Orthoptera). Part 1: General Concepts and Origin Эволюция И Таксономическое Значение Копулятивного Аппарата У Длинноусых Прямокрылых (Orthoptera: Ensifera

ZOOSYSTEMATICA ROSSICA, 23(2): 197–209 25 DECEMBER 2014

Evolution and taxonomic significance of the copulatory apparatus in Ensifera (Orthoptera). Part 1: General concepts and origin Эволюция и таксономическое значение копулятивного аппарата у длинноусых прямокрылых (Orthoptera: Ensifera). Часть 1: Общие положения и происхождение

A.V. GOROCHOV

А.В. ГОРОХОВ

A.V. Gorochov, Zoological Institute, Russian Academy of Sciences, 1 Universitetskaya Emb., St Petersburg 199034, Russia. E-mail: [email protected]

The importance of using copulatory characters in generic and higher taxonomy (not only in species taxonomy) is discussed in the light of the recent “genital clock” concept which should partly replace the old “lock-and-key” theory. This concept assumes that evolutional changes in the copulatory apparatus (if it is sufficiently complicated) follow after genetic drift, and that these processes occur at a more uniform rate than changes in the characters of external morphology, ecological properties and many other biological traits, since structure of this apparatus is less dependent upon the situation in the ecosystem. Evolution of the copulatory apparatus in the suborder Ensifera and in its ancestors may be divided into three hypothetical stages reflected in some morphological features: 1) a highly hypothetical stage without copulation and without a copulatory apparatus in the most ancient (extinct) orthopteroid insects; 2) the appearance of different organs in early Orthoptera serving for fixation of partners during copulation and for insertion of the spermatophore in the female genital chamber; 3) the development of complicated organ with consolidation of these functions. Важность использования копулятивных признаков в родовой и высшей таксономии (не только в видовой таксономии) обсуждена в свете современной гипотезы о «гениталь- ных часах», которая должна частично заместить старую теорию «ключа и замка». Эта гипотеза предполагает, что изменения копулятивного аппарата (если он достаточно сло- жен) следуют за генетическим дрейфом, и что эти процессы идут с более равномерной скоростью, чем изменения в признаках наружной морфологии, экологических свой- ствах и многих других особенностях биологии, поскольку строение этого аппарата ме- нее зависимо от ситуации в экосистеме. Эволюция копулятивного аппарата в подотряде длинноусых прямокрылых (Ensifera) и у его предков может быть подразделена на три гипотетические стадии, отраженные в некоторых морфологических чертах: 1) высоко гипотетическая стадия без копуляции и без копулятивного аппарата у наиболее древних (вымерших) ортоптероидных насекомых; 2) появление разных органов у ранних прямо- крылых, служащих для фиксации партнеров при копуляции и для введения спермато- фора в генитальную камеру самки; 3) развитие сложного органа с консолидацией этих функций. Key words: copulatory apparatus, evolution, morphology, paleontology, taxonomic importance, Orthoptera, Ensifera Ключевые слова: копулятивный аппарат, эволюция, морфология, палеонтология, таксо- номическое значение, Orthoptera, Ensifera

