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Unusual morphological adaptations and processes associated with viviparity in an epizoic dermapteran - PubMed

  • ️Mon Jan 01 2018

Unusual morphological adaptations and processes associated with viviparity in an epizoic dermapteran

Szczepan M Bilinski et al. PLoS One. 2018.

Abstract

Matrotrophic viviparity is a reproductive pattern in which offspring develop inside a female's body which provides gas exchange and nutrients necessary for development. Besides placental mammals, structural and physiological aspects of matrotrophic viviparity are poorly characterized. In insects, the majority of species is oviparous, i.e. lay eggs, and viviparous reproduction has been reported only in 11 out of 44 orders, including earwigs (Dermaptera). Among dermapterans, matrotrophic viviparity has been reported in two epizoic subgroups: Arixeniidae and Hemimeridae. Here, we provide morphological evidence for distinct adaptations for this mode of viviparity in embryonic and maternal tissues in a representative of the latter subgroup, Hemimerus talpoides. Our study reveals a novel mechanism of maternal contribution to embryonic development which operates during oogenesis and involves characteristic modification of endoplasmic reticulum cisternae. Conspicuous and apparently inactive para-crystalline stacks of the endoplasmic reticulum are deposited in the oocyte cytoplasm and become activated during early embryonic development. Our analyses indicate additionally that in Hemimerus, transformed follicular/ovarian cells (on the mother's side) and an evagination of the dorsal vessel (on the embryo's side) converge to form a cephalic vesicle, structure analogous to a placenta. The cellular architecture of this unusual "cephalic placenta" points to its participation in an exchange of low molecular weight substances between a mother and developing embryo.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Embryonic follicle and early embryo.

(A) SEM micrograph showing sequentially more advanced embryonic follicles (ef) attached to a lateral oviduct (ov), trachea (t). Scale bar: 1 mm. (B) Early embryo inside the embryonic cavity (emc); note a germ band (gb), amnion (a) and egg cytoplasm (egc) comprising stacks of ER (arrows); arrowheads indicate follicular epithelium surrounding the embryonic cavity; Nomarski interference contrast. Scale bar: 50 μm. (C) Fragment of the egg cytoplasm densely packed with highly organized ER stacks (ERst), mitochondria (m); TEM micrograph. Scale bar: 2 μm.

Fig 2
Fig 2. Embryo after dorsal flexion of the germ band.

(A) Longitudinal section through a central region of the embryo; note the egg cytoplasm (egc) surrounded by the germ band (gb); yolk cell nucleus (yn), margins of the germ band are indicated by double arrows, the wall of the embryonic follicle (ew); semithin section stained with methylene blue. Scale bar: 100 μm. (B) Individual yolk cell comprising ER stacks (arrows); yolk cell nucleus (yn); Nomarski interference contrast. Scale bar: 50 μm. (C) TEM micrograph showing dispersing ER stacks; note that marginally located ER elements (arrowheads) are partly separated from the stack (ERst) and covered with ribosomes. Scale bar: 1 μm. (D) Canonical ER network in association with ER stack (ERst); vacuoles (v); TEM micrograph. Scale bar: 1 μm.

Fig 3
Fig 3. Late embryo.

(A) Embryo soon after dorsal closure and katatrepsis (the stage during which the embryo assumes its final position on the egg surface); note the cephalic vesicle (asterisk) located between the head (hd) and the first thoracic segment (th1); photographed under a stereomicroscope. Scale bar: 1 mm. (B) SEM micrograph of a slightly older embryo; at this stage the cephalic vesicle (asterisk) is substantially smaller in relation to the head and thorax. Scale bar: 500 μm. (C) Front view of the same embryo as in b; note that the surface of the cephalic vesicle (asterisk) is covered with follicular cells. SEM micrograph. Scale bar: 100 μm. Abdomen (ab), antennae (an), cerci (ce), head (hd), first thoracic segment (th1), thoracic limbs (li), maxillary palps (mp).

Fig 4
Fig 4. Cephalic vesicle.

(A) Longitudinal section through the anterior region of the embryonic follicle containing a late embryo; note that the cephalic vesicle (asterisk) comprises a diverticulum (div) of the dorsal vessel (dv); the wall of the embryonic follicle (ew), invaginated body wall surrounding the cephalic vesicle (arrows); embryonic cavity (ec), follicular cell network present in the embryonic cavity (arrowheads), esophagus (es), head (hd), first thoracic segment (th1), tritocerebrum (tr); semithin section stained with methylene blue. Scale bar: 100 μm. (B) Transverse section through the wall of the cephalic vesicle; note basement lamina (bl) of the dorsal vessel and highly extended projections of the follicular cells (fcp) covering the lamina; magnified area (boxed in B) showing basement lamina filaments (inset). Scale bars: 2 μm, inset: 400 nm. (C) SEM micrograph of a fractured cephalic vesicle; basement lamina (bl), projections of the follicular cells (fcp), lumen of the dorsal vessel diverticulum (div) filled with haemolymph macromolecules. Scale bar: 5 μm.

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This study was funded by a research grant OPUS 11 (UMO- 2016/21/B/NZ8/00560) from Narodowe Centrum Nauki (National Science Centre, Poland) to SMB. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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