Developmental biology of annual fishes. I. Stages in the normal development of Austrofundulus myersi Dahl

Abstract

Comparative studies of annual fish development reveal a unique developmental pattern in which embryogenesis occurs within a reaggregated mass of previously dispersed cells. The normal development of Austrofundulus myersi Dahl, a representative annual fish, has been divided into 46 stages. Cleavage during Stages 1–11 produces a typical teleost blastula. At Stage 12 (a flat, hollow blastula), the blastomeres segregate into two populations. One population composed of deep blastomeres will disperse as amoeboid cells, while the other, an hemispherical shell of outer blastomeres, flattens to form the enveloping cell layer. The cells of the enveloping cell layer become multinucleate and the layer functions as an extra‐embryonic membrane which is shed at hatching. When epiboly commences (Stage 14), the deep blastomeres come together as a consolidated mass and then migrate outward as individual amoeboid cells into the space formed between the expanding enveloping cell layer and periblast. When epiboly is concluded (Stage 19), the deep blastomeres have completely dispersed over the surface of the periblast. The dispersed phase usually lasts for several days. Prior to epiboly and during the dispersed phase, no germ ring, embryonic shield, or axial organization is present. The dispersed cells come together to form a definitive aggregate (Stage 22) by day 4. Embryogenesis within the reaggregated mass of previously, dispersed cells produces a typical teleost embryo. The definitive embryonic axis and solid neural keel appear by Stage 28 (day 10). Growth and organogenesis proceeds and hatching occurs at Stage 44. Development through Stage 44 requires 39–40 days in non‐diapausing eggs. Eggs of A. myersi may enter diapause at three distinct stages: (1) dispersed cell phase; (2) long somite embryo; and (3) late pre‐hatching.

A microinjection protocol for the generation of transgenic killifish (Species: Nothobranchius furzeri)

“…It has been shown in Nothobranchius species and other closely related cyprinodont fishes that there is no embryonic shield or axial organization during the dispersed phase ( Fig. 2D; Wourms, 1972;van Haarlem, 1983;Carter and Wourms, 1991). This is in contrast to other teleost fishes, such as Fundulus heteroclitus (Betchaku and Trinkaus, 1978), Oryzias latipes (Iwamatsu, 2004), and Danio rerio (Kimmel et al, 1995) in which blastomeres aggregate before and during epiboly to form the germ ring and embryonic shield.…”

Environmental influences on prolactin cell development in the cyprinodont fish, Cynolebias whitei

“…Eggs of the annual fish Cynolebias whitei were stored in moist peat for 3 months after spawning by which time they had developed to the prehatching diapause stage (stage 43, according to Wourms 1972). Hatching was induced by im mersion of the peat in unaerated fresh water (FW).…”

Characterization of partial Hox gene sequences in annual fish of the subfamily Cynolebiatinae (Cyprinodontiformes, Rivulidae)

“…The population survives dry seasons in the form of eggs buried in the mud. During the subsequent rainy season, the ponds refill, the eggs hatch and the larvae rapidly grow to sexual maturity and reproduce (Wourms, 1967(Wourms, , 1972a. The developmental pattern of annual killifish embryos is unique compared to other teleosts, and is characterized by dispersion and subsequent reaggregation of blastomeres and the occurrence of embryonic diapause.…”

“…Thus, embryos may enter diapause even under conditions considered optimal for development. Annual killifish embryos can undergo reversible developmental diapause at one or all of three well-defined morphological stages (diapause I, II and III) (Wourms, 1967(Wourms, , 1972aHand and Podrabsky, 2000). Studies in diapausing embryos of the annual killifish Austrofundulus limnaeus reveal that during diapause II protein synthesis is substantially diminished due to depressed metabolism.…”

“…To date, early development has been studied in some Austrolebias species (subfamily Cynolebiatinae, sensu Costa 1995;1998) and available data show that members of this genus display a dispersion-reaggregation process and that they undergo facultative arrest at diapause I and II and obligate arrest at diapause III (Wourms, 1972a;Carter and Wourms, 1991;Arezo et al, 2005).…”