Cascading effects of host plant inbreeding on the larval growth, muscle molecular composition, and flight capacity of an adult herbivorous insect

Abstract

Summary 1.A primary function of adult winged insects is dispersal. Limiting larval dietary intake (partial starvation) has been shown to affect the flight muscle metabolism of adult moths reared on artificial diet, but a more ecologically relevant question is whether natural variation in host plant quality can lead to differences in the flight capacity of adult insects. 2. Recent studies have shown that inbreeding compromises plant antiherbivore defences. We created inbred and outbred progeny from locally collected horsenettle (Solanum carolinense L.) and examined how host plant inbreeding affects the growth, development, and flight muscle physiology of tobacco hornworm (Manduca sexta L.), a specialist herbivore on Solanaceae. We tested the hypothesis that within population genetic variation in host plant quality, resulting from inbreeding, can create significant changes to the larval development and flight physiology of an adult insect. 3. We found that Manduca larvae reared on inbred horsenettle plants grew faster and developed into larger pupae compared to larvae reared on outbred plants. Adult flight metabolic rate was greater in adults reared on inbred plants compared to outbred plants, and this elevation was independent of body mass when we excluded one plant family that produced small, low metabolic rate moths regardless of breeding regime. Differences in mass-specific flight metabolism were associated with changes in alternative splicing of troponin t, a flight muscle protein that regulates muscle contraction. 4. These results show that host plant inbreeding can create effects that cascade through larval and pupal development to affect dispersal-related traits of the adult stage. Hence, plant inbreeding may also impact herbivore population dynamics, particularly their ability to spread away from, and possibly into, isolated patches of inbred plants creating increased herbivore pressure on these plant populations. More generally, our findings reveal that changes in population biology at one trophic level can affect the metabolic physiology and flight capacity of an animal at a higher trophic level.

Leaf trichomes affect caterpillar feeding in an instar-specific manner

“…We recently documented post-ingestion effects of such trichomes on caterpillars, reporting the gut peritrophic matrix was punctured and ripped by trichomes passing through the gut. Given the importance of the peritrophic matrix to nutrient uptake and protection against pathogens [18], it is not surprising that larvae also grew more slowly when feeding on plants with more trichomes [19] or on artificial diet containing trichomes compared to control diet [3]. …”

Inbreeding compromises host plant defense gene expression and improves herbivore survival

“…We showed that larvae reared on inbred plants grew faster and developed into larger pupae compared to larvae reared on outbred plants. 15 Furthermore, adult mass-specific flight metabolic rates were higher in adults that were reared on inbred plants, and differences in flight metabolic rates were also associated with changes to the alternative splicing profiles of Troponin t, a flight muscle protein that regulates muscle contraction. 16,15 Our results show that feeding on inbred host plants produces changes in the insect that cascade through larval and pupal development to affect adult flight muscle protein composition and flight muscle power output-indicating that M. sexta larvae reared on inbred horsenettle plants acquired nutrients at a faster rate, and/or ingested lower levels of plant produced toxins than larvae reared on outbred plants.…”

“…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.…”

“…21 Adults were used for our flight metabolism and flight muscle gene expression experiments. 15 To determine if host plant inbreeding affected the vitality of the insects, we compared the survival ratios (two proportion z test) of M. sexta larvae that were reared on inbred vs. outbred host plants. We found that the survival ratios of inbred reared larvae were significantly higher than those reared on outbred plants (Fig.…”

“…This result provides evidence that host plant inbreeding impacts insect herbivore survival, and corroborates our earlier findings that plant inbreeding affects M. sexta growth and physiological performance. 15 To examine if insect survival differences were related to variation in expression of host plant defense genes, we quantified the expression levels of two genes in the JA pathway: LIPOXYGE-NEASE-D (LoxD) and 12-OXOPHYTODIENOATE REDUC-TASE-3 (OPR3)-both genes are upregulated in response to herbivore damage. 22 Third instar M. sexta larvae were allowed to feed on their host plants for »24 hours, after which leaf material was collected from damaged plants and control (undamaged) plants from maternal family B3.…”