Research Article |
Corresponding author: Tatiana V. Galinskaya ( nuha1313@gmail.com ) Academic editor: Vladimir Blagoderov
© 2018 Olga G. Ovtshinnikova, Tatiana V. Galinskaya, Elena D. Lukashevich.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ovtshinnikova OG, Galinskaya TV, Lukashevich ED (2018) Skeleton and musculature of the male abdomen in Tanyderidae (Diptera, Nematocera) of the Southern Hemisphere. ZooKeys 809: 55-77. https://doi.org/10.3897/zookeys.809.29032
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The structure of the male terminalia and their musculature of species of tanyderid genera Araucoderus Alexander, 1929 from Chile and Nothoderus Alexander, 1927 from Tasmania are examined and compared with each other and with published data on the likely relatives. The overall pattern of male terminalia of both genera is similar to those of most Southern Hemisphere genera, with simple curved gonostyli, lobe-like setose parameres, and setose cerci inconspicuous under the epandrium. Both genera have terminalia similarly rotated by 180° (and 90° as an intermediate stage); rotation may be either clockwise or counterclockwise. However, the similar patterns are realized differently: segment VIII is the decreased and asymmetrical due to completely membranose tergite VIII in Nothoderus (the first record of such modification in Tanyderidae), but narrow and symmetrical in Araucoderus. Accordingly, pregenital muscles are very different between the genera. Based on localization of muscle attachment sites, the hypandrial origin of the stripe between gonocoxites is shown in both genera, and entire membranization of tergite VIII and partial membranization of hypoproct is shown in Nothoderus. Tanyderidae are characterized by highly specialized sclerites and muscles of male terminalia and provide no evidence of relationship with previously studied members of Psychodidae, Blephariceridae and Ptychopteridae.
crane flies, rotation, terminalia, genitalia, morphology, Araucoderus , Nothoderus
Tanyderidae, or primitive crane flies, are a small ancient nematocerous family with amphitropical distribution and higher recent diversity in the Southern Hemisphere (
The family is important for understanding of the history of the order, but remains insufficiently studied. Male genitalia of some extant genera have been described or drawn with varying degrees of detail; both genera from the Northern Hemisphere: Protoplasa Osten-Sacken, 1860 and Protanyderus Handlirsch, 1909; and most of genera from the Southern Hemisphere: Peringueyomyina Alexander, 1921, Mischoderus Handlirsch, 1909, Araucoderus Alexander, 1929, Eutanyderus Alexander, 1928, Nothoderus Alexander, 1927 and Neoderus Alexander, 1927 (
Among the likely relatives, musculature has been examined in the blepharicerid, Edwardsina gigantea Zwick, 1977 (
Musculature of male terminalia of Tanyderidae, Psychodidae, Blephariceridae and Ptychopteridae.
Taxa | Muscle Groups | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
Abdominal muscles | Pregenital muscles | Tergosternal muscles | Muscles of the hypandrial complex | Muscles of the epandrial complex | ||||||
Muscles of VII sclerite | Hypandrial muscles | Epandrial muscles | Ejaculator muscles | Aedeagal muscles | Gonocoxal muscles | Gonostylar muscles | Muscles of hypoproct | Muscles of cercus | ||
Tanyderidae | ||||||||||
Araucoderus gloriosus (present study) | Paired asymmetrical ISM7; Paired asymmetrical ITM7 | Paired asymmetrical M18 | Paired asymmetrical M19 | M5 | M23; M30; M31 | M1+2 | not found | M27; M28 | M3 | M7 |
Nothoderus australiensis (present study) | Paired asymmetrical ISM7; Unpaired ITM7 | Unpaired M18 | not found | M5 | M23; M30; M31 | M1+2 | not found | M27; M28 | M31–2 | M7 |
Psychodidae | ||||||||||
Pericomasp. (after |
Paired slightly asymmetrical ISM7 (VLM1, VLM2 sensu |
M18 (VLM1a, VLM1b sensu |
M19 (JM8–9 sensu |
M51–2 (M6, M6a sensu |
M30 (MS1, MS2 sensu |
M1 (MS4 sensu |
not found |
M27 (M3 sensu |
M3 (M1 sensu |
M7 (M2a, M2b sensu |
Phlebotomus garnhami (after |
Paired asymmetrical ISM7 (VLM sensu |
M18 (VLM sensu |
M191–2 (DLM1–2sensu |
not found | ? M311–2 (M5, M6 sensu |
M1 (M4 sensu |
not found |
