivable from the cucujid type following the scenario sug-gested by Wilson (1930) and Crowson (1955, 1960).

Thus, the ‘parameres’ of Cucujoidea (except Coccinellidae)are not homologous with the true parameres of other beetlesderived from the paired evaginations of the post-tegminal mem-brane. Likewise, the lobes of the tegminal plate in weevils andchrysomeloids, are not homologous with the parameres of mostbeetle superfamilies other than Cucujoidea (excludingCoccinellidae), which was suspected by Crowson (1960, 1981).Hence, although homologous with the ‘cucujoid parameres’ asearlier stated by Wanat (2001), the weevil, chrysomeloid andcucujoid (except Coccinellidae) tegminal plates must not betermed parameres. This term, first defined by Verhoeff (1893)refers to lateral phallic lobes and should be reserved for thearticulated lobes typical of the eucinetid type of genital align-ment. Therefore, I propose herein to adopt the terms‘parameroid plate’ or ‘parameroid lobes’ (already used for thedivided part of the plate by some authors, for example Alonso-Zarazaga 1983, 1989; Wanat 1995) for the respective tegminalpart (tegminal plate or cap-piece) in Cucujoidea, Chryso-meloidea and Curculionoidea, to distinguish these structuresfrom true parameres of the remaining beetles.

Considering multistate genital alignment, the monophyly ofCucujoidea in the current sense seems dubious, which follows thedoubts expressed by Leschen et al. (2005), who argued for theinclusion of the Cleroidea within Cucujoidea. If phytophaganalignment of abdominal segment 9 is considered a non-homopla-sious character, the present Cucujoidea will appear paraphyleticwith respect to the ‘phytophagan’ (Curculionoidea + Chryso-meloidea) lineage, which has its sister clade among the cucujoidfamilies having 9th segment inverted plates, including theNitidulidae group, as defined by Leschen et al. (2005). Crowson’sunpublished idea to erect it as a separate superfamily Nitiduloidea(Audisio 1993) could then be justified. Crowson (1960) wasapparently right in stating that, ‘the Chrysomeloid-curculionoidstock might, ..., be a later offshoot of the cucujoid stock’.Moreover, present Cucujoidea may be polyphyletic with respectto Coccinellidae in having the eucinetid genital alignment.

Homology of male terminaliaMost agree that the beetle aedeagus (in a broad sense, i.e.including the tegmen) has been derived from either theappendages of the 9th or 10th abdominal segment, or from thetransformed ejaculatory duct, and thus it has no incorporatedsegmental plates (Sharp and Muir 1912; Muir 1915, 1918;Snodgrass 1931, 1957; Michener 1944; Wood 1952; Lawrenceand Britton 1991). There have been no legitimate claims for asegmental origin of the aedeagus, primarily because of the totalreduction of the two terminal abdominal segments in adults ofhigher insects (commonly accepted in handbooks of entomol-ogy) and basic reference to the position of the anus as terminalin the ground-plan of the insect body. Nevertheless, some fea-tures of the structure and alignment of male genitalia are con-jectural regarding the segmental origin of at least the tegmen.


These conjectures are based on the observation that the mostplesiotypic state of the genital chamber, characteristic of allstudied beetle taxa (except some cucujoids and two phytopha-gan superfamilies), is a continuation of the arrangement of bodysegmentation on the invaginated part of abdomen. This arrange-ment is clearly seen in the everted chamber (Fig. 6b), where thetegmen and aedeagus occupy the positions of two terminal seg-ments. Another observation supporting the segmental origin ofgenitalia is that all the sclerotised plates, including those of thetegmen and aedeagus, are incorporated into the genital sheathmembrane in a way analogous to ordinary segmental plates.Although this condition is commonly explained as a result of thefunctional terminalisation (see p. 165) of holometabolan geni-talia, and an adaptation to copulation, some structural similari-ties to a segmental arrangement are striking.

