The developmental biology of annual fishes. II. Naturally occurring dispersion and reaggregation of blastomeres during the development of annual fish eggs

Complete dispersion and subsequent reaggregation of pre‐embryonic blastomeres, features characteristic of annual fish development, are analyzed in Austrofundulus myersi Dahl. Cleavage produces a typical teleost blastoderm. During the mid‐blastula stages, blastomeres segregate into two populations; deep blastomeres which disperse, and outer blastomeres which form the enveloping cell layer. When epiboly of the enveloping cell layer and periblast commences, the deep blastomeres come together as a consolidated mass and then migrate outward as amoeboid cells. When epiboly has concluded, the deep blastomeres are completely dispersed. After a few days, these cells come together to form a definitive aggregate within which embryogenesis occurs. The reaggregation process was quantified in vivo by determining “coefficients of dispersion.” Amoeboid blastomeres were found to be: uniformly distributed when epiboly is completed (day 2); randomly distributed on day 3; and aggregated on day 4. The origin of the annual fish developmental pattern has involved the spatial and temporal dissociation of the processes of epiboly and embryogenesis. This has been accomplished by the interposition of the dispersion‐reaggregation phases. They may represent an exaggeration of the phases of incipient dispersion and localized aggregation which occur in most teleosts. The dispersion‐reaggregation process is considered to be a control mechanism operating on the principle of a requirement for “critical cell mass” as a necessary prelude to the primary events of embryogenesis. The survival value of the dispersed phase is discussed. Comparative studies of 43 closely related species have shown that the dispersion‐reaggregation pattern is present only in those cyprinodont fishes with annual life cycles. This group includes members of the following genera: Aphyosemion (annual species only); Austrofundulus; Cynolebias (including Cynopoecilus); Nothobranchius; Pterolebias; Rachovia; and Roloffia. Non‐annual cyprinodonts develop as do other fishes. Some Aphyosemion species have transitional developmental patterns.