Ionome and elemental transport kinetics shaped by parallel evolution in threespine stickleback

Summary Marine stickleback fish have colonized and adapted to innumerable streams and lakes formed since the last ice age, providing an exceptional opportunity to characterize genomic mechanisms underlying repeated ecological adaptation in nature. Here we develop a high quality reference genome assembly for threespine sticklebacks. By sequencing the genomes of 20 additional individuals from a global set of marine and freshwater populations, we identify a genome-wide set of loci that are consistently associated with marine-freshwater divergence. Our results suggest that reuse of globally-shared standing genetic variation, including chromosomal inversions, plays an important role in repeated evolution of distinct marine and freshwater sticklebacks, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. Both coding and regulatory changes occur in the set of loci underlying marine-freshwater evolution, with regulatory changes likely predominating in this classic example of repeated adaptive evolution in nature.

Major phenotypic changes evolve in parallel in nature by molecular mechanisms that are largely unknown. Here, we use positional cloning methods to identify the major chromosome locus controlling armor plate patterning in wild threespine sticklebacks. Mapping, sequencing, and transgenic studies show that the Ectodysplasin (EDA) signaling pathway plays a key role in evolutionary change in natural populations and that parallel evolution of stickleback low-plated phenotypes at most freshwater locations around the world has occurred by repeated selection of Eda alleles derived from an ancestral low-plated haplotype that first appeared more than two million years ago. Members of this clade of low-plated alleles are present at low frequencies in marine fish, which suggests that standing genetic variation can provide a molecular basis for rapid, parallel evolution of dramatic phenotypic change in nature.

The ionome is defined as the mineral nutrient and trace element composition of an organism and represents the inorganic component of cellular and organismal systems. Ionomics, the study of the ionome, involves the quantitative and simultaneous measurement of the elemental composition of living organisms and changes in this composition in response to physiological stimuli, developmental state, and genetic modifications. Ionomics requires the application of high-throughput elemental analysis technologies and their integration with both bioinformatic and genetic tools. Ionomics has the ability to capture information about the functional state of an organism under different conditions, driven by genetic and developmental differences and by biotic and abiotic factors. The relatively high throughput and low cost of ionomic analysis means that it has the potential to provide a powerful approach to not only the functional analysis of the genes and gene networks that directly control the ionome, but also to the more extended gene networks that control developmental and physiological processes that affect the ionome indirectly. In this review we describe the analytical and bioinformatics aspects of ionomics, as well as its application as a functional genomics tool.