The Y-shaped ventral part of the tegmen in primitive weevilsis a simple structure similar to the preceding S9 and S8, and, likethem, bears an apodeme. The example of Nemonyx (Figs 9c–e)is perhaps the most illustrative and may suggest a possiblehomology of the basal piece of the tegmen with the ventral seg-mental plate, and thus with the subsequent S10. Such an expla-nation appears to be simpler and more plausible than derivationof the third fork in the row from the ejaculatory duct as a com-pletely novel structure. Besides the weevils, an equally strikingexample of a similar structure and function for the ventral partof tegmen and the preceding S9 and S8 is provided by the cer-ambycid Asemum.

The phytophagan parameroid plate develops from a fold ofthe pretegminal membrane. Normally such telescoped foldingof the abdominal membrane is associated with the segmental


Fig. 9. (a) tegmen of Otiorhynchus (Curculionidae:Entiminae), dorsal view; (b) genital chamber ofOxycraspedus sp. (Curculionoidea:Belidae : Oxycoryninae), showing twisted genitalia and displaced anus,ventral view; (c–e) internal abdominal segments of Nemonyx (Curculionoidea:Nemonychidae), dorsal view:(c) 8th segment; (d) 9th segment; (e) tegmen.


plate border, so we could expect the tergite, 10th in thesequence, to be a part of the parameroid plate. Considering thestructure of the fold, only the ventral layer of the parameroidplate could constitute the tergum, and only the prostegiumbelongs entirely to this layer and may possibly associate withT10. The prostegium is the basal plate of the ventral layer, towhich the arms of the basal piece are attached, and it is presentin all orthocerous weevils. In derived curculionids, the proste-gium is usually shortened to form a common ring with the basalpiece, upon which more or less simplified lobes may occur(Fig. 9a). The prostegium is totally reduced, as the wholeparameroid plate, only in the Dryophthorinae and Ulomascus.However, in these groups the respective tegminal fold ofpretegminal membrane is retained, which is extended and trans-formed in dryophthorines to a special, thickened tube appar-ently consisting of three membrane layers firmly fused together.Therefore, if the prostegium is homologous with T10, theparameroid plate will be of mixed origin, that is, partly fromT10, and partly from the folded membrane of T9 (pretegminalmembrane). The tegmina in the eucinetid genital alignment,with true parameres developed from the folds of the post-tegmi-nal membrane, could conform to this scheme as well. The dorsaland ventral sclerotised parts of the basal piece (phallobase) referthen to T10 and S10 respectively, while the parameres devel-oped from the secondary membranous evaginations, if not fromthe appendages of the 10th segment. A different dorso-ventralorientation of T10 and S10 in phytophagans and cucujoids v.other beetles would not then be a major objection to the conceptof their segmental origin. Such an orientation depends only onthe relative position of the portion designated for sclerotisationin the invaginated membrane, as in the earlier discussed case ofthe 9th abdominal segment. Having T10 possibly present in theweevils and related chrysomeloids and cucujoids, and the basalpiece homologous with S10, we could consider the phytopha-gan/cucujid tegmen as constituting the 10th abdominal segment.

The basic ground-plan of the abdomen should be the same inall beetles, so the concept of the 10th segment incorporated intothe tegmen ought to be applicable to all other beetle super-families. However, the concept poses some major problems.One is the extrategminal parts of the 10th segment, claimed tobe present in several beetle superfamilies having a trilobed- orsheath-type of genitalia (for example as seen in Sharp and Muir1912; Lawrence and Britton 1991). The most problematic platethen appears to be the proctiger, which Lawrence and Britton(1991) referred to as T10. In all beetles possessing a proctiger(for example Scarabaeoidea, Elateriformia and Eucinetoidea)the fully developed parameres articulated to the basal piece arealso present (unless secondarily modified), hence a differentorigin of the tegmen in these groups should be assumed to avoidinconsistency. Following that interpretation, the dorsally unitedparaprocts, and the proctiger that follows them (for example inthe lucanid Ceruchus, Fig. 10a) are T9 and T10 respectively.However, the position of the paraprocts is different in Geotrupes(Figs 10b, c), where they are widely separated from each otherand clearly lateral, not dorsal. As a result, the capsule ofGeotrupes looks more like a complete 9th segment, where theproctiger is a tergite, the paraprocts are laterotergites, and ven-trally there is a well-developed sternite. This was the conceptadvocated by Crowson (1955, 1981), who did not recognise

