Cooption of the pteridine biosynthesis pathway underlies the diversification of embryonic colors in water striders
Proceedings of the National Academy of Sciences.
Understanding how existing genomic content can be reused to generate new phenotypes is important for understanding how species diversify. Here, we address this question by studying the origin of a phenotype consisting of bright coloration in the embryos of water striders. We found that the pteridine biosynthesis pathway, originally active in the eyes, has been coopted in the embryo to produce various colors in the antennae and legs. The coopted pathway remained stable for over 200 million years, yet resulted in a striking diversification of colors and color patterns during the evolution of water striders. This work demonstrates how the activation of a complete pathway in new developmental contexts can drive the evolution of novelty and fuel species diversification.Naturalists have been fascinated for centuries by animal colors and color patterns. While widely studied at the adult stage, we know little about color patterns in the embryo. Here, we study a trait consisting of coloration that is specific to the embryo and absent from postembryonic stages in water striders (Gerromorpha). By combining developmental genetics with chemical and phylogenetic analyses across a broad sample of species, we uncovered the mechanisms underlying the emergence and diversification of embryonic colors in this group of insects. We show that the pteridine biosynthesis pathway, which ancestrally produces red pigment in the eyes, has been recruited during embryogenesis in various extraocular tissues including antennae and legs. In addition, we discovered that this cooption is common to all water striders and initially resulted in the production of yellow extraocular color. Subsequently, 6 lineages evolved bright red color and 2 lineages lost the color independently. Despite the high diversity in colors and color patterns, we show that the underlying biosynthesis pathway remained stable throughout the 200 million years of Gerromorpha evolutionary time. Finally, we identified erythropterin and xanthopterin as the pigments responsible for these colors in the embryo of various species. These findings demonstrate how traits can emerge through the activation of a biosynthesis pathway in new developmental contexts.