No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
1 The Maternal-Embryonic Relationship in Viviparous Fishes
Abstract
This chapter discusses the maternal–embryonic relationship in viviparous fishes. Viviparity is a highly successful mode of reproduction that has evolved independently many times and with many variations in widely separated taxonomic groups. It occurs in all classes of vertebrates, except birds, and among many different groups of invertebrates. Initial steps in the evolution of viviparity involved a shift from external to internal fertilization and the retention of fertilized eggs in the female reproductive system. The osmoregulation of early embryos can be accomplished more efficiently and with less expenditure of embryonic energy in a maternally controlled uterine environment, but as development progresses to term, the embryos presumably acquire an increasing degree of osmoregulatory independence. Available evidence suggests that maternal regulation of the osmotic and chemical environment of the embryo also confers a selective advantage on viviparous teleosts. The uterine wall of most viviparous elasmobranchs and the coelocanth both delimits and defines the embryonic environment. The most spectacular maternal specializations for uterine gestation involve the uterine wall and involve (1) the amplification of the surface area in the form of folds, villi, or trophonemata; (2) the production of histotrophe or uterine milk’ (3) the compartmentalization of embryos; and (4) the development of placental attachment sites.
... In contrast, viviparity is a reproductive mode in which females give birth to live young. Viviparity may still be lecithotrophic, meaning that mothers may fully provision eggs before fertilization, but mothers may instead continue to provision the embryo after the egg is fertilized (matrotrophy) (Wourms et al. 1988;Pollux et al. 2009). Matrotrophic viviparity is not unique to therian mammals. ...
... Matrotrophic viviparity is not unique to therian mammals. It is also found in some teleost fishes (Thibault and Schultz 1978;Wourms et al. 1988), reptiles (Guillette 1993;Braz et al. 2016), and amphibians (Wake 2015;Furness and Capellini 2019). All of these other taxa lack a uterus. ...
... However, there is no high-quality reference genome available for facilitating studies of the genomic basis of placentation in Poeciliopsis. Blackstripe Livebearer (Poeciliopsis prolifica) is a species with extensive matrotrophy (Wourms et al. 1988;Reznick et al. 2002). Our preliminary transcriptome sequencing in P. prolifica revealed that only 30-40% of the RNA-seq reads could be mapped to the guppy (Poecilia reticulata) genome, the closest species with a high-quality reference genome (Kunstner et al. 2016;Fraser et al. 2020) in Poeciliids. ...
The blackstripe livebearer Poeciliopsis prolifica is a live-bearing fish belonging to the family Poeciliidae with high level of post-fertilization maternal investment (matrotrophy). This viviparous matrotrophic species has evolved a structure similarly to the mammalian placenta. Placentas have independently evolved multiple times in Poeciliidae from non-placental ancestors, which provides an opportunity to study the placental evolution. However, there is a lack of high-quality reference genomes for the placental species in Poeciliidae. In this study, we present a 674 Mbp assembly of Poeciliopsis prolifica in 504 contigs with excellent continuity (contig N50 7.7 Mb) and completeness (97.2% BUSCO completeness score, including 92.6% single copy and 4.6% duplicated BUSCO score). A total of 27,227 protein-coding genes were annotated from the merged data sets based on bioinformatic prediction and RNA sequencing and homology evidence. Phylogenomic analyses revealed that Poeciliopsis prolifica diverged from the guppy (Poecilia reticulata) ∼19 million years ago. Our research provides the necessary resources and the genomic toolkit for investigating the genetic underpinning of placentation.
... As a result of the absence of this anatomical structure, in viviparous species, the ovary is the only organ involved in gestation (Santamaría-Martín et al., 2021;Turner, 1947;Uribe et al., 2014;Wourms et al., 1988). In viviparous teleost, intraovarian gestation occurs in two different ways: intrafollicular, inside the ovarian follicles as in poeciliids; or intraluminal, into the ovarian lumen, as in goodeids and anablepids (Schindler & Hamlett, 1993;Wourms, 1981). ...
... Matrotrophic nutrition is especially important in species with intraluminal gestation (Morrison et al., 2017). The embryonic organs where this trophic exchange can be mediated are the skin, intestine, and gills (Wourms et al., 1988). Over the last two decades, different types of embryonic nutrition and the development of different placental organs have been described for various viviparous teleost species (Kwan & Patil, 2019;Uribe et al., 2014Uribe et al., , 2018Wourms, 2005). ...
... The transfer of nutrients was analyzed in several viviparous fish species such as Cymatogaster aggregata (Gibbons), Rhacochilus vacca (Girard), I. whitei, and J. lineata (Gardiner, 1978;Richter et al., 1983;Turner, 1940). While prior studies have mentioned the presence of a branchial placenta of J. lineata and describe some morphological aspects (Schindler & de Vries, 1988;Turner, 1940;Wourms et al., 1988), this is the first work where its morphology is analyzed in conjunction with histochemical changes and cell proliferation. The current study revealed the presence of the branchial placenta in ovaries corresponding to gestational stages 6-8 (López-Rodríguez et al., 2017). ...
In viviparous teleosts, intraovarian gestation occurs intrafollicularly, as in poeciliids, or intraluminally, as in goodeids and anablepids. Furthermore, there are two different forms of embryonic nutrition: lecithotrophy and matrotrophy; depending on the species, these can be exclusive or coexist during gestation. In matrotrophic species, nutrients are transmitted from the mother to the embryo and are especially important in species with intraluminal gestation. Jenynsia lineata is a South American viviparous teleost with intraluminal gestation, characterized by eggs with scarce yolk, which is resorbed when embryos are 6 mm long, thus developing a branchial placenta. Using histological, histochemical, and immunohistochemical techniques, the present study describes the characteristics and changes of the ovarian mucosa in J. lineata during gestational and nongestational phases, and analyzes the embryonic pharyngeal epithelium in the branchial placenta. The ovaries of 30 adult female specimens were processed using histological techniques and stained with hematoxylin-eosin, Masson's trichrome, and Alcian Blue pH 2.5/periodic acid Schiff reagent. To detect cell proliferation, we used antiproliferating cell nuclear antigen antibody. In nonpregnant females, eosinophilic granular cells (EGCs) and lympho-cytes were identified in the lamina propria of the tunica mucosa, and melanoma-crophage centers (MMCs) and fibroblasts were identified adjacent to tissue debris in the ovarian folds'. In the cellular debris, an embryo in resorption was observed. In pregnant females, the ovarian mucosa has thin vascularization branches entering the opercular chamber of the embryos, in close contact with the forming gill processes, thereby establishing a branchial placenta. Active cell replacement was observed in these ovarian branches. The identification of fibroblasts, lymphocytes, EGCs, and MMCs adjacent to tissue debris could indicate that these cell types are involved in the embryonic resorption process. Considering the new data obtained in this study on the branchial placenta of J. lineata, we conclude that cell proliferation could be involved in the development of maternal-embryonic interaction. K E Y W O R D S immunohistochemistry, intraluminal gestation, melanomacrophage centers, ovary, viviparous teleost J. Morphol. 2023;284:e21630. wileyonlinelibrary.com/journal/jmor
... Embryonic nutrition can be provided entirely from the maternally supplied yolk (lecithotrophy), or supplemented with post-fertilisation maternal (matrotrophy) [1,2], or paternal (patrotrophy) nutrient provisioning [1,3]. Lecithotrophy and parentotrophy represent endpoints of a complex continuum of embryonic nutritional patterns, with no definitive biological point of distinguishment [4,5], For example, small amounts of inorganic nutrient provisioning (calcium) occur in lecithotrophic-classified viviparous squamates, either mobilised from the eggshell, or via simple placentotrophy [6,7]. ...
... This suggests the ability of parentotrophic embryos to absorb nutrients from their environment may be retained from an egg-laying ancestor. This ability is a prerequisite for parentotrophy, when the absorbed nutrients are acquired from the gestating parent during pregnancy [1,2]. Applying two broad provisioning strategies to vertebrates that exhibit a continuum of nutrient provisioning abilities between lecithotrophy and parentotrophy, makes correctness and consistency difficult. ...
... This ratio has been applied to reptiles [30,31], sharks [32] and bony fishes [3,33]. Wourms et al. [2] were the first to suggest that the degree of post-fertilisation nutrient provisioning could be measured by "the ratio of dry weight of the developed embryo to that of the fertilised egg". This notion has since evolved to the dry mass of the neonate or newborn at birth divided by the dry mass of the recently fertilised egg [24,34]. ...
The source of embryonic nutrition for development varies across teleost fishes. A parentotrophy index (ratio of neonate: ovulated egg dry mass) is often used to determine provisioning strategy, but the methodologies used vary across studies. The variation in source and preservation of tissue, staging of embryos, and estimation approach impedes our ability to discern between methodological and biological differences in parentotrophy indices inter- and intra-specifically. The threshold value used to distinguish between lecithotrophy and parentotrophy (0.6–1) differs considerably across studies. The lack of a standardised approach in definition and application of parentotrophy indices has contributed to inconsistent classifications of provisioning strategy. Consistency in both methodology used to obtain a parentotrophy index, and in the classification of provisioning strategy using a threshold value are essential to reliably distinguish between provisioning strategies in teleosts. We discuss alternative methods for determining parentotrophy and suggest consistent standards for obtaining and interpreting parentotrophy indices.
... This hypothesis is supported by data showing that the assumptions of parent-offspring conflict theory are met for relevant taxa and can explain (Crespi & Semeniuk 2004): (1) the high number of independent origins of viviparity, matrotrophy (direct maternalfetal nutrient transfer), and hemochorial placentation (direct fetal access to the maternal bloodstream); (2) the extreme diversity in physiological and morphological aspects of viviparity and placentation, which usually cannot be ascribed adaptive significance in terms of ecological factors; and (3) divergent and convergent patterns in the diversification of placental structure, function, and developmental genetics. Forms of viviparity itself exhibit notable diversity within eutherian mammals (Rothchild 2003), squamate reptiles (Blackburn 1993), caecilians (Laurin et al. 2000), other amphibians (Wake 1977;Wake & Dickie 1998), and fishes (Wourms 1977(Wourms , 1981Wourms et al. 1988;Compagno 1990;Wourms & Lombardi 1992;Hamlett & Hysell 1998;Hamlett 1999;Zeh & Zeh 2000Furness et al. 2019). Such diversity extends across all taxonomic levels because closely related species, populations, or individuals within populations often differ substantially in fundamental aspects of reproductive mode (Guillette 1981;Packard et al. 1989;Blackburn 1992Blackburn , 1993Blackburn , 1995Blackburn , 1998Heap 1994;Pinella & Laurent 1996;Meisner & Burns 1997;Smith & Shine 1997;Trexler 1997;Fairbairn et al. 1998;Swain & Jones 2000;Thompson et al. 2000;Smith et al. 2001;Reznick et al. 2002). ...
... Thus, clonal reproduction is rare, and multiple paternity is virtually the rule among sexual organisms (Eberhard 1996, p. 413;Birkhead & Parker 1997;Jennions & Petrie 2000;Zeh & Zeh 2001; e.g., in viviparous taxa; Baker et al. 1999;Garner et al. 2002;Saville et al. 2002). Indeed, multiple paternity may be favored by one of the same traits that facilitates the evolution of viviparity, internal fertilization (e.g., Wourms et al. 1988). The possible resultant decrease in paternal investment may increase the offspring's optimal level and thus lead to a higher degree of conflict (Parker 1985); multiple paternity may also generate increased offspring demands through its effects on the evolution of genomic imprinting (Haig & Westoby 1989;Haig 1999Haig , 2000. ...
... Matrotrophy and placentas have evolved repeatedly in viviparous animals, including multiple invertebrate (Campiglia & Walker 1995;Hart et al. 1997;Korniushin & Glaubrecht 2003;Korneva 2005;Ostrovsky et al. 2016) and vertebrate lineages (Steward & Blackburn 1988;Wourms et al. 1988;Wake & Dickie 1998;Wildman et al. 2006). Transitions along the lecithotrophy (pre-fertilization provisioning)-matrotrophy (post-fertilization provisioning) continuum may have far reaching consequences, shaping the evolution of other traits and patterns of biological diversification. ...
... Viviparity, by contrast, is a mode of reproduction characterised by internal fertilisation and egg retention, in which embryos fully develop within the female reproductive tract and are released to the external environment as free-living animals. The condition where embryos develop with minimal interaction to the maternal tissues, beyond some gas exchange, and hence embryonic nutrition depends on the yolk, is known as lecithotrophic viviparity, whereas the condition where embryonic nutrition is provided by the mother once the egg yolk is depleted is known as matrotrophic viviparity (Wourms et al. 1988). ...
... The above route, however, has not been followed by all viviparous taxa (Blackburn 1992), and species are often in intermediate states, as in the case of caecilians that evolved dermatotrophy, a type of oviparity where oviparous new-borns ingest some modified and nutritious maternal skin (San Mauro et al. 2014;Kupfer et al. 2016). Indeed, lecithotrophy and matrotrophy are not absolute conditions, but rather are extremes of a continuum of female investment (Wourms et al. 1988;Stewart and Thompson 1996;Blackburn 1998;Riesch et al. 2014). Several species regarded as lecithotrophic, also present some form of matrotrophy (e. g. histotrophy, which is a type of embryonic nutrition based on maternal nutrients that are absorbed by the embryo through specialised structures, such as the skin or gill epithelium) at the end of the embryonic development, after hatching and before birth, such as the stingrays (Hamlett et al. 2005) or have a very simple placenta, as in some reptiles (Stewart 1992). ...