plates of the 10th segment in beetles. Following this point ofview, and the interpretation of scarabaeoid genitalia byd’Hotman and Scholtz (1990), the genital chamber alignment inGeotrupes has been diagrammatically resolved in Fig. 11a. Theparameres developed from the post-tegminal membrane (thustypically for the eucinetid alignment), have a ring-like base andare entirely encompassed by the ventral and dorsal lobes of theextraordinarily enlarged basal piece. The aedeagus is membra-nous, with only a vestigial ventral sclerite. In my opinion, latero-tergites may be unnecessary in Crowson’s concept, and theplates considered as such may actually represent lateral lobes ofthe trilobed S9, which became enlarged and moved dorsad.There is no clear evidence obtained from the studied taxa forany of these two possible homologies of the paraprocts, andassociated structural modifications of these plates might havebeen equally easily derived from both laterotergites and thelateral lobes of S9. Examples are the variously developed pairedapodeme-like extensions, connected or not with the ‘true’ S9.They always remain fully incorporated into the genital chamberwall, even if produced outside, as in the cleroid Peltis, and havea membrane between them (Fig. 10d). Such a condition may beequally easily derived from the division of a single plate andlaterad displacement of its parts (hemisternites), or from retain-ing a common membranous sheath by two independentapodemes of the laterotergites. Evidence from Peltis indicates asternal origin of the paraprocts, and that the ventral plate, that isS9, is actually a free operculum, and thus the secondarily sclero-tised fold of the membrane (Fig. 10d). If this plate was a stern-ite, it would receive intersegmental membranes at both ends.However, other groups of Coleoptera (such as Dascilloidea orScarabaeoidea) do not confirm secondary origin of the respec-tive ventral plate of segment 9. In Dascillus a transition to thestate that is expressed by Peltis can be observed, with a large,secondarily sclerotised but still free plate on the inner side of thetrue S9, the latter still retaining at the sides thin connectionswith the paraprocts. The origin and function of this plate isapparently analogous to that of the tongue-like process of themale pygidium (see p. 151).

A minor form of such a peculiar, trilobed S9 (or a complexplate including laterotergites) is present in Cucujus (Fig. 11b),and the dorsal sclerite, to which this plate articulates, is referredto as T9, not T10 or the proctiger. This appears to be inconsistwhen we compare the T9+S9 capsule of Cucujus with thesimilar capsule of Geotrupes (Fig. 10b), interpreted as having amixed T10+T9+S9 structure.

No evidence is available on the origin of such a peculiar,overdeveloped male 9th segment, and the reasons for its ubiq-uity among Coleoptera. Since this type of 9th segment is largelyextrudable from the abdomen during copulation, it might play arole in the process of eversion and retraction of genitalia and thisfunction might account for such development. The contiguousring could provide a firm tube guiding the genital apparatusduring eversion, as opposed to blood pressure propelling theeversion in the basalmost beetle groups. Likewise, the ring pro-vides for the insertion of the respective retractor muscles, whichcould improve coordination of forces and prevent stretching ofthe genital chamber when the muscles are in tension. The ringmust have evolved very early in the history of beetles, since thefully united paraprocts are widespread in the basalmost lineages


of the Polyphaga (Eucinetoidea, Dascilloidea, Elateroidea,Hydrophiloidea and Staphylinoidea), as well as in theAdephaga. However, the ring remains broadly disjunct dorsallyin the Archostemata, as illustrated by Crowson (1981) forOmma stanleyi Newman. The dorsally united paraprocts occurin those groups possessing eucinetid genital alignment, whichhave no associated sclerotised rods or apodemes (for exampleEucinetus and Dascillus) or have variably long extensions stillconnected or subarticulated terminally with the base of S9 (forexample Cicindela, Silpha, Hydrophilus, Denticollis, Byrrhus,Ceruchus, Geotrupes and so on). However, in the latter groupthe dorsal position of the paraprocts may be different, even iftheir ventral connection with S9 remains the same (for examplein Ceruchus and Geotrupes). Major differences may thenconcern even closely related families, like Lucanidae andGeotrupidae. In the groups with separate (though always con-nected to each other by a membrane) apodemes that are welldeveloped (like Peltis and Allecula), the paraprocts are more orless divided dorsally. This may indicate that the reinforcing roleof united paraprocts lost its significance and various extents oftheir separation became possible following development of theapodemes and associated abductor and retractor muscles chang-ing the mechanism of genital eversion and retraction. Strikingly,in the cucujoids with a non-inverted 9th segment (Byturus,Cucujus), where the mechanism of genital retraction has beenfurther modified due to development of tegminal apodeme(s),the trilobed S9 has become distinctly smaller, with the lobeslateral, not dorsal. Inclusion of the tegmen into the process ofretraction of the male genitalia probably allowed for further

