Hotter droughts alter resource allocation to chemical defenses in piñon pine

Heat and drought affect plant chemical defenses and thereby plant susceptibility to pests and pathogens. Monoterpenes are of particular importance for conifers as they play critical roles in defense against bark beetles. To date, work seeking to understand the impacts of heat and drought on monoterpenes has primarily focused on young potted seedlings, leaving it unclear how older age classes that are more vulnerable to bark beetles might respond to stress. Furthermore, we lack a clear picture of what carbon resources might be prioritized to support monoterpene synthesis under drought stress. To address this, we measured needle and woody tissue monoterpene concentrations and physiological variables simultaneously from mature piñon pines (Pinus edulis) from a unique temperature and drought manipulation field experiment. While heat had no effect on total monoterpene concentrations, trees under combined heat and drought stress exhibited ~ 85% and 35% increases in needle and woody tissue, respectively, over multiple years. Plant physiological variables like maximum photosynthesis each explained less than 10% of the variation in total monoterpenes for both tissue types while starch and glucose + fructose measured 1-month prior explained ~ 45% and 60% of the variation in woody tissue total monoterpene concentrations. Although total monoterpenes increased under combined stress, some key monoterpenes with known roles in bark beetle ecology decreased. These shifts may make trees more favorable for bark beetle attack rather than well defended, which one might conclude if only considering total monoterpene concentrations. Our results point to cumulative and synergistic effects of heat and drought that may reprioritize carbon allocation of specific non-structural carbohydrates toward defense.

Diversification and selection pattern of CYP6B genes in Japanese Papilio butterflies and their association with host plant spectra

Herbivorous insects are thought to have evolved counteradaptations to conquer chemical defenses in their host plants in a stepwise co-evolutionary process. Papilio butterflies use CYP6B gene family members to metabolize furanocoumarins in their Rutaceae or Apiaceae host plants. CYP6Bs have functionally diverged among Papilio species to be able to metabolite diverse types of furanocoumarins in their host plants. In this study, we examined the diversification and selection patterns of CYP6B among nine Papilio species in Japan (eight Rutaceae specialists and one Apiaceae specialist) and their association with host plant spectra and furanocoumarin profiles. We compared host plant spectrum of eight Rutaceae feeding Papilio species and also performed a furanocoumarin profiling of their host plants. In addition, we reconstructed CYP6B gene phylogeny and performed selection analysis based on the transcriptome data of those nine Papilio species. Among Rutaceae-feeding Papilio species, host plant spectrum differences were correlated with their furanocoumarin profiles. However, all tested Papilio species had similar duplicated sets of CYP6B, with no apparent lineage-specific or host plant-specific pattern of CYP6B diversification. Selection analysis showed a signature of positive selection on a CYP6B branch. The positively selected sites located at predicted substrate recognition sites and we also found that these CYP6B genes were observed only in Rutaceae-feeding species. These findings indicate that most CYP6B diversification occurred in ancestral species of these Papilio species, possibly in association with specific host plant chemical defenses and subsequent gene loss due to host specialization. These processes would have shaped the complex diversification patterns of the CYP6B gene family in Papilio butterflies. Our results also show potentially important CYP6B clades among Papilio species which likely to have diverged functions and associated with host plant phytochemicals in ancestral Papilio species.

The genetic architecture of a host shift: An adaptive walk protected an aphid and its endosymbiont from plant chemical defenses

Host shifts can lead to ecological speciation and the emergence of new pests and pathogens. However, the mutational events that facilitate the exploitation of novel hosts are poorly understood. Here, we characterize an adaptive walk underpinning the host shift of the aphid Myzus persicae to tobacco, including evolution of mechanisms that overcame tobacco chemical defenses. A series of mutational events added as many as 1.5 million nucleotides to the genome of the tobacco-adapted subspecies, M. p. nicotianae, and yielded profound increases in expression of an enzyme that efficiently detoxifies nicotine, both in aphid gut tissue and in the bacteriocytes housing the obligate aphid symbiont Buchnera aphidicola. This dual evolutionary solution overcame the challenge of preserving fitness of a mutualistic symbiosis during adaptation to a toxic novel host. Our results reveal the intricate processes by which genetic novelty can arise and drive the evolution of key innovations required for ecological adaptation.

Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)

Phytochemical diversity is thought to result from coevolutionary cycles as specialization in herbivores imposes diversifying selection on plant chemical defenses. Plants in the speciose genus Erysimum (Brassicaceae) produce both ancestral glucosinolates and evolutionarily novel cardenolides as defenses. Here we test macroevolutionary hypotheses on co-expression, co-regulation, and diversification of these potentially redundant defenses across this genus. We sequenced and assembled the genome of E. cheiranthoides and foliar transcriptomes of 47 additional Erysimum species to construct a phylogeny from 9868 orthologous genes, revealing several geographic clades but also high levels of gene discordance. Concentrations, inducibility, and diversity of the two defenses varied independently among species, with no evidence for trade-offs. Closely related, geographically co-occurring species shared similar cardenolide traits, but not glucosinolate traits, likely as a result of specific selective pressures acting on each defense. Ancestral and novel chemical defenses in Erysimum thus appear to provide complementary rather than redundant functions.

Does corn phenological stage alter the attractiveness of herbivore-induced plant volatiles to the predatory lacewing Chrysoperla externa (Hagen, 1861)?

Plant chemical defenses can affect herbivores directly or indirectly through the emission of herbivore-induced plant volatiles (HIPVs) that recruit natural enemies. Corn seedlings have high concentrations of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) that deter aphids, but as concentration decreases over the course of plant phenology, plants become less resistant. We investigated whether corn phenological stage influences the attractiveness of Rhopalosiphum maidis (Fitch, 1856) - infested corn seedling volatiles to the predatory lacewing Chrysoperla externa (Hagen, 1861). In olfactometer, lacewings preferentially oriented to volatiles from aphid-infested over those by uninfested corn seedlings at V6 or V7 stages, but did not discriminate between volatiles from uninfested and aphid-infested V5-stage seedlings. Greater numbers of aphids died in V5 corn seedlings relative to those in V6 and V7 seedlings. Our results indicate that the lack of discrimination of the predatory lacewing to HIPVs emitted by V5 corn seedlings is due to insufficient induction given that they were more resistant to R. maidis.

Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance

Insect herbivores are frequently reported to metabolize plant defense compounds, but the physiological and ecological consequences are not fully understood. It has rarely been studied whether such metabolism is genuinely beneficial to the insect, and whether there are any effects on higher trophic levels. Here, we manipulated the detoxification of plant defenses in the herbivorous pest diamondback moth (Plutella xylostella) to evaluate changes in fitness, and additionally examined the effects on a predatory lacewing (Chrysoperla carnea). Silencing glucosinolate sulfatase genes resulted in the systemic accumulation of toxic isothiocyanates in P. xylostella larvae, impairing larval development and adult reproduction. The predatory lacewing C. carnea, however, efficiently degraded ingested isothiocyanates via a general conjugation pathway, with no negative effects on survival, reproduction, or even prey preference. These results illustrate how plant defenses and their detoxification strongly influence herbivore fitness but might only subtly affect a third trophic level.