ISSN 0013-8738, Entomological Review, 2017, Vol. 97, No. 1, pp. 1–9. © Pleiades Publishing, Inc., 2017.
The Musculoskeletal System of Male Genitalia in Curetis bulis Westwood, 1851 (Lepidoptera, Lycaenidae: Curetinae) and Paralaxita damajanti (C. Felder et R. Felder, 1860) (Lepidoptera, Riodinidae: Nemeobiinae)1 A. A. Stekolnikov and A. I. Korzeev St. Petersburg State University, St. Petersburg, 199034 Russia e-mail:
[email protected];
[email protected] Received December 8, 2016
Abstract—The muscles of the male genitalia were studied for the first time in two species endemic to the Oriental zoogeographical region, namely Curetis bulis from the subfamily Curetinae (Lycaenidae) and Paralaxita damajanti from the tribe Abisarini (Riodinidae). Both taxa possess a common plan of musculature reflected in the positions of muscles m1, m2(10), m5(7), m7(6), m21, and m28. Two new autapomorphies of Curetis bulis were discovered: the splitting of m4 into two muscles and a shift of the attachment site of one of these muscles onto the dorsal area of the anellus. Apomorphic differences in the position of the genital muscles were found between Paralaxita damajanti and the previously studied Polycaena tamerlana from the family Riodinidae. A new synapomorphy between the latter two species, namely splitting of the aedeagus protractors m6(5), was also found. DOI: 10.1134/S0013873817010018
Until now, the musculature of the male genitalia of Lycaenidae has been mostly studied in the Palaearctic representatives of the subfamilies Lycaeninae, Theclinae, and especially Polyommatinae (Kuznetzov and Stekolnikov, 1998, 2001; Stekolnikov and Kuznetzov, 2005; Stekolnikov, 2010; Stekolnikov et al., 2013). There has been no data on the genital muscles of members of the tropical subfamilies of Lycaenidae, in particular Curetinae.
2015). Other authors, however, proposed different interpretations of the phylogenetic relations between the genus Curetis and other taxa of Lycaenidae (de Jong et al., 1996; Ackery et al., 1999). In the cited works, Riodinidae were considered as a subfamily of Lycaenidae and as a sister group with respect to the rest of this family, including Curetinae. Our morphological study of the musculoskeletal system of the male genitalia in Curetis bulis (Curetinae) is the first step toward understanding the phylogeny of the basal taxa of Lycaenidae. Another problem which may be approached by studying the male genital muscles is that of the phylogenetic relations between the taxa of Lycaenidae and Riodinidae.
The subfamily Curetinae includes a single genus Curetis Hübner, 1819 distributed in Southeast Asia and in the southeastern part of the Palaearctic (Japan). The genus comprises 18 species (Vane-Wright and de Jong, 2003). The morphology of the genital skeleton of Curetis bulis was studied by Eliot (1973), and recently and in greater detail, by the Indian researchers (Kumar et al., 2010). The subfamily Curetinae is usually regarded as one of the basal taxa within Lycaenidae, together with Poritinae, Lipteninae, Liphyrinae, Miletinae, and Aphnaeinae. This view of the phylogenetic position of Curetinae was recently confirmed by molecular genetic data (Campbell and Pierce, 2003; Wahlberg et al., 2005; Heikkilä et al., 2012; Espeland,
The mostly Neotropical family Riodinidae includes three subfamilies [Euselasiinae + (Nemeobiinae + Riodininae)]. Until now, the muscles of Riodinidae have been studied in only one Palaearctic species Polycaena tamerlana (Nemeobiinae, Nemeobiini) (Kuznetzov and Stekolnikov, 1998). We have studied another species of this subfamily, namely Paralaxita damajanti from the Oriental tribe Abisarini (Espeland et al., 2015).
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Riodinidae has been for a long time considered as a sister group of Lycaenidae (Ehrlich, 1958; Wahlberg
This article was originally submitted by the authors in Russian and is first published in translation.