INTRODUCTION RESULTS

The sexual traits are among the most The primary and secondary sexual important characters used in biological characters and intraspecific stability taxonomy. In botany, they have been used The widely accepted subdivision of the for species-level and higher classifications sexual characters into primary and second- since Linnaeus’s times, whereas in zool- ary ones may be based on the sequence of ogy, the importance of these characters their historical development, on their im- was realized with some delay. This delay portance in individual development or on is especially distinct in taxonomy of some their importance for reproduction (Zava- groups of orthopteroid insects. Many of dovskij, 1922; Ghilarov, 1989: the articles the old descriptions and keys to the order “Primary sex characteristics” and “Second- Dermaptera, suborder Blattina, superfam- ary sexual characteristics”). The first two ily Grylloidea, and some other groups are principles force us to use the name “primary” almost unsuitable for the species and ge- for only characters of the gonads, some ac- neric identifications. Moreover, at present cessory sex glands, and their ducts, since all some specialists use the sexual characters the other sexual characters (including the mainly in species taxonomy but try to find penis and the ovipositor) appeared later, or mainly non-sexual characters for generic their appearance may have been caused by taxonomy (Otte & Alexander, 1983; Ke- the activity of the above-mentioned glands. van & Jin, 1993; Nickle, 2003; Liu & Zhou, Thus, these principles are not in accor- 2007). Their opinion may reflect the old dance with the most common views, but idea that sexual characters should not be consistent use of the third principle (the used in generic taxonomy since they are principle of importance for reproduction) is present in only one of the two sexes (Bey- also not exactly congruent with these views. Bienko, 1971). This idea has no sufficient Reproduction is almost the only function scientific ground, but for substantiation of of the genitalia, gonads and other internal an opposite idea, it is necessary to propose sexual organs of higher animals (under the more logical hypotheses for explanation of natural conditions, organisms which have the following phenomena: the presence lost these organs can survive but not re- of a certain stability of sexual characters produce); the characters of these organs are in the same species in many cases; the ab- usually termed “primary” sexual characters. sence of such stability in other cases; the All the other morphological sexual charac- presence of distinct sexual differences ters of these animals are considered “second- between some species which are very simi- ary” ones; many of them are associated with lar in other characters; and the absence of two or more principal functions (the repro- these differences between some species ductive function being only one of them: for showing distinct differences in non-sexual example, an increase in the body size of the characters. These hypotheses must be con- males of some mammals reduces the pres- sistent with the recent knowledge about sure of predators and also helps in sexual the general regularities of evolutionary competition) or are not critically important process and with the evolutionary trends for reproduction (their disappearance may revealed during the study of concrete taxa. destroy the potential for sexual competition The paper is based on the material on but not for reproduction itself: development this topic presented by the author at the of antlers, tusks, or a mane only or mainly 10th International Congress of orthopter- in male). However, some other “second- ology (21–25 June 2009, Antalya, Turkey) ary” sexual characters are also very impor- and briefly mentioned in the abstract of this tant for reproduction of higher animals, as presentation (Gorochov, 2009). these animals cannot have any reproductive

© 2014 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 23(2): 197–209 A.V. GOROCHOV. COPULATORY APPARATUS IN ENSIFERA (ORTHOPTERA). 1 199 success under natural conditions without ent individuals to have the widest choice of sexual behavior and/or attractive signal- sexual partners and to form their posterity ization; moreover, there are special organs with the minimal breach of its development participating only or mainly in the actions during the most vulnerable early stages (for connected with reproduction: the tail in the example, the stability of the ovipositor struc- male of peacock, the sound-producing or- ture ensures the most similar conditions for gans in many animals, and some others. oviposition and thus for egg development). The use of this classification of sexual This stability is so important for the repro- characters for lower animal (invertebrates) ductive success of the species that natural leads to additional difficulties. The male selection supports such stability, although copulatory apparatus of some insects is in many cases this selection supports certain rather complex; it includes the structures diversity in other structures (such diversity adapted to insertion of the spermatophore allows species to have certain preadaptations tube into the spermathecal duct (somewhat to different changes of the environment). Di- analogous to the penis in mammals) as well versity in sexual characters may also be use- as the structures used for fixation of the fe- ful since some of these characters belong to male during copulation (the epiphallus and the special structures participating in sexual ectoparameres in the genitalia of Gryllidae, competition, and their strong development the cerci in most Tettigoniidae, hooks on in some individuals may disrupt their cryptic the paraprocts and abdominal tergites in appearance and reduce their survival during many representatives of Stenopelmatoidea, increasing predator pressure. So, it seems to the characteristic claspers formed from dis- me that it is reasonable to divide all sexual tinctly curved hind tibiae and strong ventral characters into primary and secondary ones teeth of the hind femora in some Ensifera on the basis of their stability within the same and Phasmatoptera, and specialized attach- species. Such a classification is somewhat ment organs of the fore legs in diving bee- different from the most commonly accepted tles). If one classified all the characters of the one, but it may more exactly reflect the im- structures mainly adapted to this fixation portance of these characters for reproduc- as “secondary” ones (because in higher ani- tion. This approach still faces some problems, mals, this function is usually performed by as it permits the presence of intermediate unspecialized organs), then the characters of variants; for example, the characters of the gryllid male genitalia would be divided into male stridulatory apparatus in many repre- “primary” and “secondary” ones; moreover, sentatives of Grylloidea and Tettigonioidea in some cases parts of the same structure are usually stable and may be considered pri- participating in the female fixation as well mary sexual characters, but in some of them as in the spermatophore tube insertion (the having two or three morphological forms ectoparameres of some gryllids) would have (f. macroptera, f. brachyptera and intermedi- to be classified as “secondary” and “primary” ate one) there are certain differences in the characters at the same time. Another prob- size of the sound-radiating areas within the lem appears if one attempts to divide the same species (due to some reduction of the characters of the fixing devices into “sec- tegmina in the latter forms). ondary” or “primary”, as it is necessary to Interspecific sexual differences: find an objective criterion for establishing a the “lock-and-key” and “genital clock” sufficient (for this division) level of repro- hypotheses ductive importance of these characters. One of these criterions may be the value In many animals (including most in- of variability in sexual characters within the sects), the sexual characters having a cer- same species. A certain stability of the most tain intraspecific stability and distinct important sexual characters allows differ- interspecific differences at the same time