M27 (M2, M21 sensu |
M3 (M7 sensu |
M7 (M8 sensu |
Blephariceridae | ||||||||||
Edwardsina gigantea (after |
not examined |
M18 (described without numbering |
M19 (described without numbering |
M51–2 (described without numbering |
? M30 (M7 sensu |
M1 (M1 sensu |
not examined |
M27 (M3 sensu |
M3 (described without numbering |
M7 (described without numbering |
Ptychopteridae | ||||||||||
Ptychoptera lacustris (after |
Paired symmetrical ISM7 (VLM sensu Just, 1973); Paired symmetrical ITM7 (DLM sensu Just, 1973) | Paired symmetrical M18 (VLM2 sensu Just, 1973) | Paired symmetrical M19 (DLM2 sensu Just, 1973) | M5 (M1 sensu Just, 1973) | M31 (M11 sensu Just, 1973) | M11–4 (M3, M8, M9, M7 sensu Just, 1973); M21–2 (M6, M10 sensu Just, 1973) | M33 (M2, sensu Just, 1973); | M27 (M4 sensu Just, 1973); M28 (M5 sensu Just, 1973) | M31–3 (M12, M13, M14 sensu Just, 1973) | M71–2 (M15, M16 sensu Just, 1973) |
Study of the musculature is helpful not only for specifying the functions of genital sclerites, but also for revealing the homology of some poorly traced structures (
The purpose of this study was to investigate the skeleton and musculature of the male genitalia of two genera of Tanyderidae from the Southern Hemisphere. The muscles and sclerites of the male abdomen of Nothoderus australiensis (Alexander, 1922) from Tasmania and the muscles of the male abdomen of Araucoderus gloriosus (Alexander, 1920) from Chile are described for the first time.
This study is based on males of Tanyderidae collected in Nothofagus-dominated forests in Chile and Tasmania by D. Shcherbakov and E. Lukashevich in 2014 and 2015. Specimens studied herein will be deposited in the Zoological Institute RAS, St-Petersburg, Russia. Additional specimens are deposited in the National Museum of Natural History, Santiago, Chile (Araucoderus) and Tasmanian Museum and Art Gallery, Hobart, Australia (Nothoderus).
Scanning electron micrographs of uncoated and coated males were taken with a Tescan Vega microscope using backscattered electron (BSE) and secondary electron (SE) detectors.
The terminology of the male genital sclerites mainly follows
The muscular systems of male genitalia were studied by manually dissecting the material (preserved fresh in 70% alcohol) with microknives in water under a Leica MZ95 stereomicroscope. The pictures were taken using the image capture function of the Leica MZ95 trinocular head and subsequently processed. The male terminalia muscles were classified into several groups: muscles of the epandrial complex, muscles of the hypandrial complex, tergosternal muscles, and pregenital muscles. The muscles were numbered according to the classification previously accepted by Ovtshinnikova with the following modifications M21 = M3, M29 = M7 and M32 = M23 based on homologization of muscles (
List of abbreviations: aed – aedeagus; cerc – cercus; ej apod– ejaculatory apodeme; ep – epandrium; goncx – gonocoxite; gonst – gonostylus; hypd – hypandrium; hypp – hypoproct; ISM – abdominal intersegmental sternal muscles; ITM – abdominal intersegmental tergal muscles; lepr – lateral ejaculatory process; M1–M33 – pregenital and genital muscles; pm db – dorsal bridge of paramere; pm dme – dorsomedial element of paramere; pm gbl – paramere lobe at gonocoxite base; pm lme – lateromedial element of paramere; spm sac – sperm sac; st – sternite; tes – testis; th – thorax; tg – tergite; TSM – abdominal tergosternal muscles.
The subfamily includes nine extant and five extinct genera with relatively short gonopods. Musculature of male terminalia is here examined for only two members of the subfamily.
Tanyderidae are characterized by abdominal segments with intersegmental tergal (ITM), intersegmental sternal (ISM) and tergosternal (TSM) muscles and by pregenital muscles (M18, M19). Male genital muscles of Tanyderidae are classified into several groups: tergosternal muscles (M5); muscles of the hypandrial complex (3 pairs of ejaculator muscles M23, M30, M31; aedeagal muscle M1+2; 2 pairs of gonostylar muscles M27, M28); muscles of the epandrial complex (muscles M3, connecting epandrium with hypoproct (=X sternite); muscles M7, connecting hypoproct with cerci).
