Divergent selection for secondary metabolites between wild populations of Brassica oleracea and its implications for plant-herbivore interactions

Abstract

Significant differences occur in the levels and types of aliphatic glucosinolates in leaves of plants of four Brassica oleracea populations in Dorset. Plants in grassland at St Aldhelm's Head and Winspit have high levels of 3-butenyl glucosinolate, whereas plants of an adjacent population growing on and along the top of cliffs at Kimmeridge have low levels of 2-hydroxy-3-butenyl, 2-propenyl and methylsuiphinylalkyl glucosinolates. Plants growing in a variable habitat at Worbarrow Tout have intermediate levels. The differences in occurrence of individual glucosinolates result from allelic variation at four loci. The level of total aliphatic glucosinolates is under more complex genetic control, but is shown to be highly heritable. Allele frequencies at isozyme loci indicate that genetic variation for glucosinolate production is unlikely to have arisen or to be maintained by founder effects or genetic drift. It is suggested that there is selection for high levels of butenyl glucosinolates at St Aldhelm's Head and Winspit because of grazing by generalist herbivores, whereas there is selection for low levels of 2-hydroxy-3-butenyl and other non-butenyl aliphatic glucosinolates at Kimmeridge because of two factors. First, plants effectively escape from generalist herbivores because of physical aspects of the habitat and association with other plant species which provide physical and chemical defences. Thus there is selection for individuals which do not carry the hypothetical metabolic costs of glucosinolate biosynthesis. Secondly, herbivory by specialist cruciferous insects at Kimmeridge, which is enhanced because of the local abundance of B. nigra, selects for individuals which have low levels of 2-hydroxy-3-butenyl glucosinolates.

Differences in Effects of Pyrrolizidine Alkaloids on Five Generalist Insect Herbivore Species

“…The diversity in related secondary metabolites may also be maintained by selection pressure from different herbivores (Simms, 1990;Mithen et al, 1995;Juenger and Bergelson, 1998). The experiments with the thrips and the aphid show that generalist insect species can respond differently to the same PA.…”

“…Additionally, related compounds can act synergistically on herbivores (Adams and Bernays, 1978;Lindroth et al, 1988;Berenbaum et al, 1991). Furthermore, the diversity can be maintained through selection by several different herbivores and/or pathogens (Simms, 1990;Mithen et al, 1995;Juenger and Bergelson, 1998).…”

The prevalence and spatial distribution of viruses in natural populations of Brassica oleracea

“…The plants in the northernmost sites are phenotypically similar to modern cabbage varieties and are probably recent escapes from cultivation. Compared with modern cultivars, southern populations of wild cabbage are more variable morphologically and have higher concentrations of glucosinolates (Greenhalgh & Mitchell, 1976 ;Mithen et al, 1995) and, therefore, might be unconnected to past cultivation. Nevertheless, it is possible that all wild cabbage in Britain originated from escapes because almost all populations are found near sites of ancient habitation .…”

“…Seed dispersal is also limited, with most seed falling within 4 m of the parent plant (Gray et al, 1996). Populations show large and significant heterozygote deficits at isozyme loci (Mithen et al, 1995 ;Gray et al, 1996).…”

“…There were several reasons for choosing this system. First, wild cabbage occurs in several discrete populations, individuals are easy to identify and a great deal is known about the history, ecology and population genetics of the species in this area Mitchell & Richards, 1979 ;Mithen et al, 1995 ;Gray et al, 1996 ;Raybould et al, 1998). Second, BWYV, CaMV and TuMV infections are common in horticultural and agricultural brassicas in the UK and can cause complete crop failure (Broadbent, 1957 ;Hardwick et al, 1994).…”