Diverse strategies for vertical symbiont transmission among subsocial stinkbugs

PLoS One. 2013 May 31;8(5):e65081. doi: 10.1371/journal.pone.0065081. Print 2013.

Abstract

Sociality may affect symbiosis and vice versa. Many plant-sucking stinkbugs harbor mutualistic bacterial symbionts in the midgut. In the superfamily Pentatomoidea, adult females excrete symbiont-containing materials from the anus, which their offspring ingest orally and establish vertical symbiont transmission. In many stinkbug families whose members are mostly non-social, females excrete symbiont-containing materials onto/beside eggs upon oviposition. However, exceptional cases have been reported from two subsocial species representing the closely related families Cydnidae and Parastrachiidae, wherein females remain nearby eggs for maternal care after oviposition, and provide their offspring with symbiont-containing secretions at later stages, either just before or after hatching. These observations suggested that sociality of the host stinkbugs may be correlated with their symbiont transmission strategies. However, we found that cydnid stinkbugs of the genus Adomerus, which are associated with gammaproteobacterial gut symbionts and exhibit elaborate maternal care over their offspring, smear symbiont-containing secretions onto eggs upon oviposition as many non-social stinkbugs do. Surface sterilization of the eggs resulted in aposymbiotic insects of slower growth, smaller size and abnormal body coloration, indicating vertical symbiont transmission via egg surface contamination and presumable beneficial nature of the symbiosis. The Adomerus symbionts exhibited AT-biased nucleotide compositions, accelerated molecular evolutionary rates and reduced genome size, while these degenerative genomic traits were less severe than those in the symbiont of a subsocial parastrachiid. These results suggest that not only sociality but also other ecological and evolutionary aspects of the host stinkbugs, including the host-symbiont co-evolutionary history, may have substantially affected their symbiont transmission strategies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Evolution, Molecular
  • Female
  • Gammaproteobacteria / physiology
  • Genes, Insect
  • Genetic Fitness
  • Genome Size
  • Heteroptera / classification
  • Heteroptera / microbiology*
  • Heteroptera / physiology*
  • Molecular Sequence Data
  • Oviposition
  • Ovum / ultrastructure
  • Phenotype
  • Symbiosis*

Associated data

  • GENBANK/AB781081
  • GENBANK/AB781082
  • GENBANK/AB781083
  • GENBANK/AB781084
  • GENBANK/AB781085
  • GENBANK/AB781086
  • GENBANK/AB781087
  • GENBANK/AB781088

Grants and funding

This study was supported by the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry (BRAIN), Grant-in-Aid for JSPS Fellows (236923), and Grant-in-Aid for Scientific Research (B) (21370011) from the Japan Society of the Promotion of Science. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.