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Evolutionary origin and functioning of pregenital abdominal outgrowths in a viviparous insect, Arixenia esau - PubMed

  • ️Tue Jan 01 2019

Evolutionary origin and functioning of pregenital abdominal outgrowths in a viviparous insect, Arixenia esau

Waclaw Tworzydlo et al. Sci Rep. 2019.

Abstract

Although pregenital abdominal outgrowths occur only rarely in pterygote insects, they are interesting from the evolutionary viewpoint because of their potential homology to wings. Our previous studies of early development of an epizoic dermapteran, Arixenia esau revealed that abdominal segments of the advanced embryos and larvae, growing inside a mother's uterus, are equipped with paired serial outgrowths. Here, we focus on the origin and functioning of these outgrowths. We demonstrate that they bud from the lateral parts of the abdominal nota, persist till the end of intrauterine development, and remain in contact with the uterus wall. We also show that the bundles of muscle fibers associated with the abdominal outgrowths may facilitate flow of the haemolymph from the outgrowths' lumen to the larval body cavity. Following completion of the intrauterine development, abdominal outgrowths are shed together with the larval cuticle during the first molt after the larva birth. Using immunohistochemical and biochemical approaches, we demonstrate that the Arixenia abdominal outgrowths represent an evolutionary novelty, presumably related to intrauterine development, and suggest that they are not related to serial wing homologs.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1

Pregenital abdominal outgrowth development. (a,b) Fragments of embryo abdomens during the dorsal closure. Arrowheads point to the region where epithelial flanks meet and fuse during the dorsal closure. Asterisks indicate abdominal outgrowths (a) or their lobes (b); Cerci (ce), legs (le). (c) Lateral view of the first instar larva after liberation from the egg envelope. Head (h), thorax (th), abdomen (ab). Note that lobes of the abdominal outgrowths (asterisks) are arisen and protrude almost perpendicularly from the abdomen. (a,b) SEM, (c) stereomicroscope.

Figure 2
Figure 2

Pregenital abdominal outgrowth fate. (a–e) Larval exuvies shed during the 1st molt after birth. Antennae (an), head (h), thorax (th), abdomen (ab), cerci (ce). Only two pairs of legs (le) were retained after the molt. Note that in addition to bristles, the abdomens bear collapsed serial outgrowths (arrows in b,c) located on lateral sides of abdominal nota (terga). (d) Collapsed, folded inwards, outgrowth (white arrowheads). (e) Inner surface of collapsed outgrowth with small pieces of decomposed tissue attached. (f) Abdominal nota of older larvae are flat, devoid of outgrowths or their remnants and bear elongated bristles only. (a–c) stereomicroscope; (d–f) SEM.

Figure 3
Figure 3

Detection of Vestigial (Vg) in Arixenia embryo tissues. Immunoblots with antibodies against Vg; MW – molecular weight markers.

Figure 4
Figure 4

Structure of pregenital abdominal outgrowth. (a–c) The lumen of the outgrowth. Note muscle fibers (mu) surrounded by fat body stripes (fb). Uterus wall (uw), arrows point to the muscle attachments. (d–f) Basal part of epithelial cells (ep), basal lamina (bl). Note that the muscle fibers (mu) are attached to filamentous basal lamina (bl). Mitochondrion (m), epithelial cell nucleus (n). Filaments of the basal lamina are parallel arranged with characteristic regular axial periodicity. Cross-sectioned filaments are shown and measured in (e). (a,c) SEM, (b) LM, (d–f) TEM.

Figure 5
Figure 5

Organization of pregenital abdominal outgrowth. (a,b) Computer aided 3D reconstruction of the abdominal outgrowth. For these reconstructions 120 serial sections were used. Muscle fibers (red), muscle attachments (orange), epithelial cells (blue, omitted in b), arrowheads indicate muscles attached to the cuticle surrounding the outgrowth base. (c–e) Partial 3D reconstructions of the outgrowth “empty” lobe. For these reconstructions 10 serial sections were used. Muscle fibres (red), muscle attachments (orange), epithelial cells (blue), cuticle (gray), fat body (green), white arrows and corresponding numbers indicate rotation angle. (f,g) Fragments of the representative sections used for the reconstructions shown in. (a,b) Epithelial cells (ep), fat body (fb), muscle fibers (mu). Arrows point to the muscle attachments. (f–g) LM.

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