... Such adaptations are sometimes shared by several species but seem to be the result of multiple origins (reviewed in Blackburn 2015b). Substantial matrotrophy has also evolved in the form of histotrophy, histophagy (ingestion of maternal secretion via specialised structures), placentotrophy, oophagy, embryophagy, or a combination among teleosts (Turner 1936;Wourms et al. 1988;Wourms 1994, 1995;Meisner and Burns 1997), and Chondrichthyans (Springer 1948;Gilmore et al. 1983;Wourms et al. 1988;Hamlett and Hysell 1998). Relatively, lecithotropic chondrichthyans may also present some degree of staggered embryo provisioning, in the form of oophagy and histotrophy (Wourms 1977;Wourms et al. 1988;Compagno 2001). ...
Viviparity has evolved from oviparity approximately 142 times among vertebrates. Different theories have been proposed to explain the evolution of each of its traits in the different taxa. None, however, is applicable to all the viviparous vertebrates, since the derived ecological advantages such as controlling incubating temperature or protecting eggs against predation differ amongst clades. Most theories have been developed under a co-adaptive perspective, whereas less attention has been paid to conflict. We developed a broad panorama of the gradual evolution, from oviparity to advanced forms of viviparity, that includes the different environmental and co-adaptive selective pressures that have been suggested to be at the root of the different instances of viviparity and of the diverse maternal–foetal adaptations for nutrient transfer seen amongst vertebrates. Furthermore, we highlight the importance of conflict as a crucial driver of the evolution of many of those traits, including the evolution of epigenetic control of maternal resources. We suggest that the different types of matrotrophic viviparity, and probably also some reversals to oviparity, have been the result of an antagonistic coevolution between mothers, fathers and offspring, and their genomes. We additionally suggest that the appearance of a trait that allowed or favoured the evolution of internal development and matrotrophy generates a new selective environment that promotes further adaptations or counteradaptations, leading to the observed diversity of forms of embryonic development, nourishment, and transfer of maternal nutrients, and ultimately to the diversity of extant viviparous taxa.
... This mode of provisioning is called matrotrophy. The complexity of the placenta of poeciliid species is often approximated using the Matrotrophy Index (MI), which is defined as the weight of the offspring at birth divided by the weight of the egg at fertilization (Wourms et al. 1988). Lecithotrophic species provide all nutrients before fertilization, which means the offspring at birth will have lost weight relative to the egg at fertilization due to metabolic costs, leading to a MI lesser than 1. ...
... MI values in the Poeciliidae range from 0.6 for fully lecithotrophic species to 117 for the highly matrotrophic Poeciliopsis retropinna (Pollux et al. 2014). Morphological studies show that these MI values correlate well with complexity of the placental tissue of the species: both the thickness and the degree of folding of the follicular tissue surrounding the embryo correlates well with MI (Wourms et al. 1988; Grove and Wourms 1991;Grove and Wourms 1994;Kwan et al. 2015). Therefore, in this thesis, MI will be used as a proxy for placental complexity in poeciliid fish. ...
... The degree of maternal provisioning in the family Poeciliidae has been quantified in the Matrotrophy Index (MI), which is the estimated dry mass of offspring at birth divided by the dry mass of the egg at fertilization (Wourms et al. 1988). Poeciliid fish have a MI ranging from 0.6 for non-placental (lecithotrophic) species to more than 100 for species with a highly complex placenta (matrotrophic), with species exhibiting intermediate values also being present (Reznick et al. 2002). ...
... The germinal epithelium contains oogonia, situated among somatic epithelial cells [3,13,17,18]. The internal position of the germinal epithelium in the saccular ovary defines that the ovulation in oviparous teleosts occurs into the lumen, instead of into the coelom as happens in all other vertebrates [2,3,13,16,19]. ...
... Viviparity is basically related to the evolution of reproductive behavior, insemination and fertilization are essential requirements for viviparity. In viviparous species, as poeciliids and goodeids, the internal fertilization involves the insemination, with the entrance of spermatozoa to the female reproductive system, through the transfer of sperm from the male to the female gonoduct, and the sequence of the entrance of the sperms, from the gonoduct to the germinal zone of the ovary, where occurs the internal fertilization [1,19,[30][31][32]. The secretory activity of the ovarian epithelium, having a trophic function for the spermatozoa, contributes for their survival during the appropriate time for the fertilization. ...
... Consequently, both types of gestation, intrafollicular and intraluminal, define different relationships between the tissues of the embryos and the mother and successively, diverse adaptations for metabolic interchanges between them, reflected mainly in the type of embryonic nutrition. Nutrition during gestation in viviparous species reflects essential strategies which impact in the evolution of vertebrate viviparity, as occurs in goodeids and poeciliids [19,38,39]. ...
The intraovarian gestation, occurring in teleosts, makes this type of reproduction a such complex and unique condition among vertebrates. This type of gestation of teleosts is expressed in special morphological and physiological characteristic where occurs the viviparity and it is an essential component in the analysis of the evolutionary process of viviparity in vertebrates. In viviparous teleosts, during embryogenesis, there are not development of Müllerian ducts, which form the oviducts in the rest of vertebrates, as a result, exclusively in teleosts, there are not oviducts and the caudal region of the ovary, the gonoduct, connects the ovary to the exterior. The lack of oviducts defines that the embryos develop into the ovary, as intraovarian gestation. The ovary forms the oocytes which may develop different type of oogenesis, according with the storage of diverse amount of yolk, variation observed corresponding to the species. The viviparous gestation is characterized by the possible intimate contact between maternal and embryonic tissues, process that permits their metabolic interchanges. So, the nutrients obtained by the embryos could be deposited in the oocyte before fertilization, contained in the yolk (lecithotrophy), and may be completed during gestation by additional provisioning from maternal tissues to the embryo (matrotrophy). Then, essential requirements for viviparity in poeciliids and goodeids are characterized by: a) the diversification of oogenesis, with the deposition of different amount of yolk in the oocyte; b) the insemination, by the transfer of sperm to the female gonoduct and their transportation from the gonoduct to the germinal region of the ovary where the follicles develop; c) the intrafollicular fertilization; d) the intraovarian gestation with the development of embryos in intrafollicular gestation (as in poeciliids), or intraluminal gestation (as in goodeids); and, e) the origin of embryonic nutrition may be by lecithotrophy and matrotrophy. The focus of this revision compares the general and specific structural characteristics of the viviparity occurring into the intraovarian gestation in teleosts, defining this reproductive strategy, illustrated in this review with histological material in a poeciliid, of the species Poecilia latipinna (Lesueur, 1821) (Poeciliidae), and in a goodeid, of the species Xenotoca eiseni (Rutter, 1896) (Goodeidae).
... and immunological processes (Blackburn, 2015(Blackburn, , 2018Carter, 2012;Ferner & Mess, 2011;Lombardi, 1996;Stewart & Blackburn, 2015;Uribe et al., 2018;Wake, 1992;Wourms, 1981;Wourms et al., 1988). ...
... Viviparity characterizes the goodeid subfamily Goodeinae, a group of 49 species endemic to the central plateau of Mexico (Domínguez-Domínguez et al., 2010;Fishbase, 2021). Their embryos undergo gestation in the ovarian lumen (Turner, 1940a;Uribe et al., 2010;Wourms et al., 1988;Wourms & Lombardi, 1985). ...
... Goodeid embryos develop extraordinary absorptive specializations for nutrient uptake known as "trophotaeniae." These structures are long, vascularized extensions of the hindgut that grow into the ovarian lumen (Fitzsimons, 1979;Iida et al., 2019;Schindler, 2005;Schindler & Hamlett, 1993;Turner, 1940a;Wourms, 2005;Wourms et al., 1988). ...
In viviparous Mexican fishes of the family Goodeidae, embryos develop in the maternal ovarian lumen. They typically absorb maternal nutrients during gestation by means of “trophotaeniae”, i.e., specialized, elongated extensions of the hindgut that are exposed to the fluids, which occupy the ovarian lumen. The sole exception is Ataeniobius toweri, whose embryos lack trophotaeniae but are nevertheless matrotrophic. Thus, how its embryos obtain maternal nutrients is unclear. We studied a series of non‐pregnant and pregnant ovaries of A. toweri using histology to identify the mechanism of maternal‐embryo nutrient transfer. By early‐gestation, embryos have depleted their yolk supplies. Yolks are released into the ovarian lumen and are ingested by the developing embryos, as shown by yolk material in their digestive tracts. The embryonic gut is lined by an epithelium consisting of columnar cells with apical microvilli, providing a means for nutrient absorption. Contrary to statements in the literature, embryos develop minuscule trophotaenial rudiments that extend slightly into the ovarian lumen. These structures are formed of an absorptive epithelium that overlies a vascular stroma, similar to the trophotaeniae of other goodeids. Through late gestation, vitellogenic follicles form and oocytes are discharged into the ovarian lumen, contributing to embryonic nutrition. Thus, histological evidence suggests that embryos chiefly obtain nutrients from ingestion of yolk and maternal secretions released into the ovarian lumen. This function possibly is supplemented by uptake via the small hindgut protrusions and other absorptive surfaces (e.g., the skin and the gill epithelium). Our observations are consistent with two evolutionary interpretations of the hindgut protrusions: (a) that they are rudimentary, evolutionary precursors of trophotaeniae formed by exteriorized hindgut; and (b) that they are vestigial remnants of trophotaeniae that were lost during a switch to a form of matrotrophy involving nutrient ingestion.
... Maternal structures guarantee the physiologically optimal environment and provide all the nutrients and substances (like gases and/or other vital molecules) required for the embryonic development, while embryos have developed diverse structures that allow efficient nutrient and gas uptake from maternal tissues (Blackburn, 2015;Wourms et al., 1988;Wourms & Lombardi, 1992). The term "embryo" is used here in the broad sense, including offsprings, larvae, and fetuses, according to Blackburn and Starck (2015). ...
... This intraovarian gestation of teleosts is unique among vertebrates and occurs in the ovarian lumen (intraluminal gestation) or inside the follicle (intrafollicular gestation). In the latter, maternal tissues, that is, the follicular epithelium and the subjacent net of capillaries, and embryonic structures involved in the exchange of substances establish the maternal-embryonic relationships during gestation (Turner, 1940a;Wourms, 1981;Wourms et al., 1988). ...
... All species of Poeciliidae have intrafollicular gestation (Turner, 1947;Uribe et al., 2009Uribe et al., , 2019Wourms, 1981;Wourms et al., 1988), and show specific adaptations regarding the type of nutrients transfer they have. Poeciliids have two basic types of nutrient transfer from mother to embryos: (a) lecithotrophy, in which the source of nutrients is the yolk deposited in oocytes during oogenesis and (b) matrotrophy, in which the scarce yolk of the oocyte is complemented by nutrient The ORICID ID for the first author José Luis Ponce de Le on of this article was included on 10 April 2021 after original online publication. ...
We used histological techniques to describe the morphology of the yolk and pericardial sacs in developing embryos of the lecithotrophic species Girardinus creolus, Gambusia puncticulata, Limia vittata and Quintana atrizona, in comparison with the extreme matrotrophic Heterandria formosa. In lecithotrophic species, the yolk sac was enlarged and lasted until the final stages of development, while in H. formosa it was completely absorbed soon after fertilization. Lecithotrophic poeciliids showed a pericardial sac with a single layer of blood vessels covering the dorsal surface of the cephalic region only, whilst H. formosa showed a more complex largely vascularized pericardial sac covering the entire dorsal surface, except the caudal region. In advanced gestation of G. creolus, a vascular plexus of the yolk sac reaches the pharyngeal region, behind the gills, suggesting that the pharynx may play a role in embryonic nutrition in lecithotrophic species. These morphological evidences suggest that matrotrophy derives from lecithotrophy.
... viviparity in teleosts (Turner, 1947), such as the ovarian morphology (Amoroso, 1968;Uribe et al., 2019;Wourms, 1981;Wourms et al., 1988). In viviparous teleosts, the ovary is usually an unpaired hollow organ whose cavity is continuous with a caudal extension, the gonoduct, which opens to the exterior at the gonopore. ...
... In viviparous teleosts, the ovary is usually an unpaired hollow organ whose cavity is continuous with a caudal extension, the gonoduct, which opens to the exterior at the gonopore. During embryogenesis, teleost females do not develop Müllerian ducts, so when they reach sexual maturity they do not have oviducts (Wake, 1985;Wourms et al., 1988). Because of this distinct structure, several researchers (Amoroso, 1968;Campuzano-Caballero & Uribe, 2014Langerhans, 2011;Potter & Kramer, 2000;Turner, 1947;Uribe Aranzábal et al., 2009;Wootton & Smith, 2015;Wourms, 1981) considered that the ovary is formed by two portions: the anterior germinal region, containing the oocytes, where oogenesis occurs and the embryos develop during gestation. ...