© 2014 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 23(2): 197–209 200 A.V. GOROCHOV. COPULATORY APPARATUS IN ENSIFERA (ORTHOPTERA). 1 belong mainly to the copulatory appara- similar and may be considered more or less tus. To explain these characteristics of the constant as compared to the rate of chang- copulatory apparatus, the “lock-and-key” es in many non-sexual or secondary sexual hypothesis was proposed. This hypothesis characters. In the environment highly com- supposes that this apparatus functions as petitive for a concrete species, the change one of the isolation mechanisms prevent- of its life form is very difficult because all ing interbreeding of sympatric species (for accessible adaptive areas are occupied by additional information about this hypoth- numerous species with high competitive esis see Rentz, 1972). The absence of any ability. The adaptive evolution under such distinct differences in the copulatory ap- conditions proceeds slowly, without quick paratus of many sympatric species may be changes in important adaptive characters, explained by the presence of some other and the genetic drift is reflected mainly in isolation mechanisms (behavioral, acoustic, the change of characters less closely associ- visual, and others). However, this hypoth- ated with the environment, for example, in esis cannot explain the presence of distinct the structure of the male genitalia (Goro- differences in the copulatory apparatus of chov, 2001a). In the less competitive envi- many closely related allopatric species and ronment, this species may have quick adap- of many closely related species which pos- tive radiation, since change of its life form sess additional isolation mechanisms (for can happen easily (because of the absence example, acoustic ones) preventing inter- or a small number of serious competitors). specific copulation. Moreover, although At the same time, the characters less closely the presence of copulatory isolation mecha- connected with the environment (for exam- nisms must be especially important for the ple, the structure of the copulatory appara- most closely related species, these species tus) have a more stable rate of changes, simi- usually do not have any distinct differenc- lar to that of the genetic drift, and therefore es in copulatory apparatus; also, although this rate may be distinctly slower than that copulatory isolation mechanisms seems to of the characters more closely connected be less important for remotely related spe- with the environment. These two types of cies (for example, from different genera) be- evolution correspond to the “coherent evo- cause they usually have greater differences lution” and “non-coherent evolution” con- in their behavior and ecological preferences cepts, respectively (Krassilov, 1969). strongly reducing the possibility of inter- Thus, changes in the compound com- specific copulation even without special plex of primary sexual characters as well as copulatory isolation mechanisms, but such the molecular changes may be considered a species have more distinct differences in the certain kind of biological clock. This con- copulatory apparatus. clusion is important for taxonomy since it These facts have allowed me to propose a means that bigger differences in these char- somewhat other explanation for the above- acters are evidence of older divergence be- mentioned characteristics of the copula- tween species. This regularity is certainly tory apparatus (Gorochov, 2005) which is not absolute, but it allows one to imagine referred to herein as the “genital clock” hy- (very roughly) the process of species di- pothesis. It does not reject the “lock-and- vergence as the following sequence: (1) key” hypothesis but distinctly limits its subdivision of a single species into several application. The “genital clock” hypothesis very closely related ones having indistinct supposes that the rate of changes in the com- (invisible) changes in the complex of their plex of primary (stable) sexual characters (if primary sexual characters and using the iso- this complex is sufficiently complicated: for lation mechanisms not connected with this example, in the compound copulatory appa- complex (this stage is present in many spe- ratus) and the rate of genetic drift are rather cies of the cricket subgenus Thliptoblemmus