Chile, Nothofagus-dominated forest, on riparian vegetation. Alerce Andino National Park: Lenca River, 340 m asl (41°30'S, 72°37'W), 6–8.i.2014, 12–18.i.2015, D.E. Shcherbakov, E.D. Lukashevich, 8 males; Puyehue National Park: Anticura River near Anticura Waterfall, 400 m asl (40°40'S, 72°10'W), 14.i.2014, E.D. Lukashevich, 1 male; Chanlefu River at Aguas Calientes, 470 m asl (40°44'S, 72°18'W), 16.i.2014, D.E. Shcherbakov, 1 male; Huerquehue Natianal Park: near Tiquilco Lake, 780 m asl, (39°10'S, 71°44'W), 22.xii.2014, E.D. Lukashevich, 1 male; near La Junta, Rio Palena, 70 m asl, (43°49'S, 72°21'W), 5.i.2015, E.D. Lukashevich, 1 male. The specimens will be deposited in the Zoological Institute RAS, St-Petersburg, Russia.
The male terminalia were described in great detail by
Thoracic muscles. One pair of tergal muscles, connecting thorax and medial part of tergite I; one pair of sternal muscles, connecting thorax and anterolateral margin of sternite II (Figure
Abdominal muscles. One pair of long intersegmental tergal muscles ITM1 connecting medial part of tergite I and medial part of tergite II (Figure
Pregenital muscles. Paired short asymmetrical muscles M18: right muscle M18 long, connecting middle of right side of sternite VIII to narrow sclerotized stripe or hypandrium between gonocoxite bases; left wide short muscle M18 connecting middle of left side of sternite VIII to narrow sclerotized stripe between gonocoxite bases (Figures
Tergosternal muscles. Paired, wide symmetrical M5 connecting anterolateral parts of epandrium to lateral thickenings of dorsal bridge of paramere in the point of connection of pm db with gonocoxites (= gonocoxal apodeme) (Figures
Muscles of the hypandrial complex. Paired long retractors M1+2 extending from anterior edges of gonocoxites to aedeagal condyle, and several muscle filaments of M1+2 extending from anterior edges of gonocoxites to posterior margin of dorsomedial element of paramere pm dme (Figure
Muscles of the epandrial complex. Paired short wide M3 extending from most of inner epandrium surface to hypoproct (X sternite) (Figure
Tasmania, Nothofagus-dominated forest, on riparian vegetation. Lake Saint Clair National Park (42°6'S, 146°9'E), 7.xii.2015, D.E. Shcherbakov, 2 males; Mystery Creek Cave (43°28'S, 146°51'E), 13.xii.2015, D.E. Shcherbakov, E.D. Lukashevich, 4 males. The specimens will be deposited in the Zoological Institute RAS, St-Petersburg, Russia.
Abdomen: tergite I about 0.6 times as long as tergite II, sternite I about 0.3 times as long as sternite II (Figure
Abdominal muscles. Tergosternal muscles TSM1 of segment I not found. Segments II–VII with one pair of wide short tergosternal muscles (TSM2–TSM7) (Figure
Pregenital muscles. Short unpaired muscle M18 connecting sternite VIII to narrow sclerotized stripe or hypandrium between gonocoxite bases (Figure
Tergosternal muscles. Paired, wide symmetrical M5 connecting anterolateral parts of epandrium to lateral thickenings of dorsal bridge of paramere in the point of connection of pm db with gonocoxites (= gonocoxal apodeme) (Figure
Muscles of the hypandrial complex. Paired long retractors M1+2 extending from anterior edges of gonocoxites to aedeagal condyle, and also several muscle filaments of M1+2 extending from anterior edges of gonocoxites to posterior margin of dorsomedial element of paramere pm dme (Figure
Muscles of the epandrial complex. Two pairs of M3 muscles; M31 extending from lateral parts of epandrium to anterolateral parts of hypoproct (X sternite); M32 extending from posterolateral parts of epandrium to membrane between epandrium and cercus (Figure
The sclerites and musculature of Araucoderus and Nothoderus are similar, but differ in several features. The overall pattern of male terminalia of both genera is similar to most of the Southern Hemisphere genera, with simple curved gonostyli, lobe-like setose parameres, and setose cerci inconspicuous under the epandrium. The terminalia of Nothoderus are distinct from genitalia of Araucoderus in shape of epandrium with tiny concave median lobe, absence of sclerotized protruding parameral elements and simple aedeagus. However, these differences in structure of terminalia in Araucoderus and Nothoderus are not associated with differences in musculature. Thus, in Araucoderus parameral elements are more diverse and developed and the structure of trifid and simple aedeagus is different; but the aedeagal muscles M1+2 and ejaculatory muscles M23, M30 and M31 look very similar in both genera.
