Genetic and sexual separation between insect resistant and susceptible Barbarea vulgaris plants in Denmark

Abstract

Co-evolution between herbivores and plants is believed to be one of the processes creating Earth's biodiversity. However, it is difficult to disentangle to what extent diversification is really driven by herbivores or by other historical-geographical processes like allopatric isolation. In the cruciferous plant Barbarea vulgaris, some Danish individuals are resistant to herbivory by flea beetles (Phyllotreta nemorum), whereas others are not. The flea beetles are, in parallel, either resistant or susceptible to the plants defenses. To understand the historical-evolutionary framework of these interactions, we tested how genetically divergent resistant and susceptible plants are, using microsatellite markers. To test whether they are reproductively fully compatible, resistant and susceptible plants were grown intermixed in an outdoor experiment, and the paternity of open-pollinated offspring was determined by analysis of molecular markers. Resistant and susceptible Danish plants were genetically strongly differentiated and produced significantly fewer hybrids than expected from random mating or nearest neighbour mating. Our results suggest that the two types belong to different evolutionary lineages that have been (partly) isolated at some time, during which genetic and reproductive divergence evolved. A parsimonious scenario could be that the two plant types were isolated in different refugia during the previous ice age, from which they migrated into and met in Denmark and possibly neighbouring regions. If so, resistance and susceptibility has for unknown reasons become associated with the different evolutionary lineages.

Genetic and geographic structure of an insect resistant and a susceptible type of Barbarea vulgaris in western Europe

“…The strong genetic divergence between the Danish G and P types of B. vulgaris, and linkage disequilibrium among several phenotypic traits, suggest that they are probably old, and that genes for resistance and susceptibility have been associated with these different evolutionary lineages for considerable time (Toneatto et al 2010). In agreement with this, the two plant types predominantly grow in separate populations in Denmark, hybrids are relatively rare, and when they occur they are frequently sterile (JK Nielsen, unpublished).…”

“…Plant material for this study included (1) three Danish populations characterized as G-type, and three characterized as P-type, collected by JK Nielsen in 2006 (also included in Toneatto et al 2010); (2) seeds from 26 other European populations kindly provided by botanical gardens and individual contacts (Table 1; Fig. 1; Acknowledgements); all accessions were collected from wild populations.…”

“…Five nuclear microsatellite (SSR) loci were amplified using the primers reported in Toneatto et al (2010). Two chloroplast microsatellite (SSR) loci were amplified using primers MF-7 and MF-8 from Flannery et al (2006); they are positioned in plastid gene regions TrnM-atpE and rbcL-accD.…”

“…Resistance to flea beetles, and other specialist herbivores (Renwick 2002;Shinoda et al 2002), is mediated by specific saponin compounds which are present only in the G plants (Kuzina et al 2009). The resistant G type additionally differs from the susceptible P type by producing different glucosinolates (Agerbirk et al 2003) and flavonoids (Dalby-Brown et al 2011), by having fewer chromocenters in somatic cells (Ørgaard and Linde-Laursen 2007), and by a somewhat different phenology (Agerbirk et al 2001(Agerbirk et al , 2003Toneatto et al 2010). Recent genetic analyses have shown that the Danish G and P-type plants are quite divergent, somewhat reproductively incompatible (Toneatto et al 2010), and that resistance, hairiness and one of the differentiating glucosinolates are not physically linked, but associated by strong linkage disequilibrium (Kuzina et al 2011).…”

UDP-Glycosyltransferases from the UGT73C Subfamily in Barbarea vulgaris Catalyze Sapogenin 3-O-Glucosylation in Saponin-Mediated Insect Resistance

“…Much later, B. vulgaris differentiated into the G-and P-types, possibly during one of the last ice ages Toneatto et al, 2012). Thus, the two plant types are genetically and geographically differentiated, reproductively somewhat incompatible, and differ for several traits apart from insect resistance and saponin structure (Toneatto et al, 2010;Dalby-Brown et al, 2011). Thus, the most likely scenario suggests that the P-type lost resistance to P. nemorum during this allopatric separation.…”