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Editorial
doi: 10.1186/1742-9994-3-2.

A review of the correlation of tergites, sternites, and leg pairs in diplopods

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Editorial

A review of the correlation of tergites, sternites, and leg pairs in diplopods

Ralf Janssen et al. Front Zool..

Abstract

In some arthropods there is a discrepancy in the number of dorsal tergites compared to the number of ventral sternites and leg pairs. The posterior tergites of the Diplopoda (millipedes) each cover two sternites and two pairs of legs. This segment arrangement is called diplosegmentation. The molecular nature of diplosegmentation is still unknown. There are even conflicting theories on the way the tergites and sternites/leg pairs should be correlated to each other. The different theories are based either on embryological analyses or on studies of the adult morphology and turned out to be not compatible with each other. We have previously used the expression patterns of segmentation genes in the pill millipede Glomeris marginata (Myriapoda: Diplopoda) to study millipede segmentation. Here we review the existing models on the alignment of tergites and leg pairs in millipedes with special emphasis on the implications the gene expression data have on the debate of tergite and leg pair assignment in millipedes. The remarkable outcome of the gene expression analysis was that (1) there is no coupling of dorsal and ventral segmentation and, importantly, that (2) the boundaries delimiting the tergites do neither correlate to the embryonic boundaries of the dorsal embryonic segments nor to the boundaries of the ventral embryonic segments. Using these new insights, we critically reinvestigated the correlation of tergites, sternites, and leg pairs in millipedes. Our model, which takes into account that the tergite boundaries are different from the dorsal embryonic segment boundaries, provides a solution of the problem of tergite to sternite/leg pair correlation in basal milipedes with non-fused exoskeletal elements and also has implications for derived species with exoskeletal rings. Moreover, lack of coupling of dorsal and ventral segmentation may also explain the discrepancy in numbers of dorsal tergites and ventral leg pairs seen in some other arthropods.