reduction of the segment 9 capsule, followed by its inversionand subsequent reduction of T9 in beetle possessors of thephytophagan genital alignment. Explanations as to why theordinary junction of T9 and S9 was insufficient to form a rigidsegmental ring in the course of beetle evolution are unclear; alonger tube might be necessary to support a mechanical func-tion, a direct junction of ventro-lateral apodeme-like structuresto the ring was required for efficiency, or a sensory function ofthe T9 margin prevented the stronger sclerotisation required formechanical purposes. The trilobed S9 (if laterotergites are dis-regarded as paraproct precursors) itself might have developed tocombine its sensory and mechanical functions, since its medianlobe corresponds to T9 and both constitute the margin of a func-tional abdominal orifice, while the function of united laterallobes is mostly mechanical.

Lymexylon (Fig. 11c) is another example of the seeminglyfree T10. However, judging from the proximity of the rectalopening, the indefinite plate in the position of T10 may be anevagination or extension of the T9 membrane, unless the expla-nation given above for the proctiger can apply here as well.

Both T10 and S10 were observed in the colydine Enarsus(currently Pristoderus) by Sharp and Muir (1912). When exam-ined, Pristoderus showed a complicated puzzle of internal platesbut no trace of the plate corresponding to T10, and the anus wassituated normally behind T9. On the ventral side there is anadditional sclerotised plate between the S9 and the tegmen,apparently S10 as noted by Sharp and Muir (1912). However,the mode of its incorporation into the genital sheath indicates asecondary origin for sclerotisation. The plate has been devel-


Fig. 10. Ninth abdominal segment: (a) Ceruchus (Scarabaeoidea:Lucanidae), dorsal view; (b) Geotrupes (Scarabae-oidea:Geotrupidae), dorsal view; (c) same, lateral view; (d) Peltis (Cleroidea:Trogossitidae).


oped either to reinforce the membrane, displace the associatedfold farther from the S9 margin for perhaps an improvement ofgenitalia eversion, or to provide a kind of hinge with the basalpiece, causing the latter to deflect down when everted. Similarsclerites, located exactly in the same position although usuallymore firmly adjoined to the inner surface of S9, were found inLygistopterus, Byrrhus and Dascillus. Muir (1915, 1918)inferred the sequence of the anus, internal sternites and tergitesand the aedeagus from their spatial position relative to eachother in repose, not from their actual order in the course of thegenital sheath membrane. Thus, some mistakes were madesometimes, such as the anus placed between the author’s inter-pretation of ‘S10’ and the aedeagus in Pristoderus.

Alternative interpretations are available for all extrategminalplates serving as parts of the 10th segment that could supportthe concept of its homology with the tegmen. However, evenmore serious objections to this concept derive from the structureof the larval abdomen and ontogenetic rules of postembryonicdevelopment. First, there is an expectation of a correlation ofsegment number in the larval abdomen with a 9- or 10-seg-mented adult abdomen. The correlation, however, is notunequivocal although the 10-segmented larval abdomen wasrecorded for a majority of beetles having a proctiger (Lawrence1991a). Lawrence et al. (2000) provided several examples of9-segmented larval abdomens in those beetle groups in whichthe male adult has an evident proctiger (for example in someHydrophilidae, Eucnemidae, Elateridae, Nosodendridae,Scarabaeidae). Considering the position of the proctiger, alwaysanterior to the anus in the course of abdominal segmentation,this would seem a further argument against its homology withT10. However, the 10-segmented larval abdomen is consideredancestral (Lawrence 1991a), and is recorded (Lawrence et al.2000) in chrysomeloids, curculionoids, and cucujoids, of whichonly Byturus has a recognisable proctiger. This raises a seriousobjection to the concept of the tegmen being equal to segment10. Since the anus is primitively and almost invariably terminal

