Kaiwa Nahomi, Hosokawa Takahiro, Nikoh Naruo, Tanahashi Masahiko, Moriyama Minoru, Meng Xian-Ying, Maeda Taro, Yamaguchi Katsushi, Shigenobu Shuji, Ito Motomi, Fukatsu Takema
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.
National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan.
Curr Biol. 2014 Oct 20;24(20):2465-70. doi: 10.1016/j.cub.2014.08.065. Epub 2014 Sep 25.
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.
母体对后代生长和生存的投入在各种生物中广泛存在。通过母体传递进行垂直共生体传播对于许多生物后代的生长和生存也至关重要。因此，可以预期垂直共生体传播可能会与母体对后代投入的各种生物体特征共同进化。在此，我们报告了一种新的表型综合征，该综合征涉及扁蝽科昆虫在母体投入和垂直共生体传播方面的形态学、组织学、行为学和生态学特化。成年雌性扁蝽发育出因多糖分泌而过度膨大的巨大卵巢，拥有用于垂直传播一种细菌共生体（“暂定立川胶状菌”）的与产卵器相关的新器官，并产下覆盖着大量补充了共生体的果冻状物质的卵。新生儿在仲冬孵化，仅以这种果冻状物质为食，获取共生体，并在冬季生长。在春季，这些昆虫开始取食植物汁液，此时共生体定位于一个特化的中肠区域，并提供宿主食物中缺乏的必需氨基酸。共生体基因组的缩减以及宿主 - 共生体的共同物种形成表明它们在进化时间上存在专性关联。实验性剥夺果冻状物质会导致若虫死亡，而恢复提供果冻状物质则会使若虫生长恢复，这证实了果冻状物质支持若虫在冬季生长。化学分析表明，基于半乳聚糖的果冻状物质含有足够数量的氨基酸，能够维持若虫生长至三龄期。含有共生体的卵覆盖果冻状物质的多种生物学作用突出了母体资源投入与垂直共生体传播之间复杂的进化相互作用，这对于后代的生长、生存和生态适应通常都很重要。