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et al., 2005; Heikkilä et al., 2012), and sometimes as a subfamily within Lycaenidae (Kristensen, 1976). Some authors place Lycaenidae at the base of the pair of sister families Riodinidae and Nymphalidae (Robbins, 1988) or include Lycaenidae in one clade with Nymphalidae and Pieridae (Martin and Pashley, 1992). The various views on the phylogenetic relations between Nymphalidae, Riodinidae, and Lycaenidae were considered by Ackery and co-authors (1999). In some later publications (Campbell and Pierce, 2003; Wahlberg et al., 2005; Heikkilä et al., 2012; Espeland et al., 2015) Riodinidae was regarded as a sister clade of Lycaenidae. We consider the study of the male genital muscles in Curetis bulis (Lycaenidae) and Paralaxita damajanti (Riodinidae) and their comparison with the previously studied muscles of Polycaena tamerlana (Riodinidae) (Kuznetzov and Stekolnikov, 1998) as the first step toward understanding the phylogenetic relations between Lycaenidae and Riodinidae. MATERIALS AND METHODS A large series of males of Curetis bulis (Westwood, 1851) was collected by A.L. Monastyrsky in Vietnam. Two males of Paralaxita damajanti (C. Felder et R. Felder, 1860) were captured by V.V. Tikhonov on Sumatra, and two more males, by V.D. Ivanov and S.I. Melnitsky in Malaysia (Cameron Highlands). The butterflies of both species were fixed in 70% ethanol immediately upon collection. The skeleton and the muscle topography were studied by the manual dissection method. The genitalia were dissected in water using microsurgical scissors and a scalpel, the fat tissue was removed, and the muscles were stained with aqueous eosin or Evans Blue. The dissection technique was described in detail in an earlier publication (Stekolnikov and Speidel, 2009).
The tegumen (Fig. 1) is dome-shaped and wide; together with the unpaired uncus it forms a hood-like structure projecting over the ventral portion of the genitalia. The tegumen has lateral membranous windows which may facilitate the downward bending of the lamellar, apically pointed uncus (Fig. 2). The posterior ventrolateral processes of the tegumen, which outline the anterior margin of the membranous windows, are articulated to the bases of the subunci. The ventrocranial processes of the uncus form the second articulation of the bases of the crescent-shaped subunci. The anal cone has a large oval subanal plate that is invaginated considerably inside the abdomen beyond segment IX (Figs. 1, 2). Its dorsal (inner) surface is convex; the ventral (outer) surface is correspondingly concave, forming a large pouch above the base of the anellus. The vinculum (Fig. 1) is relatively narrow as compared with the tegumen but has a dorsomedian dilation and a well-developed median apodemal saccus. The vinculo-tegminal articulation has limited mobility due to sclerotization of the articulatory membrane connecting the two parts of segment IX (the tegumen and the vinculum). The valvae are well differentiated (Figs. 1, 3) and articulated to the vinculum with a wide base. The ventral lobe of the valva is narrow, elongate, relatively soft, and covered with fine scales and hairs. It extends caudally from the ventral base of the valva. The dorsal base is almost completely membranous and only its margins are sclerotized. The short, sclerotized, hook-shaped harpe is articulated to the dorsal base of the valva. The two valvae are positioned close together ventrally.
Curetis bulis Westwood, 1851 (Lycaenidae: Curetinae)
The structures of the anellus (Fig. 3). The narrow juxta lies between the valvae on the ventral side of the anellus. The distal portion of the juxta is abruptly dilated, and its margins are connected to the so-called dorsal plate (according to Eliot, 1973), densely covered with spines of varying size.
The skeleton of the male genitalia. The dorsal portion of the genital segment comprises the tegumen, the uncus with subunci, and the subanal plate. The ventral portion consists of the vinculum, the valvae articulated to it, and the anellus with the dorsal plate and the juxta. The aedeagus passes inside the anellus.
The aedeagus (Fig. 4) is massive, with a short basal outgrowth and two rows of spicular cornuti. The suprazonal part of the aedeagus is surrounded by the modified anellus. With the genitalia retracted, the basal outgrowth of the aedeagus lies at the level of the boundary between segments VI and V.
