Branchial placenta in the viviparous teleost Ilyodon whitei (Goodeidae)

Abstract

Intraluminal gestation, as it occurs in viviparous goodeids, allows a wide diversity of embryo-maternal metabolic exchanges. The branchial placenta occurs in embryos developing in intraluminal gestation when ovarian folds enter through the operculum, into the branchial chamber. The maternal ovarian folds may extend to the embryonic pharyngeal cavity. A branchial placenta has been observed in few viviparous teleosts, and there are not previous histological analyses. This study analysis the histological structure in the goodeid Ilyodon whitei. The moterno ovarian folds extend through the embryonic operculum and reach near the gills, occupying part of the branchial chamber. These folds extend also into the pharyngeal cavity. In some regions, the epithelia of the ovarian folds and embryo were in apposition, developing a placental structure in which, maternal and embryonic capillaries lie in close proximity. The maternal epithelium has desquamated cells which may enter through the branchial chamber to the pharyngeal cavity and the alimentary tract. The complex processes that occur in the ovaries of viviparous teleosts, and its diverse adaptations for viviparity, as the presence of branchial placenta, are relevant in the study of the evolution of vertebrate viviparity.

Ovarian structure and oogenesis of the extremophile viviparous teleostPoecilia mexicana(Poeciliidae) from an active sulfur spring cave inSouthernMexico

“…Oogenesis is similar to that in lecithotrophic poeciliids, which accumulate abundant yolk during the SG Stage (Uribe et al, ) as in X. helleri (Bailey, ), P. gracilis (Uribe, De la Rosa‐Cruz, García‐Alarcón, Guerrero‐Esteves, & Aguilar‐Morales, ), P. reticulata (Lambert, ), P. latipinna (Uribe et al, ), Cnesterodon decemmaculatus (Parenti, Lo Nostro, & Grier, ), Gambusia affinis (Koya, Itazu, & Inoue, ) and H. formosa (Uribe & Grier, ). During the PG Stage, Poecilia mexicana oocytes progressively increase in size and their cytoplasm becomes deeply basophilic, as in all vertebrates (Selman & Wallace, ; Wallace & Selman, ).…”

“…As with oogenesis, the origin of new ovarian follicles in fish is poorly understood (Franca, Grier, & Quagio‐Grassiotto, ). However, from observations of folliculogenesis in several teleost species (Grier, ; Grier et al, ; Nakamura, Kobayashi, Nishimura, Higashijima, & Tanaka, ; Quagio‐Grassiotto, Grier, Mazzoni, Nobrega, & Paulo de Arruda, ; Uribe et al, ; Uribe, De la Rosa‐Cruz, & García‐Alarcón, ) it has been suggested that folliculogenesis is a process conserved in fishes and other vertebrates (Grier, ; Grier et al, ; Franca et al, ; Parenti & Grier, ). Here, observations of folliculogenesis of P. mexicana , added evidence to support the conserved form and function of germinal epithelium through vertebrate evolution (Grier et al, ).…”

Morphological specializations for fetal maintenance in viviparous vertebrates: An introduction and historical retrospective

“…For example, Claire Weekes' enormously fruitful decade of contributions (1925)(1926)(1927)(1928)(1929)(1930)(1931)(1932)(1933)(1934)(1935) was followed by a half century that yielded few papers on squamate placentation, some of which were of questionable quality (for reviews, see Blackburn, 1993bBlackburn, , 1998Stewart, 1993). Likewise, after an extended period of remarkable productivity marked by work of the late John P. Wourms (Ptacek, 2005), William C. Hamlett, and their colleagues and students, morphological research on piscine matrotrophy appears to be experiencing a similar lull (however, see Schindler, 2015;Kwan et al, 2015;and Uribe et al, 2014). As another example, recognition of the marsupial reproductive pattern as "alternative" (rather than "inferior") to that of eutherians (Renfree, 1981(Renfree, , 1983(Renfree, , 2010Tyndale-Biscoe and Renfree, 1987) helped stimulate more than three decades of fruitful research on these animals.…”

Change of lecithotrophic to matrotrophic nutrition during gestation in the viviparous teleost Xenotoca eiseni (Goodeidae)

“…An additional structure of matrotrophy clearly developed in X. eiseni is the branchial placenta, a structure also identified in other species, as in embryos of Cymatogaster aggregata (Turner, ), Jenynsia lineata (Richter et al, ; Schindler & Greven, ), and Ilyodon whitei (Uribe et al, ). These authors coincided that the ovarian folds extended through the embryonic opercular clefts into the branchial chamber suggest an essential nutritive role of this structure.…”

“…Thus, the embryos may absorb nutrients from maternal tissues in addition to the yolk during gestation, developing diverse embryo‐maternal metabolic exchanges. Absorption of histotrophe in goodeids may occur via several structures of the embryo such as digestive tract, skin, branchial placenta (formed during late gestation when folds of ovarian tissue enter into the embryonic branchial chamber) (Lombardi, ; Mendoza, ; Richter, Lombardi, & Wourms, ; Schindler & Greven, ; Turner, ; Uribe, De la Rosa‐Cruz, & García‐Alarcón, ), and mainly by flattened extensions of the caudal portion of the intestine called trophotaeniae, which grow into the ovarian lumen (Turner, , ; Richter et al, ; Schindler & Greven, ; Uribe et al, ; Wourms & Lombardi, 1985; Wourms et al, ).…”