Abstract
The pea aphid (Acyrthosiphon pisum), a phloem-sucking insect, has undergone a rapid radiation together with the domestication and anthropogenic range expansion of several of its legume host plants. This insect species is a complex of at least 15 genetically different host races that can all develop on the universal host plant Vicia faba. However, each host race is specialized on a particular plant species, such as Medicago sativa, Trifolium pratense, or Pisum sativum, which makes it an attractive model insect to study ecological speciation. Previous work revealed that pea aphid host plants produce a specific phytohormone profile depending on the host plant – host race combination. Native aphid races induce lower defense hormone levels in their host plant than non-native pea aphid races. Whether these changes in hormone levels also lead to changes in other metabolites is still unknown. We used a mass spectrometry-based untargeted metabolomic approach to identify plant chemical compounds that vary among different host plant-host race combinations and might therefore, be involved in pea aphid host race specialization. We found significant differences among the metabolic fingerprints of the four legume species studied prior to aphid infestation, which correlated with aphid performance. After infestation, the metabolic profiles of M. sativa and T. pratense plants infested with their respective native aphid host race were consistently different from profiles after infestation with non-native host races and from uninfested control plants. The metabolic profiles of P. sativum plants infested with their native aphid host race were also different from plants infested with non-native host races, but not different from uninfested control plants. The compounds responsible for these differences were putatively identified as flavonoids, saponins, non-proteinogenic amino acids and peptides among others. As members of these compound classes are known for their activity against insects and aphids in particular, they may be responsible for the differential performance of host races on native vs. non-native host plants. We conclude that the untargeted metabolomic approach is suitable to identify candidate compounds involved in the specificity of pea aphid – host plant interactions.
Highlights
Insects are the most diverse group of eukaryotic species on earth (Stork, 1993), and herbivorous species constitute a major group of insects (Strong et al, 1984; Mitter et al, 1988)
principal component analyses (PCAs) plots showed a clear separation of all four plant species in both ionization modes (Figure 1)
To find out how plant metabolic profiles were modified after infestation by the various pea aphid host races, PCAs were performed based on the 5% of metabolomic features that changed most among plants infested with different pea aphid host races and uninfested control plants
Summary
Insects are the most diverse group of eukaryotic species on earth (Stork, 1993), and herbivorous species constitute a major group of insects (Strong et al, 1984; Mitter et al, 1988). Adaptation to multiple plant species can lead to the formation of host races or biotypes within a species of an insect herbivore and might play an important role in insect speciation. Various plants can react differently to a specific insect herbivore (Arimura et al, 2005; Wu and Baldwin, 2010; Hogenhout and Bos, 2011; SanchezArcos et al, 2016). Such differential plant responses can become apparent in changes in i.e., the plant metabolome (Jansen et al, 2009; Tzin et al, 2015)
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