Gyrodactylid developmental biology: historical review, current status and future trends

Cable, Joanne ORCID: https://orcid.org/0000-0002-8510-7055 2002. Gyrodactylid developmental biology: historical review, current status and future trends. International Journal for Parasitology 32 (3) , pp. 255-280. 10.1016/S0020-7519(01)00330-7

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Abstract

In the viviparous gyrodactylids, embryos develop one inside another within the parental uterus, a phenomenon with major implications for the biology of this species-rich group. Development occurs via two routes: first-born daughters develop at the centre of an embryo cluster in utero, whereas all other daughters develop from oocytes. The resulting offspring are, however, morphologically indistinguishable. We review here the history of gyrodactylid embryology in the context of current knowledge and, present additional cytogenetic and ultrastructural observations of embryonic development. These progenetic parasites are highly modified for viviparity; oocyte maturation and sperm storage occur in a single chamber, the Egg Cell Forming Region, and a mature oocyte passes into the uterus after the birth of the preceding, fully developed offspring. The uterus has a syncytial lining derived from anterior and posterior cap cells. These cells are the first to differentiate in the female reproductive system and may be involved in controlling development. Embryos receive nutrients via the uterus rather than from vitelline cells. Traditionally, development of the first-born daughter has been considered a form of polyembryony, although paedogenesis has also been suggested. In contrast to previous studies, we could not trace lineage of the first-born daughter to a single quiescent macromere. However, only mitotic divisions have been conclusively observed in the intraembryonic generation, indicating an asexual origin. All other daughters are formed from meiotically derived oocytes by sexual reproduction or automictic parthenogenesis. The latter may involve pre-meiotic doubling of chromosomes, but the precise mechanism and the relative proportion of sexual and parthenogenetic offspring are unknown. Exceptionally, cleavage in Gyrodactylus spp. occurs by duets rather than quartets (a pattern previously only recorded in acoels) and is characterised by extensive cell rearrangements. Blastomeres may be connected by fine cytoplasmic processes or completely disassociated and are readily redistributed by the muscular actions of the parental uterus. This process resembles ‘Blastomeren-Anarchie’ of rhabdocoels but without the structural support of vitelline cells. It prevents generation of early cell fate maps and indicates regulative, rather than mosaic, development. Structures such as the gut and excretory system differentiate late, and are highlighted, together with the attachment apparatus, as examples of post-embryonic differentiation. Molecular and cellular techniques are now essential to further elucidate mechanisms of gyrodactylid reproduction, which will in turn contribute to current debates with animal embryology.

Item Type:	Article
Date Type:	Publication
Status:	Published
Schools:	Biosciences
Subjects:	Q Science > QH Natural history > QH301 Biology Q Science > QH Natural history > QH426 Genetics Q Science > QL Zoology
Uncontrolled Keywords:	Gyrodactylus; Embryology; Cleavage; Blastomere anarchy; Chromosome
Additional Information:	Review article.
Publisher:	Elsevier
ISSN:	0020-7519
Last Modified:	27 Oct 2022 08:17
URI:	https://orca.cardiff.ac.uk/id/eprint/61873

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