... Because of this distinct structure, several researchers (Amoroso, 1968;Campuzano-Caballero & Uribe, 2014Langerhans, 2011;Potter & Kramer, 2000;Turner, 1947;Uribe Aranzábal et al., 2009;Wootton & Smith, 2015;Wourms, 1981) considered that the ovary is formed by two portions: the anterior germinal region, containing the oocytes, where oogenesis occurs and the embryos develop during gestation. Theposterior region represents the gonoduct and formed by the caudal growth of the ovarian wall (Wourms, 1981;Wourms et al., 1988). It is a portion of the ovary which functions as a barrier between the germinal region of the ovary and the exterior during all reproductive stages. ...
During embryogenesis, teleost females do not develop Müllerian ducts, which form the oviducts in all other vertebrates. Thus, when they reach sexual maturity they do not have oviducts. In viviparous teleosts, the lack of oviducts means that the development of the embryos occurs as an intraovarian gestation, unique among vertebrates. The ovary is an unpaired hollow organ whose cavity is continuous with the caudal portion, the gonoduct, characterized by the absence of germinal cells, which opens to the exterior at the gonopore. The gonoduct attains essential function as a barrier between the germinal region of the ovary and the exterior during all reproductive stages. This study describes the functional morphology of the gonoduct in the viviparous teleost Cnesterodon decemmaculatus during non‐gestation (previtellogenesis and vitellogenesis) and gestation. The ovaries were processed using histological techniques and stained with hematoxylin‐eosin, and periodic acid Schiff. The gonoduct has two regions: cephalic and caudal, and is formed by three histological layers, which are, from inside to the periphery: 1) tunica mucosa; 2) tunica muscularis; and 3) tunica serosa. In the cephalic region there are mucosal folds extending into the lumen and forming a structure similar to a cervix. The histology of the gonoduct indicates essential functions, i.e.,i) the control of the luminal diameter in the limit to the germinal region of the ovary by the presence of a cervix; ii) during insemination the gonoduct receives the spermatozoa, may store and transport them to the germinal region; iii) the presence of melano‐macrophage centers indicates support of immunological processes, especially during gestation when these centers increase in size; iv) production of exocrine secretions; and v) it is the birth canal , internally lined by an ciliated epithelium and surrounded by smooth musclesboth tissues supposedly supporting the birth process. .
... The Goodeinae may represent an adaptive radiation, but multiple features may have influenced this, including the evolution of livebearing, sexual selection, or ecological radiation. All species within the Mexican Goodeinae are viviparous and matrotrophic, with rapid offspring development dependent on maternal provisioning (Wourms et al. 1988;Vega-López et al. 2007) via a placental analogue called the trophotaenia (Wourms et al. 1988;Hollenberg and Wourms, 1995). Within the Cyprinodontiformes (including the Goodeidae and Poecilidae) speciation rate is higher in live-bearing fish (Helmstetter et al. 2016), so genes associated with this reproductive mode might be expected to be key elements in the radiation of the Goodeinae. ...
... The Goodeinae may represent an adaptive radiation, but multiple features may have influenced this, including the evolution of livebearing, sexual selection, or ecological radiation. All species within the Mexican Goodeinae are viviparous and matrotrophic, with rapid offspring development dependent on maternal provisioning (Wourms et al. 1988;Vega-López et al. 2007) via a placental analogue called the trophotaenia (Wourms et al. 1988;Hollenberg and Wourms, 1995). Within the Cyprinodontiformes (including the Goodeidae and Poecilidae) speciation rate is higher in live-bearing fish (Helmstetter et al. 2016), so genes associated with this reproductive mode might be expected to be key elements in the radiation of the Goodeinae. ...
Understanding the phylogeographic history of a group and identifying the factors contributing to speciation is an important challenge in evolutionary biology. The Goodeinae are a group of live-bearing fishes endemic to Mexico. Here, we develop genomic resources for species within the Goodeinae and use phylogenomic approaches to characterise their evolutionary history. We sequenced, assembled and annotated the genomes of four Goodeinae species, including Ataeniobius toweri , the only matrotrophic live-bearing fish without a trophotaenia in the group. We estimated timings of species divergence and examined the extent and timing of introgression between the species to assess if this may have occurred during an early radiation, or in more recent episodes of secondary contact. We used branch-site models to detect genome-wide positive selection across Goodeinae , and we specifically asked whether this differs in A. toweri , where loss of placental viviparity has recently occurred. We found evidence of gene flow between geographically isolated species, suggesting vicariant speciation was supplemented by limited post-speciation gene flow, and gene flow may explain previous uncertainties about Goodeid phylogeny. Genes under positive selection in the group are likely to be associated with the switch to live-bearing. Overall, our studies suggest that both volcanism-driven vicariance and changes in reproductive mode influenced radiation in the Goodeinae .
... of this species (Vooren and Klippel, 2005). Pseudobatos horkelii is a yolk sac viviparous species (Lessa et al., 1986;Wourms, 1988), i.e., the embryo develops mainly through the yolk available in the mature oocyte, but other nutritional sources have recently been discovered (Wosnick et al., 2022). On the continental shelf of southern Brazil, the reproductive cycle is synchronized at the population level, so that adult females give birth at the same time of the year. ...
... Thus, exorbitant catches like this one, demonstrate that P. horkelii, a Critically Endangered species, continues to be over captured, even during the reproductive period, in the southern coast of Brazil, were females migrate in warmer month for parturition. seudobatos but it was already in a state of decomposition P horkelii is a viviparous species, and in comparison to oviparous species, the viviparous reproduction of those species depending solely on a yolk sac, and tends to be associated with a more moderate reproductive rate (Wourms, 1988). The specificity of the lower reproductive rate of this species coupled with its dependence on coastal areas for reproductive purposes, continuously increases the vulnerability of the local population (Vooren and Klippel, 2005). ...
In this article, the capture of two pregnant females of the Brazilian Guitarfish, Pseudobatos horkelii, is recorded. Although the species is Critically Endangered and it capture is prohibited, the illegal catches occur nevertheless.
... MI or PI = 0.6-0.7) due to metabolic costs associated with embryonic growth and development (Reznick et al. 2002;Wourms 1981;Wourms et al. 1988). If parental provisioning of nutrients occurs, embryos will either lose less dry weight than embryos of lecithotrophic species, or will gain dry weight throughout development (MI or PI > 0.7). ...
... In contrast, there was no significant difference between the dry mass of newly fertilised H. abdominalis eggs and neonates (PI = 1), meaning that a small amount of dry mass must have been gained during gestation. The MI of lecithotrophic teleosts is approximately 0.6-0.7 due to embryonic catabolism of nutrients during development (Wourms et al. 1988;Wourms 1981;Reznick et al 2002). However, these MI values are based on dry mass losses in embryos of lecithotrophic viviparous poeciliids, and other oviparous teleosts (Clupea harengus and Salmo irideus). ...
Vertebrates that incubate embryos on or within the body cavity exhibit diverse strategies to provide nutrients to developing embryos, ranging from lecithotrophy (solely yolk-provided nutrition) to substantial matrotrophy (supplemental nutrients from the mother before birth). Syngnathid fishes (seahorses, pipefishes and sea dragons) are the only vertebrates to exhibit male pregnancy. Therefore, they provide a unique opportunity for comparative evolutionary research, in examining pregnancy independent of the female reproductive tract. Here, we tested the hypothesis that the most complex form of syngnathid pregnancy involves nutrient transport from father to offspring. We compared the dry masses of newly fertilised Hippocampus abdominalis eggs with those of fully developed neonates to derive a patrotrophy index. The patrotrophy index of H. abdominalis was 1, indicating paternal nutrient supplementation to embryos during gestation. We also measured the lipid content of newly fertilised eggs and neonates and found that there was no significant decrease in lipid mass during embryonic development. Since lipids are likely to be the main source of energy during embryonic development, our results suggest that lipid yolk reserves being depleted by embryonic metabolism are replaced by the brooding father. The results of our study support the hypothesis that nutrient transport occurs in the most advanced form of male pregnancy in vertebrates.
... These strategies have been quantified using the matrotrophic index (MI), a measure that assesses how much weight an offspring gains from fertilization to birth. Simply, the offspring of a matrotrophic species will gain weight and have an MI > 1, indicating that the mother provided a lot of nutrition throughout pregnancy (Wourms et al. 1988;Reznick et al. 2002). Conversely, the offspring of a lecithotrophic species loses weight and corresponds to an MI < 1, indicating that the mother provided the required nutrition before fertilization (Wourms et al. 1988;Reznick et al. 2002). ...
... Simply, the offspring of a matrotrophic species will gain weight and have an MI > 1, indicating that the mother provided a lot of nutrition throughout pregnancy (Wourms et al. 1988;Reznick et al. 2002). Conversely, the offspring of a lecithotrophic species loses weight and corresponds to an MI < 1, indicating that the mother provided the required nutrition before fertilization (Wourms et al. 1988;Reznick et al. 2002). The reproductive strategy of matrotrophy implies the presence of a structure that can provide for an offspring throughout pregnancy, this is the placenta. ...
Placentation evolved many times independently in vertebrates. While the core functions of all placentas are similar, we know less about how this similarity extends to the molecular level. Here we study Poeciliopsis, a unique genus of live-bearing fish that have independently evolved complex placental structures at least three times. The maternal follicle is a key component of these structures. It envelops yolk rich eggs and is morphologically simple in lecithotrophic species, but has elaborate villous structures in matrotrophic species. Through sequencing the follicle transcriptome of a matrotrophic, P. retropinna, and lecithotrophic, P. turrubarensis, species we found genes known to be critical for placenta function expressed in both species despite their difference in complexity. Additionally, when we compare the transcriptome of different river populations of P. retropinna, known to vary in maternal provisioning, we find differential expression of secretory genes expressed specifically in the top layer of villi cells in the maternal follicle. This provides some of the first evidence that the placental structures of Poeciliopsis function using a secretory mechanism rather than direct contact with maternal circulation. Finally, when we look at the expression of placenta proteins at the maternal-fetal interface of a larger sampling of Poeciliopsis species, we find expression of key maternal and fetal placenta proteins in their cognate tissue types of all species, but follicle expression of Prolactin is restricted to only matrotrophic species. Taken together, we suggest that all Poeciliopsis follicles are poised for placenta function, but require expression of key genes to form secretory villi.
... Secondly, we expected that sexual dimorphism would affect the type and amount of food items ingested by each sex within both species. This assumptions are based on a number of sex-specific traits found in Poeciliids: 1-males are smaller (Rosen & Bailey, 1963;; 2-males show lower feeding activity compared to females, given that males spend more time harassing females and seeking copulation (Köhler et al., 2011); and 3-female poeciliids need a higher energetic budget for reproduction than males given that egg formation as well as embryonic nourishment and development, are femaleexclusive processes (Wourms, et al., 1988;Meffe & Snelson, 1989). ...
... Post maturation sex-specific levels of energy consumption are related to differential reproductive roles and vary drastically between female and male poeciliids. Females devote large amounts of energy in egg formation and often in embryonic nourishment (Wourms, et al., 1988;Meffe and Snelson, 1989). Male poeciliids, in contrast, need lower amounts of energy to accomplish their reproductive role which, in Gambusia fishes, is reduced to pursuing females and copulate (Pilastro, et al., 1997;Deaton, 2008). ...
Centro de Investigaciones Marinas Universidad de La Habana revista de investigaciones marinas ARTICULO ORIGINAL Partial troPhic segregation in co-occurring Gambusia sPecies (cyPrinodontiformes: Poeciliidae) in a natural wetland of cuba Segregación trófica parcial entre especies de Gambusia (Cyprinodontiformes: Poeciliidae) en un humedal natural de Cuba
... The S. marmoratus stands out due to its unique reproductive strategy of ovoviviparity. In this distinctive method, the eggs are fertilized within the mother's body, retained, and then develop in the reproductive system of the mother [17]. This reproductive adaptation provides an advantage for its adaptability in specific ecological environments. ...
Artificial enhancement and release activity is an important method in the restoration of fishery resources. In order to understand the possible genetic effect of hatchery-released populations on wild populations during the artificial enhancement and release activities of Sebastiscus marmoratus in Zhoushan waters, we utilized mitochondrial DNA control region sequences to examine the genetic diversity in four S. marmoratus populations, including one farmed population, one released population and two wild populations. A total of 68 haplotypes from 123 individuals were detected, including 3 shared haplotypes. Haplotype diversity ranged from 0.944 to 0.980, with a mean of 0.966. The nucleotide diversity ranged from 0.020 to 0.025, with a mean of 0.022. Analysis of Molecular Variance (AMOVA) indicated that the primary genetic variation occurs within populations and the index of genetic differentiation between populations (FST) among the four populations showed no differentiation. The results indicate that the current artificial enhancement and release has not impacted the S. marmoratus population in Zhoushan waters. Continued long-term monitoring is essential to protect the high-quality germplasm resources of S. marmoratus.