The muscles are named according to the emended nomenclature of Kuznetzov and co-authors (2004). RESULTS
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Figs. 1–5. Curetis bulis Westwood, 1851, skeleton and muscles of male genitalia: (1) skeleton of genitalia, lateral view, aedeagus not shown; (2) dorsal portion, ventral view; (3) valvae and anellus, dorsal view, aedeagus not shown; (4) aedeagus, lateral view; (5) ventral portion, sagittal section, aedeagus not shown; m1, m2(10), m4, m4a, m4b, m5(7), m6(5), m6(5)a, m6(5)b, m7(6), m8(3), muscles; c. pn, coecum penis; crn, cornuti; d. pl, dorsal plate; h, harpe; jx, juxta; lw, lateral window; sac, saccus; san. pl, subanal plate; stf, stiffener; sunc, subuncus; teg, tegumen; unc, uncus; vin, vinculum; vlv, valva; vl. vlv, ventral lobe of valva.
The muscles of the male genitalia. All the muscles found in the genitalia of Curetis bulis belong to the ground plan of Papilionoformes (Kuznetzov and Stekolnikov, 2001). These are muscles m1, m2(10), m4, ENTOMOLOGICAL REVIEW Vol. 97 No. 1 2017
m5(7), m6(5), m7(6) (Figs. 2–5), and also the inner phallic muscles m21 and m28. The only elements of the ground plan of Papilionoformes not found in this species were the ancient muscles m8(3) and m20.
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Muscles m1 are depressors of the uncus (Fig. 2). These muscles arise on the anterior margin of the tegumen and extend as two wide bands to the ventral wall of the uncus. Muscles m2(10) are retractors of the anal cone (Fig. 2). They originate paramedially on the anterior margin of the tegumen, extend to the narrowing distal end of the subanal plate, and are inserted at some distance from it. Muscles m4 are divided into two separate muscles m4a and m4b. Muscles m4a are adductors of the valvae (Fig. 5). They arise laterally on the caudal margin of the vinculum. Their insertion site lies on the rounded costal (dorsal) margin of the extensive valva base. Muscles m4b may be levators of the dorsal plate though their exact function is not clear (Figs. 3, 5). They arise on the apex of the vinculum not far from its articulation with the tegumen, extend downwards, and are inserted on the caudal margin of the dorsal plate of the anellus, reaching the dorsolateral angles of the juxta. Muscles m5(7) are the intravalvar muscles (Fig. 5). They extend from the longitudinal stiffening rib at the base of the sacculi to the median wall of the valva at the base of the harpe. Contraction of the intravalvar muscles leads to transverse bending of the valvae and fixation of the female terminalia with the hook-shaped harpes. The phallic muscles (Figs. 4, 5). There are two pairs of outer muscles m6(5) and m7(6), and two inner muscles m21 and m28. Muscles m6(5) are retractors of the aedeagus (Figs. 4, 5). These massive paired muscles originate laterally on the caudal margin of the vinculum and are inserted on the apex of the basal outgrowth of the aedeagus. Muscles m7(6) are protractors of the aedeagus (Figs. 4, 5). They are represented by a single pair of well-developed muscles connecting the saccus to the aedeagus in the perizonal area. Muscle m21 is the inner longitudinal phallic muscle (retractor of the vesica); m28 is the transverse phallic muscle positioned in the bulbus ejaculatorius. These muscles are not shown in the drawings.
