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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 spectrometrybased
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.