Evolution of resistance and tolerance to herbivores: testing the trade-off hypothesis

Abstract

Background. To cope with their natural enemies, plants rely on resistance and tolerance as defensive strategies. Evolution of these strategies among natural population can be constrained by the absence of genetic variation or because of the antagonistic genetic correlation (trade-off) between them. Also, since plant defenses are integrated by several traits, it has been suggested that trade-offs might occur between specific defense traits.Methodology/Principal Findings. We experimentally assessed (1) the presence of genetic variance in tolerance, total resistance, and leaf trichome density as specific defense trait, (2) the extent of natural selection acting on plant defenses, and (3) the relationship between total resistance and leaf trichome density with tolerance to herbivory in the annual herb Datura stramonium. Full-sib families of D. stramonium were either exposed to natural herbivores (control) or protected from them by a systemic insecticide. We detected genetic variance for leaf trichome density, and directional selection acting on this character. However, we did not detect a negative significant correlation between tolerance and total resistance, or between tolerance and leaf trichome density. We argue that low levels of leaf damage by herbivores precluded the detection of a negative genetic correlation between plant defense strategies.Conclusions/Significance. This study provides empirical evidence of the independent evolution of plant defense strategies, and a defensive role of leaf trichomes. The pattern of selection should favor individuals with high trichomes density. Also, because leaf trichome density reduces damage by herbivores and possess genetic variance in the studied population, its evolution is not constrained.

Genome‐wide association analysis reveals distinct genetic architectures for single and combined stress responses in Arabidopsis thaliana

“…We reasoned that these accessions displayed tolerance to the treatment. Because tolerance and resistance traits have a different genetic basis (Strauss & Agrawal, 1999;Carmona et al, 2011;Karinho-Betancourt & Nunez-Farfan, 2015), we only included data for accessions displaying a reduction in biomass under the treatment compared with control conditions (Table S1). This dataset was used for all downstream analyses.…”

“…Plant traits that influence the degree of damage caused by insects can be classified into resistance (traits that limit the damage by the insect) and tolerance (traits that allow plants to compensate for insect damage) (Strauss & Agrawal, 1999;Stout, 2013). Furthermore, resistance and tolerance are mediated by distinct genetic mechanisms (Strauss & Agrawal, 1999;Carmona et al, 2011;Karinho-Betancourt & Nunez-Farfan, 2015). Resistance can be further divided into constitutive or induced defences (Schoonhoven et al, 2005;Mithofer & Boland, 2012;Stout, 2013).…”

Tolerance to deer herbivory and resistance to insect herbivores in the common evening primrose (Oenothera biennis)

“…The O. biennis genotypes examined in this experiment showed comparable responses to deer herbivory in that they experienced similar reductions in fitness following damage. The absence of genetic variation in tolerance to herbivore damage is not uncommon and has been found in a broad range of systems from herbaceous weeds to trees (Bach, ; Houle & Simard, ; Osier & Lindroth, ; Silfver et al ., ; Muola et al ., ; Kariñho‐Betancourt & Núñez‐Farfán, ). For example, similar to our study, Ivey et al .…”

“…We did not detect significant genetic correlations between tolerance to early‐season deer damage and resistance to any of the natural insect herbivores that attacked O. biennis during our experiment (Table ). These results support the growing empirical evidence that these two strategies need not be mutually exclusive (Leimu & Koricheva, ; Muola et al ., ; Hakes & Cronin, ; Carmona & Fornoni, ; Puentes & Ågren, ; Kariñho‐Betancourt & Núñez‐Farfán, ; but see e.g. Hoque & Avila‐Sakar, ).…”

Variation in host susceptibility to different pathogens: an experimental and phylogenetic study of Drosophila-viruses

“…In this way, as defence mechanisms against parasites may represent a cost in fitness for hosts (Sheldon & Verhulst, 1996) and as hosts have limited resources, hosts need to deal with trade-offs among investment in resistance or fitness, or among resistance traits. The trade-off among resistance traits means that an increase in resistance or tolerance to one pathogen must be balanced by an increase in susceptibility to another pathogen (Kariñho-Betancourt & Núñez-Farfán, 2015). For example, it has been showed that plants express different resistant traits against herbivory depending on the place they are (Berenbaum & Zangerl, 2006) and on the time (Wäckers & Bonifay, 2004).…”