Paralaxita damajanti C. Felder et R. Felder, 1860 (Riodinidae: Abisarini) The skeleton of the male genitalia. The dorsal portion of the genital segment, similar to Curetis bulis, comprises the tegumen, the uncus with subunci, and the subanal plate. The ventral portion consists of the vinculum articulated to the valvae, the transtilla, anellus, and the aedeagus passing inside the anellus. The tegumen (Fig. 6). The wide convex tegumen and the unpaired uncus lie in the dorsal genital area of Paralaxita damajanti. The uncus is truncated but has a minute pointed apical outgrowth. A pair of lateral membranous windows is present between the tegumen and the uncus. The bases of the subunci are articulated to the laterocaudal margins of the tegumen and the laterocranial angles of the uncus. The arms of the subunci are crescent-shaped, with ends pointing caudad. The anal cone (Figs. 6, 7) has a triangular subanal plate which is considerably narrowed in the cranial portion but is not invaginated inside the abdomen beyond segment IX. The vinculum (Fig. 6) is narrow dorsally and slightly dilated laterally, with a short saccus on the ventral side. The vinculo-tegminal articulation is absent. The valvae are conical and pointed (Figs. 6, 8), with their bases positioned close together ventrally. A pair of short lobes extends dorsally from the valvae. The structures of the anellus (Fig. 8). There is a rectangular protrusion positioned between the dorsal lobes of the valvae and connected to them. The bases of the dorsal lobes and the median protrusion together form the dorsal surface of the anellus. The anterior margin of the anellus includes a heavily sclerotized band corresponding to the transtilla. The juxta is absent due to reduction of the ventral part of the anellus. The aedeagus (Fig. 9) is straight, with a welldeveloped basal outgrowth. The muscles of the male genitalia. All the muscles found in the genitalia of P. damajanti belong to the ground plan of Papilionoformes (Kuznetzov and Stekolnikov, 2001). These are muscles m1, m2(10), m4, m5(7), m6(5), m7(6), m8(3) (Figs. 6–9), and also the inner phallic muscles m21 and m28. The only elements of the ground plan of Papilionoformes not found in this species were the ancient muscles m20. ENTOMOLOGICAL REVIEW Vol. 97 No. 1 2017
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Figs. 6–9. Paralaxita damajanti (C. Felder et R. Felder, 1860), skeleton and muscles of male genitalia: (6) lateral view; (7) dorsal portion, ventral view; (8) valvae and anellus, dorsal view; (9) aedeagus, lateral view; aed, aedeagus; an. t, anal tube; anl, anellus; dl. vlv, dorsal lobe of valva; mp. d. pl, median prominence of dorsal lobe; trs, transtilla; other abbreviations as in Figs. 1–5.
Muscles m1 are depressors of the uncus (Fig. 7). They arise paramedially on the anterior margin of the tegumen and extend to the ventral wall of the uncus. Muscles m2(10) are retractors of the anal cone (Fig. 7). They originate on the tegumen together with m1 and extend medially to the lateral margins of the subanal plate. ENTOMOLOGICAL REVIEW Vol. 97 No. 1 2017
Muscles m4 originate on the dorsal part of the vinculum, extend ventro-medially, and are inserted on the transtilla at the base of the dorsal portion of the anellus (Figs. 6, 8). They may be levators of the valvae. Muscles m8(3) connect the base of the valvae to the caudal margin of the ventral part of the vinculum, from which they extend paramedially (Figs. 6, 8).
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Muscles m5(7) are the intravalvar muscles (Fig. 6). Their fibers extend from the lateral wall of the valva base to the base of its pointed apex. Muscles m7(6) are retractors of the aedeagus (Figs. 6, 9) They are merged together into an unpaired muscle that connects the saccus to the aedeagus at the zona, being inserted ventrally and laterally on the aedeagus body. Muscles m6(5) are protractors of the aedeagus; there are two pairs of such muscles. Muscles m6(5)a are primary protractors of the aedeagus (Figs. 6, 9), extending from the lateral parts of the vinculum to the basal outgrowth of the aedeagus. Muscles m6(5)b are secondary protractors of the aedeagus (Figs. 6, 9) which are also inserted in its basal outgrowth. They originate on the vinculum much more ventrally than m6(5)a, namely on the median margin of the vinculum in close proximity to its articulation to the valvae. Muscles m21 and m28 (the retractor of the vesica and the transverse phallic muscle, respectively) are present; they are not shown in the drawings. Analysis of Characters of the Musculoskeletal System of the Male Genitalia of Curetis bulis Autapomorphies of Curetis bulis (Curetinae) 1. In the dorsal portion of the genitalia, a noticeable apomorphy of Curetis bulis is invagination of the subanal plate inside the abdomen (Fig. 2). Very rare cases of the subanal plate shifting inside the abdomen also occur in other, phylogenetically distant lepidopteran taxa, for example in Atabyria bucephala Snellen, 1884 among Tineidae or in Brachodes appendiculata (Esper, 1783) among Brachodidae (Kuznetzov and Stekolnikov, 2001). This character is also present in Polycaena tamerlana but absent in another studied species of Riodinidae, namely Paralaxita damajanti (Fig. 7). Thus, invagination of the base of the subanal plate inside the abdomen in Curetinae has originated independently and should be regarded as a non-unique autapomorphy. 2. Reduction of the adductors of the valvae m8(3) in C. bulis is a non-unique autapomorphy since this variant appears independently in different groups of Lepidoptera (Stekolnikov, 2008), including some members of Theclinae (Lycaenidae).