... The ovary is typically an unpaired hollow organ in viviparous teleosts, and its cavity is continuous with the gonoduct, a caudal extension that opens to the outside at the gonopore. Teleost females do not generate Müllerian ducts during development; therefore, when they reach sexual maturity, they lack oviducts [17,18]. The germinal epithelium, stroma, smooth muscle, and peritoneum (serosa) are the four histological layers that make up the ovarian wall of Molly fish. ...
Citation: Sayed, R.K.A.; Mokhtar, D.M.; Hashim, M.A.; Aly, A.S.; Zaccone, G.; Albano, M.; Alesci, A.; Abdellah, N. Immune Cell Profiling in the Ovarian Stroma of a Viviparous Fish during the Breeding Season: A Histological and Immunohistochemical Investigation. Abstract: The molly fish is a member of viviparous teleosts that are characterized by the fusion of the right and left ovaries during their early embryonic development. This fusion results in a singular and saccular ovary, where the germinal epithelium lines the internal lumen. The present study aimed to identify the immune cells in the ovarian stroma of Molly fish during the breeding season using histological and immunohistochemical analysis. Histological examination of the ovaries displayed oocytes at all different stages of development and degeneration. The ovocoel, a lymph-filled space, remains in the center of the ovary and branches posteriorly, creating the lumen of the gonoduct. The ovarian wall is composed of three layers: the mesothelium, tunica albuginea, and germinal epithelium. The developing ova were held together by the stroma, which consisted of vascular collagenous connective tissue clustered with immune cells. Immunohistochemical analysis revealed the presence of clusters of macrophages expressing APG5, IL-1β, TGF-β, S100, NF-κB, CD68, Iba-1, and Ach. Monocytes demonstrated positive immunoreactivity for both APG5 and IL-1β, whereas dendritic cells expressed only APG5. Furthermore, rodlet cells exhibited immunoreactivity for S100 protein, IL-1β, NF-κB, CD68, Nrf2, Ach, myostatin, SOX9, and Iba-1. In contrast, stem cells displayed immunoreactivity for Nrf2, myostatin, and SOX9. In conclusion, the ovarian stroma of Molly fish demonstrated a notable presence of immune cells, indicating their active involvement in immune reactions. Key Contribution: The expressions of various inflammatory and stem cell markers in the ovarian stroma of Molly fish highlight the high prevalence of immune cells in the ovary, indicating the contribution of the ovarian stroma in immune reactions.
... The ovary is typically an unpaired hollow organ in viviparous teleosts, and its cavity is continuous with the gonoduct, a caudal extension that opens to the outside at the gonopore. Teleost females do not generate Müllerian ducts during development; therefore, when they reach sexual maturity, they lack oviducts [17,18]. The germinal epithelium, stroma, smooth muscle, and peritoneum (serosa) are the four histological layers that make up the ovarian wall of Molly fish. ...
The molly fish is a member of viviparous teleosts that are characterized by the fusion
of the right and left ovaries during their early embryonic development. This fusion results in a
singular and saccular ovary, where the germinal epithelium lines the internal lumen. The present
study aimed to identify the immune cells in the ovarian stroma of Molly fish during the breeding
season using histological and immunohistochemical analysis. Histological examination of the ovaries
displayed oocytes at all different stages of development and degeneration. The ovocoel, a lymphfilled
space, remains in the center of the ovary and branches posteriorly, creating the lumen of the
gonoduct. The ovarian wall is composed of three layers: the mesothelium, tunica albuginea, and
germinal epithelium. The developing ova were held together by the stroma, which consisted of
vascular collagenous connective tissue clustered with immune cells. Immunohistochemical analysis
revealed the presence of clusters of macrophages expressing APG5, IL-1β, TGF-β, S100, NF-κB,
CD68, Iba-1, and Ach. Monocytes demonstrated positive immunoreactivity for both APG5 and IL-1β,
whereas dendritic cells expressed only APG5. Furthermore, rodlet cells exhibited immunoreactivity
for S100 protein, IL-1β, NF-κB, CD68, Nrf2, Ach, myostatin, SOX9, and Iba-1. In contrast, stem cells
displayed immunoreactivity for Nrf2, myostatin, and SOX9. In conclusion, the ovarian stroma of
Molly fish demonstrated a notable presence of immune cells, indicating their active involvement in
immune reactions.
... Maternal care in viviparous reproduction can be broadly categorized into two forms: matrotrophy and lecithotrophy. Lecithotrophy (vitellogenesis) involves maternal investment in nutrients prior to fertilization, with embryos acquiring nutrients from the yolk sac (Wourms et al. 1988). In contrast, matrotrophy involves direct nutrient provision from the mother to developing embryos through uterine secretions (histotrophic nutrition), the embryos feeding on eggs produced by the ovary (oophagy), embryos consuming other embryos (adelphophagy), or the formation of a placenta that enables nutrient transfer through an intimate association of embryonic and uterine tissues (Reznick & Yang 1993;Hamlett et al. 2005;Sato et al. 2016;Buddle et al. 2019). ...
The reproductive mode of viviparity has independently evolved in various animal taxa. It refers to the condition in which the embryos or young develop inside the female’s body during gestation, providing advantages such as protection, nutrition, and improved survival chances. However, parasites and diseases can be an evolutionary force that limit the host’s resources, leading to physiological, morphological, and behavioral changes that impose additional costs on both the pregnant female and her offspring. This review integrates the primary literature published between 1980 and 2021 on the parasitism of viviparous hosts. We describe aspects such as reproductive investment in females, offspring sex ratios, lactation investment in mammals, alterations in birth intervals, current reproductive investment, variations between environments, immune system activity in response to immunological challenges, and other factors that can influence the interaction between viviparous females and parasites. Maintaining pregnancy incurs costs in managing the mother’s resources and regulating the immune system’s responses to the offspring, while simultaneously maintaining an adequate defense against parasites and pathogens. Parasites can significantly influence this reproductive mode: parasitized females adjust their investment in survival and reproduction based on their life history, environmental factors, and the diversity of encountered parasites.
... El ovario de Girardinus microdactylus se corresponde de manera general con lo descrito para otras especies de poecílidos (Grier et al., 2005, Greven, 2010, Uribe y Grier, 2018, ene forma ovoide con un lumen central en contacto con el epitelio germinal a través de las lamelas ovígeras. En esta especie como en todos los poecílidos, la fer lización y la gestación ocurren en el folículo ovárico (Wourms et al., 1988, Ponce de León, 2011. La comunicación del ovario con el exterior se establece por la parte posterior del ovario que carece de células germinales, llamada gonoducto. ...
RESUMEN La reproducción es de vital importancia para la con nuidad de las especies y el adecuado manejo de sus poblaciones; sin embargo, son pocos los estudios que abordan la reproducción de las especies cubanas de poecílidos. Estos peces enen una gran importancia para la salud humana y del ecosistema, al ser controladores biológicos e indicadores de la calidad de las aguas, por ello se necesita ampliar el conocimiento de su historia natural, especialmente de sus aspectos reproduc vos. El obje vo de este trabajo es la descripción histológica de las gónadas femeninas de Girardinus microdactylus, poecílido endémico de la región occidental de Cuba. Para este estudio se recolectaron 24 hembras en los meses de diciembre a febrero. Las gónadas de seis ejemplares se some eron a la técnica histológica clásica, se ñeron con HE y se analizaron al microscopio óp co de campo claro. Se encontró que el peso de la hembra depende del tamaño corporal y del peso gonadal, y este úl mo del estado de desarrollo de los folículos ováricos. Las hembras más grandes enen capacidad para un mayor número de crías. Se iden ficaron todas las etapas de desarrollo del ovocito: croma na nucléolo, perinucleolar, alvéolos cor cales, vitelogénesis, ovocito maduro y embriones en desarrollo dentro de los folículos ováricos. Las hembras en etapa de no gestación tuvieron numerosos espermatozoides en el gonoducto. El apareamiento ocurre, aunque los ovocitos no estén listos para la fecundación, lo que indica una posible separación temporal entre el apareamiento y la fer lización. Palabras clave: gónada, hembra, peces dulceacuícolas, ovocito ABSTRACT Reproduc on is vital for the con nuity of the species and for the proper management of their popula ons; however, there are few studies that address the reproduc on of Cuban species of poeciliids. These fish are of great
... The Goodeinae are proposed to have become viviparous after diverging from oviparous species of the family in the early Miocene, before subsequent diversification of matrotrophic adaptations (Webb et al. 2004). Across goodeins, matrotrophy is prevalent and is linked to the evolution of a novel, placental analog consisting of a maternal component, the internal ovarian epithelium, and an embryonic component, the trophotaenia (Lombardi and Wourms 1985;Wourms et al. 1988;Schindler 2015). Nutrients provided by the mother are absorbed via the trophotaenia Yusuf et al. · https://doi.org/10.1093/molbev/msad208 ...
The transition from oviparity to viviparity has occurred independently over 150 times across vertebrates, presenting one of the most compelling cases of phenotypic convergence. However, whether the repeated, independent evolution of viviparity is driven by redeployment of similar genetic mechanisms and whether these leave a common signature in genomic divergence remains largely unknown. Although recent investigations into the evolution of viviparity have demonstrated striking similarity among the genes and molecular pathways involved across disparate vertebrate groups, quantitative tests for genome-wide convergent have provided ambivalent answers. Here, we investigate the potential role of molecular convergence during independent transitions to viviparity across an order of ray-finned freshwater fish (Cyprinodontiformes). We assembled de novo genomes and utilized publicly available genomes of viviparous and oviparous species to test for molecular convergence across both coding and noncoding regions. We found no evidence for an excess of molecular convergence in amino acid substitutions and in rates of sequence divergence, implying independent genetic changes are associated with these transitions. However, both statistical power and biological confounds could constrain our ability to detect significant correlated evolution. We therefore identified candidate genes with potential signatures of molecular convergence in viviparous Cyprinodontiformes lineages. Motif enrichment and gene ontology analyses suggest transcriptional changes associated with early morphogenesis, brain development, and immunity occurred alongside the evolution of viviparity. Overall, however, our findings indicate that independent transitions to viviparity in these fish are not strongly associated with an excess of molecular convergence, but a few genes show convincing evidence of convergent evolution.
... A few teleosts exhibit viviparity, which is characterized by the ability to give birth to live offspring. The ovaries of viviparous teleosts are associated with both egg production and gestation 29 . Gambusia affinis is a viviparous fish belonging to the family Poeciliidae that exhibits intraovarian gestation. ...
Although the accumulation of pharmaceutical drugs in aquatic bodies has increased rapidly in recent years, the effect of rifampicin (RIF), a first-line anti-tuberculosis drug, on fish feeding, growth, and embryonic development is unknown. This investigation aimed to determine the impact of RIF on growth and embryonic developmental profile in the mosquitofish Gambusia affinis. Experimental groups included controls, which were kept in normal water for 21 days, whereas those in the second, third, and fourth groups were exposed to 50, 200, and 500 mg RIF/L water, respectively. The food intake rate and Specific Growth Rate (SGR) showed a concentration-dependent significant decrease in RIF-treated fish compared with controls, and a strong positive correlation was found between food consumption and SGR. A significant decrease in the number of embryos at an early stage of development and the total number of embryos in RIF-treated fish was associated with several congenital anomalies such as lack of vitellogenin accumulation, yolk sac regression, decreased pigmentation, aggregations of blood vessels, and curvature of the spinal cord compared with controls. Together, these results reveal for the first time that RIF treatment not only impacts feeding and growth, but also exerts potential teratogenic effect on embryonic developmental stages in the mosquitofish G. affinis.
... Morpho-histology of N. gerreiodes and E. splendens had an unpaired ovary has been reported from several species including ponyfish (Seah et al., 2009;Acharya and Naik, 2015) and viviparous teleosts Crenichthys baileyi and Empetrichthys latos (Uribe et al., 2012). Fish generally have a paired ovary as reported in Kurtus gulliveri (Berra et al., 2007) and Acanthopagrus schlegeli (Lee et al., 2008), and the unpaired ovary is considered to be the result of the fusion of paired ovary, which might take place during their embryonic development (Wourms et al., 1988;Schindler and Hamlett, 1993). ...
... Among live-bearing fishes, superfetation is a more common reproductive strategy, being found in at least three different families from three distantly related orders: Clinidae (order Blenniiformes), Poeciliidae (order Cyprinodontiformes), and Zenarchopteridae (order Beloniformes) (Gunn & Thresher, 1991;Pollux et al., 2009Pollux et al., , 2014Reznick et al., 2007;Reznick & Miles, 1989;Scrimshaw, 1944;Turner, 1937;Wourms, 1981;Wourms et al., 1988). Superfetation is especially well-studied within the family Poeciliidae. ...