We have found different degrees of sclerotization of the hypoproct in Araucoderus and Nothoderus, and correlated differences in muscles of the epandrial complex. The hypoproct is recessed deeply within the genitalia; its location is possibly the reason why the hypoproct was not mentioned by some previous researchers (
One interesting difference associated with rotation was found in the abdominal structure. Nothoderus is characterized by the 180° rotation of segments VII–IX, of the six specimens examined, four males demonstrated clockwise rotation (two of them only 160°; Figure
Araucoderus is also characterized by 180° rotation of segments VII–IX. However, of the 12 males of Araucoderus examined by us, seven had partially rotated terminalia (about 90°) and five males had terminalia with 180° rotation; eight specimens had clockwise rotation and 4 males had counterclockwise rotation (such males are illustrated in Figures
Araucoderus is characterized by the narrow segment VIII, but not reduction of the separate sternite and tergite VIII. Nothoderus has segment VIII strongly reduced, with tergite VIII totally membranous and sternite VIII as a narrow sclerite. Accordingly, attachment sites and thickness of pregenital muscles are greatly different between the genera: reduction of muscles M19 and unpaired M18 was found in Nothoderus, whereas Araucoderus has paired symmetrical M18 and M19 (see below, Table
The attachment sites of muscles ISM7 and M18 confirm the origin of sternite VIII, and the attachment sites of muscles ITM7 confirm the entire membranization of tergite VIII of Nothoderus (Figure
The reduction and asymmetry of segment VIII is noted for Tanyderidae for the first time. Such reduction of segment VIII contradicts Alexander’s opinion of Nothoderus as “the most generalized of the living Tanyderidae” (
One more interesting difference was found in the structure of abdominal intersegmental muscles of VII sclerites. These muscles are asymmetrical and the sternal muscles ISM7 are paired in both genera, whereas the tergal muscles ITM7 are paired in Araucoderus but in Nothoderus only one unpaired ITM7 was found (Table
As it was discussed in the introduction, different authors cluster Tanyderidae with Blephariceridae, Ptychopteridae or Psychodidae. Data on skeleton and musculature of male terminalia in Tanyderidae, Psychodidae, Blephariceridae and Ptychopteridae are compared in Tables
Among these families only Tanyderidae are characterized by ejaculator muscles M23 (in addition to muscles M30 and M31, present in other families). Muscles M23 connect only sclerites or membranes of aedeagal complex consisting of ejaculatory apodeme and aedeagus. Up to now these muscles were recorded in the only one nematocerous family, Trichoceridae, and in Brachycera (as M32 in
It can be assumed that muscles M30 and M31 of Tanyderidae, attached to different parts of the ejaculatory apodeme, have the opposite functions of muscles M30 and M31 of Blephariceridae and Bibionidae and most of Brachycera, muscles M31 of Psychodidae and Ptychopteridae. Muscles M30 of Tanyderidae are, probably, protractors, muscles M31 of Tanyderidae are, probably, retractors as in Trichoceridae (
Only Tanyderidae are characterized by the merging of aedeagal muscles M1 and M2. Psychodidae, Blephariceridae, and Ptychopteridae are characterized by separate aedeagal muscles: the protractors M1 and retractors of aedeagus M2 and two pairs of aedeagal muscles are part of the dipteran groundplan (one pair M1 and one pair of M2). Tanyderidae are characterized only by retractors M1+2 that should lead to changing in mechanism of aedeagus functioning.