3. The presence of a harpe, serving for insertion of m5(7), on the median wall of the strongly differentiated valva of Curetis bulis is not known in Lycaenidae, but this variant has been found in Nymphalidae (Simonsen, 2006). The harpe of Curetinae seems to have originated independently. 4. Complex apomorphic changes are observed in the valvar adductors m4 of Curetis bulis (Fig. 5). These muscles are split into two pairs of separate muscles that have not been found in other Lycaenidae. One pair, m4a, preserves the ancestral vinculo-valvar position (extending from the lateral part of the vinculum to the anterodorsal part of the valva) and the function of adductors of the valvae. By contrast, the derived muscles m4b have changed both their attachment sites and their function. Their origin has shifted onto the dorsal part of the vinculum, and their insertion site has shifted from the anterodorsal part of the valvae onto the distal part of the dorsal plate homologous to the dorsal fultura. Such a shift of muscles m4b is unique among Lycaenidae; therefore we consider the splitting of m4 and the insertion of m4b on the dorsal plate of the anellus as autapomorphies. Characters of the Ground Plan in Curetis bulis (Curetinae) 1. The skeleton of the male genitalia of C. bulis has many primitive features, which is consistent with the basal position of Curetinae in the family Lycaenidae. Curetis bulis differs from representatives of three evolutionarily advanced subfamilies (Theclinae, Lycaeninae, and Polyommatinae) in the dome-shaped tegumen and the unpaired uncus (see Fig. 1), whereas in the evolution of Lycaenidae the bilobed process originating from the narrow tergite develops on the basis of an unpaired uncus. By contrast, the unpaired uncus in some genera of Polyommatinae, such as Cupido, Everes, and Tongeia, is the result of secondary simplification (Stekolnikov et al., 2013). 2. The muscles of the male genitalia of C. bulis reveal a complex of common primitive characters. In particular, muscles m1, m2(10), m21, and m28 have the same topography not only in Lycaenidae but within all the Papilionoformes. Correspondingly, these characters are to be excluded from phylogenetic analysis. Among the other muscles present in Curetis bulis, the primitive position is retained by the intravalvar muscles m5(7), the aedeagus protractors m6(5), and the aedeagus retractors m7(6) (Figs. 4, 5). ENTOMOLOGICAL REVIEW Vol. 97 No. 1 2017
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3. The longitudinal position of muscles m5(7) in C. bulis (Fig. 5) corresponds to the ground plan of Lepidoptera (Kuznetzov and Stekolnikov, 2001). In other representatives of Lycaenidae studied in this respect, these muscles have been extensively transformed or reduced (in some Theclinae) (Kuznetzov and Stekolnikov, 1998; Stekolnikov, 2010).
4. The aedeagus retractors m7(6) extend from the saccus to the basal outgrowth of the aedeagus. By contrast, in Paralaxita damajanti these muscles retain the ancestral position, being inserted on the median part of the aedeagus.
4. Among Lycaenidae, the basal attachment of the aedeagus protractors m6(5) (Fig. 5) to the lateral part of the vinculum has been found, besides C. bulis, only in Cigaritis epargyros (Aphnaeinae); this variant is considered to be primitive. In all the other studied members of Lycaenidae the origin of m6(5) is shifted dorsally on the surface of the vinculum and positioned immediately below or at the same level as the site of origin of m1. Finally, in Polyommatinae m6(5) arise from the tegumen dorsally to the attachment site of m1 (Kuznetzov and Stekolnikov, 1998). The lateral attachment of the aedeagus protractors to the vinculum is primitive for the whole nymphaloid clade. According to Kuznetzov and Stekolnikov (2001), in Riodinidae and most Nymphalidae, including the subfamilies Libytheinae and Danainae occupying the basal position within the family (Heikkilä et al., 2012), muscles m6(5) also originate laterally on the vinculum.