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Figures

Figure 1
Figure 1
Myriapod groups with differences in dorsal and ventral segmentation. (A) A maleScutigerella immaculata(Myriapoda: Symphyla). Note the different number of dorsal units (15 tergites) and ventral units (twelve pairs of trunk legs). (B) Specimen ofPauropus huxleyi(Myriapoda: Pauropoda). Note that nine pairs of trunk legs are present, contrasting with only seven tergites (including anal plate). Both species are shown in dorsal aspect, anterior to the left. After [19].
Figure 2
Figure 2
Dorsoventral discrepancies in millipedes (Myriapoda: Diplopoda). (A) Dorsal view of a femaleGlomeris marginata, anterior to the top. This species has twelve tergites. (B) Ventral view of a femaleGlomeris marginata. This view reveals the presence of 17 pairs of trunk legs. Also note the lateral pleurites, which are not fused to the tergites or sternites. This species does not form exoskeletal rings. (C) A generalized juliform diplopod, lateral aspect, anterior to the left. In this diplopod group sternites, pleurites and tergites are fused into rigid armour rings, which give the trunk its annulated ("segmented") appearance. Only the first tergite, the neck-shield or collum, is free,i.e.not fused to any other component. Note that the first three armour rings bear a single pair of legs, whereas all following rings have two leg-pairs each. A and B are drawn after specimens preserved in methanol. C has been modified and simplified from [19].
Figure 3
Figure 3
Model for tergite – sternite/leg pair correlation in millipedes based on morphological evidence from adult ring-forming millipedes. The model is based on the way the tergites and sternites are fused into rings in ring-forming millipede species. Tergites are denoted with roman numbers (I–VI), sternites and leg pairs are denoted with Arabic numbers (1–8). For explanatory reasons, the post-maxillary segment is drawn between the head and the first trunk segment; in fact this segment is the last segment of the head. The way the tergites and sternites fuse into rings in ring-forming species as indicated by same shade of blue for one ring in panel B. This fusion into rings is used in this model to correlate tergites with sternites/leg pairs. The hypothetical extrapolation for the tergite – sternite/leg pair correlation in non-ring-forming species is depicted in panel A. For details, see text.
Figure 4
Figure 4
Summary of the formation of dorsal tissue during embryonic development inGlomeris marginata. Embryos are stained with the nuclear fluorescent dye DAPI. The developmental stages are as indicated; note that these stages are before dorsal closure, the lateral tissue on both sides of the germ band is the future dorsal tissue (details see text). (A) Trunk region of a stage 3 embryo (staging see [4,6]). At this stage the head segments (only gnathal segments visible here) and the first four metameric units of the ventral trunk have formed. Additional trunk metameric units will be added from the posterior growth zone (gz). At this stage thede novoformation and outgrowth of the dorsal tissue (lateral plates) commences (filled circle and asterisks). The asterisks mark the dorsal tissue aligned with the trunk segments. The filled circle marks the common dorsal tissue of the gnathal segments. (B) Stage 4 embryo. The outgrowth of the lateral plates proceeds (asterisks). Note that the growth zone now gives rise to ventral as well as dorsal tissue (arrowhead). (C) Stage 4.1 embryo. The fifth ventral trunk metamere has formed from the growth zone. (D) Stage 5 embryo. The embryo starts to bend in to form the characteristic shape of a "pill". The sixth ventral trunk metamere has formed. Note that the fifth and sixth ventral metameres share one common dorsal tissue that has been added from the growth zone. (E) Stage 6.1 embryo. The embryo has bent in completely. Roman numerals denote the future tergites. (F) Stage 7 embryo. The bipartite body plan of the millipede composed of head and trunk becomes clear. The outgrowth of the dorsal plates has almost finished and the dorsal tissues meet at the back of the embryo to complete dorsal closure. Note that the constrictions between the tergites are clearly visible at this late embryonic stage. Anterior is always to the left. A–D are ventral views, E and F are lateral views. Abbreviations: lb: labrum; an: antennal segment; pmd: pre-mandibular segment; md: mandibular segment; mx: maxillary segment; p: post-maxillary segment; gz: growth zone; 1–6: ventral leg bearing metameric unit 1–6; I–VI: tergites I–VI.
Figure 5
Figure 5
Model for tergite – sternite/leg pair correlation in millipedes based on embryonic evidence from basal non-ring-forming millipedes. The model is based on the way the dorsal and ventral metameric units form in the embryo. Tergites are denoted with roman numbers (I–VI), sternites and leg pairs are denoted with Arabic numbers (1–8). This model assumes that the tergites are directly derived from the dorsal embryonic segments, and accordingly correlates the tergites with the sternites and leg pairs (panel A). Panel B: hypothetical extrapolated model for ring-forming millipedes. The situation in ring-forming millipedes can only be explained by assuming a shift in the fusion of dorsal and ventral exoskeletal elements (indicated as blue shades in panel B). For instance, the first ring in the ring-forming millipedes forms via the fusion of tergite II to the leg pair 1, the second ring via the fusion of tergite III with leg pair 2, and so on; the different shades of blue in panel B represent the rings in adult specimen. The first tergite is the collum that is not fused to any leg pair. This model leads to a different tergite – sternite/leg pair correlation as in the 'adult morphological' model in Fig. 3. For details, see text.