in the larvae, a mechanism explaining how it could ‘move’ itsopening to the membrane of T9 in the male adult is not available.Thus, considering any part of the tegmen homologous with T10seems implausible. Even though the metamorphosis undoubt-edly causes radical changes to the insect body in the pupal andadult stages, such a ‘jumping’ anus seems rather unlikely.Moreover, since the entire genitalia develop from the area oflarval epidermis situated at or close to the posterior margin ofS9, the homology of subsequent larval segment with the tegmenoriginating from the developing genital invagination becomesproblematic. That is, unless we misinterpret the part of thebeetle larval abdomen situated behind the last visible constric-tion as the 10th segment. Because of commonly missing or ill-defined sternal and tergal plates in the larva, and equallycommon modifications of the posterior larval body that isdevoid of typical segmental structures like spiracles or nervousganglia, the pattern of segmentation is much more uncertainthan in the adult, and segments are inferred from superficialexternal lines and constrictions. Actually the 10th larvalsegment always has a notably different shape and structure fromthe 9th one, being small to vestigial, divided into a variousnumber of fields, lobes or papillae surrounding the anus, and isdevoid of appendages such as urogomphi, which are alwaysassociated with the 9th segment when present (Crowson 1960;Lawrence 1991a). Its true nature remains uncertain and is prob-ably complex. It may even be a membrane of segment 9, or theevaginated membrane of the rectum itself, despite its segment-like appearance or development of pygopods in some taxa. Thismight be the case for weevils in which the anus is surrounded bya varied number of lobes (two, three or four), the segmentalnature of which remains uncertain. Brenda May, the greateststudent of weevil larvae, always referred to the terminal part ofthe larval abdomen as anal lobes or the anus as such (forexample May 1993, 1994), not as the true 10th abdominalsegment. If a true segment 10 is really present in the larvalabdomen of weevils or other beetles, so that the anus is poste-

E

PM

R

(T10?)

AE

S8

S9

T9

T8

LT9

AE

PM

BP

ed

BP(S10?)

S9

T9

segment 8

segment 9

pr

pr

ps

R

(a)

(c)

(b)

Fig. 11. (a) diagram of genital alignment (eucinetid type) in Geotrupes (Scarabaeoidea:Geotrupidae);(b) 9th abdominal segment of Cucujus (Cucujoidea), ventral view showing trilobed S9; (c) 8th and 9thabdominal segments of Lymexylon (Lymexyloidea), dorsal view.


rior to it, and the genital anlage anterior to it, developmentalbiologists would advise us to forget the homology of the tegmenwith the 10th abdominal segment.

The aedeagus is usually interpreted as a secondary out-growth of the ejaculatory duct, having nothing in common withabdominal segmentation. However, like the tegmen, the aede-agus possesses several characters that may indicate a segmentalorigin. In weevils and other beetles (such as Chrysomeloidea,Dascilloidea and Eucinetoidea) the aedeagus primitively con-sists of two plates: a dorsal tectum and ventral pedon, which areeither fully separated by a lateral membrane, or connate only attheir bases. The flagellum, a secondary structure originatingfrom the ejaculatory duct (as suggested for the entire aedeagus),never develops into a distinctive pair of dorsal and ventralplates. Even the coccinellid sipho, being an overdeveloped flag-ellum replacing aedeagal function, forms a simple sclerotisedtube showing no trace of a two-plated structure. Imaging tripli-cation of a simple tube of the ejaculatory duct and developmentof such complex, double-telescoping tubes in primitive beetleswithout an evolutionary background of segmentation is diffi-cult. Like the preceding tegmen, the aedeagus is incorporatedinto the abdominal membrane of the genital sheath, which isattached to the bases of the tectum and pedon, and continued atthe apical orifice to form a terminal invagination, the endophal-lus. Moreover, during development of male beetles from pupae,the aedeagus originates from the primary fold of the genitalinvagination, as does the tegmen. Thus, if the tegmen is consid-ered the 10th segment, consequently the aedeagus would be the11th. The objections to involvement of the 11th abdominalsegment in the development of the aedeagus are the same asthose listed above against tegminal homology with the 10thsegment. If these arguments are confirmed, thoughts on a seg-mental origin of the aedeagus should be abandoned.

