Plant sex and the evolution of plant defenses against herbivores

Abstract

Despite the importance of plant-herbivore interactions to the ecology and evolution of terrestrial ecosystems, the evolutionary factors contributing to variation in plant defenses against herbivores remain unresolved. We used a comparative phylogenetic approach to examine a previously untested hypothesis (Recombination-Mating System Hypothesis) that posits that reduced sexual reproduction limits adaptive evolution of plant defenses against arthropod herbivores. To test this hypothesis we focused on the evening primrose family (Onagraceae), which includes both sexual and functionally asexual species. Ancestral state reconstructions on a 5-gene phylogeny of the family revealed between 18 and 21 independent transitions between sexual and asexual reproduction. Based on these analyses, we examined susceptibility to herbivores on 32 plant species representing 15 independent transitions. Generalist caterpillars consumed 32% more leaf tissue, gained 13% greater mass, and experienced 21% higher survival on functionally asexual than on sexual plant species. Survival of a generalist feeding mite was 19% higher on asexual species. In a field experiment, generalist herbivores consumed 64% more leaf tissue on asexual species. By contrast, a specialist beetle fed more on sexual than asexual species, suggesting that a tradeoff exists between the evolution of defense to generalist and specialist herbivores. Measures of putative plant defense traits indicate that both secondary compounds and physical leaf characteristics may mediate this tradeoff. These results support the Recombination-Mating System Hypothesis and suggest that variation in sexual reproduction among plant species may play an important, yet overlooked, role in shaping the macroevolution of plant defenses against arthropod herbivores.coevolution ͉ herbivory ͉ phylogenetics ͉ plant-insect ͉ tradeoff

Plant mating system transitions drive the macroevolution of defense strategies

“…Prior theoretical work has predicted the evolution of greater plant defense in sexual vs. asexual taxa, potentially as a result of differential recombination rates (24) or reduced mutation accumulation (25). This prediction has been supported by a large study of constitutive plant resistance in the Onagraceae (evening primroses) (26) and complements research on the role of parasites in the evolution of sex (27). However, it remains unknown whether variation in sexual reproduction should similarly influence defense evolution, in part because recombination rates may be widely variable in all but extremely or obligately selfing taxa.…”

“…Future work could compare these results with responses to herbivores with different feeding modes or host ranges. Although sex per se (vs. asexuality) is long thought to have been favored in part by coevolution of antagonistic interactions (26,27,52), we have demonstrated that such interactions may also coevolve with variation in the mode and expression of sexual reproduction. These findings also complement prior research showing that intraspecific variation in mating systems (32) and associated traits such as sex (33) can alter plant defense trait expression, with the potential for herbivores to influence the evolution and maintenance of plant reproduction within populations (30,32).…”

“…Thus, neither obligate outcrossing (SI) nor its loss confers a consistent evolutionary advantage in terms of the magnitude of overall plant resistance. Theoretical models (24) and some data (26) suggest an association between effective recombination and evolution of increased defense against antagonists. The marginally greater constitutive resistance in SI taxa is consistent with this hypothesis, although we note that our study was not designed to test the role of recombination per se.…”

“…Our question arises from two complementary hypotheses discussed above: first, theory (24) and some data (26) suggest that outcrossing may favor higher levels of constitutive defense. Second, SI loss could alter natural selection on defense strategies by allowing plant colonization of novel habitats, thereby reducing the probability and intensity of herbivore attack (16).…”

Mechanisms of plant defense against insect herbivores

“…32 It limits the entry of pathogens by blocking physically or increasing the leaf toughness that reduces the feeding by herbivores, and also decreases the nutritional content of the leaf. 33 Lignin synthesis has been found to be induced by herbivory or pathogen attack and its rapid deposition reduce further growth of the pathogen or herbivore fecundity. 33 Increase in expression of lignin associated genes (CAD/ CAD-like genes) in plants infected with pests and pathogens have been documented.…”