Figure 6
Figure 6
Expression of theengrailedgene in the embryo of the millipedeGlomeris marginata. Shown is the localisation ofengrailedtranscripts via in situ hybridisation. The embryo proper is located on the surface of a large yolk mass that is consumed as the embryo develops. In the stages shown, the yolk mass is still very large, so that the embryo proper is still open dorsally. This is the reason why the future dorsal tissue is still located "laterally", i.e. next to the ventral tissue (indicated in the figures). This will change in very late stages, when the yolk is consumed entirely and the "lateral" portions of the germ band fuse dorsally (dorsal closure). The ventralengrailedexpression marks the posterior part of the ventral segmental units. The ventral stripes are marked with p,1,2,3,4,5,6,7. Dorsally, theengrailedtranscripts are in stripes (asterisks) localised at a different intrasegmental position as on the ventral side. The dorsal stripe ofengrailedexpression is not associated with any morphological structure at this stage, but is in the middle of the dorsal metameric units, which also becomes obvious if one compares with figure 7 B and D. The location of the future ventral and dorsal tissue is marked (dorsal-ventral-dorsal or d-v-d). Note that the dorsal tissue is on the lateral part on both sides of the germ band at this stage; during dorsal closure these tissues fuse on the dorsal side to give rise to one dorsal tissue. The head segments are marked in the embryo in panel D, for details we refer to [4,6]. (A and B): embryo at stage 4.1, (C and D): embryo at stage 5 (staging see [4,6]). Panel A and C show the bright field micrograph of the in situ hybridisation staining; panel B and D show the epifluorescence image of the embryo in A and C, respectively, in which the nuclear DAPI staining becomes bright, and the in situ hybridisation staining appears dark due to quenching of the fluorescence. Abbreviations: d: dorsal; v: ventral; lb: labrum; oc: ocular segment; an: antennal segment; pmd: pre-mandibular segment; md: mandibular segment; mx: maxillary segment; p: post-maxillary segment; 1–7: ventral leg bearing segment 1–7.
Figure 7
Figure 7
Expression of thewinglessgene in the embryo of the millipedeGlomeris marginata. Shown is the localisation ofwinglesstranscripts via in situ hybridisation. The ventralwinglessexpression is located just anterior to the position of theengrailedstripe (see Fig 6). Dorsally, nowinglesstranscripts are detected. The asterisks mark the dorsal metameric units, which are the lateral plates of Dohle [4]. The location of the future ventral (v) and dorsal (d) tissue is marked, see also figure 6. (A and B): embryo at stage 4, (C and D): embryo at stage 4.1 (staging see [4,6]). Panel A and C show the bright field micrograph of the in situ hybridisation staining; panel B and D show the epifluorescence image of the embryo in A and C, respectively, in which the nuclear DAPI staining becomes bright, and the in situ hybridisation staining appears dark due to quenching of the fluorescence. Abbreviations: d: dorsal; v: ventral; lb: labrum; an: antennal segment; pmd: pre-mandibular segment; md: mandibular segment; mx: maxillary segment; p: post-maxillary segment; 1–6: ventral leg bearing segment 1–6, s: stomadeum.
Figure 8
Figure 8
Dorsalengrailedstripes mark the forming tergite borders. Shown is an in situ hybridisation forengrailedin a stage 6Glomerisembryo. At this stage the embryo rolls in (see leg pairs at ventral side in B) and it becomes clear that the dorsal stripes ofengrailedexpression are co-localised with the tergite borders. Panel A shows a bright field image of the in situ hybridisation staining, panel B shows an epifluorescence image of the same embryo, in which the nuclear DAPI staining becomes bright, and the in situ hybridisation staining appears dark due to quenching of the fluorescence. The future tergites are denoted with roman numbers (I–VI).
Figure 9
Figure 9
Model for tergite – sternite/leg pair correlation in millipedes based on the lack of coupling of dorsal and ventral segmentation. Our model is based on the way the dorsal and ventral metameric units form in the embryo as well as on gene expression data that imply a lack of coupling of dorsal and ventral segmentation. Key in the model is the fact that the tergite boundaries do neither correlate to dorsal embryonic segment boundaries, nor to ventral embryonic segment boundaries. Tergites are denoted with roman numbers (I–VI), sternites and leg pairs are denoted with Arabic numbers (1–8). (A) The tergite boundaries form in approximately the middle of the dorsal metameric units (red line); consequently the tergites are shifted compared to the ventral segmental units in basal non-ring-forming millipedes likeGlomeris. (B) The model can be extrapolated to ring-forming millipedes as indicated by blue shading. In most ring-forming millipedes tergite II will fuse with ventral segment 1, tergite III with ventral segment 2, and so on. (C) However, in some ring-forming millipedes (Spirobolida) tergite II will fuse with ventral segment 2, tergite III with ventral segment 3, and so on. For details, see text.
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