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, 8 (1), 19

Structural Aspects of Leg-To-Gonopod Metamorphosis in Male Helminthomorph Millipedes (Diplopoda)

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Structural Aspects of Leg-To-Gonopod Metamorphosis in Male Helminthomorph Millipedes (Diplopoda)

Leandro Drago et al. Front Zool.

Abstract

Background: In the adult males of helminthomorph millipedes, one or two pairs of legs in the anterior part of the trunk are strongly modified into sexual appendages (gonopods) used for sperm transfer during the copula. Gonopods differentiate in an advanced phase of post-embryonic development, in most cases as replacement for the walking legs of the seventh trunk ring, as these first regress to tiny primordia, to eventually develop into gonopods at a subsequent stadium. These extremely localized but dramatic changes have been described as a non-systemic metamorphosis. In the present study we describe morphological and anatomical changes of trunk ring VII associated with non-systemic metamorphosis in four helminthomorph species.

Results: As documented here for the first time by means of traditional histology methods and new techniques based on confocal laser scanning microscopy, the external modifications caused by non-systemic metamorphosis are associated to a huge rearrangement of internal anatomy, mostly due to the development of gonopod apodemes and extrinsic muscles.

Conclusions: Internal changes in the seventh trunk ring, locally leading to the dorsal displacement of the ventral nerve cord and the digestive tract, are modulated in a taxon-specific manner, and are very conspicuous in the blaniulids Nopoiulus kochii and Blaniulus guttulatus, with likely major functional consequences.

