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

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.

Morphogenesis of the ovarian follicular epithelium during initial stages of embryogenesis of the viviparous earwig, Hemimerus talpoides

“…The early phase of Hemimerus development is highly modified (derived) revealing important adaptations to the viviparous mode of development and/or matrotrophy (Bilinski, Jaglarz, Halajian, & Tworzydlo, ; Hagan, ; Heymons, ). Moreover, the organization of the Hemimerus embryo is so unusual that even its main axes (antero‐posterior and dorso‐ventral) are difficult to define or recognize.…”

“…After initiation of the embryonic development, the translucent vacuoles populating the cytoplasm of fully developed oocytes (compare Bilinski, Halajian, & Tworzydlo, ) start to expel their content to the perioocytic space, that is, the space between the oocyte/embryo and surrounding follicular epithelium (Figure ). This process leads to substantial reduction of the embryo volume and simultaneous formation of a spacious incubation chamber (pseudoplacental cavity in Hagan, ) in which the embryo develops (Bilinski, Halajian, & Tworzydlo, ; Bilinski, Jaglarz, Halajian, & Tworzydlo, ). As subsequent vacuoles expel their contents, the chamber gradually expands.…”

“…(b) Anterior part of the embryo during organogenesis. Note posterior part of the head (hd), anterior part of the thorax (th) and diverticulum (div) of the dorsal vessel (dv) projecting outside of the embryo through the opening in the body wall (for the comprehensive description of this stage see Bilinski, Jaglarz, Halajian, & Tworzydlo, ). am, amnion; egc, egg cytoplasm; es, esophagus; gb, germ band; ic, incubation chamber; tFC, transformed FC; tri, tritocerebrum…”

“…Specimens of Hemimerus talpoides Walker (1871) were collected from the fur of Gambian pouched rats (Cricetomys gambianus) trapped in Lajuma Research Centre (see Bilinski, Halajian, & Tworzydlo, 2017;Bilinski, Jaglarz, Halajian, & Tworzydlo, 2018 for further details). Ten specimens of H. talpoides were used.…”

“…This extreme reproduction mode coincides well with specific traits (characters) of hemimerid oogenesis: the fully developed oocytes of this taxon are completely yolkless and not protected by thick and rigid egg envelopes, instead their cytoplasm is loaded with characteristic, noncannonical organelles: highly organized (paracrystalline) stacks of the endoplasmic reticulum and irregular, translucent vacuoles (Bilinski, Halajian, & Tworzydlo, ; Bilinski, Jaglarz, & Tworzydlo, ). Our preceding electron microscopy studies have shown that these organelles are essential during early stages of the embryonic development (Bilinski, Jaglarz, Halajian, & Tworzydlo, ; Bilinski, Jaglarz, & Tworzydlo, ).…”