Autapomorphies of Paralaxita damajanti (Abisarini)
5. The retractors of the aedeagus are represented by a single pair of muscles m7(6) in C. bulis (Figs. 4, 5). In all the other studied members of Lycaenidae except Cigaritis epargyros (Aphnaeinae), these muscles are split into two pairs of separate bundles. Analysis of Characters of the Musculoskeletal System of the Male Genitalia of Polycaena tamerlana and Paralaxita damajanti (Riodinidae, Nemeobiinae) Autapomorphies of Polycaena tamerlana (Nemeobiini) 1. The elongated subanal plate is invaginated into the abdomen, similar to that of C. bulis. Since in Paralaxita damajanti the subanal plate is not invaginated into the abdomen, this invagination has appeared independently within Riodinidae and constitutes an autapomorphy of Polycaena tamerlana. 2. The presence of the transverse intervalvar muscle m18 in the male genitalia. 3. The muscle bundle separated due to the splitting of the aedeagus protractor m6(5) is inserted not on the vinculum, as in Paralaxita damajanti, but on the dorsal angle of the valva base. ENTOMOLOGICAL REVIEW Vol. 97 No. 1 2017
5. The transtilla has a pair of long distal processes.
1. Reduction of the juxta. Muscles m8(3) pass from the vinculum directly to the valvae (Fig. 8), whereas in Polycaena tamerlana the juxta is well developed and muscle m8(3) has the ancestral vinculo-juxtal position. Among Lycaenidae, reduction of the juxta was described for the most specialized representatives of Theclinae (Tomarini and Eumeini) (Kuznetzov and Stekolnikov, 1998: table 2); however, in the latter case muscles m8(3) were also reduced, which is not observed in P. damajanti. 2. The transtilla is narrow and sclerotized, without processes. Synapomorphies of Abisarini and Nemeobiini (an Autapomorphy of Nemeobiinae) 1. Muscles m6(5) (Fig. 5). The aedeagus protractors are split into two muscle bundles in both species of Nemeobiinae. No splitting of these muscles was found in any studied representative of Lycaenidae. 2. Muscles m4. The valvar adductors are attached medially to the structure homologous to the transtilla, in the dorsal area of the anellus (Fig. 8). The transtillar insertion of muscles m4, originating on the apex of the vinculum, may be considered as an autapomorphy of Nemeobiinae. Characters of Uncertain Phylogenetic Significance in Lycaenidae and Riodinidae 1. The presence of crescent-shaped subunci is typical of all the Lycaenidae and Riodinidae; this character may be regarded as their synapomorphy only if an independent origin of subunci in Satyrinae within Nymphalidae is demonstrated. 2. A similar shift of the attachment site of m4 from the vinculum onto the dorsal surface of the anellus in Curetis bulis (Curetinae), Paralaxita damajanti, and Polycaena tamerlana (Riodinidae) may constitute an important synapomorphic character of Lycaenidae and Riodinidae. The main difference between C. bulis
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and the two studied species of Riodinidae, which is inconsistent with the synapomorphic nature of this character, is that in C. bulis muscles m4 are split and only the derived muscles m4b are shifted onto the anellus while muscles m4a remain in the original vinculo-valvar position. An additional study of the topography of muscles m4 in a larger set of ancestral groups within both Riodinidae and Lycaenidae is required in order to decide whether the shift of m4 onto the dorsal part of the anellus is a true synapomorphy of Lycaenidae and Riodinidae. Such a study would be all the more important because Riodinidae are represented in our analysis only by the subfamily Nemeobiinae, while data on the more phylogenetically ancient subfamily Euselasiinae are absent. Common Characters of the Ground Plan (Symplesiomorphies) in Riodinidae and Lycaenidae Similar to Curetis bulis, the two species of Nemeobiinae have common characters