The most significant discrepancy between postulatedhomologies for the genitalia discussed above, from the currentviews on beetle development, concerns the replacement of theanus with the gonopore at the terminal body position. A termi-nal anus is an ontogenetic, and to some extent philosophical,paradigm resulting from the study of insect embryonic develop-ment. The beetle starts its development as an 11-segmentedembryo, and ends up as a 9-segmented adult, passing throughlarval instars and a pupal stage, with the loss of the last twoabdominal segments during the process. Ideas about the homol-ogy of beetle genitalia with these two lost segments must soundcontroversial to anybody working on insect development, asthey did to Muir in 1915. Accepting the homology would meanaccepting a displacement of the terminal embryonic position ofthe anus to the membrane of the 9th abdominal segment in theadult, if we consider that those two following segments areretained. Such structural change is difficult to accept from adevelopmental point of view, unless a kind of peculiar evolu-tionary ‘trick’ is invoked, combined with selective pressure forfunctional terminalisation of a single gonopore in the earlyhistory of Pterygota. Unlike in larvae, in adult beetles the func-tional terminal anus seems disadvantageous compared to a func-tional terminal gonopore in terms of evolutionary profits. Asingle terminal gonopore allowed development of specialisedmale copulatory organs and mechanisms of direct sperm trans-fer, as well as a specialised ovipositor in the female. These adap-

tations must have been especially desirable in beetles with an‘armoured’ body and terminal abdominal parts concealedwithin the abdomen. Therefore, terminalisation of the gonoporecould have been one of the more important conditions explain-ing the evolutionary success of beetles in terms of diversity oftheir life modes and species richness. According to longaccepted developmental theories, this terminalisation of geni-talia is purely functional, and it must have been preceded byreduction of the last two abdominal segments in the adult. Anyevolutionary ‘event’ leading to structural terminalisation musttherefore explain how the two terminal abdominal segmentscould ‘survive’ the metamorphosis and reappear behind the anusin the adult. A reduction of the 10th and 11th abdominal seg-ments to the respective undiversified imaginal disc in a maturelarva, and its subsequent development into genital segments inthe adult, could explain this process, although with objectionsfrom developmental biologists. Among the extant hexapodgroups, proturans exhibit developmental changes in segmenta-tion, where abdominal segments 9, 10, and 11 are subsequentlyadded between the 8th segment and the terminal telson duringanamorphic development (Chapman 1998). The telson is absentfrom derived insects or retained only in the embryo of somegroups (Richards and Davies 1977), hence such a process wouldbe a terminal addition of segments in beetles. There must againbe a group of cells from which the missing segments develop inthe Protura, but since the anus remains terminal after complet-ing the anamorphosis, logically these cells must form a ringaround the rectum. This seems a basic difference between pro-turans and beetles, in which the genitalia anlage lies entirely onone side of the rectum, leading to an anus that is either terminalin proturans, or situated behind the 9th segment in adult beetles.Such a change from a concentric to a side-by-side arrangementof the rectum and genital chamber in the early evolution ofinsects is problematic, but perhaps not impossible. If this rear-rangement happened, it would certainly be advantageous, as itwould directly allow for terminal genitalia. Perhaps proturanslook like proturans today because of their retention of a termi-nal anus. Evolution more frequently involves existing bodystructures and mechanisms for novelties than new ones, so theconversion of the last two abdominal segments into genitalstructures could have taken place, but requires a plausiblemorphological mechanism.

The above assumptions will be found by many to be too far-fetched. My intention is not to ‘revolutionise’principles of insectdevelopment, no

alignment and homology of male terminalia in curculionoidea ...franz/weevilcourseresources/...male...

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