Cooption of the pteridine biosynthesis pathway underlies the diversification of embryonic colors in water striders

Abstract

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.

Ommochrome pathway genes kynurenine 3-hydroxylase and cardinal participate in eye pigmentation in Plutella xylostella

“…Although ommochromes are the only eye pigments thought to be involved in B. mori, the situation in DBM remains unexplored. The presence of pteridine pathway products in Drosophila have been reported to exhibit yellow and red pigmentation [30]. Putative homologs of Drosophila pteridine synthesis pathway genes, such as punch and purple, could also be found in DBM with BlastP.…”

Identification and age-dependence of pteridines in bed bugs (Cimex lectularius) and bat bugs (C. pipistrelli) using liquid chromatography-tandem mass spectrometry

“…www.nature.com/scientificreports www.nature.com/scientificreports/ pteridines was included in bed bug eyes. However, recently it was found that the pteridine biosynthesis pathway has been co-opted in the embryo to produce various pteridines in the antennae and legs 55 . This might explain non-significant difference of Pte between head cuticle and whole head capsule.…”

Genome-wide identification and gene-editing of pigment transporter genes in the swallowtail butterfly Papilio xuthus

“…Tyrosine-derived melanin metabolites are well known to play central roles in body color of all kinds of insects [ 4 ]. Tryptophan-derived ommochromes and guanine-derived pteridine have been verified to contribute to eye color in many insects independently (e.g., flour beetle Tribolium casstaneum ) [ 5 – 9 ], or jointly (e.g., fruit fly Drosophila melanogaster , cotton ballworm Helicoverpa armigera , water strider Limnogonus franciscanus ) [ 10 – 14 ]; they also play important roles in coloration of larval epidermis and wing etc. [ 15 , 16 ].…”