pertaining to the ground plan of the genital skeleton (the dome-shaped tegumen and the unpaired uncus), and also the same attachment sites of muscles m1, m2(10), and m7(6). CONCLUSIONS Our study of the musculoskeletal system of the male genitalia of Curetis bulis has confirmed the phylogenetic conclusions about the basal position of Curetinae in the system of Lycaenidae based on molecular data (Heikkilä et al., 2012; Espeland et al., 2015). The musculoskeletal system of the male genitalia of this species revealed many ancestral traits, as compared with the genitalia of the studied members of Lycaenidae (Kuznetzov and Stekolnikov, 2001). The previously established autapomorphies of Curetinae, namely the presence of paired retractile androconial brushes on abdominal segment II in the males (Scott and Wright, 1990) and paired cylindrical tubules on abdominal segment XI in the larvae (DeVries, 1984), were supplemented with new ones: (1) the splitting of the valvar adductors m4 into two pairs of muscles and (2) the shift of one pair of muscles from the valvae onto the dorsal part of the anellus. Thus, Curetinae may be regarded as an ancient taxon with some unique morphological characters. No synapomorphies were found in the genital muscles of Curetinae and other taxa of Lycaenidae studied in this respect. The new data on the genital skeleton and muscle morphology of Paralaxita damajanti (Nemeobiinae)
showed considerable symplesiomorphic similarity between this species and Curetis bulis. At the same time, the position of m4 on the dorsal part of the anellus may indicate synapomorphic similarity of Curetinae and Nemeobiinae. So far, the only possible synapomorphy of Nemeobiinae and Curetinae is the presence of crescent-shaped subunci. Since similar subunci can also be found in Satyrinae, they may have originated twice in the nymphaloid clade: in the families Riodinidae + Lycaenidae and in Satyrinae within the family Nymphalidae. The noticeable apomorphic differences between Paralaxita damajanti and Polycaena tamerlana coexist with a new autapomorphy of the subfamily Nemeobiinae, namely the splitting of the aedeagus protractors m6(5). ACKNOWLEDGMENTS We are very grateful to V.D. Ivanov and S.I. Melnitsky (St. Petersburg, Russia), V.V. Tikhonov (Pyatigorsk, Russia), and A.L. Monastyrsky (Hanoi, Vietnam) for help with material collection. This work was financially supported by the Russian Foundation for Basic Research (project 14-04-00139-a) and performed with the use of equipment of the Research Resource Center for Molecular and Cell Technologies of St. Petersburg State University. REFERENCES 1. Ackery, P.R., de Jong, R., and Vane-Wright, R.I., “The Butterflies: Hedyloidea, Hesperoidea and Papilionoidea,” in Lepidoptera, Moths and Butterflies. 1. Evolution, Systematics and Biogeography, Ed. by N.P. Kristensen (de Gruyter, Berlin, 1999), pp. 263–300. 2. Campbell, D.L. and Pierce, N.E., “Phylogenetic Relationships of the Riodinidae: Implications for the Evolution of Ant Association,” in Butterflies as Model Systems (Chicago University Press, 2003), pp. 395–408. 3. De Jong, R., Vane-Wright, R.I., and Ackery, P.R., “The Higher Classification of Butterflies (Lepidoptera): Problems and Prospects,” Entomologica Scandinavica 27 (1), 65–101 (1996). 4. DeVries, P.J., “Of Crazy-Ants and the Curetinae: Are Curetis Butterflies Tended by Ants?” Zoological Journal of the Linnean Society 79, 59–66 (1984). 5. Ehrlich, P.R., “The Comparative Morphology, Phylogeny and Higher Classification of the Butterflies (Lepidoptera: Papilionoidea),” University of Kansas Science Bulletin 39 (8), 305–370 (1958). 6. Eliot, J., “The Higher Classification of the Lycaenidae: A Tentative Arrangement,” Bulletin of the British Museum (Natural History), Entomology Series 28 (6), 373–505 (1973). ENTOMOLOGICAL REVIEW Vol. 97 No. 1 2017
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