Saussure, 1898 and in all species from many and one belonging to the female. The copu- genera of Acrididae); (2) gradual formation latory and communicative components of of small but distinct interspecific differences this system are also divided into two parts, between such complexes in the descendants which may be very unequal. Usually the of the above-mentioned species with simul- male has the more significant part of these taneous stabilization of these complexes in components which include numerous and each of these species (this stage is charac- often compound structures; in this case, the teristic of most species from many genera of female may have only one simple structure Gryllidae and from some genera of Tettigo- or a few ones (many representatives of Tetti- nioidea and Stenopelmatoidea; it is possible gonioidea and Grylloidea). The latter struc- that the copulatory apparatus may begin to ture (or structures) has a limited ability to function as an additional isolation mecha- form of different modifications, as many nism only at this stage); (3) slow develop- of them almost inevitably recur (includ- ment of big and very big differences between ing partial return to the ancestral condi- the complexes of primary sexual characters tion). Such simple structures (for example, accompanied by their intraspecific stabili- the copulatory papilla in Gryllidae) do not zation (such differences characterize relat- provide any good characters for generic and ed subfamilies, families, orders, etc.; for very higher taxonomy. If the female has only sim- high-ranked taxa, establishment of homolo- ple copulatory and communicative devices, gies in these complexes is often very diffi- it is necessary to use mainly the male sexual cult or even practically impossible). If this characters; but if these devices are rather hypothesis is correct or even partly correct, simple in both sexes (some Stenopelmatoi- the primary sexual characters (for example, dea), the use of characters of these devices those of the copulatory and stridulatory in generic and higher taxonomy is rather dif- devices if the latter device is specialized to ficult owing to numerous parallelisms. sexual communication) must be necessarily It should be added that the simple struc- used in the generic and higher taxonomy, as ture of such devices may create the illusion the total value of their differences may indi- of little divergence between species, since rectly reflect a total value of genetic differ- the evolutionary drift of the characters of ences between the species more adequately these devices may be imagined as prolonged than most of the other characters often used fluctuations (“Brownian motion”) near the in taxonomy. once established successful variant. Some However, the latter conclusion is only compound complexes of primary sexual valid for compound complexes of these characters may remain stable for longer characters or their significant parts, because time than some others (for example, the such complexes and parts are less subjected gonads and sometimes the stridulatory ap- to parallel evolution than many other com- paratus in comparison with the copulatory plexes (for example, less compound com- apparatus). This situation is possibly con- plexes or complexes of adaptive characters). nected with the usefulness of stability in The combination of all the primary sexual such complexes, if their characters are in characters (including the stable sexual char- highly balanced condition with respect to acters of the stridulatory apparatus, dif- each other and to the non-sexual complexes ferent attractive glands, and devices for of high adaptive significance. For example, fixation of partners during copulation) in the male tegmina of the gryllid genus Trelli- dioecious species may be regarded as a cer- us Gorochov, 1988 have two main functions tain system, which is comparable to the di- (one of them is highly adaptive to the en- gestive, nervous or circulatory systems but vironment and thus important for preserva- differs from them in being divided into two tion of the life form, while the other is sexu- unequal parts: one belonging to the male, al, communicative), and changes in its com-

