Ultrastructure and protein uptake of the embryonic trophotaeniae of four species of goodeid fishes (Teleostei: Atheriniformes)

Abstract

Embryos of most species within the viviparous teleost family Goodeidae develop characteristics perianal processes that are considered to be derivatives of the embryonic hindgut. These processes, termed trophotaeniae, are covered with an epithelium that is continuous with the absorptive epithelium lining the hindgut. Gestation is intraovarian, and trophotaeniae mediate the uptake of maternally provided nutrients into the embryo from the ovarian fluid. Ultrastructural examination of the trophotaeniae of four goodeid species reveals substantial diversity in the organization of the epithelium within the family. The trophotaeniae of Alloophorus robustus, Zoogoneticus quitzeoensis, and Ilyodon furcidens have morphological features associated with the endocytosis of macromolecules and can be shown to endocytose the exogenous protein tracer horseradish peroxidase (HRP) rapidly. The trophotaenial epithelia of these species differ from one another with respect to other morphological features such as cell height, organization of the brush border, and the complexity of the intercellular spaces. The trophotaeniae of Goodea atripinnis lack an endocytotic apparatus and do not endocytose HRP. However, the overall organization of G. atripinnis trophotaenial cells suggests a function as a transporting epithelium. The cells have a dense brush border, numerous mitochondria, and many mitochondria that are enveloped by lamellar sheets of intracellular membrane. Post-fixation with osmium and potassium ferrocyanide reveals a marked difference in the complexity of the subepithelial connective tissue. Alloophorus robustus and Z. quitzeoensis exhibit an extremely electron-dense ground substance containing many acellular components. Goodea atripinnis exhibits an electron-lucid ground substance with few acellular components. © 1994 Wiley-Liss, Inc.

Functional morphology of embryonic development in the Port Jackson shark Heterodontus portusjacksoni (Meyer)

“…As the embryo grows the surface area may become limiting in its ability to facilitate oxygen uptake and other surfaces resume the respiratory role (Hughes & Al‐Kadhomiy, 1988). During embryonic development in fishes, it is common for unusual structures such as elongate fin rays, tentacles, eyestalks, trophotaeniae and external filaments to form, only to be lost later in development (Ballard, 1973; Blaxter, 1988; Hollenberg & Wourms, 1994). These structures effectively increase the surface area of the developing embryo, in order to facilitate nutrient transfer and enhance respiratory surface area.…”

Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis

“…Literature sources: 1) Boehlert and Yoklavich, ; 2) Bürgin, ; 3) Cohen and Wourms, ; 4) Dobbs, ; 5) Fricke and Frahm, 1992; 6) Grove and Wourms, ; 7) Grove and Wourms, ; 8) Heemstra and Greenwood, ; 9) Hollenberg and Wourms, ; 10) Hollenberg and Wourms, ; 11) Igarishi, ; 12) Igarishi, ; 13) Knight et al, ; 14) Korsgaard, ; 15) Korsgaard, ; 16) Korsgaard, ; 17) Korsgaard, ; 18) Korsgaard and Anderson, ; 19) Kunz, ; 20) Lombardi and Wourms, ; 21) Lombardi and Wourms, ; 22) Macfarlane and Bowers, ; 23) Marsh‐Matthews, ; 24) Meisner and Burns, ; 25) Nakamura et al, ; 26) Nakamura et al, ; 27) Pires et al, ; 28) Pollux and Reznick, ; 29 Renesto and Stockar, ; 30) Reznick et al, ; 31) Reznick et al, ; 32) Schindler, ; 33) Schindler and De Vries, ; 34) Schindler and De Vries, ; 35) Shimizu et al, ; 36) Skov et al, ; 37) Skov et al, ; 38) Suarez, ; 39) Smith et al, ; 40) Takemura et al, ; 41) Thibault and Schultz, ; 42) Turner, ; 43) Turner, ; 44) Turner, ; 45) Turner, ; 46) Turner, ; 47) Turner, ; 48) Turner, ; 49) Turner, ; 50) Turner, ; 51) Veith, ; 52) Veith and Cornish, ; 53) Webb and Brett, ; 54) Webb and Brett, ; 55) Wen et al, ; 56) Wourms, ; 57) Wourms, ; 58) Wourms and Cohen, ; 59) Wourms and Lombardi, ; 60) Wourms et al, ; 61) Wourms et al, ; 62) Yo...…”

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

“…Among papers that have appeared in the Journal of Morphology are several "firsts" that warrant mention. These include the following: one of the Grove and Wourms, 1991 Follicular placenta Heterandria formosa (Poeciliidae) Grove and Wourms, 1994 Follicular placenta Heterandria formosa (Poeciliidae) Hollenberg and Wourms, 1994 Trophotaeniae, matrotrophy Goodeidae Jollie and Jollie, 1964a Pregnant ovarian follicle Lebistes reticulatus (Poeciliidae) Jollie and Jollie, 1964b Follicular placenta Lebistes reticulatus (Poeciliidae) Kokkala and Wourms, 1994 Trophotaenial placenta Goodeidae Knight et al, 1985 Follicular placenta, development Anableps (Anablepidae) Kwan et al, 2015 Follicular placenta Poeciliopsis (Poeciliidae) Lombardi and Wourms, 1985a Trophotaenial placenta Ameca splendens (Goodeidae) Lombardi and Wourms, 1985b* Trophotaenial placenta Ameca splendens (Goodeidae) Lombardi and Wourms, 1988 Placental function, matrotrophy Ameca splendens (Goodeidae) Meisner and Burns, 1997 Specializations for matrotrophy Hemiramphidae Mendoza, 1937 Trophotaenial resorption Goodeidae Mendoza, 1956 Trophotaeniae and ovary Hubbsina turneri (Goodeidae) Mendoza, 1958 Specializations for matrotrophy Goodea luitpoldii (Goodeidae) Mendoza, 1972 Trophotaeniae Xenotoca eiseni (Goodeidae) Parenti et al, 2010 Reproductive histology Tomeurus gracilis (Poeciliidae) Schindler and de Vries, 1986 Trophotaeniae Girardinichthys viviparus (Goodeidae) Schindler and de Vries, 1988a Specializations for matrotrophy Jenynsia lineata (Anablepidae) Turner, 1933a Viviparity Goodeidae Turner, 1936 Trophotaeniae Parabrotula dentiens (Brotulidae) Turner, 1937 Trophotaeniae Goodeidae Turner, 1938a Ovarian viviparity, matrotrophy Cymatogaster aggregatus (Embiotocidae) Turner, 1938b Specializations for matrotrophy Anableps anableps Turner, 1940a Specializations for matrotrophy Jenynsia (Anablepidae) Turner, 1940b Specializations for matrotrophy Anablepidae Turner, 1940c Specializations for matrotrophy Poeciliidae Turner, 1940d Specializations for matrot...…”