A Taxonomic Survey of Female Oviducal Glands in Chondrichthyes: A Comparative Overview of Microanatomy in the Two Reproductive Modes.

Martina Francesca Marongiu,Noemi Pascale,Riccardo Porceddu,Andrea Bellodi,Maria Cristina Follesa,Paola Pesci,Antonello Mulas,Cristina Porcu,Alessandro Cau

doi:10.3390/ani11092653

Martina Francesca Marongiu, Noemi Pascale + Show 7 more

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https://doi.org/10.3390/ani11092653

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Abstract

Simple SummaryThe oviducal gland (OG) is a specialized region of the reproductive female system in cartilaginous fish located in the anterior oviduct. Its biological importance is closely related to the reproductive modalities of these species, and its basic function is the production of the egg jellies, the tertiary envelope formation (egg case in oviparous and candle case in viviparous) and sperm storage. Since knowledge on the overall process of Chondrichthyes reproduction is still scarce, in this study we conducted morphological and morphometrical analysis on the OGs belonging to several cartilaginous fish displaying two different reproductive modalities (oviparity and viviparity). Moreover, we paid particular attention to the fate of spermatozoa in the female reproductive tract, which would be useful to better understand the ecology and population dynamics of these species.Oviducal glands (OGs) are distinct expanded regions of the anterior portion of the oviduct, commonly found in chondrichthyans, which play a key role in the production of the egg in-vestments and in the female sperm storage (FSS). The FSS phenomenon has implications for understanding the reproductive ecology and management of exploited populations, but little information is available on its taxonomic extent. For the first time, mature OGs from three lecithotrophic oviparous and four yolk-sac viviparous species, all considered at risk from the fishing impacts in the central western Mediterranean Sea, were examined using light microscopy. The OG microanatomy, whose morphology is generally conserved in all species, shows differences within the two reproductive modalities. Oviparous species show a more developed baffle zone in respect to viviparous ones because of the production of different egg envelopes produced. Among oviparous species, Raja polystigma and Chimaera monstrosa show presence of sperm, but not sperm storage as observed, instead, in Galeus melastomus and in all the viviparous sharks, which preserve sperm inside of specialized structures in the terminal zone.

Highlights

Chondrichthyes, as well as being the only anamniote vertebrate class that exclusively employs internal fertilization during reproduction [1], have several features in common, all resulting in low reproductive potential that makes them highly vulnerable to overfishing (e.g., [2,3])
The goal of this study is to provide a broader taxonomic survey of female oviducal glands across different reproductive modes present in some demersal chondrichthyans inhabiting the Mediterranean Sea
Oviparous females were classified into six stages on the basis of ovary structure and Oviducal glands (OGs) and uterus dimension and texture as follows: stage 1, immature (F1); stage 2, developing (F2); stage 3a, spawning capable (F3A); stage 3b, actively spawning (F3B); stage 4a, regressing (F4A); and stage 4b, regenerating (F4B)

Summary

Introduction

Chondrichthyes, as well as being the only anamniote vertebrate class that exclusively employs internal fertilization during reproduction [1], have several features in common (low growth rate, delayed maturity and long gestation), all resulting in low reproductive potential that makes them highly vulnerable to overfishing (e.g., [2,3]). Chondrichthyan fish exhibit two main modes of reproduction, spanning both oviparity and viviparity. Oviparity (i.e., eggs are enclosed within an egg case and deposited in the sea) is restricted to the orders. Carcharhiniformes, Heterodontiformes, Orectolobiformes, Rajiformes and Chimaeriformes, while viviparity is prevailing in all other chondrichthyan orders [4]. Viviparous species are further subcategorized as lecithotrophic and matrotrophic [5,6]. Depending on the pattern of embryonic nutrition, in the lecithotrophic mode, embryos do not receive any maternal nourishment, which is granted, instead, by a yolk-sac (yolk reserves); in the matrotrophic mode, embryos receive nourishment through ingestion of lipids or mucous (histotrophy) produced by the uterine walls of the mother [5,6]. Oophagy and intrauterine cannibalism (those that eat eggs or other embryos) are enclosed in the matrotrophic reproductive mode [5,6]

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