© 2014 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 23(2): 197–209 202 A.V. GOROCHOV. COPULATORY APPARATUS IN ENSIFERA (ORTHOPTERA). 1 pound tegminal stridulatory apparatus are attachment to the substrate (Fig. 1, a), and strongly slowed down since these changes in the female, for searching the spermato- would be practically impossible without phore on the substrate and for controlling corresponding changes in the structure of its fixation in or near the female gonopore other parts of the tegmina and thus in their (Fig. 1, g). Among the later representa- adaptive characteristics. tives of Pterygota, such styli were found in the males of Ephemeroptera and ancient Early evolution of sexual characters roaches (Vishnjakova, 1971); however, in in orthopteroid insects the first order these styli have changed into The spermatophore of Arthropoda, in copulatory hooks (Fig. 1, b), and in the lat- accordance to the widely known theory by ter insects, the styli possibly had a different Giljarov (1970), appeared independently sensory function associated with the pres- in different groups during their adaptation ence of the copulatory structures (Fig. 1, c). to life on land. It is most probable that the The shortened remnants of such styli were spermatophore was initially transferred also preserved in some taxa of Pterygota: as from male to female without copulation. copulatory sensory structures in the male This method of spermatophore transfer is (many recent representatives of Dictyop- preserved in very primitive apterous insects tera and Orthoptera), as sensory structures (Thysanura) and in some terrestrial repre- participating in control over the position of sentatives of other classes of Arthropoda. the ovipositor apex during oviposition in There are also indirect evidences suggest- the female (Fig. 1, h, i), and as rudiments ing that the copulatory apparatus was origi- in female nymphs (Fig. 1, j, k). The lat- nally absent in some earliest representatives ter nymphal rudiments are now present in of Pterygota and independently formed in Grylloblattida and in some other groups of some oldest branches of this subclass. One Polyneoptera, but they are absent in adult such evidence is the development of a “sec- females of all the known (recent and fos- ondary penis” from processes of the second sil) representatives of Polyneoptera (with and third abdominal sternites in the male of the only exception of Tarragoilus Goro- Odonata (the male transfers sperm to this chov, 2001, one of the recent hagloid genera copulatory device from its own gonopore). with a reduced, almost nymphal ovipositor; It is considered (Bechly et al., 2001) that Gorochov, 2001b); nevertheless their pres- such a copulatory device could have ap- ervation may be explained by the great im- peared only in case of the original absence portance of sensory styli for the females of of copulation in an ancestor of the recent the earliest orthopteroid insects. taxa of Odonata (possibly the male of this The recent hypothesis about early evo- ancestor began to attach its spermatophore lution of the infraclass Polyneoptera (=or- not to any surrounding substrate but to its thopteroid insects) (Gorochov, 2004), own body surface). based on analysis of recent and fossil ma- Another evidence is the characteristic terials, supposes that the common ancestor structure of abdominal sexual organs in the of Polyneoptera may have had the follow- male and especially in the female visible on ing sexual characters: the coxopodites of some oldest (Carboniferous) imprints of the 9th abdominal sternite of the male were Pterygota from the orders Palaeodictyop- approximately the same as those of Gryl- tera and Meganeurida (Brauckmann, 1991; loblattida, ancient roaches (Vishnjakova, Bechly et al, 2001). The long and possibly 1971), and the possible representatives of segmented styli of these insects may have Eoblattida (Vilesov & Novokshonov, 1993), functioned as sensory organs serving in the i.e. not fused with this sternite and with one male for assessment of the substrate condi- another (Figs 1, c–f); the styli situated on tions and spermatophore position during its these coxopodites were long and segmented

Fig. 1. Scheme of abdominal apex in some fossil and recent Pterygota (after Gorochov, 2004). a, b, male, lateral view: (a, Namurotypus (Meganeurida), Carboniferous; b, recent Ephemeroptera); c–f, male, ventral view: (c, Aktassoblatta (Dictyoptera), Jurassic; d, recent Grylloblattida; e, Blattogryl- lus (Grylloblattida), Jurassic; f, Tillyardembia (Eoblattida?), Permian); g–i, female, lateral view: (g, Homoioptera (Palaeodictyoptera), Carboniferous; h, Permuralia (Diaphanopterida), Permian; i, recent Odonata); j, k, recent Grylloblattida, lateral view: (j, protonymph of female; k, deutonymph of female). Abbreviations: 8g, 9g, gonapophyses of 8th and 9th abdominal segments; 8s, 9s, 8th and 9th abdominal sternites; 8t–10t, 8th–10th abdominal tergites; c, coxopodite of 9th abdominal segment; ce, cercus; e, epiproct; p, paraproct; pc, paracercus; st, stylus.

(as in Fig. 1, c); the male genitalia consisted folds or areas near them and for structures of only membranous folds around the gono- of female genital chamber), participated pore (the name “genitalia” is used here only mainly in the formation of the spermato- for the structures originating from these phore, and were probably more or less ho-