The examined tanyderids are characterized by muscles M1+2 connecting gonocoxites partly to the aedeagus, partly to the dorsomedial element of the parameres pm dme, and by muscles M31 connecting posterior part of ejaculatory apodeme to medial part of dorsal bridge of paramere pm db. Tanyderidae as well as Psychodidae and Blephariceridae are characterized by a sclerotized bridge forming through medial merging of parameres and “connecting the gonocoxites dorsally via the gonocoxal apodemes” (
Blephariceridae are distinct from Tanyderidae in tergosternal muscles M5 divided into two pairs and the absence of terminalia rotation (Table
Characters of male terminalia of Tanyderidae, Psychodidae, Blephariceridae and Ptychopteridae, discussed in the text (1 – after
Rotation | Trifid aedeagus | Sperm pump hypertrophied | Aedeagal muscles | Tergosternal muscles M5 | Ejaculator muscles | Gonocoxal muscles M33 | ||||
M1 | M2 | M23 | M30 | M31 | ||||||
Tanyderidae | ||||||||||
Araucoderus gloriosus | + | + | – | one pair | one pair | one pair | one pair | one pair | – | |
Nothoderus australiensis | + | – | – | one pair | one pair | one pair | one pair | one pair | – | |
Psychodidae | ||||||||||
Pneumia palustris 1 | + | – | – | one pair | one pair | two pairs | – | one pair | one pair | – |
Phlebotomus garnhami 1 | + | – | – | one pair | one pair | – | – | – | two pairs | – |
Blephariceridae | ||||||||||
Edwardsina gigantea 2 | – | + | – | one pairs | one pair | two pairs | – | one pair | two pairs | – |
Ptychopteridae | ||||||||||
Ptychoptera lacustris 1 | – | – | + | four pairs | two pairs | one pair | – | – | one pair | one pair |
Ptychopteridae are also distinct from Tanyderidae in the absence of terminalia rotation, and share plesiomorphic characters only, such as tergosternal muscles M5 not divided (Table
Psychodidae is the single family under discussion with male terminalia rotation (for details see in
It is worth noting that Psychodidae are extremely diverse and the scarce data on their musculature confirms this diversity: e.g., Psychodinae are characterized by tergosternal muscles M5 divided into two pairs, whereas Phlebotominae are characterized by absence of muscles M5 (
The Tanyderidae are characterized by very specialized sclerites and muscles of male terminalia; these structures provide no evidence of relationship with previously studied members of Psychodidae, Blephariceridae and Ptychopteridae. Within these three families, only Psychodidae have obligatory 180° male terminalia rotation and only Blephariceridae have a trifid aedeagus. Although our initial hypothesis was the similarity of Tanyderidae and Psychodidae and we looked for evidence using the analysis of musculature characters that had not previously been investigated; the musculature of male terminalia offers little confirmation of this relatedness. The absence of evidence is probably connected with the absence of data on musculature of the primitive psychodid subfamilies Bruchomyiinae, Sycoracinae and Horaiellinae.
E.D. Lukashevich is grateful to Dmitry Shcherbakov (Borissiak Paleontological Institute RAS, Moscow) for the opportunity to collect Tanyderidae in Chile and Tasmania. E.D. Lukashevich is also grateful to Cathy Byrne and Simon Grove (both Tasmanian Museum and Art Gallery, Hobart) for their hospitality and invaluable help in facilitating field work of the Russian team in Tasmania and to Mario Elgueta (National Museum of Natural History, Santiago) for facilitating fieldwork in Chile. We also thank Roman Rakitov (Borissiak Paleontological Institute of Russian Academy of Sciences, Moscow) for helping in taking scanning electron images and for other assistance. We are deeply indebted to Rolf G. Beutel (Institut für Spezielle Zoologie und Evolutionsbiologie, Jena) and Bradley J. Sinclair (Canadian National Collection of Insects and Canadian Food Inspection Agency, Ottawa) for insightful comments on the manuscript and linguistic advice.
The work of O.G. Ovtshinnikova was supported by the Zoological Institute of Russian Academy of Sciences (State Research Program AAAA-A17-117030310205-9) and the Russian Foundation for Basic Research (project no. 18-04-00354-a). The work of T.V. Galinskaya was supported by the Russian Science Foundation (project no. 14-14-00208). The research of E.D. Lukashevich was partly supported by grants from the Russian Foundation for Basic Research, projects no. 13-04-01839 and 16-04-01498.