Dissemination of Fusarium proliferatum by mealworm beetle Tenebrio molitor

PLoS One. 2018 Sep 27;13(9):e0204602. doi: 10.1371/journal.pone.0204602. eCollection 2018.

Abstract

Background: Plant pathogenic fungi of the genus Fusarium infect a wide array of crops and produce numerous health-threatening mycotoxins. Recently, we found that larvae of the common pest of stored products Tenebrio molitor preferably fed on grains colonized with Fusarium proliferatum. We draw the hypothesis that the increased attractiveness of infected grains for mealworms facilitates dispersal of the fungus. In this work we examined the dissemination of F. proliferatum and further Fusarium spp. by adults of T. molitor.

Results: Mealworm beetle Tenebrio molitor transmitted Fusarium species F. avenaceum, F. culmorum, F. poae, and F. proliferatum to wheat grains with varying efficiency. F. proliferatum was disseminated most efficiently: 20 days after feeding on Fusarium cultures, the beetles still transmitted F. proliferatum to most grains exposed to feeding. The transmission of F. culmorum gradually declined over time and the transmission of the other Fusarium spp. ceased completely 20 d after beetles feeding of fungal cultures. Propagules of F. proliferatum and F. culmorum were traceable in beetles' feces for 20 days while no colonies of F. poae and F. avenaceum were detectable after 5 days. Because F. proliferatum was transmitted by mealworms most efficiently, this species was further investigated. Mealworm beetles T. molitor preferred feeding on grains colonized with F. proliferatum as compared to uninfected grains. Male beetles infected with F. proliferatum transmitted the fungus by copulation.

Conclusions: Efficient dissemination of F. proliferatum by mealworm beetle together with the feeding preference of the beetle for grains colonized with F. proliferatum show that the chemical phenotype of the fungus responsible for the enhanced attractiveness of infected grains is subjected to positive selection. This indicates that adaptation of F. proliferatum to transmission by insects involved an alteration of insects' feeding preferences.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Copulation
  • DNA, Fungal / analysis
  • DNA, Fungal / genetics
  • Edible Grain / microbiology
  • Female
  • Food Microbiology
  • Food Preferences
  • Fusarium / genetics
  • Fusarium / growth & development
  • Fusarium / pathogenicity*
  • Insect Vectors / microbiology
  • Insect Vectors / physiology
  • Male
  • Microscopy, Electron, Scanning
  • Mycotoxins / analysis
  • Plant Diseases / microbiology
  • Tenebrio / microbiology*
  • Tenebrio / physiology

Substances

  • DNA, Fungal
  • Mycotoxins

Grants and funding

This research was partly supported by German Research Foundation (DFG, AL902/4-1 to B.A. www.dfg.de), the PLANTFOODSEC project of the European Union (FP7/2007-2013, No. 261752, https://cordis.europa.eu/project/rcn/100052_en.html) and China Postdoctoral Science Foundation (No. 2017M622304 support to ZG, www.chinapostdoctor.org.cn). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.