Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations

Abstract

Through artificial selection, domesticated plants often contain modified levels of primary and secondary metabolites compared to their wild progenitors. It is hypothesized that the changed chemistry of cultivated plants will affect the performance of insects associated with these plants. In this paper, the development of several specialist and generalist herbivores and their endoparasitoids were compared when reared on a wild and cultivated population of cabbage, Brassica oleracea, and a recently established feral Brassica species. Irrespective of insect species or the degree of dietary specialization, herbivores and parasitoids developed most poorly on the wild population. For the specialists, plant population influenced only development time and adult body mass, whereas for the generalists, plant populations also affected egg-to-adult survival. Two parasitoid species, a generalist (Diadegma fenestrale) and a specialist (D. semiclausum), were reared from the same host (Plutella xylostella). Performance of D. semiclausum was closely linked to that of its host, whereas the correlation between survival of D. fenestrale and host performance was less clear. Plants in the Brassicaceae characteristically produce defense-related glucosinolates (GS). Levels of GS in leaves of undamaged plants were significantly higher in plants from the wild population than from the domesticated populations. Moreover, total GS concentrations increased significantly in wild plants after herbivory, but not in domesticated or feral plants. The results of this study reveal that a cabbage cultivar and plants from a wild cabbage population exhibit significant differences in quality in terms of their effects on the growth and development of insect herbivores and their natural enemies. Although cultivated plants have proved to be model systems in agroecology, we argue that some caution should be applied to evolutionary explanations derived from studies on domesticated plants, unless some knowledge exists on the history of the system under investigation.

Fig. 1

Glucosinolate (GS) concentrations (mean ± SE) in leaf tissues of a cultivated (a), feral (b), and wild (c) Brassica population. Concentrations were measured in leaf tissue from plants that were undamaged (black bars), damaged by unparasitized P. xylostella larvae (white bars) and damaged by parasitized (D. semiclausum) larvae (gray bars). GS abbreviations and scientific names: TOT total GS concentration, GBC glucobrassicin (= indol-3-ylmethyl GS), IBE glucoiberin (= 3-methylsulfinyl propyl GS), GNA gluconapin (= 3-butenyl GS), NEO neoglucobrassicin (= 1-methoxyindol-3-ylmethyl GS), RAP glucoraphanin (= 4-methylsulfinyl butyl GS), SIN sinigrin (= 2-propenyl GS), PRO progoitrin (= 2(R)-2-hydroxy-3-butenyl GS), GBN glucobrassicanapin (= 4-pentenyl GS), GNL gluconapoleiferin (= 2-hydroxy-4-pentenyl GS), ALY glucoallyssin (= 5-methylsulfinyl pentyl GS), 4OH 4-hydroxyglucobrassicin (= 4-hydoxyindol-3-ylmethyl GS), 4MeOH, 4-methoxyglucobrassicin (= 4-methoxyindol-3-ylmethyl GS), and NAS gluconasturcin (= 2-phenylethyl GS). ND not detectable

Fig. 2

Egg-to-adult development time (a) and adult dry mass (b) of P. xylostella males (white bars) and females (gray bars) reared on either a cultivated, a feral, or wild Brassica population. Bars (mean ± SE) with different letters are significantly different from each other (Tukey multiple comparisons, α = 0.05). Numbers of individuals (N) were on the cultivar, escape, and wild population, respectively: males, 21, 22, and 31; females 23, 22, 18

Fig. 3

Larval to adult survival of two specialist herbivores, P. xylostella and P. rapae, and one generalist, Mamestra brassica, when reared on either a cultivated, feral or wild Brassica population. P. xylostella was also reared on a wild population of B. nigra

Fig. 4

Egg-to-adult development time (a) and adult dry mass (b) of P. rapae males (white bars) and females (gray bars) reared on either a cultivated, feral, or wild Brassica population. Bars (mean ± SE) with different letters are significantly different from each other (Tukey multiple comparisons, α = 0.05). Numbers of individuals (N) were on the cultivated, feral, and wild population, respectively: males, 22, 10, and 19; females 16, 20, 20

Fig. 5

Egg-to-adult development time (a) and adult dry mass (b) of M. brassicae reared on either a cultivated, feral, or wild Brassica population. Bars (mean ± SE) with different letters are significantly different from each other (Tukey multiple comparisons, α = 0.05). Numbers of individuals (N) were on the cultivated, feral, and wild population, respectively: 21, 29, and 2

Fig. 6

Egg-to-adult development time (a) and adult dry mass (b) of D. semiclausum males (white bars) and females (gray bars) reared on P. xylostella feeding on either a cultivated, feral, or wild Brassica population. Bars (mean ± SE) with different letters are significantly different from each other (Tukey multiple comparisons, α = 0.05). Numbers of individuals (N) were on the cultivated, feral, and wild population, respectively: 87, 69, and 81 for males and 11, 12, 10 for females

Fig. 7

Egg-to-adult survival of a specialist parasitoid, D. semiclausum, and a generalist parasitoid, D. fenestrale, when reared from the host, P. xylostella, on either a cultivated, feral, or wild Brassica population. D. fenestrale was also reared from P. xylostella on a wild population of B. nigra

Fig. 8

Egg-to-adult development time (a) and adult dry mass (b) of D. fenestrale males reared on P. xylostella feeding on either a cultivated, feral, or wild Brassica population. Bars (mean ± SE) with different letters are significantly different from each other (Tukey multiple comparisons, α = 0.05). Numbers of individuals (N) were on the cultivar, escape, and wild population, respectively: 44, 18, and 14