Symbiont-supplemented maternal investment underpinning host's ecological adaptation

Nahomi Kaiwa, Takahiro Hosokawa, Naruo Nikoh, Masahiko Tanahashi, Minoru Moriyama, Xian Ying Meng, Taro Maeda, Katsushi Yamaguchi, Shuji Shigenobu, Motomi Ito, Takema Fukatsu

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41 Citations (Scopus)

Abstract

Maternal investment for offspring's growth and survival is widespread among diverse organisms [1-3]. Vertical symbiont transmission via maternal passage is also pivotal for offspring's growth and survival in many organisms [4-6]. 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 [7-9]. 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 specializedmidgut 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 eggcovering 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.

Original languageEnglish
Pages (from-to)2465-2470
Number of pages6
JournalCurrent Biology
Volume24
Issue number20
DOIs
Publication statusPublished - Oct 20 2014
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

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    Kaiwa, N., Hosokawa, T., Nikoh, N., Tanahashi, M., Moriyama, M., Meng, X. Y., Maeda, T., Yamaguchi, K., Shigenobu, S., Ito, M., & Fukatsu, T. (2014). Symbiont-supplemented maternal investment underpinning host's ecological adaptation. Current Biology, 24(20), 2465-2470. https://doi.org/10.1016/j.cub.2014.08.065