© 2014 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 23(2): 197–209 204 A.V. GOROCHOV. COPULATORY APPARATUS IN ENSIFERA (ORTHOPTERA). 1 mologous to the “penis” of Thysanura; in teran orders: their copulatory structures are the female, the 8th abdominal sternite was very different, and no homologies between well developed (it is absent or strongly re- many of them (Dictyoptera, Dermaptera, duced in the recent females of Polyneop- Phasmatoptera, etc.). Moreover, even with- tera except Grylloblattida and probably in a single order Orthoptera (which is one Mantophasmatodea), the operculum was of the old orders known since the Late Car- absent (this structure is often named “geni- boniferous) it is possible to propose three tal plate” or “subgenital plate”, but these variants of the appearance of copulation names are also used for a different structure and the copulatory apparatus: they could in the male), and the 9th abdominal sternite have appeared (1) in the ancestors of this and its coxopodites were presented by the order before its separation, (2) in an ancient parts of the ovipositor which was more or species of Orthoptera ancestral to all the re- less similar to that of Grylloblattida; the cent taxa of this order, or (3) independently upper valves of ovipositor were shorter in a few extinct representatives of Orthop- than other valves (gonapophyses) and had tera ancestral to the different recent higher free, rather long, and articulated styli at the taxa of this order. apex; the copulatory structures for fixation of the partner and stridulatory organs for General trends in the evolution of its attraction were absent in both sexes. The the ensiferan copulatory apparatus sexual characters listed above are mainly The suborder Ensifera is an oldest sub- the primary ones; they belong to the organs order of the order Orthoptera; it is consid- which may provide the formation and non- ered as ancestral for the suborder Caelifera copulative transfer of the spermatophore (Sharov, 1968; Gorochov, 1995). The struc- as well as oviposition. There are no other ture of the copulatory apparatus in the most grounded ideas about the sexual characters ancient, Carboniferous ensiferans is un- in the earliest orthopteroid insects. known. Their abdominal sexual characters The hypotheses about the origin and were possibly more or less similar to those phylogeny of the orders of Polyneoptera of the above-mentioned hypothetical an- proposed in the same publication (Goro- cestor of Polyneoptera. However, the Early chov, 2004) provide an additional morpho- Permian representatives evidently had a logical basis for the old idea of holophyly of copulatory apparatus similar to that of some this infraclass (this idea was also supported primitive recent ensiferans: the male genital by the recent paleontological and molecu- plate consisted of the coxopodites and the lar data: Rohdendorf & Rasnitsyn, 1980; 9th abdominal sternite fused together; the Rasnitsyn & Quicke, 2002; Whiting et al., styli were short and unarticulated; the male 1997; Whiting, 2002) and show that these cerci were unspecialized, lacking hooks and orders diverged from each other during or processes; the male genitalia were probably around the Carboniferous (Fig. 2), with the membranous, consisting of membranous possible exception of two smaller taxa with folds for spermatophore formation (Goro- a very obscure origin: the “order” Embiop- chov, 1995). Some females of that time, tera and the enigmatic taxon Mantophas- judging by the material of Sharov (1968) matodea (in Fig. 2, the latter taxon is ten- and my original data, probably had a devel- tatively included in Titanoptera). Thus, the oped 8th abdominal sternite (as in recent great age of these (large) orders allows one grylloblattids) and no genital plate (this to suppose that in each of them (or in each plate in Orthoptera and the operculum in superorder at least), the copulatory appara- Phasmatoptera evidently have independent tus appeared independently. Some support origins), but their imaginal ovipositor had of this opinion comes from the structure of the upper valves (the coxopodites of the this apparatus in the different polyneop- 9th abdominal sternite) not shorter than

Fig. 2. Paleophylogram of Polyneoptera (after Gorochov, 2004) [order of isolation of two superor- ders and four orders from Eoblattida and Titanoptera is not clear]. the other valves of the ovipositor and was tive superfamily Hagloidea and in many lacking the styli. recent groups in all the other main phylo- Based on the morphological study of nu- genetic lineages (Tettigonioidea, Stenopel- merous recent ensiferans, Gorochov (1984) matoidea, and Grylloidea) which probably supposed that the male genitalia originally originated from Hagloidea. If the common consisted of only two main membranous ancestor of all these taxa had copulation, folds around the gonopore: dorsal fold and its male copulatory device may have origi- ventral fold (Fig. 3, a, b). These folds partic- nated from some structures other than geni- ipated in spermatophore formation which tal ones: from specialized processes or hooks took place inside the cavity between them. of the hind abdominal tergites (as in some This hagloid type of male genitalia is pres- recent representatives of Stenopelmatoi- ent in all the recent species of the primi- dea), from processes of the paraprocts (as

