Genetic Variation in Defense Chemistry in Wild Cabbages Affects Herbivores and Their Endoparasitoids

Abstract

Abstract. Populations of wild Brassica oleracea L. grow naturally along the Atlantic coastlines of the United Kingdom and France. Over a very small spatial scale (i.e., ,15 km) these populations differ in the expression of the defensive compounds, glucosinolates (GS). Thus far, very few studies have examined interactions between genetically distinct populations of a wild plant species and associated consumers in a multitrophic framework. Here, we compared the development of a specialist (Pieris rapae) and a generalist (Mamestra brassicae) insect herbivore and their endoparasitoids (Cotesia rubecula and Microplitis mediator, respectively) on three wild populations and one cultivar of B. oleracea under controlled greenhouse conditions. Herbivore performance was differentially affected by the plant population on which they were reared. Plant population influenced only development time and pupal mass in P. rapae, whereas plant population also had a dramatic effect on survival of M. brassicae. Prolonged development time in P. rapae corresponded with high levels of the indole GS, neoglucobrassicin, whereas reduced survival in M. brassicae coincided with high levels of the aliphatic GS, gluconapin and sinigrin. The difference between the two species can be explained by the fact that the specialist P. rapae is adapted to feed on plants containing GS and has evolved an effective detoxification system against aliphatic GS. The different B. oleracea populations also affected development of the endoparasitoids. Differences in foodplant quality for the hosts were reflected in adult size in C. rubecula and survival in M. mediator, and further showed that parasitoid performance is also affected by herbivore diet.

Formation of Simple Nitriles upon Glucosinolate Hydrolysis Affects Direct and Indirect Defense Against the Specialist Herbivore, Pieris rapae

“…In fact, P. rapae is known to avoid laying eggs on plants that are infested with conspecific larvae or that carry conspecific eggs (Rothschild and Schoonhoven 1977;Schoonhoven et al 1990;Sato et al 1999). Nitriles, acting as indicators of feeding and defecating larvae, may not only signify the presence of competitors but may also hint at increased levels of glucosinolates and other defense compounds in the host plant as a result of induction that have a negative influence on the performance of the offspring (e.g., Agrawal and Kurashige 2003;Mewis et al 2005Mewis et al , 2006Gols et al 2008). Accordingly, cabbage plants that were treated with jasmonic acid, a key hormone involved in induced plant defense, received significantly fewer eggs from P. rapae than respective control plants (Bruinsma et al 2007).…”

“…Moreover, glucosinolates and isothiocyanates often serve as attractants or oviposition and feeding stimulants for these insects (Van Loon et al 1992;Wittstock et al 2003;Miles et al 2005;Schoonhoven et al 2005;Renwick et al 2006;Barth and Jander 2006;Smallegange et al 2007). Still, several studies have shown negative correlations between the glucosinolate content of the diet and the larval performance of herbivorous insects specialized on Brassicaceae (Mewis et al 2005(Mewis et al , 2006Gols et al 2007Gols et al , 2008Kim and Jander 2007).…”

“…A few studies have demonstrated that parasitoids are attracted to isothiocyanates (Titayavan and Altieri 1990;Pivnick 1993;Murchie et al 1997;Bradburne and Mithen 2000;Reddy et al 2002;Blande et al 2007). However, parasitoid and predator performance is also known to correlate negatively with glucosinolate content (Harvey et al 2003;Kazana et al 2007;Gols et al 2008). This negative relationship might favor a behavioral response of predators and parasitoids to plant volatiles that contain simple nitriles instead of isothiocyanates.…”

Alteration of plant primary metabolism in response to insect herbivory

“…Specialist herbivores are generally limited to feeding from plants in a specific family or even genus, and are typically able to tolerate the characteristic defensive metabolites (Agrawal and Kurashige, 2003;Gols et al, 2008). In contrast, generalist herbivores have a wider host range, typically show a lower tolerance of specialized plant toxins, and tend to feed from lessdefended parts of the host plant (Ballhorn et al, 2010; e.g.…”

Intraspecific variation in defense against a generalist lepidopteran herbivore in populations of Eruca sativa (Mill.)

“…2006; Gols et al. 2008). Bidart‐Bouzat and Kliebenstein (2008) similarly associated intraspecific GS concentrations in 20 natural accessions of Arabidopsis with resistance against insects, but found a positive correlation between total GS concentration and the extent of the damage caused by specialists in field experiments.…”