Adaptations for matrotrophy in the female reproductive system in the pseudoscorpion Chelifer cancroides (Chelicerata: Pseudoscorpiones, Cheliferidae)

Abstract

Pseudoscorpiones (pseudoscorpions, false scorpions) is an order of small terrestrial chelicerates. While most chelicerates are lecithotrophic, that is, embryos develop due to nutrients (mostly yolk) deposited in the oocyte cytoplasm, pseudoscorpions are matrotrophic, that is, embryos are nourished by the female. Pseudoscorpion oocytes contain only a small amount of yolk. The embryos develop within a brood sac carried on the abdominal site of the female and absorb nutrients by a pumping organ. It is believed that in pseudoscorpions nutrients for developing embryos are produced in the ovary during a postovulatory (secretory) phase of the ovarian cycle. The goal of our study was to analyze the structure of the female reproductive system during the secretory phase in the pseudoscorpion Chelifer cancroides, a representative of the family Cheliferidae, considered to be one of the most advanced pseudoscorpion taxa. We use diverse microscopic techniques to document that the nutritive fluid is produced not only in the ovaries but also by the epithelial cells in the oviducts. The secretory active epithelial cells are hypertrophic and polyploid and release their content by fragmentation of apical parts. Our observations also indicate that fertilization occurs in the oviducts. Moreover, in contrast to previous findings, we show that secretion of the nutritive material starts when the fertilized oocytes reach the brood sac and thus precedes formation of the pumping organ. Summing up, we show that C. cancroides exhibits traits of advanced adaptations for matrotrophy due to coordinated secretion of the nutritive fluid by the ovarian and oviductal epithelial cells, which substantially increases the efficiency of nutritive fluid formation. Since the secretion of nutrients starts before formation of the pumping organ, we suggest that the embryos are able to absorb the nutritive fluid also in the early embryonic stages.

Small body size of pseudoscorpions and a distinct architecture of the ovary: A step to miniaturization?

“…In C. museorum (Figures 2a and 5a,c) and A. ferum (Figure 1b The structure of the female gonads in pseudoscorpions has been ana lyzed in a very few pseudoscorpion species including Garypus japonicus (Beier, 1952) (Garypidae) (Makioka, 1976(Makioka, , 1979, Pselaphochernes scorpioides (Hermann, 1804) (Chernetidae) (Weygoldt, 1969), and C. cancroides (Cheliferidae) (Badian & Ogorzałek, 1982;Jędrzejowska & Garbiec, 2020;Jędrzejowska et al, 2013). These studies unam biguously indicate that the mature ovaries in pseudoscorpions are unpaired tubular and grape shaped organs.…”

“…During the first phase, termed oogenic, the oocytes grow and mature. In the second phase, named secretory, which starts after ovulation, the oocyte growth is ceased and the ovarian and oviductal epithelial cells secrete the nutritive fluid to nourish developing embryos (Jędrzejowska & Garbiec, 2020;Jędrzejowska et al, 2013;Makioka, 1976Makioka, , 1979.…”

“…In our previous papers, we focused on two different as pects of the ovary structure in Chelifer cancroides (Linnaeus, 1758), that is, differentiation of the ovarian somatic cells during ovarian development (Jędrzejowska et al, 2013) and synthesis of the nutritive fluid during the secretory phase (Jędrzejowska & Garbiec, 2020). In this contribution, we aimed to describe the ovary structure of Cheiridium museorum (Leach, 1817) and Apocheiridium ferum (Simon, 1879), pseudoscorpions from the family Cheiridiidae.…”

Spectacular alterations in the female reproductive system during the ovarian cycle and adaptations for matrotrophy in chernetid pseudoscorpions (Pseudoscorpiones: Chernetidae)

“…Due to this hypertrophy, the postovulatory stalks become the most voluminous structures in the ovary. Our quite recent findings 32 revealed that in Chelifer two organs of the female reproductive system, that is, the ovary and the oviducts, are involved in the synthesis of the nutritive fluid. We also showed that during the secretory phase of the ovarian cycle, stalk cells together with epithelial wall cells of the ovary and oviducts undergo multistep hypertrophy and polyploidization and show structural similarities of secretory active cells 32 .…”

“…The embryonic development of C. cancroides is considered to show the most specialized traits 16 . Our previous investigations 32 revealed that in C. cancroides , secretion of the nutritive fluid is amplified due to the involvement in this process not only the epithelial cells of the ovary but also the oviducts. We also showed that the somatic cells that participate in the synthesis of nutritive fluid become highly enlarged as a result of multistep hypertrophy and polyploidization.…”