Fig. 3. Scheme of male genitalia (partly after Gorochov, 1984, 1995), dorsal view (upper row) and sagittal section (lower row) [sclerotized parts dotted]: a, b, hagloid type; c–e, grylloid type (c, d, simple variant; e, complicated variant); f–j, tettigonioid type (f, g, simple variant; h, i, complicated variant characteristic of Gryllotalpa and partly convergent to complicated variant of grylloid type; j, same but without distal part of epiphallus). Abbreviations: d, dorsal fold; e, epiphallus; g, rachis (= guiding rod); s, spermatophore cavity; t, titillators (= small sclerites of dorsal fold: in Gryllotalpa, larger proximal titillator is named epiphallus, and smaller titillators on apical part of dorsal fold together with this apical part form rachis); v, ventral fold. in recent species of Hagloidea and some short sensory styli at the male subgenital recent groups of Stenopelmatoidea and plate of many ensiferan taxa (from all re- Grylloidea) or of the subgenital plate (as in cent superfamilies except Grylloidea) lack- some recent species of Hagloidea, Tettigo- ing any special device for exact orientation nioidea, and Grylloidea), from the special- of the spermatophore aperture opposite fe- ized epiproct (as in many species of Tettigo- male spermathecal opening, since a possible nioidea), and/or from the cercal hooks (as function of such styli is the control over the in most Tettigonioidea and some genera of position of the ventral half of the male ab- Grylloidea). The latter origin of the male dominal apex during copulation (this con- copulatory device is less probable for this trol is necessary for the exact orientation ancestor, as the cerci of all the ancient fossil of the spermatophore aperture; Fig. 4, a, b). ensiferans with known abdominal apex are This function of the male styli in the ances- not hooked. The female of this ancestor may tor (ancestors) of all the recent ensiferans have had some copulatory cavities, process- appeared probably to ensure copulation, es, rough areas, and other catches on the ex- and the establishment of contact between ternal part of its abdominal apex serving for the copulatory structures of the partners fixation of the male copulatory structures. led to the shortening of these styli and pos- However, no visible traces of these hooks sibly whole subgenital plate (its shorten- and other catches in the rare Palaeozoic im- ing could be one of reasons of fusion of its prints of the ensiferan abdomen. components: the sternite and coxopodites). Such a copulatory apparatus may have If male genitalia acquire fixing devices pro- appeared once or more than once, but in viding such orientation of the spermato- either case, it is most probable that in the phore aperture, or if additional structures male, it was originaly represented only by for fixation of the ventral half of the male the structures of the dorsal half of the ab- abdominal apex appear, the sensory styli dominal apex, i.e. by tergal, paraproctal, usually become reduced or disappear (the and/or epiproctal specializations. This as- ventral fixation of the male abdominal apex sumption follows from the preservation of and its dorsal fixation in two places create

Fig. 4. Scheme of abdominal apices of male (white) and female (black) during copulation, ventral view (position of spermatophore aperture is designated by small cross; position of spermathecal opening, by small circle): a, normal copulative position with styli touching base of ovipositor (position of aperture of spermatophore located within male genitalia and position of spermathecal opening coinciding with one another); b, possible displacement of ventral half of male abdominal apex in relation to female one (positions of above-mentioned aperture and opening not coinciding with one another); c, rigid attachment of ventral half of male abdominal apex to ovipositor base by lateral processes of genital (=subgenital) plate (styli disappear). Abbreviations: c, cercus; h, copulatory hook of dorsal half of male abdominal apex; o, ovipositor; p, lateral process of genital (=subgenital) plate; sg, genital (=subgenital) plate; st, stylus. a rather rigid triangle preventing displace- talia. This sclerotization is named “epiphal- ment of the spermatophore aperture during lus”. It is probable that the grylloid type of copulation; Fig. 4, c). Such dependence of genitalia (and thus of the epiphallus) ap- the presence or absence of styli on the struc- peared independently in different families ture of the male copulatory apparatus is not of Grylloidea and in some representatives absolute; it is only one of the general trends of Stenopelmatoidea and Tettigonioidea. In in the evolution of this apparatus, and some the primitive grylloid genitalia (Fig. 3, d), other variants are possible (for example, this lobe may be almost semimembranous control over the position of ventral half of and have more sclerotized small structures the male abdominal apex may be ensured by not isolated from the epiphallic main body the sensory hairs of the subgenital plate, in and not articulated with it (some species which case reduction and disappearance of of Meconematinae, Gryllacridinae, and the styli are also possible; another example Rhaphidophoridae). In the more special- is one species of Cyphoderris Uhler, 1864 ized grylloid genitalia, the epiphallus is which has partly duplicating devices at the more sclerotized, and the ventral surface male subgenital plate: the normal sensor of the dorsal fold forms a special median styli and copulatory hook between them). process (Fig. 3, e) named the “guiding rod” The first variant of reduction and disap- (Alexander & Otte, 1967) and probably en- pearance of the styli is often forced by devel- suring of the insertion of the spermatophore opment of the grylloid type of male genitalia, apex (with the aperture) into the female and the second one is sometimes observed spermathecal opening (such genitalia are in the male genitalia of the tettigonioid type. characteristic of some primitive represen- The grylloid type is characterized by general tatives of Gryllidae and Arachnocephalini, sclerotization of the dorsal fold (Fig. 3, c–e) but also of the specialized genus Euanisous which is membranous in the hagloid geni- Hebard, 1922 from Meconematinae). The

