Interrelationships Among Inbreeding, Herbivory, and Disease on Reproduction in a Wild Gourd

Abstract

Because inbreeding, herbivory, and disease are common in plants and their separate impacts on fitness are well documented, investigators have begun to examine the consequences of inbreeding on plant-herbivore and plant-pathogen interactions. In this study, we examined the interrelationships among inbreeding, herbivory, and disease on reproductive output through both male (pollen production and pollen performance) and female (fruit and seed production and seed germination) functions. Inbred (selfed) and outbred plants from five families of a wild gourd (Cucurbita pepo ssp. texana) were grown in five 0.2-ha randomized blocks in an experimental garden. Half of the inbred and half of the outbred plants were sprayed weekly with a contact pesticide to control herbivores. The other half of the plants served as the controls (no-spray treatment). The spray treatment significantly reduced damage by cucumber beetles and aphid infestation levels, the two primary herbivores of the wild gourd. Moreover, because these herbivores are the sole vectors for the five most common viral diseases of cucurbits (Watermelon mosaic-2, Cucumber mosaic, Zucchini yellow mosaic, Papaya ringspot, and Squash mosaic), the spray treatment also significantly reduced the amount and severity of the symptoms of viral diseases. Our analyses reveal that (1) there is variation for resistance to herbivores and pathogens among the five families used in the study, indicating that there is broad-sense heritability for resistance; (2) inbred plants suffer greater herbivore damage and have more symptoms of viral infection than outbred plants, i.e., there is inbreeding depression for herbivore/pathogen resistance; (3) the impacts of insecticide applications and inbreeding on reproduction are mostly additive; (4) both male and female functions are significantly affected by the spray treatment and inbreeding; and (5) the adverse effects of both inbreeding and the increased exposure to herbivores/pathogens in the no-spray treatment are greater for female function than for male function, indicating that the impact of genetic and environmental stress can differentially affect the two sexual functions. Together, these findings have important implications for the evolution of selfing, the conservation of small populations, and the establishment and transmission of diseases within populations.

Inbreeding compromises host plant defense gene expression and improves herbivore survival

“…6,7 Compared to outbred plants, inbred plants are more susceptible to herbivores -under both field and lab conditions, [8][9][10] and herbivores perform better when they feed on inbred plants. [11][12][13] Previous studies using horsenettle (Solanum carolinense L.), a perennial weed native to the United States, showed that tobacco hornworm caterpillars (Manduca sexta L.) preferred to feed on inbred plants more than outbreds.…”

“…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). Our findings provide further evidence that plant inbreeding can produce biochemical changes in host plants that can impact the health and vigor of animals at a higher trophic level.…”

Costs associated with the evolution of selfing in North American populations of Arabidopsis lyrata?

“…Kuntze, but response was more variable in selfing populations (Hoebe et al 2011). Herbivory has been shown to magnify inbreeding depression Stephenson et al 2004;Leimu et al 2008) as well as outbreeding depression (Leimu and Fischer 2010). Indeed, antagonists have frequently been implied as a selective force favouring outcrossing in plants (Levin 1975;Busch 2004).…”

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

“…inbreeding depression). Although investigators have only recently begun to document the impacts of inbreeding on plant -insect interactions, several recent studies show that inbred plants suffer higher levels of herbivory than outbred plants [24,25], and that herbivores develop more rapidly on inbred plants [26,27]. The mechanisms underlying such effects are not well studied, but may include indirect effects mediated by a general reduction in vigour associated with inbreeding [23,24,28], as well as the direct disruption of plant defences-for example, through the effects of deleterious recessives on the expression of genes involved in plant defence pathways [29,30].…”