Inbreeding in horsenettle (Solanum carolinense) alters night-time volatile emissions that guide oviposition byManduca sextamoths

Abstract

Plant volatiles serve as key foraging and oviposition cues for insect herbivores as well as their natural enemies, but little is known about how genetic variation within plant populations influences volatile-mediated interactions among plants and insects. Here, we explore how inbred and outbred plants from three maternal families of the native weed horsenettle (Solanum carolinense) vary in the emission of volatile organic compounds during the dark phase of the photoperiod, and the effects of this variation on the oviposition preferences of Manduca sexta moths, whose larvae are specialist herbivores of Solanaceae. Compared with inbred plants, outbred plants consistently released more total volatiles at night and more individual compounds-including some previously reported to repel moths and attract predators. Female moths overwhelmingly chose to lay eggs on inbred (versus outbred) plants, and this preference persisted when olfactory cues were presented in the absence of visual and contact cues. These results are consistent with our previous findings that inbred plants recruit more herbivores and suffer greater herbivory under field conditions. Furthermore, they suggest that constitutive volatiles released during the dark portion of the photoperiod can convey accurate information about plant defence status (and/or other aspects of host plant quality) to foraging herbivores.

Preference for outbred host plants and positive effects of inbreeding on egg survival in a specialist herbivore

“…We also predict that outbred plants attract parasitoids and predators more efficiently because they are suspected to emit more volatile compounds than the inbred plants [7,13]. Lastly, we expect that parasitoids and predators favour outbred herbivore eggs because they are of higher quality than inbred eggs.…”

“…Theory predicts that female insects deposit their eggs on a site that maximizes the performance of the offspring [18][19][20], although this does not always hold true in practice [21][22][23]. Accordingly, inbred plants, which were of higher quality to the larvae, were favoured over outbred plants for oviposition by the adult hawk moths (Manduca sexta) [13]. Once the eggs have been laid, plants can react against the eggs directly by hypersensitive and toxic responses and indirectly by releasing volatile chemical compounds or inducing changes in leaf surface chemicals that attract natural enemies of the insect eggs [17,24,25].…”

“…The traits that are central in the nonfeeding life-history stages of the interaction, such as the eggs and in some species the adults, can be equally important for the antagonistic interaction as those in the feeding stage [12]. These traits can also be modified by inbreeding [13], and thereby further complicate the effects of inbreeding on plant-herbivore interactions. Plant quality and chemical cues direct the oviposition of adult insects [14][15][16] and they can alter plant apparency or attractiveness to the herbivore and lead to avoidance of egg deposition [17].…”

Inbreeding compromises host plant defense gene expression and improves herbivore survival

“…This hypothesis is supported by a preliminary microarray study comparing the response of inbred and outbred herbivore damaged horsenettle genets-which revealed that the jasmonic acid (JA) pathway (a key biochemical pathway employed to defend against chewing herbivores such as M. sexta) was compromised due to inbreeding. 18 Results from Kariyat et al 18 suggest that variation in the gene expression levels of plant produced defense compounds, due to inbreeding, could be responsible for changes to growth, 15 oviposition, 14 and flight capacity 15 of M. sexta. However, no studies have directly compared relative expression levels (RA) of genes in the JA pathway between inbred and outbred horsenettle plants, or linked differences in defense gene RAs, due to inbreeding, to changes in herbivore performance.…”

“…26,15 It also might explain why inbred plants are preferred in choice experiments by both M. sexta larvae 12,10 and ovipositing females. 14 Inbreeding in horsenettle causes significant reductions in the plant's induced defense responses 18,23 and resistance to herbivory. [8][9][10] We used only minimal manipulation, a single generation of host plant inbreeding, to produce differences (inbred vs. outbred) in the host plants of an indigenous plant-insect system (horsenettle-tobacco hornworm).…”