© 2014 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 23(2): 197–209 208 A.V. GOROCHOV. COPULATORY APPARATUS IN ENSIFERA (ORTHOPTERA). 1 highly specialized grylloid genitalia have similar to the grylloid type (Gryllotalpidae articulated sclerites for the fixation of the and possibly Malgasiinae). Appearance and female copulatory structures, and/or a very complication of tettigonioid genitalia, i.e. long guiding rod for the deep insertion of appearance and complication of small fixing the spermatophore tube into the female structures of male genitalia which usually spermathecal duct (such genitalia are pres- do not replace the non-genital ones (excep- ent in many gryllids, in some non-primitive tions occur: for example, the male fixing ap- genera of Mogoplistidae, and possibly in paratus in some genera of Aemodogryllinae Myrmecophilidae). The development of is presented by only one small denticulate the grylloid genitalia is often accompanied plate of the genitalia), is the third general by replacement of all the non-genital fixing trend in the evolution of the ensiferan copu- devices by the genital ones. Independent latory apparatus. appearance and improvement of grylloid genitalia is the second general trend in the ACKNOWLEDGEMENTS evolution of the ensiferan copulatory apparatus (the first highly hypothetical trend is The work is supported by the Presidium the appearance of the copulatory apparatus of the Russian Academy of Sciences (Program “Biosphere Origin and Evolution of Geo-biolog- with a non-genital fixing device in the an- ical Systems”). cient ancestors of the recent ensiferans). The tettigonioid type of male genitalia is REFERENCES more or less similar to the hagloid one, but it differs in the appearance of a sclerite or Alexander R.D. & Otte D. 1967. The evolution sclerites on a small area (areas) of the dor- of genitalia and mating behavior in crickets sal fold or near it (Figs 3, f, g); usually such (Gryllidae) and other Orthoptera. Miscel- sclerotizations originate from the proximal laneous publications, Museum of Zoology, part of the dorsal surface of this fold, from University of Michigan, 133: 1–62. its lateral parts, from the apex of its lateral Bechly C., Brauckmann C., Zessin W. & Gron- ing E. 2001. New results concerning the projections, and/or from the areas between morphology of the most ancient dragonflies them. These sclerotizations may bear di- (Insecta: Odonatoptera) from the Namurian verse processes, hooks and denticles, and of Hagen-Vorhalle (Germany). Journal of represent fixing devices additional to those zoological Systematics and evolutionary Re- of the dorsal half of the male abdominal search, 39: 209–226. apex; they usually do not eliminate the need Bey-Bienko G.Ja. 1971. The revision of bush- for the styli. In Tettigoniidae, some of these crickets of the genus Xiphidiopsis (Orthop- sclerotizations as well as the paraproc- tera, Tettigonioidea). Entomologicheskoje Obozrenije, 50(4): 827–848. (In Russian). tal hooks in Mogoplistidae are sometimes Brauckmann C. 1991. Morphologie und Vari- named “titillators” (Love & Walker, 1979; abilität von Homoioptera vorhallensis (In- Storozhenko, 2004), but it may be more rea- secta: Palaeodictyoptera; Ober-Karbon). sonable to use this name for a certain kind of Geologica et Palaeontologica, 25: 193–213. genital sclerites only. The tettigonioid type Giljarov M.C. 1970. Zakonomernosti prispo- has independently appeared in very many sobleniya chlenistonogikh k zhizni na sushe genera from different subfamilies of Tetti- [Regularities in adaptations of arthropods to goniidae (or even in one subgenus within a the terrestrial life]. Moscow: Nauka. 276 p. genus), in some genera and tribes of Steno- (In Russian). Ghilarov M.S. (Ed.).1989. Biologicheskiy entsik- pelmatoidea (Diaphanogryllacris Karny, lopedicheskiy slovar’ [Biological encyclope- 1937 and Aemodogryllini) and possibly in dic dictionary]. Moscow: Sovetskaya entsik- some higher taxa of Grylloidea. Sometimes lopediya. 864 p. (In Russian). this type may be transformed into a com- Gorochov A.V. 1984. A contribution to the clas- plicated variant (Figs 3, h–j) more or less sification of recent Grylloidea (Orthoptera)

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