Superfetation, the ability to carry several overlapping broods at different developmental stages, has evolved independently multiple times within the live-bearing fish family Poeciliidae. Even though superfetation is widespread among poeciliids, its evolutionary advantages remain unclear. Theory predicts that superfetation should increase polyandry by increasing the probability that temporally overlapping broods are fertilized by different fathers. Here, we test this key prediction in two poeciliid species that each carry two temporally overlapping broods: Poeciliopsis retropinna and P. turrubarensis. We collected 25 females per species from freshwater streams in South-Eastern Costa Rica and assessed multiple paternity by genotyping all their embryos (420 embryos for P. retropinna; 788 embryos for P. turrubarensis) using existing and newly developed microsatellite markers. We observed a high frequency of unique sires in the simultaneous, temporally overlapping broods in P. retropinna (in 56% of the pregnant females) and P. turrubarensis (79%). We found that the mean number of sires within females was higher than the number of sires within the separate broods (2.92 sires within mothers vs. 2.36 within separate broods in P. retropinna; and 3.40 vs 2.56 in P. turrubarensis). We further observed that there were significant differences in the proportion of offspring sired by each male in 42% of pregnant female P. retropinna and 65% of female P. turrubarensis; however, this significance applied to only 9% and 46% of the individual broods in P. retropinna and P. turrubarensis, respectively, suggesting that the unequal reproductive success of sires (i.e. reproductive skew) mostly originated from differences in paternal contribution between, rather than within broods. Together, these findings tentatively suggest that superfetation may promote polyandry and reproductive skew in live-bearing fishes.
... It is found across a vast array of invertebrates [e.g. cockroaches, terrestrial and aquatic gastropods, clams, reviewed in Ostrovsky et al. (2016)] and all vertebrate taxa, except birds [fish (Wourms et al., 1988); amphibians (Greven, 1998); reptiles (Blackburn, 1992)]. Placental or matrotrophic females have small-size eggs at fertilization that grow throughout gestation as the female provides the developing embryos with nutrients (Blackburn, 1992). ...
The placenta is a complex organ that shows high morphological diversity. Among fish, the first vertebrates that have evolved a placenta, the family Poeciliidae exhibits very diverse modes of maternal provisioning even among congeneric species. Here, we investigated the embryonic growth curve across seven recently-described species of the highly diverse genus Phalloceros (Eigenmann, 1907). We also investigated possible intraspecific differences and whether other female characteristics affected embryo mass. We found that embryo mass decreased until around stage 20 and then increased, resulting in a 1.5 to 3-fold mass gain from fertilization to birth. Embryo mass changed non-linearly with stage of development and was affected by species identity (or locality) and female somatic dry mass. This initial loss then gain of embryonic mass during development is unique among other Poeciliidae species and was conserved across populations and species, even though size at birth can vary. Other species instead either lose mass if they lack placentas or gain mass exponentially if they have placentas. The Phalloceros mode of maternal provisioning could thus represent a different form from that seen in other species of Poeciliidae.
... Mammals, amphibians, reptiles and teleost fish have independently evolved viviparity many times (Wourms et al., 1988;Blackburn, 2015;Schindler, 2015;Wake, 2015;Li et al., 2017), but only the seahorses and pipefishes have evolved this mechanism in males. Gestation length in the male seahorse ranges from 2 to 3 weeks, during which time the embryos become attached to the inner lining of the pouch and are partially embedded in goblet-like structures formed by skin folds in the internal surfaces (Stölting and Wilson, 2007;Novelli et al., 2015). ...
The Syngnathidae (seahorses and pipefishes) are a group of teleost fishes in which, uniquely, developing embryos are hosted throughout pregnancy by males, using a specialized brood pouch situated on the abdomen or tail. Seahorses have evolved the most advanced form of brood pouch, whereby zygotes and embryos are intimately connected to the host's circulatory system and also bathed in pouch fluid. The pouch is closed to the external environment and has to perform functions such as gaseous exchange, removal of waste and maintenance of appropriate osmotic conditions, much like the mammalian placenta. Fertilization of the oocytes occurs within the brood pouch, but unlike the mammalian situation the sperm transport mechanism from the ejaculatory duct towards the pouch is unclear, and the sperm: egg ratio (about 5:1) is possibly the least of any vertebrate. In this review, there is highlighting of the difficulty of elucidating the sperm transport mechanism, based on studies of Hippocampus kuda. The similarities between seahorse pouch function and the mammalian placenta have led to suggestions that the pouch provides important nutritional support for the developing embryos, supplementing the nutritional functions of the yolk sac provided by the oocytes. In this review, there is a description of the recent evidence in support of this hypothesis, and also emphasis, as in mammals, that embryonic development depends on nutritional support from the placenta-like pouch at important stages of the gestational period ("critical windows").
... According to Mossman ([10], p. 156), a placenta is "any intimate apposition or fusion of the fetal organs to the maternal tissues for physiological exchange". Whereas vertebrate placentae are mostly (although not always) of a similar origin involving sexual ducts and embryonic envelopes (reviewed in [4,6,9,[11][12][13][14]), the placental analogues of invertebrates originated from a plethora of tissues and organs and sometimes involve embryonic envelopes as well. Generally, a 'placental analogue' is any local zone of enhanced nutritional transport developing during incubation, from simple apposition of nonspecialized epithelia to specialized parental-embryonic tissue/cell complexes that increase the entire secreting and absorbing surfaces. ...
Background
Placentation has evolved multiple times among both chordates and invertebrates. Although they are structurally less complex, invertebrate placentae are much more diverse in their origin, development and position. Aquatic colonial suspension-feeders from the phylum Bryozoa acquired placental analogues multiple times, representing an outstanding example of their structural diversity and evolution. Among them, the clade Cyclostomata is the only one in which placentation is associated with viviparity and polyembryony—a unique combination not present in any other invertebrate group.
Results
The histological and ultrastructural study of the sexual polymorphic zooids (gonozooids) in two cyclostome species, Crisia eburnea and Crisiella producta, revealed embryos embedded in a placental analogue (nutritive tissue) with a unique structure—comprising coenocytes and solitary cells—previously unknown in animals. Coenocytes originate via nuclear multiplication and cytoplasmic growth among the cells surrounding the early embryo. This process also affects cells of the membranous sac, which initially serves as a hydrostatic system but later becomes main part of the placenta. The nutritive tissue is both highly dynamic, permanently rearranging its structure, and highly integrated with its coenocytic ‘elements’ being interconnected via cytoplasmic bridges and various cell contacts. This tissue shows evidence of both nutrient synthesis and transport (bidirectional transcytosis), supporting the enclosed multiple progeny. Growing primary embryo produces secondary embryos (via fission) that develop into larvae; both the secondary embyos and larvae show signs of endocytosis. Interzooidal communication pores are occupied by 1‒2 specialized pore-cells probably involved in the transport of nutrients between zooids.
Conclusions
Cyclostome nutritive tissue is currently the only known example of a coenocytic placental analogue, although syncytial ‘elements’ could potentially be formed in them too. Structurally and functionally (but not developmentally) the nutritive tissue can be compared with the syncytial placental analogues of certain invertebrates and chordates. Evolution of the cyclostome placenta, involving transformation of the hydrostatic apparatus (membranous sac) and change of its function to embryonic nourishment, is an example of exaptation that is rather widespread among matrotrophic bryozoans. We speculate that the acquisition of a highly advanced placenta providing massive nourishment might support the evolution of polyembryony in cyclostomes. In turn, massive and continuous embryonic production led to the evolution of enlarged incubating polymorphic gonozooids hosting multiple progeny.
... According to Mossman ([10], p. 156), a placenta is "any intimate apposition or fusion of the fetal organs to the maternal tissues for physiological exchange". Whereas vertebrate placentae are mostly (although not always) of a similar origin involving sexual ducts and embryonic envelopes (reviewed in [4,6,9,[11][12][13][14]), the placental analogues of invertebrates originated from a plethora of tissues and organs and sometimes involve embryonic envelopes as well. Generally, a 'placental analogue' is any local zone of enhanced nutritional transport developing during incubation, from simple apposition of nonspecialized epithelia to specialized parental-embryonic tissue/cell complexes that increase the entire secreting and absorbing surfaces. ...
Background
Placentation has evolved multiple times among both chordates and invertebrates. Although they are structurally less complex, invertebrate placentae are much more diverse in their origin, development and position. Aquatic colonial suspension-feeders from the phylum Bryozoa acquired placental analogues multiple times, representing an outstanding example of their structural diversity and evolution. Among them, the clade Cyclostomata is the only one in which placentation is associated with viviparity and polyembryony—a unique combination not present in any other invertebrate group.
Results
The histological and ultrastructural study of the sexual polymorphic zooids (gonozooids) in two cyclostome species, Crisia eburnea and Crisiella producta , revealed embryos embedded in a placental analogue (nutritive tissue) with a unique structure—comprising coenocytes and solitary cells—previously unknown in animals. Coenocytes originate via nuclear multiplication and cytoplasmic growth among the cells surrounding the early embryo. This process also affects cells of the membranous sac, which initially serves as a hydrostatic system but later becomes main part of the placenta. The nutritive tissue is both highly dynamic, permanently rearranging its structure, and highly integrated with its coenocytic ‘elements’ being interconnected via cytoplasmic bridges and various cell contacts. This tissue shows evidence of both nutrient synthesis and transport (bidirectional transcytosis), supporting the enclosed multiple progeny. Growing primary embryo produces secondary embryos (via fission) that develop into larvae; both the secondary embyos and larvae show signs of endocytosis. Interzooidal communication pores are occupied by 1‒2 specialized pore-cells probably involved in the transport of nutrients between zooids.
Conclusions
Cyclostome nutritive tissue is currently the only known example of a coenocytic placental analogue, although syncytial ‘elements’ could potentially be formed in them too. Structurally and functionally (but not developmentally) the nutritive tissue can be compared with the syncytial placental analogues of certain invertebrates and chordates. Evolution of the cyclostome placenta, involving transformation of the hydrostatic apparatus (membranous sac) and change of its function to embryonic nourishment, is an example of exaptation that is rather widespread among matrotrophic bryozoans. We speculate that the acquisition of a highly advanced placenta providing massive nourishment might support the evolution of polyembryony in cyclostomes. In turn, massive and continuous embryonic production led to the evolution of enlarged incubating polymorphic gonozooids hosting multiple progeny.
... Two important components of a complex intrauterine embryonic nutrition (matrotrophy) have been reported by several authors for C. coelolepis and C. owstonii, an unexpected feature in a supposedly strictly lecitotrophic species (Compagno, 1984;Compagno et al., 2005), comprising the presence of villi on the uterine lining and an abundant and sticky mucus covering the embryos (Yano and Tanaka, 1983;Girard and Du Buit, 1999;Veríssimo et al., 2003;Moura et al., 2011). Therefore there is strong evidence supporting the assumption that this intrauterine conspicuous mucus may, in fact, be the incipient histotrophe (sensu Hamlett et al., 2005) to be absorbed by the embryo's skin, mouth, external gill filaments and spiracles (Garrick, 1959;Yano and Tanaka, 1987;Wourms et al., 1988;Girard and Du Buit, 1999;Veríssimo et al., 2003;Hamlett et al., 2005). Further spaced dermal denticles are distinctively visible in embryos ( Fig. 7a in (Yano and Tanaka, 1983)), suggesting increasing proximity of dermal denticles after birth, as exhibited in Fig. 7b in Yano and Tanaka (1983) and Fig. 7 in Mas et al. (2020). ...
The Roughskin Dogfish Centroscymnus owstonii is a poorly known species with eventual records along the Western South Atlantic. Different dermal denticles have been historically reported for juveniles and adults, which presupposes changes from a juvenile denticle type to an adult denticle type during growth. The present study was based on a male neonate 324 mm in total length (TL) captured with crab pots on the northeastern continental slope of Brazil, between 400-450 meters. This was considered a newborn based on its small size, very similar to previously reported large embryo dimensions and close to the expected birth size in literature. Three different dermal denticles were observed, alternating from the rostrum to the branchial slits, where a tricuspidated denticle type extended covering the rest of the posterior portion of the body. Dermal denticle types and distribution suggest that the replacement process of dermal denticles begins before birth or early after birth, undergoing at least three changes until reaching the adult dermal denticle type. These different types may be related to uterine epithelial histotroph absorption or embryo movement within the mucous environment, which would be enhanced by largely spaced denticles. The reported fragmented distribution of this species along the Brazilian coast is probably related to insufficient sampling coverage.
... The existence of two ovaries was previously reported in the two extant Hiodontiformes, Hiodon alosoides and Hiodon tergisus, whereas the occurrence of one (left) functional ovary was noted in Arapaima gigas, in which the rarely observed right gonad was atrophic, suggesting its reduction during development (Godinho et al., 2005;Pankhurst et al., 1986;Talajic, 1980). The presence of paired gonads is a general condition in other Teleostei except Fundulus heteroclitus, Oryzias latipes, Synbranchus marmoratus, poecilids and goodeids, in which single ovary is a derived feature (Bailey, 1933;Brummett et al., 1982;Devlin & Nagahama, 2002;Grier et al., 2009;Lo Nostro et al., 2003;Mendoza, 1965;Nagahama, 1983;Ravaglia & Maggese, 2002;Strüssmann & Nakamura, 2002;Turner, 1947;Uribe et al., 2005;Uribe et al., 2016;Wourms, 1981;Wourms et al., 1988;Yamamoto & Yamazaki, 1961). This may suggest that occurrence of paired gonads is a primitive state among osteoglossomorphs, and the presence of a single ovary might have evolved in this group after the divergence of the Pantodontidae from the other Osteoglossiformes (Figure 1). ...
