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

Abstract

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.

Divergent karyotypes of the annual killifish genus Nothobranchius (Cyprinodontiformes, Nothobranchiidae)

“…They inhabit temporary pools that dry out during the dry season and have specific adaptations for extreme environments. Annual fishes are characterised by specific life history traits of extremely short lifespan and diapause in embryonic development (Furness 2015, Nagy 2015). Their unique biology makes them a model taxon with which to investigate aging, embryonic development, ecology, and natural selection (Cellerino et al 2015).…”

Manipulating waterbody hydroperiod affects movement behaviour and occupancy dynamics in an amphibian

“…rapid early growth rate, early maturity, a short lifespan and high fecundity; Blazek, Polacik, & Reichard, 2013;Furness, 2016). rapid early growth rate, early maturity, a short lifespan and high fecundity; Blazek, Polacik, & Reichard, 2013;Furness, 2016).…”

Non-model model organisms

“…The first phase takes place during the rainy season and consists of a compressed lifecycle (~40 days from embryos to embryos of the next generation), in which the turquoise killifish grows fast, reproduces fast, and, likely as a consequence of these constraints, also ages fast. The second phase takes place during the dry season and consists of a state of suspended development called diapause, which enables embryos laid during the rainy season to survive through the drought—lasting months or even years [299]. Notably, to hedge the risk, some embryos naturally skip diapause and exhibit a continuous lifecycle [300] (C-KH and AB, unpublished data).…”