Abstract
BackgroundOnychophorans, commonly known as velvet worms, display a remarkable diversity of reproductive strategies including oviparity, and placentotrophic, lecithotrophic, matrotrophic or combined lecithotrophic/matrotrophic viviparity. In the placentotrophic species, the embryos of consecutive developmental stages are attached to the uterus via a placental stalk, suggesting they might be transported passively towards the vagina due to proximal growth and distal degeneration of tissue. However, this assumption has never been tested using specific markers. We therefore analyzed the patterns of cell proliferation and apoptosis in the genital tracts of two placentotrophic peripatids from Colombia and a non-placentotrophic peripatopsid from Australia.ResultsAll three species show a high number of apoptotic cells in the distal portion of the genital tract near the genital opening. In the two placentotrophic species, additional apoptotic cells appear in ring-like vestigial placentation zones of late embryonic chambers. While moderate cell proliferation occurs along the entire uterus in all three species, only the two placentotrophic species show a distinct proliferation zone near the ovary as well as in the ring-like implantation zone of the first embryonic chamber. In contrast to the two placentotrophic species, the non-placentotrophic species clearly does not show such regions of high proliferation in the uterus but exhibits proliferating and apoptotic cells in the ovarian stalks. While cell proliferation mainly occurs in stalks carrying maturating oocytes, apoptosis is restricted to stalks whose oocytes have been released into the ovarian lumen.ConclusionsOur results confirm the hypothesis that the uterus of placentotrophic onychophorans grows proximally but is resorbed distally. This is supported by the detection of a proximal proliferation zone and a distal degenerative zone in the two placentotrophic species. Hence, cell turnover might be responsible for the transport of their embryos towards the vagina, analogous to a conveyor belt. Surprisingly, the distal degenerative zone is also found in the non-placentotrophic species, in which cell turnover was unexpected. These findings suggest that the distal degenerative zone is an ancestral feature of Onychophora, whereas the proximal proliferation zone might have evolved in the last common ancestor of the placentotrophic Peripatidae.
Highlights
Onychophorans, commonly known as velvet worms, display a remarkable diversity of reproductive strategies including oviparity, and placentotrophic, lecithotrophic, matrotrophic or combined lecithotrophic/ matrotrophic viviparity
The implantation of the embryo is typically accompanied by a modification. This confirms previous, histological and light microscopical observations on the genital tracts of the placentotrophic onychophorans Macroperipatus torquatus and Epiperipatus trinidadensis [14, 20], where the proximal uterus might comprise a constantly growing region with new fertilized eggs becoming implanted at regular intervals, while resorption of the uterus wall is evident throughout the lower uterus containing the two largest embryos [14, 20]
Our results confirm a previous assumption that the genital tracts of the placentotrophic viviparous Peripatidae is constantly growing at the proximal end while tissue is resorbed at the distal end near the genital opening, retaining a constant length of the uterus while the embryos are transported towards the genital opening in a conveyor-like fashion
Summary
Onychophorans, commonly known as velvet worms, display a remarkable diversity of reproductive strategies including oviparity, and placentotrophic, lecithotrophic, matrotrophic or combined lecithotrophic/ matrotrophic viviparity. The embryos of consecutive developmental stages are attached to the uterus via a placental stalk, suggesting they might be transported passively towards the vagina due to proximal growth and distal degeneration of tissue. This assumption has never been tested using specific markers. Placentotrophic viviparity might be a derived feature of the Neopatida (neotropical Peripatidae) alone or the Neopatida plus the peripatid Mesoperipatus tholloni from tropical Africa, as the reproductive mode and embryonic development are unknown from the latter [1, 2]
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