In this study, we assessed the ovary structure and early oogenesis in representatives of Osteoglossomorpha, one of the most basal Teleostei groups. We aimed to perform a comparative analysis between internally fertilizing Pantodon buchholzi (Pantodontidae) and externally fertilizing Osteoglossum bicirrhosum (Osteoglossidae), Marcusenius cyprinoides, Brevimyrus niger, Gnathonemus petersii and Mormyrus rume (Mormyridae). Our results indicated differences in ovary structure between P. buchholzi and the externally fertilizing species, as well as a considerable disparity in oocyte organization in all studied species. All species possess ovaries of the cystovarian type. In P. buchholzi, the epithelium lining the lumen was columnar and formed crypts with ciliated and microvillus cells as well as deep invaginations with secretory cells, whereas in the remaining species epithelium was squamous. The organization of oogonia and one‐nucleolus oocytes did not differ between species, there were variations in oocytes at subsequent steps of primary growth, including symmetry/asymmetry of the inner cell structure, differences in Balbiani body formation, presence/absence of zonation of the ooplasm, and differences in the order in which cortical alveoli and oil droplets appeared. These differences may be caused by a long and separate evolution of the families as well as adaptation to insemination in the family Pantodontidae.
... Arraias de água doce, assim como os elasmobrânquios em geral, possuem um perfil ecológico com características de organismos k-estrategistas, apresentando uma alta longevidade, maturação reprodutiva tardia, crescimento lento, fertilização interna, baixa fecundidade e um longo período de gestação vivípara matrotrófica (Wourms et al. 1988;Araújo et al. 2004). Além disso, apresentam uma importante relação entre o recrutamento e o tamanho da população reprodutiva (Stevens et al. 2000). ...
A família Potamotrygonidae compreende um grupo de peixes cartilaginosos classificados atualmente em duas subfamílias, Styracurinae e Potamotrygoninae, e quatro gêneros que contam com uma diversidade conhecida de 38 espécies. Ocorrem em diferentes ambientes, sendo Styracura uma linhagem marinha e os demais gêneros exclusivamente dulcícolas das bacias hidrográficas da América do Sul: Heliotrygon, Paratrygon, Plesiotrygon e Potamotrygon. As relações filogenéticas em Potamotrygonidae permanecem mal compreendidas, especialmente a validação do grupo marinho como subfamília em Potamotrygonidae, assim como quando ocorreu a origem de suas linhagens. Desta forma, o presente trabalho buscou apresentar uma hipótese acerca da filogenia do grupo, com datação molecular, a partir de uma abordagem multilocus, com regiões genômicas mitocondriais (COI, Cytb e Região controle) e nucleares (RAG1 e ECN1), utilizando os métodos de Máxima verossimilhança – ML e Inferência Bayesiana – IB. As árvores filogenéticas baseadas em 2,4 kb confirmaram a monofilia da família, assim como a classificação da subfamília Styracurinae em Potamotrygonidae. Heliotrygon mostrou ser o gênero menos derivado entre a subfamília Potamotrygoninae, que está proximamente relacionado a Paratrygon. Nossos resultados recuperaram parafilia entre Plesiotrygon e Potamotrygon, desta forma também podemos sugerir possível sinonímia entre estes taxa. A datação molecular recuperou a origem da família no Eoceno (44-38 Ma), concordando com registros fósseis recentes. Os potamotrygonídeos marinhos mostraram ter se originado em um período precedente à formação do Istmo do Panamá, já as linhagens dulcícolas indicam ter se diversificado a partir de um evento vicariante, como as incursões marinhas do Eoceno (35-28 Ma). Possivelmente, o estabelecimento do Sistema Pebas tenha favorecido a diversificação dos gêneros Heliotrygon e Paratrygon, já o gênero Plesiotrygon mostrou que se diversificou entre 28-25 Ma, ambos no Oligoceno. Potamotrygon mostrou ter se diversificado a partir do Mioceno (~23 Ma), que coincide com a formação do deságue do rio Amazonas em direção ao Oceano Atlântico. Assim, a disponibilidade de ambientes a partir deste período poderia explicar a ampla radiação em Potamotrygon, assim como as politomias entre as espécies do gênero. Este trabalho apresenta uma análise molecular que esclareceu algumas lacunas acerca das relações filogenéticas e padrões de diversificação da família Potamotrygonidae.
... therefore, it is better to classify them as two "sources" rather than as two modes. In many viviparous vertebrates, the embryos receive nutrients from these two sources (Wourms et al., 1988;Stewart, 1992;Thompson et al., 2000;Marsh-Matthews, 2011). Based on the bipartite system combined with the reproductive pattern (oviparity or viviparity), vertebrates have been classified as having four reproductive strategies: lecithotrophic oviparity, lecithotrophic viviparity, matrotrophic oviparity, and matrotrophic viviparity (or viviparous matrotrophy) (Blackburn, 2015). ...
Sebastes schlegelii is a commercially important fish with a special viviparous reproductive system that is cultured in near-shore seawater net cages in East Asia. In the gonadal development of the species, the gonad of males mature before those of females, which mature after mating. Mating in male/female fishes occurs in October of each year. Then, females undergoing oocyte maturation complete fertilization using stored sperm in March of the following year. The pregnancy is completed when larvae are produced in the ovary. It has been reported that embryonic nutrient supply originates entirely from the female viviparous reproductive systems. However, until now, the nutritional patterns and the processes of nutrient provision in S. schlegelii before parturition have not been clear. The goal of this research was to study the embryos, larvae and juveniles of S. schlegelii during pregnancy. Anatomical observations, light microscopy and scanning electron microscopy were used to study the developmental characteristics of early embryos and larvae and the connecting structures between the mother and the fetus. The results showed the following: (1) Placental-like structures were found during the process of embryonic development in S. schlegelii, and these placental-like structures proliferated after fertilization. (2) The embryos of S. schlegelii were encased by a saclike structure composed of blood vessels, connective tissue, and surface epithelial cells. The vessels near the embryo existed in the thecal layer. Vascularized proliferation was detected following embryonic development. (3) Starting in the gastrula stage, connections between the embryo and surrounding cells loosened, and ovarian fluid became abundant. In addition, a large number of small holes and cristae were observed on the surface of the embryo. We speculate that embryos may be able to absorb nutrients from the ovarian fluid. (4) Yolk was present throughout embryo development. (5) Two types of nutritional modes were observed, lecithotrophic and matrotrophic during embryonic development. Three forms of placental analogs may exist in S. schlegelii: (1) external epithelial absorptive surfaces; (2) trophonemata, with modifications of the ovarian epithelia for absorbing the histotroph; and (3) a follicular pseudoplacenta, with close apposition between follicle cells and embryonic absorptive epithelia.
... The structure of an elasmobranch placenta is physiologically distinct from that of mammals with varying degrees of maternal-embryo interfacing. The form of placentotrophy used by most sharks is the yolk-sac placenta, where the embryonic yolk sac is modified during development forming a connection to the uterine wall with subsequent formation of an umbilical stalk (Wourms et al. 1988) through which embryos receive nutrients from their mother. Prior to establishment of this connection, embryos primarily rely on energy stores found in their external yolk sacs, supplied by their mothers prior to ovulation (Hamlett, Jones et al. 2005a, b). ...
For species that do not provide parental care after birth, excess maternal provisioning during development, beyond what is required for embryogenesis, provides offspring with resources to increase their chances of survival. Maternally derived resources are expected to be important for buffering offspring against limited food resources at birth or time needed to learn how to properly feed. Young-of-the-year (YOY) cryptic Scalloped Hammerheads (Sphyrna lewini) and Carolina Hammerheads (Sphyrna gilberti) were sampled from nurseries along the US Atlantic Coast and compared for a number of biological condition metrics across three developmental stages. Large declines in liver lipid content and hepatosomatic indices were found in neonatal sharks, using umbilical scar healing as a proxy for time since birth. Feeding commenced quickly as 96% of sharks had prey remnants in their stomachs. The combination of rapid exhaustion of maternally provided resources and high occurrence of stomachs with prey contents indicate that nursery quality, with respect to prey availability, may be important for YOY hammerhead survivorship. While externally the two species are morphologically similar, longer length-at-birth in S. lewini and higher hepatic condition in neonatal S. gilberti suggest that aspects of reproductive biology, including physiology, may differ between species. While more information is needed to distinguish life history differences between these two species, data collected from YOY may serve as a useful proxy to inform management when adult samples of cryptic species are difficult to collect.
... Species that retain fertilized eggs internally for a significant period of time during which embryos develop to an advanced stage are generally referred to as viviparous [Wourms, 1981;Wourms et al., 1988;Wourms and Lombardi, 1992;Blackburn, 2005]. Based on the trophic relationship between the mother fish and embryo, the viviparous mode of reproduction can be classified as either lecithotrophic, if nutrients come from yolk exclusively, or matrotrophic, if there is an alternative supply route of maternal nutrients [Wourms, 1981;Knight et al., 1985;Blackburn, 2005]. ...
We characterized the ontogeny and dynamics of gonadal development, embryogenesis, and gestation in captive stocks of the viviparous redtail splitfin, Xenotoca eiseni. Using histology, we showed that gonads were fully differentiated at the time of birth with a male:female sex ratio of 1:1 in the captive stock. External secondary sex features included a modified anal fin and a distinctive orange tail coloration. These features first appeared at 4 weeks after birth and were discriminative for males thereafter. There was no sex-related dichotomy in body size, and X. eiseni reached sexual maturity at approximately 12 weeks of age. We found no evidence for sperm storage in females. Gestation normally took 6 weeks, and there was a positive correlation between female body size and the number of offspring produced, with up to 27 offspring for a single pregnancy. Yolk is the main food source for developing embryos for the period up to 2 weeks, and thereafter, trophotaeniae in embryos act as nutrient exchange surfaces in the ovarian lumen, which subsequently undergo complete regression within 2 weeks of birth. In our final analysis, we discuss the great potential of X. eiseni as a model for studying the effects of chemicals on sexual development.
... The Mexican Central Plateau is an area of intense anthropogenic activity (agriculture, urbanization, industrial discharges), the wastes of which are discharged into water bodies (De la Vega-Salazar and Macías-Garcia 2005;Favari et al. 2002). In this region, freshwater bodies are populated by Goodea atripinnis, a viviparous fish of the subfamily Goodeinae that is endemic to Mexico (Domínguez-Domínguez, Mercado-Silva, and Lyons 2005) and includes 40 viviparous species characterized by matrotrophy, internal fertilization, and marked sexual dimorphism (Schindler 2015;Wourms, Grove, and Lombardi 1988). The Goodeinae is a group of fish of high ecological, evolutionary, and biogeographical significance, currently threatened by the presence of emerging pollutants in their habitat, including BPA (Díaz-Torres et al. 2013;Olivares-Rubio et al. 2015). ...
Bisphenol A (BPA) is an emerging pollutant of global concern. Viviparous fish Goodea atripinnis is endemic to the Central Mexican Plateau where BPA was detected; however, few studies examined the influence of this chemical on native viviparous fish. The effects of BPA (sublethal dose) were determined on DNA integrity and Foxl2 expression in G. atripinnis gonads, and interactions of BPA with FOXL2 protein. Genotoxicity analysis revealed that % comets, at 14 and 28 days and comet tail length (at 14 days) were significantly higher in exposed compared to controls. In general, the % DNA tail was not markedly higher in BPA-treated fish; however, tail moment related to tail length exhibited significant increases in DNA damage. RT-qPCR assays showed Foxl2 overexpression after 14 and 28 days of exposure in females; while in males, Foxl2 was overexpressed after 28 days. In silico analysis demonstrated that BPA interacted with seven residues located in FOXL2 homeodomain. In summary, sublethal BPA doses induced DNA damage and changes in Foxl2 expression in gonadal cells of G. atripinnis, which may adversely affect reproduction in BPA-exposed wild populations. Foxl2 overexpression and BPA-FOXL2 interaction suggested alterations in processes involving Foxl2. Viviparous fish may thus serve as potential non-conventional models for assessing pollutants effects.
Gamma-aminobutyric acid (GABA) functions as the primary inhibitory neurotransmitter within the central nervous system (CNS) of vertebrates. In this study, we examined the distribution pattern of GABA immunoreactive (GABA-ir) cells and fibres in the CNS of the viviparous teleost Poecilia sphenops using immunofluorescence and immunocytochemical methods. GABA immunoreactivity was seen in the glomerular, mitral, and granular layers of the olfactory bulbs, as well as in most parts of the dorsal and ventral telencephalon. The preoptic area consisted of a small cluster of GABA-ir cells, whereas extensively labelled GABA-ir neurons were observed in the hypothalamic areas, including the paraventricular organ, tuberal hypothalamus, nucleus recessus lateralis, nucleus recessus posterioris, and inferior lobes. In the thalamus, GABA-positive neurons were only found in the ventral thalamic and central posterior thalamic nuclei, whereas the dorsal part of the nucleus pretectalis periventricularis consisted of a few GABA-ir cells. GABA-immunoreactivity was extensively seen in the alar and basal subdivisions of the midbrain, whereas in the rhombencephalon, GABA-ir cells and fibres were found in the cerebellum, nucleus of glossopharyngeal and vagal nerves, nucleus commissuralis of Cajal, and reticular formation. In the spinal cord, GABA-ir cells and fibres were observed in the dorsal horn, ventral horn, and around the central canal. Overall, the extensive distribution of GABA-ir cells and fibres throughout the CNS suggests several roles for GABA, including neuroendocrine, viscerosensory, and somatosensory functions, for the first time in a viviparous teleost.
