title: Symbiont-supplemented maternal investment underpinning host's ecological adaptation.
abstract: Maternal investment for offspring's growth and survival is widespread among diverse organisms. Vertical symbiont transmission via maternal passage is also pivotal for offspring's growth and survival in many organisms. Hence, it is expected that vertical symbiont transmission may coevolve with various organismal traits concerning maternal investment in offspring. Here we report a novel phenotypic syndrome entailing morphological, histological, behavioral, and ecological specializations for maternal investment and vertical symbiont transmission in stinkbugs of the family Urostylididae. Adult females develop huge ovaries exaggerated for polysaccharide excretion, possess novel ovipositor-associated organs for vertical transmission of a bacterial symbiont ("Candidatus Tachikawaea gelatinosa"), and lay eggs covered with voluminous symbiont-supplemented jelly. Newborns hatch in midwinter, feed solely on the jelly, acquire the symbiont, and grow during winter. In spring, the insects start feeding on plant sap, wherein the symbiont localizes to a specialized midgut region and supplies essential amino acids deficient in the host's diet. The reduced symbiont genome and host-symbiont cospeciation indicate their obligate association over evolutionary time. Experimental deprivation of the jelly results in nymphal mortality, whereas restoration of the jelly leads to recovered nymphal growth, confirming that the jelly supports nymphal growth in winter. Chemical analyses demonstrate that the galactan-based jelly contains a sufficient quantity of amino acids to sustain nymphal growth to the third instar. The versatile biological roles of the symbiont-containing egg-covering jelly highlight intricate evolutionary interactions between maternal resource investment and vertical symbiont transmission, which are commonly important for offspring's growth, survival, and ecological adaptation.
authors.affiliation: National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan; Department of General Systems Studies, Graduate School of Arts and Science, the University of Tokyo, Tokyo 153-8902, Japan.
authors.forename: Nahomi
authors.initials: N
authors.lastname: Kaiwa
authors.affiliation: National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan.
authors.forename: Takahiro
authors.initials: T
authors.lastname: Hosokawa
authors.affiliation: Department of Liberal Arts, the Open University of Japan, Chiba 261-8586, Japan.
authors.forename: Naruo
authors.initials: N
authors.lastname: Nikoh
authors.affiliation: National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan.
authors.forename: Masahiko
authors.initials: M
authors.lastname: Tanahashi
authors.affiliation: National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan.
authors.forename: Minoru
authors.initials: M
authors.lastname: Moriyama
authors.affiliation: National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan.
authors.forename: Xian-Ying
authors.initials: XY
authors.lastname: Meng
authors.affiliation: National Institute for Basic Biology, Okazaki 444-8585, Japan.
authors.forename: Taro
authors.initials: T
authors.lastname: Maeda
authors.affiliation: National Institute for Basic Biology, Okazaki 444-8585, Japan.
authors.forename: Katsushi
authors.initials: K
authors.lastname: Yamaguchi
authors.affiliation: National Institute for Basic Biology, Okazaki 444-8585, Japan.
authors.forename: Shuji
authors.initials: S
authors.lastname: Shigenobu
authors.affiliation: Department of General Systems Studies, Graduate School of Arts and Science, the University of Tokyo, Tokyo 153-8902, Japan.
authors.forename: Motomi
authors.initials: M
authors.lastname: Ito
authors.affiliation: National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan. Electronic address: t-fukatsu@aist.go.jp.
authors.forename: Takema
authors.initials: T
authors.lastname: Fukatsu
mesh_terms: D000818:Animals; D005260:Female; D006801:Humans; D007313:Insecta / Q000382:microbiology* / Q000502:physiology*; D010063:Ovum / Q000382:microbiology*; D012098:Reproduction / Q000502:physiology; D012621:Seasons; D013559:Symbiosis