The evolution of an annual life cycle in killifish: adaptation to ephemeral aquatic environments through embryonic diapause.

An annual life cycle is characterized by growth, maturity, and reproduction condensed into a single, short season favourable to development, with production of embryos (seeds, cysts, or eggs) capable of surviving harsh conditions which juveniles or adults cannot tolerate. More typically associated with plants in desert environments, or temperate-zone insects exposed to freezing winters, the evolution of an annual life cycle in vertebrates is fairly novel. Killifish, small sexually dimorphic fishes in the Order Cyprinodontiformes, have adapted to seasonally ephemeral water bodies across much of Africa and South America through the independent evolution of an annual life history. These annual killifish produce hardy desiccation-resistant eggs that undergo diapause (developmental arrest) and remain buried in the soil for long periods when fish have perished due to the drying of their habitat. Killifish are found in aquatic habitats that span a continuum from permanent and stable to seasonal and variable, thus providing a useful system in which to piece together the evolutionary history of this life cycle using natural comparative variation. I first review adaptations for life in ephemeral aquatic environments in killifish, with particular emphasis on the evolution of embryonic diapause. I then bring together available evidence from a variety of approaches and provide a scenario for how this annual life cycle evolved. There are a number of features within Aplocheiloidei killifish including their inhabitation of marginal or edge aquatic habitat, their small size and rapid attainment of maturity, and egg properties that make them particularly well suited to the colonization of ephemeral waters.

Furness AI 《-》

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

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 direct-developing 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.

Furness AI ，Reznick DN ，Springer MS ，Meredith RW ... -  《-》

Embryonic developmental arrest in the annual killifish Austrolebias charrua: A proteomic approach to diapause III.

Chalar C ，Clivio G ，Montagne J ，Costábile A ，Lima A ，Papa NG ，Berois N ，Arezo MJ ... -  《PLoS One》

Adaptation in a variable environment: Phenotypic plasticity and bet-hedging during egg diapause and hatching in an annual killifish.

Two ways in which organisms adapt to variable environments are phenotypic plasticity and bet-hedging. Theory suggests that bet-hedging is expected to evolve in unpredictable environments for which reliable cues indicative of future conditions (or season length) are lacking. Alternatively, if reliable cues exist indicating future conditions, organisms will be under selection to produce the most appropriate phenotype -that is, adaptive phenotypic plasticity. Here, we experimentally test which of these modes of adaptation are at play in killifish that have evolved an annual life cycle. These fish persist in ephemeral pools that completely dry each season through the production of eggs that can remain in developmental arrest, or diapause, buried in the soil, until the following rainy season. Consistent with diversified bet-hedging (a risk spreading strategy), we demonstrate that the eggs of the annual killifish Nothobranchius furzeri exhibit variation at multiple levels-whether or not different stages of diapause are entered, for how long diapause is entered, and the timing of hatching-and this variation persists after controlling for both genetic and environmental sources of variation. However, we show that phenotypic plasticity is also present in that the proportion of eggs that enter diapause is influenced by environmental factors (temperature and light level) that vary seasonally. In nature there is typically a large parameter zone where environmental cues are somewhat correlated with seasonality, but not perfectly so, such that it may be advantageous to have a combination of both bet-hedging and plasticity.

Furness AI ，Lee K ，Reznick DN 《-》

Dispersion/reaggregation in early development of annual killifishes: Phylogenetic distribution and evolutionary significance of a unique feature.

Annual killifishes are members of the Aplocheiloidea and live in ephemeral habitats that desiccate regularly during the dry season and refill during the rainy season. Populations of these fishes survive the dry season by producing drought-resistant diapausing eggs that are buried in the substrate. When the pool refills during the rainy season the juveniles hatch, grow rapidly and reproduce until the pool desiccates again during the next dry season. The association with such unpredictable habitats has led to the evolution to a variety of developmental adaptations such as a dispersed/reaggregation phase of the deep blastomeres, three possible diapause stages, extreme tolerance to high salinity and anoxia, an efficient DNA repair system and an extremely short life span. Here, we review the course of the dispersed/reaggregation phase, its evolution and phylogenetic distribution and diversity within the Aplocheiloidea. The phenomenon of blastomere dispersion/reaggregation in these fishes was first described in the 1960s and 70s. Blastomeres of most teleost fishes segregate into three groups that give rise to the enveloping cell layer, the yolk syncytial layer and the deep blastomeres that will form the embryo itself. When epiboly commences, the deep blastomeres form a more or less coherent cell sheet with a so called embryonic shield at it marginal zone marking the area where gastrulation takes place. In annual killifishes, the deep blastomeres segregate when epiboly starts and disperse when epiboly commences. After epiboly has been completed, the deep blastomeres are randomly distributed and migrate all over the enveloping cell layer. After several days they start to reaggregate and form the actual embryo that starts gastrulation. The evolutionary origin and mechanism behind this peculiar developmental pathway have puzzled developmental biologists for almost 50 years. However, several of these annual killifishes (Nothobranchius furzeri, Austrofundulus limnaeus, Austrolebias charrua and Austrolebias bellottii) have become model organisms in studies on developmental physiology, aging and stress tolerance. This has led to the establishment of modern genetic techniques such as transgenesis and cell fate mapping that are now used to tackle questions about the origin and mechanisms behind the dispersal/reaggregation phase.

Naumann B ，Englert C 《-》