Feeding offspring is a form of care common in animals. How food shapes offspring fitness, and thus selection on parents, is limited by plasticity in offspring growth and development, and such limitation may shape the evolution of parental care. We compared plastic responses to egg feeding, food availability in the nursery, and nursery size in larvae of two poison frogs: Ranitomeya imitator, regularly fed trophic eggs by their mothers in the wild, and R. variabilis tadpoles, which only rarely have the opportunity to consume eggs. Hand‐reared R. imitator, but not R. variabilis, were heavier at metamorphosis when offered eggs. Although R. imitator ate more of the eggs we offered, perhaps explaining this proximately, the greater plasticity of R. imitator persisted when we manipulated the quantity of an egg‐free diet meant to approximate food in a natural nursery. Egg feeding did not influence the length of the larval period, and only tadpole R. variabilis took longer to complete metamorphosis in more food‐rich nurseries, as is predicted for amphibians generally. In large nurseries, individuals of both species spent longer as tadpoles and were heavier at metamorphosis, an effect independent of food, and one that reflects the complex relationship between ecology and amphibian development. These species differences highlight how tadpole traits might constrain the evolution of egg feeding: R. imitator feed eggs to their tadpoles, and their tadpoles, unlike R. variabilis (a presumptive proxy for the non‐feeding ancestor), offer high returns on such investment. Comparative work will offer the exciting opportunity to assess the extent to which egg feeding selected for this growth response to food availability and/or this plasticity facilitated the evolution of care. Parent Ranitomeya imitator feed their young with trophic eggs, while parent R. variabilis do not. On a diet that substituted for natural invertebrate, algae, and detritus forage, R. imitator (a) and R. variabilis (c) were similar size at metamorphosis. When fed eggs, however, R. imitator (b) were heavier, but R. variabilis (d) were not, and this plasticity difference persisted when we manipulated only the quantity of substitute forage offered. Tadpole plasticity may constrain the evolution of egg feeding.
There are few detailed descriptions of the morphology of the male external genitalia, the urogenital papilla (UGP), of the Black Rockfish (Sebastes schlegelii Hilgendorf, 1880). The purpose of this study was to evaluate this organ histologically and to determine the time of development of the UGP in Black Rockfish. Twelve adult males, three adult females and around 500 juveniles were used in the experiment. The juveniles were divided into normal developmental and androgen groups. The androgen group was exposed to methyltestosterone (100 ug/L) for 2 h daily for 38 days. Samples (N=10 per sampling) were randomly selected for analysis every 5 days from 30–116 days after birth. Parameters assessed included the type of epithelium, composition of connective tissue, muscular tissue, and the timing of UGP development. Differences in these parameters between normal developmental and androgen groups were evaluated. The results indicated that the UGP of the adult fish contains the sperm duct and ureter, which have the function of transporting sperm and urine respectively. The androgen‐treated juvenile fish developed the UGP earlier than the normal development group. This study provides a reference for understanding the external genitalia of other viviparous fishes by studying the UGP of the male Black Rockfish. This article is protected by copyright. All rights reserved.
The sub-order Scorpenoidei appears to be particularly interesting due to the presence of intermediate stages between oviparity and viviparity in several species. The present study aims to describe the ovarian morphology, using a histological and histochemical approach, in four ovuliparous species belonging to Scorpaena genus compared with a zygoparous species, H. dactylopterus, focusing also on the assessment of the ovarian dynamics in the populations of such species in Sardinia waters (central–western Mediterranean). Ovarian sections of all species were examined using light microscopy. All species showed a specialized ovary, cystovarian type II-3, strictly related to the production of gelatinous matrices surrounding the eggs. Some microscopic peculiarities in the oogenesis process were found: thin zona pellucida, small and low cortical alveoli, and a specialized ovarian wall during the spawning period. All species analyzed were batch-spawners with an asynchronous ovarian organization. A continuous recruitment of oocytes and the occurrence of de novo vitellogenesis was also observed. During the spawning period, low atresia intensity was detected, while a marked increase in this intensity found in the ovaries at the end of spawning season. Our observations may support an indeterminate fecundity type for these species.
In viviparous fish, a considerable degree of variation in placental structures have been described. However, no distinct structures are reported in Scorpaenidae. In this study, we demonstrate a new type of folliculogenesis and follicular placentation in Sebastes schlegelii. Before copulation, the germinal epithelium gradually surrounds the oocytes and develops to individually follicles with a stalk-like structure hanging on the ovigerous lamella, which ensures each follicle have access to spermatozoa after copulation. From stage V to early gestation, the cyp17-I highly expressed accompanied by cyp19a1a signals disappearance, and 11-ketotestosterone level keeps rising and peaks at blastula stage, while 17β-estradiol declines to the bottom. Meanwhile, the theca cells rapidly proliferate and invade outwards forming a highly hypertrophied and folded microvillous placenta. This unbalance of hormone might be an important factor driving the theca cells proliferation and invasion. Additionally, some conserved genes related to mammalian placentation are significantly high expression in follicular placenta suggesting the high convergence in vertebrate placenta evolution.
Oocyte morphology and spermatozoa ultrastructure are studied in the representatives of the genera Parascorpaena and Scorpaenopsis. Oocytes of P. aurita and S. cirrosa are attached to peduncles originated from ovigerous stroma located in the central part of the ovary. Oocyte diameter at the final phases of vitello-genesis is 450 and 500 μm, respectively. The oogenesis is asynchronous and continuous. Spermatozoa of four species (P. aurita, P. mossambica, S. cirrosa, and S. diabolus) possess similar morphology: spermatozoon head width is slightly larger than its length. The genera Parascorpaena (three species) and Scorpaenopsis (four species) differ in three from four indices designating spermatozoon head and midpiece shapes, size of nuclear fossa in the spermatozoon nucleus base (20-25 vs. 0-12% of head length), and relative location of proximal and distal centrioles (coaxial and orthogonal, respectively). The irregular shape of the nuclear fossa in the spermatozoon nucleus base of P. aurita can be interpreted as apomorphy.
The monoaminergic neurotransmitter serotonin (5-HT) acts as a neuromodulator and is associated with a wide range of functions in fish. In this investigation, 5-HT immunoreactivity was studied in the central nervous system (CNS) of the viviparous mosquitofish Gambusia affinis. 5-HT-immunoreactive (5-HT-ir) cells/fibres were observed throughout the subdivisions of ventral and dorsal telencephalon including the olfactory bulb. Several intensely stained 5-HT-ir cells and/or fibres were detected in different areas of the hypothalamus as well as the proximal pars distalis of the pituitary gland. 5-HT-ir cells were restricted to the dorsal and ventral part of the pretectal diencephalic cluster, but only fibres were detected in the anterior, ventromedial and posterior subdivisions of the thalamic nucleus and in the preglomerular complex. In the mesencephalon, 5-HT-ir perikarya, and fibres were seen in the optic tectum, midbrain tegmentum and torus semicircularis. A cluster of prominently labelled 5-HT-ir neurons was observed in the superior raphe nucleus, whereas numerous 5-HT-ir fibres were distributed throughout the rhombencephalic divisions. In addition, a bundle of rostrocaudally running 5-HT-ir fibres was noticed in the spinal cord. This is the first detailed neuroanatomical study in a viviparous teleost, reporting a widespread distribution of 5-HT-ir somata and fibres in the CNS. The results of this study provide new insights into the evolutionarily well conserved nature of the monoaminergic system in the CNS of vertebrates and suggest a role for 5-HT in regulation of several physiological, behavioural and neuroendocrine functions in viviparous teleosts.
The reproduction strategies of invertebrates, oviparity, ovoviviparity and viviparity, always reflect the relationship between individuals and their surroundings. There is plasticity in the reproductive strategies of sarcosaphagous flies as they adjust to rapidly changing circumstances. The transition from oviparity to ovoviviparity or viviparity involves numerous changes in physiology, morphology and immunology. Demonstrating these processes can make the application of entomology work in forensic practice more reliable. This essay reviews means of reproduction in sarcosaphagous flies and identifies related features. It is shown that not only the reproduction traits, such as fast location of carrion, and uncommon number of ovaries and oogenesis, but also some morphological features are related to viviparity. In general, viviparous flies have larger adult bodies but smaller eggs and chorions. Moreover, the length of terminalia and the shape of the vagina also varies among those three modes. Reproductive plasticity is a bridge between the three reproductive modes, and it can greatly influence the inference of the post-mortem interval (PMImin).
How and why complex organs evolve is generally lost to history. The mammalian placenta, for example, was derived from a single common ancestor that lived over 100 million years ago.1, 2, 3 Therefore, the selective factors favoring this complex trait remain obscure. Species in the live-bearing fish family Poeciliidae have independently evolved placentas numerous times while retaining closely related non-placental sister species.4, 5, 6, 7 This provides the raw material to test alternative hypotheses for the evolution of the placenta. We assemble an extensive species-level dataset on reproductive mode, life histories, and habitat, and then implement phylogenetic comparative methods to test adaptive hypotheses for the evolution of the placenta. We find no consistent family-wide associations between placentation and habitat. However, placental species exhibit significantly reduced reproductive allotment and have a higher likelihood of exhibiting superfetation (the ability to gestate multiple broods at different developmental stages). Both features potentially increase body streamlining and enhance locomotor performance during pregnancy, possibly providing selective advantage in performance-demanding environments such as those with high predation or fast water flow. Furthermore, we found significant interactions between body size and placentation for offspring size and fecundity. Relative to non-placental species, placentation is associated with higher fecundity and smaller offspring size in small-bodied species and lower fecundity and larger offspring size in large-bodied species. This pattern suggests that there may be two phenotypic adaptive peaks, corresponding to two selective optima, associated with placentation: one represented by small-bodied species that have fast life histories, and the second by large-bodied species with slow life histories.
Female teleosts fishes do not develop Müllerian ducts; consequently, they do not have oviducts, and uniquely, the ovary forms the reproductive system. Therefore, the ovary is divided into two zones: germinal and gonoduct. The gonoduct of Poecilia reticulata is divided into three regions: anterior, middle, and posterior. The histological components of the gonoduct are epithelium, connective tissue, longitudinal smooth muscle, and visceral peritoneal epithelium at the periphery. The connective tissue contains macrophage, eosinophils, lymphocytes, and melanomacrophage centers. To conclude, the gonoduct is involved in essential aspects of reproduction such as secretory and immunological activities, receives the sperms during the insemination, and is the passage of embryos during birth.
Across teleost fishes, a wide range of parental care strategies have been observed. However, despite this large variation in parental care behaviors, postnatal nutritional provisioning has rarely been documented in fishes. In other taxa, anecdotal evidence suggests that nutritional provisioning of offspring via mucus secretion by parents may occur, although this phenomenon has received little attention from evolutionary biologists, especially in fishes. To address this knowledge gap, we investigate the intra- and interspecific differences, functions, and the costs and benefits of provisioning behaviors that have potentially evolved independently in different teleost clades. Furthermore, we review and discuss within an ecological and evolutionary context, the anecdotal reports and limited available empirical evidence that shows support for mucus provisioning in teleost fishes.
Embryos of the viviparous dwarf ornate wobbegong shark (Orectolobus ornatus) develop without a placenta, unattached to the uterine wall of their mother. Here, we present the first light microscopy study of the uterus of O. ornatus throughout pregnancy. At the beginning of pregnancy, the uterine luminal epithelium and underlying connective tissue become folded to form uterine ridges. By mid to late pregnancy, the luminal surface is extensively folded and long luminal uterine villi are abundant. Compared to the nonpregnant uterus, uterine vasculature is increased during pregnancy. Additionally, as pregnancy progresses the uterine epithelium is attenuated so that there is minimal uterine tissue separating large maternal blood vessels from the fluid that surrounds developing embryos. We conclude that the uterus of O. ornatus undergoes an extensive morphological transformation during pregnancy. These uterine modifications likely support developing embryos via embryonic respiratory gas exchange, waste removal, water balance, and mineral transfer. The uterus of the viviparous dwarf ornate wobbegong (Orectolobus ornatus) undergoes a morphological transformation during pregnancy. This image shows the uterine wall of a late pregnant female that contains embryos just prior to birth. The extensive vascularization by the increase in blood vessels in the long uterine villi (v), uterine connective tissue and muscle layers, likely support embryonic gas exchange, waste removal, water balance, and mineral transfer.