Figures

Figure 1
Figure 1
Phylogenetic relationships among the millipede taxa cited in the text. Colob., Colobognatha; Pen., Penicillata; Pentaz., Pentazonia. After [10,59,60].
Figure 2
Figure 2
Anamorphic development of the millipede species studied in the present paper. The post-embryonic developmental stadia are numbered progressively. Walking legs are depicted as short lines, ventrally attached to the corresponding trunk ring, gonopod primordia as small ventral blobs on trunk ring VII, gonopods (two pairs in A-C, one pair in D) as complex structures also attached to trunk ring VII. (A) Nopoiulus kochii. (B) Blaniulus guttulatus. (C) Nemasoma varicorne. (D) Oxidus gracilis. From stadium VI on, in B. guttulatus only the anterior trunk is shown; in N varicorne, gonopods are sometimes formed at stadium VI.
Figure 3
Figure 3
Main stages of non-systemic metamorphosis in three millipede species of the order Julida. (A-C) N. kochii; (D-F) B. guttulatus; (G-I) N. varicorne. A, D and G, last stadium with walking legs on ring VII (asterisk); SEM, latero-ventral view. B, E and H, gonopod primordia; SEM, ventral view. C, F and I, gonopods; SEM, ventral view. Yellow, coxal process; Green, anterior gonopod telopodite; Blue, posterior gonopod telopodite. Anterior to the left, scale bars 200 μm.
Figure 4
Figure 4
Julida ring VII sections. (A-E) N. kochii male, para-midsagittal (A-C) and frontal (D-E) paraffin sections of rings VI-VIII during post-embryonic stadia IV-VI. Mallory's triple stain. A, last stadium with walking legs on ring VII. B, stadium with gonopod primordia. C-E, adults with gonopods. (F-G) N. varicorne male, frontal paraffin sections of rings VI-VIII during post-embryonic stadium V. Mallory's triple stain. Labels a-d in panel C mark the levels of sections in Figure 9. agA, anterior gonopod apodeme; aga, anterior gonopod abductor muscle; agr, anterior gonopod retractor muscle; gt, gut; nc, nerve cord; pgr, posterior gonopod retractor muscle; ph, prophragma; arrows, possibly undifferentiated tissue. Asterisks, ring VII legs. Anterior to the left, scale bars 100 μm.
Figure 5
Figure 5
N. kochii, adult male. Fused EDF-stack. (A) Seventh trunk ring, after digestion of internal soft tissues. Posterior view. (B) Dissected anterior gonopods after digestion of soft tissues. Chlorazol black stain. Asterisks, anterior gonopod apodemes. Ventral view, anterior to the top, scale bars 200 μm.
Figure 6
Figure 6
Adult males of julidan millipedes. (A-B) N. kochii, (C-D) B. guttulatus. (E-F) N. varicorne. A, C and E, seventh trunk ring, SEM after the digestion of the internal soft tissue; posterior view. B, D, and F, CLSM after digestion of the internal soft tissue. Projection at maximum intensity of serial pictures. ag, anterior gonopod; pg, posterior gonopod. Arrowhead, posterior gonopod apodeme. Asterisk, anterior gonopod apodeme. Para-midsagittal view, anterior to the left, scale bars 200 μm.
Figure 7
Figure 7
Schematic representation of the extrinsic musculature of the left gonopods of N. kochii. agA, anterior gonopod apodeme; agp, anterior gonopod protractor muscle; agr, anterior gonopod retractor muscle; gs, gonopodal sac; pgA, posterior gonopod apodeme; pgp, posterior gonopod protractor muscle; pgr, posterior gonopod retractor muscle; ph, prophragma; tA, tracheal pouch apodeme. Anterior to the left.
Figure 8
Figure 8
Transverse trunk sections of adult julidan millipedes. Mallory's triple stain. (A-D) N. kochii. (E-H) B. guttulatus. (I-L) N. varicorne. Sections A, E and I are at the level marked as a in Figure 8C; sections B, F and J are at level b, sections C, G and K are at level c, and sections D, H and L are at level d of the same figure. agA, anterior gonopod apodeme; aga, anterior gonopod abductor muscle; agp, anterior gonopod protractor muscle; agr, anterior gonopod retractor muscle; gt, gut; nc, nerve cord. Scale bars 100 μm.
Figure 9
Figure 9
Individual variation and left-right asymmetry in the shape of gonopod primordia. (A-C) N. kochii. (D-F) B. guttulatus. Ventral view, anterior to the left, scale bars 50 μm.
Figure 10
Figure 10
N. varicorne adult male. Schematic reconstruction of the extrinsic musculature of the left anterior and posterior gonopods. (A) Lateral view, anterior to the left. (B) Posterior view. agA, anterior gonopod apodeme; agp, anterior gonopod protractor muscle; agr, anterior gonopod retractor muscle; f, flagellum; gs, gonopodal sac; pgA, posterior gonopod apodeme; pgad, posterior gonopod adductor muscle; pgp, posterior gonopod protractor muscle; pgr, posterior gonopod retractor muscle; ph, prophragma; tA, tracheal pouch apodeme.
Figure 11
Figure 11
Trunk rings VI-VIII of O. gracilis during developmental stadia III-VIII. All male specimens except for the one in A, whose sex is undetermined because of the lack of sexual dimorphism at the corresponding developmental stadium. Ventral views, SEM. (A) Stadium III. (B) Stadium IV. (C) Stadium V. (D) Stadium VI. (E) Stadium VII. (F) Stadium VIII. Asterisk, trunk ring VII; s, spiracles associated with the eighth pair of appendages; arrowheads, gonopod primordia at their first appearance; arrows, gonopods. Anterior to the left, scale bars 200 μm.
Figure 12
Figure 12
Left male gonopod of O. gracilis. (A) Mesal view, anterior to the left. (B) Solenomerite and medial branch of the solenophore of the telopodite, lateral view, anterior to the right. False colour SEM. Pale green, gonocoxa; Green, solenomerite; Yellow, prefemur; Pale blue, base of the telopodite; Red, tibiotarsus; Blue, femoral process; Violet, solenophore. Scale bars: A, 200 μm; B, 20 μm.
Figure 13
Figure 13
O. gracilis male sections. Para-midsagittal (A-D, G-H), frontal (E) and transverse (F) paraffin sections of ring VII during stadia IV-VIII. Mallory's triple stain. (A) Stadium IV. (B) Stadium V. (C) Stadium VI. (D) Stadium VII. (E-H) Stadium VIII. gA, gonopod apodeme; ga, gonopod abductor muscle; gp, gonopod protractor muscle; gr, gonopod retractor muscle; gt, gut; mf, muscle fiber; nc, nerve cord; pe, prefemur extensor muscle; sa, solenomerite abductor muscle; tA, tracheal pouch apodeme; arrowheads, possibly undifferentiated tissue. Anterior to the left, scale bars 200 μm.
Figure 14
Figure 14
O. gracilis male late stadium VII (pharate phase). Three sub-phases are distinguishable. (A-C) Fused EDF-stacks; lateral view. (D-F) Para-midsagittal paraffin sections; Mallory's triple stain. A and D, first step of the pharate phase: the gonopod primordium is formed by three parts, separated by two constrictions; in section only the epidermis is visible (arrowhead). B and E, second step of the pharate phase: an elongated structure is visible inside the detached cuticle of the gonopod primordium; the gonopod primordium contains a mass of tightly packaged cells, distally branched (arrow). C and F, third step of the pharate phase (see text): the distal processes of the gonopod telopodite are recognizable under the transparent old cuticle; branching of distal telopodite parts is very advanced (arrows). Anterior to the left, scale bars 100 μm.
Figure 15
Figure 15
O. gracilis adult male. Cuticle structure of trunk ring VII (front view) with a scheme of extrinsic musculature of left gonopod. SEM after the digestion of the internal soft tissues. gA, gonopod apodeme; ga, gonopod abductor muscle; gp, gonopod protractor muscle; gr, gonopod retractor muscle; tA, tracheal pouch apodeme. Scale bar 200 μm.

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