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Open Access Publications from the University of California

The Evolution of an Annual Life Cycle in Killifish: Adaptation to Seasonally Ephemeral Aquatic Habitat Across Two Continents

  • Author(s): Furness, Andrew Ian
  • Advisor(s): Reznick, David N
  • et al.

Across the tree of life there is a great deal of variation in life cycles, life histories, and reproductive strategies. Explaining this diversity in terms of selective pressures and ecological conditions is one of the grand challenges within the field of evolutionary biology. Studying the extremes, or the ends on this spectrum of life cycle variation, can provide a fuller understanding of how different strategies evolve and allow for population persistence. My dissertation research is united by two themes - the evolution of reproductive mode, and adaptation to ephemeral and variable environments. Killifish, small oviparous fishes within the Order Cyprinodontiformes, have evolved an annual life cycle and are adapted to life in seasonally ephemeral aquatic habitats. The most prominent adaptation of these short-lived killifish are embryos capable of undergoing diapause (halting development) at one or more of three different stages during embryology and remaining buried in the soil for much of the year. In this dissertation I combine a phylogenetic, comparative, and experimental approach to study the evolution of this life cycle and how through embryonic diapause these fish have adapted to ephemeral and variable aquatic habitat.

In chapter one I demonstrate convergent evolution of alternative developmental trajectories associated with diapause in African and South American killifish species. Adaptation to seasonal aquatic environments in annual killifish imposes strong selection during the embryo stage leading to marked diversification during a mid-embryogenesis period that is otherwise highly conserved during vertebrate development. In chapter two, I demonstrate that the embryos of an annual killifish Nothboranchius furzeri exhibit a combination of phenotypic plasticity and bet-hedging (a risk spreading strategy). Specifically, whether embryos enter diapause is influenced by environmental factors (temperature and light level) that vary seasonally but also exhibits a measure of intrinsic variability, even after controlling genetics and environment. In chapter three, I compile available evidence from the literature and my own comparative experiments and provide a plausible scenario for how an annual life cycle evolved through intermediate steps. 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 embedded in a phylogenetic context.

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