Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou, China.
Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, China.
Mol Biol Evol. 2022 Mar 2;39(3). doi: 10.1093/molbev/msac042.
Insects have evolved numerous adaptations and colonized diverse terrestrial environments. Several polyneopterans, including dictyopterans (cockroaches and mantids) and locusts, have developed oothecae, but little is known about the molecular mechanism, physiological function, and evolutionary significance of ootheca formation. Here, we demonstrate that the cockroach asymmetric colleterial glands produce vitellogenins, proline-rich protein, and glycine-rich protein as major ootheca structural proteins (OSPs) that undergo sclerotization and melanization for ootheca formation through the cooperative protocatechuic acid pathway and dopachrome and dopaminechrome subpathway. Functionally, OSP sclerotization and melanization prevent eggs from losing water at warm and dry conditions, and thus effectively maintain embryo viability. Dictyopterans and locusts convergently evolved vitellogenins, apolipoprotein D, and laminins as OSPs, whereas within Dictyoptera, cockroaches and mantids independently developed glycine-rich protein and fibroins as OSPs. Highlighting the ecological-evolutionary importance, convergent ootheca formation represents a successful reproductive strategy in Polyneoptera that promoted the radiation and establishment of cockroaches, mantids, and locusts.
昆虫进化出了许多适应性，并在多样化的陆地环境中得以生存。一些多足类昆虫，包括直翅目昆虫（蟑螂和螳螂）和蝗虫，已经发展出了卵鞘，但对于卵鞘形成的分子机制、生理功能和进化意义知之甚少。在这里，我们证明蟑螂不对称的收集器腺产生卵黄蛋白、富含脯氨酸的蛋白和富含甘氨酸的蛋白，作为卵鞘结构蛋白（OSP）的主要成分，通过合作的原儿茶酸途径和多巴醌和多巴胺醌亚途径经历硬化和黑化，从而形成卵鞘。在功能上，OSP 的硬化和黑化可以防止卵在温暖和干燥的条件下失水，从而有效地维持胚胎的活力。直翅目昆虫和蝗虫趋同进化出卵黄蛋白、载脂蛋白 D 和层粘连蛋白作为 OSP，而在直翅目昆虫中，蟑螂和螳螂则独立地将富含甘氨酸的蛋白和丝心蛋白作为 OSP 进化出来。这突出了生态进化的重要性，趋同的卵鞘形成代表了多足类昆虫的一种成功的繁殖策略，促进了蟑螂、螳螂和蝗虫的辐射和建立。
