The Evolution of Chorionic Ultrastructure, Delayed Hatching, and Desiccation Tolerance in Annual Killifishes
Open AccessFishes are the most diverse vertebrates on the planet with over 33,000 species. They have colonized every major body of water from caves, toxic environments, the deepest oceans, to temporary pools. Some species in these extreme environments belong to a group of fishes known as killifishes (Cyprinodontiformes: Aplocheiloidei). Often popular pets, killifishes contain over 700 species. These small, colorful fish can be found in habitats inhospitable to all other species of fishes. Killifishes inhabit seasonal pools that dry up, resulting in the death of all adults in the pond. The population is able to survive dry periods as embryos with specialized egg envelopes, unique diapause stages, and desiccation tolerance. We use an integrative approach of scanning electron microscopy (SEM), comparative transcriptomics, and phylogenomics to investigate the evolutionary patterns and genetic processes that led to the evolution of this remarkable trait. We present new data and inferences on egg structure of multiple lineages, hundreds of candidate genes involved diapause and desiccation tolerance, as well as a robust phylogenomic hypothesis for Aplocheiloidei. Specifically, we document egg structure in 52 aplocheiloid species for the first time with SEM. We examine the convergence/parallelism of egg structural characters in a phylogenetic framework. In addition, we use whole transcriptomes to study the evolution of annualism in Aplocheiloidei. Specifically, we find evidence of transcriptional convergence in dormancy across metazoa after identifying significantly differentially expressed transcripts during diapause in the annual killifish Nematolebias whitei. We also identify differentially expressed genes during delayed hatching and desiccation tolerance in the non-annual killifish Aplocheilus lineatus providing evidence that delayed hatching is not a form of dormancy. Lastly, we construct a species tree of Aplocheiloidei with 8,000 orthologous loci and verify the convergent/parallel evolution of annualism with “big data.”
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