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

Abstract

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. 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. 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. 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.