Different hypotheses have been proposed to explain the adaptive value of matrotrophy, which is the postfertilization maternal provisioning to developing embryos. The Trexler–DeAngelis model proposes that matrotrophy provides fitness advantages when food abundance is high and availability is constant. If food availability is low or unpredictable, prefertilization maternal provisioning (lecithotrophy) should be favored over matrotrophy. In this study, we tested this model in two fish species from the family Poeciliidae, Poeciliopsis gracilis and P. infans, using field and laboratory data. In the field study, we explored the effects of population, season, and food abundance on the degree of matrotrophy. In P. infans, we found evidence that supports this model: In the population where food abundance decreased during the dry season, females reduced the amount of postfertilization provisioning and thus exhibited a more lecithotrophic strategy. In P. gracilis, we observed patterns that were partially consistent with this model: Food abundance decreased during the wet season in three populations of this species, but only in one of these populations, females exhibited less postfertilization nutrient transfer during this season. In the laboratory study, we tested the effects of constant, fluctuating, and low food availability on the relative amounts of pre‐ and postfertilization provisioning of P. infans. Our laboratory results also support the Trexler–DeAngelis model because both low and fluctuating food regimes promoted a more lecithotrophic strategy. Together, our findings indicate that the benefits of matrotrophy are more likely to occur when females have constant access to food sources.
Research Highlights
• Food availability affects how females from two viviparous fish species transfer nutrients to developing embryos.
• Lecithotrophy occurred when food availability was low or fluctuating.
• Matrotrophy occurred when food was abundant and constantly available.
By studying embryonic mass increase, yolk availability and embryonic oxygen consumption, it was established that the embryos of C. superciliosus rely almost entirely on maternal secretions for their nutrients and the species therefore displays an advanced form of viviparity. They breed throughout the year and the species also exhibits superembryonation (superfoetation -sic) with as many as 12 broods developing simultaneously. Furthermore, it was found that the relationships between the body mass and the gonad masses and number of embryos produced, are linear. It was suggested that these phenomena, coupled to the territoriality exhibited by the species, are factors whereby the species overcomes the problem of a reduction in the number of embryos produced, a phenomenon normally encountered in viviparous fishes.By die bestudering van embrioniese massa-toename, dooier- beskikbaarheid en embrioniese suurstofverbruik, is vasgestel dat die embrios van C. superciliosus feitlik heeltemal staatmaak op moederlike sekresies vir hulle voedsel en daarom toon die spesies 'n gevorderde vorm van vivipariteit. Hulle broei dwarsdeur die jaar en die spesies toon ook super- embrionasie (super-fetasie - sic) met soveel as 12 broeisels wat gelyktydig ontwikkel. Verder is ook gevind dat die verhoudings tussen die liggaamsmassa en die teelkliermassas en die aantal embrios geproduseer, linieer is. Dit is voorgestel dat hierdie verskynsel, gekoppel aan die territorialiteit getoon deur hierdie spesies, faktore is waarby die spesies die probleem van 'n verlaging in die aantal embrios geproduseer oorbrug - 'n verskynsel wat normaalweg aangetref word by viviparige visse.
Thesis (Ph. D.)--University of Delaware, 1964. Photocopy.
In this paper we examine what is known of selected morphological and physiological aspects of reproduction in cyclostomes and chondrichthyan fishes and attempt to evaluate the contribution this makes to our knowledge of the ways in which reproduction may have evolved in these animals and in general. The reproductive biology of both groups is of exceptional interest in this context in view of their long phylogenetic history, their long separation from each other, and the diverse range of reproductive specializations they have adopted. Not only are both groups phylogenetically ancient, they both contain two subgroups which are themselves old. The cyclostomes are classified into myxinoids (hagfish) and petromyzonids (lampreys) and, according to Jarvik (1968), their probable respective ancestors, the heterostracans and cephalaspids, diverged during the Pre-Cambrian period, more than 600 million years ago. The chondrichthyans are subdivided into elasmobranchs (sharks and rays) and holocephalans (chimaeras and ratfishes). These are probably sister groups, sharing a common ancestor from which they diverged some 350 million years ago (see Dodd, 1983 for references). As might be expected, the basic difference in ancestry between cyclostomes and chondrichthyans is reflected in the reproductive structures and functions of the two groups.
The nidamental gland of the dog-fish (Fig. 1) secretes an egg-case whose median layer is composed of a collagenic material1,2 of sheets displaying a plywood structure3. We have observed the extrusion of the collagenic protein by scanning electron microscopy and tried to locate the sites where the precursors of this material are being synthesized.
Although common in invertebrate animals extracellular secreted structural materials wholely separate from the soma are uncommon in the vertebrates. Keratinized structures for example are intracellular and for their functional life part of the animal epidermal organization.
This chapter discusses some of the principal features of the relationship between hormones and reproductive behavior in fishes. The term “reproductive behavior” encompasses a diverse range of activities involved in a propagative function. It includes sexual, parental, and nest building behaviors. Agonistic and migratory behavior is also considered “reproductive,” as they are essential preliminaries involved in reproduction. Hormones, such as gonads and anterior pituitary, play a major role in controlling the reproductive processes; there is some evidence that neurohypophysial and thyroid hormones are also directly involved in the regulation of certain components of reproductive behavior in fish. Little is known of the details of the mechanisms by which hormones exert their effects on the behavior. Furthermore, this chapter reveals an apparent diversity and lack of agreement in the studies of the role of hormones and behavior in fish.
This chapter presents an overview of the internal morphology of gills. Each gill arch skeleton is jointed with the posterior skull dorsally and with the copula ventrally. The septum contains nerves and blood vessels and bears the filaments. Two rows of filaments are generally inserted on each gill arch. This whole forms the so-called holobranchs. The mode of the insertion of filaments on the gill arch depends on the morphology of the septum and varies with the group of fish. In some groups (Chondrostei and the holostean Lepisosteus), certain arches—the hyoidean and the mandibular only—bear a single row of filaments, called “hemibranchs.” In other groups or species, these arches are completely devoid of filaments or absent, such as in Amia (Holostei), which has a mandibular but no hyoidean arch. The presence of lamellae on gill arches corresponds with the distribution of true aortic arches. The pattern of branchial arch organization is relatively constant among teleosts, but differs significantly in lower groups. In Myxinoidei, the variable number of gill slits correspond to a series of pouches connected by narrower tubes with the gut and body surface.
Eleven specimens of Pseudocarcharias kamoharai, consisting of 8 males and 3 females, were collected from the central Pacific in June, 1979.One of the females, 985mm TL, was pregnant and contained four large embryos (401-428 mm TL) in the uteri.The embryos had no trace of umbilical scar.But, their abdomens were distended and, when dissected, their stomachs contained considerable amount of egg yolk material which accounted for about 25 % of the weight of the body.This suggests that the embryos of P.kamoharai nourish themselves by feeding on ova in the uteri of the female.Another pregnant female, 982 mm in TL, contained both small embryos (37.9-40.8mm TL) with yolk sacs and many egg capsules in the uteri.These small embryos had still been absorbing yolk material from the yolk sac, and showed no signs of feeding on ova in the uteri.
Embryos of Clinus dorsalis absorb nutrients from the embiyotrophe, secreted by the follicular epithelium. Autoradiographic studies revealed that the principal areas of nutrient absorption are the embryonic gut and epidermis. A histological and electron microscopic study of embryonic structure revealed an extensively hypertrophied gut with numerous flngerlike villi projecting into the gut lumen. A brushborder of microvilli is, furthermore, characteristic of the columnar gut epithelium. Epidermal surface area is increased apically on individual epidermal cells, particularly on the ventral pericardial surface. Micro ridges further increase epidermal surface area. Epidermal surface area is reduced and a mucous layer is secreted prior to parturition.Embrio's van Clinus dorsalis absorbeer voedsel vanuit die embriotroof wat deur die follikuldre epiteel gesekreteer word. Outoradiograflese studies het getoon dat die belangrlkste geblede vir voedselabsorpsie die embrioniese spysverteringskanaal en epidermis is. 'n Histologiese en elektronmlkroskopiese ontleding van hlerdie embrioniese strukture het getoon dat die spysverteringskanaal gehipertrofeer is en dat talle vingeragtige villi in die S.V.K.- lumen voorkom. Die sllinderepiteel van die S.V.K. is ook 2 voorsien met 'n goed ontwikkkelde borselrant bestaande uit mikrovilli. Die epldermale oppervlakte van die embrio's word vergroot deur bulte wat gevorm word deur die apikale 5 oppervlakte van indiwiduele epidermale selle veral op die ventrale perikardiale oppervlakte van die embrio's. Mikrorlwwe vergroot die epldermale oppervlakte verder.Voor geboorte word die epidermale oppervlakte verminder en 'n slymlaag word gesekreteer.
This chapter describes the general anatomy of the gills in fish. The gills form a highly characteristic feature of fishes and their presence has a marked effect on the anatomy and functioning of the rest of the animal. A gill septum separates two adjacent gill pouches and a series of filaments is attached to its surface. In the most primitive groups, the septum forms a complete partition between the pharynx and the outer body wall. Its extension forms a flap-valve for the next posterior slit. In more advanced groups, there is a progressive reduction in the septum and the consequent freeing of the filaments at their tips. Filaments form the most distinctive respiratory structure of fish gills and are sometimes referred to as “primary lamellae.” In adult fish, the number of filaments does not increase so markedly as during the juvenile growth period, but there is a very significant increase in the length of each of them as the fish grows. The lamellae are the most important units of the gill system from the point of view of gas exchange. The rest of the basic anatomy is directed to providing a suitable support for these structures and to enable the water and blood to come into close proximity.
This chapter discusses the functional morphology of teleost gonads. Information presented in this chapter indicates that there are several processes of germ cell development, which are closely associated with changes in cellular activities of somatic cell elements. Recent studies on biochemical aspects of vitellogenesis in teleosts have shown that the hepatic and ovarian yolk proteins are similar to those of amphibian species. An in vitro method involving the separation of the follicular components has facilitated investigations of the detailed mechanism of the production of two major follicular steroid hormones. As a result of the usage of this technique, a two cell-type model involving thecal and granulosa cell layers has been proposed for the production of these two steroids for the first time in lower vertebrates. With further refinements this well characterized incubation procedure should provide an excellent system for studying the molecular basis of the mechanism of gonadotropin action on follicular steroidogenesis.
The vitelline syncytium of the embryonic rockfish, Sebastes schlegeli, was examined by electron microscopy.The syncytium encloses the entire yolk mass in the yolksac, separating it from the embryonic body and the circulating fetal blood.Numerous small yolk droplets fused into coagulated masses were detected in the syncytial cytoplasm near the border with the yolk mass.Two structurally different regions were distinguished in the syncytium: one characterized by an extensive network of the smooth surfaced endoplasmic reticulum, numerous mitochondria and a large number of glycogen granules, and the other by compactly arranged cisternae of the rough surfaced endoplasmic reticulum and developed Golgi complexes.In some surface areas where the endothelial wall of blood vessels is incomplete and the fetal blood is in direct contact, the syncytium showed finely vacuolated cytoplasm forming an intricate structure between the cytoplasmic processes of the blood cells.These characteristic features of the vitelline syncytium are discussed in view of its functional significance in yolk absorption.
The anatomy and histology of the ovaries of C. superciliosus and C. dorsalis are described. The ovaries are extensively modified as trophic organs since embryos of both species develop intrafollicuiarly and are dependent on maternal nutrient secretions during development. The follicular epithelia of the two species are modified to perform a secretory function and follicular cells are hypertrophied in areas producing embryotrophe. In non-hypertrophied areas the follicular cells remain thin to bring about close contact between the embryos and the maternal vascular system underlying the epithelium. In C. superciliosus embryonic epidermal macroridges are closely aligned to areas of follicular hypertrophy thus forming a pseudoplacenta. A similar arrangement is not found in C. dorsalis.Die anatomie en histologie van die ovaria van C. superciliosus en C. dorsalis word beskryf. Die ovaria is omvorm tot trofiese organe aangesien embrio's van beide spesies intrafollikulêr ontwikkel en van moederlike voedselsekresies afhanklik is tydens hul ontwikkeling. Die follikuläre selle van die twee spesies het 'n sekretoriese funksie, en is verdik in gebiede wat embriotroof produseer. In ander gebiede is die follikuläre selle afgeplat om sodoende noue kontak tussen die embrios en die moederlike bloedsisteem, wat onder die epiteel voorkom, te bewerkstellig. In C. superciliosus is embrioniese epidermale makroriwwe teenaan gebiede van follikuläre hipertrofie geleë om 'n pseudoplasenta te vorm. 'n Soortgelyke situasie kom nie by C. dorsalis voor nie.
This chapter discusses the reproduction in cartilaginous fishes (chondrichthyes). The cartilaginous fishes are phylogenetically the oldest of the jawed vertebrates and therefore of special interest to comparative reproductive physiologists. All elasmobranchs studied except possibly the basking shark, have yolky eggs, but nothing is known about vitellogenesis except in S. caricukz and there are no detailed fine structural studies. This is the only vertebrate group of which this is true. Corpora atretica are present in the ovary as in other vertebrate ovaries, and postovulatory follicles (corpora lutea), showing varying degrees and types of activity before they disappear, are also present, but whether or not these structures have any functional significance remains unknown. There is a case for believing that the situation regarding these might be different in viviparous species, especially placentals, from that in oviparous species, but what little evidence there is for this is equivocal and nothing is known of any endocrine function the gonads, pituitary, and placenta may have in gestation and parturition.