Convergent evolution of alternative developmental trajectories associated with diapause in African and South American killifish

Abstract

Annual killifish adapted to life in seasonally ephemeral water-bodies exhibit desiccation resistant eggs that can undergo diapause, a period of developmental arrest, enabling them to traverse the otherwise inhospitable dry season. Environmental cues that potentially indicate the season can govern whether eggs enter a stage of diapause mid-way through development or skip this diapause and instead undergo direct development. We report, based on construction of a supermatrix phylogenetic tree of the order Cyprinodontiformes and a battery of comparative analyses, that the ability to produce diapause eggs evolved independently at least six times within African and South American killifish. We then show in species representative of these lineages that embryos entering diapause display significant reduction in development of the cranial region and circulatory system relative to directdeveloping embryos. This divergence along alternative developmental pathways begins mid-way through development, well before diapause is entered, during a period of purported maximum developmental constraint (the phylotypic period). Finally, we show that entering diapause is accompanied by a dramatic reduction in metabolic rate and concomitant increase in long-term embryo survival. Morphological divergence during the phylotypic period thus allows embryos undergoing diapause to conserve energy by shunting resources away from energetically costly organs thereby increasing survival chances in an environment that necessitates remaining dormant, buried in the soil and surrounded by an eggshell for much of the year. Our results indicate that adaptation to seasonal aquatic environments in annual killifish imposes strong selection during the embryo stage leading to marked diversification during this otherwise conserved period of vertebrate development.

The origin and biogeographic diversification of fishes in the family Poeciliidae

“…The minimum age is based on undescribed poeciliid fossils that are known from the Lumbrera Formation in Argentina [51]. As noted by Furness et al [29], geological data suggest an upper Ypresian-lower Lutetian age for the Faja Verde of the Lumbrera Formation. However, the minimum age in only 39.9 Ma based on U/Pb zircon dating of a tuff bed that overlies this formation [51].…”

Fatty acid synthase 2 contributes to diapause preparation in a beetle by regulating lipid accumulation and stress tolerance genes expression

“…One way ANOVA followed by Turkey’s HSD multiple comparison tests was used to compare the expression of FAS2 in different tissues and on different days ( P  < 0.05). Log-rank (Mantel-Cox) test in Kaplan-Meier survival analysis was used to show the difference in the duration of diapause preparation between dsGFP and dsFAS2 groups49. The significance of differences between experimental groups in remaining experiments was assessed using Independent-Samples t Test (* P  < 0.05, ** P  < 0.01).…”

Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish

“…Entrance into diapause II is an alternative developmental pathway in annual killifishes that can be controlled by maternal inputs during oogenesis (61,145). However, the embryonic incubation environment can alter this initial programming, and, for example, a 5°C increase in incubation temperature can force 100% of the embryos to bypass diapause II and develop directly to diapause III (145).…”