Susan R. Whitehead

Domestication impacts on plant–herbivore interactions: a meta-analysis

For millennia, humans have imposed strong selection on domesticated crops, resulting in drastically altered crop phenotypes compared with wild ancestors. Crop yields have increased, but a long-held hypothesis is that domestication has also unintentionally decreased plant defences against herbivores. To test this hypothesis, we conducted a phylogenetically controlled meta-analysis comparing insect herbivore resistance and putative plant defence traits between crops and their wild relatives. Our database included 2098 comparisons made across 73 crops in 89 studies. We found that domestication consistently reduced plant resistance to herbivores, although the magnitude of the effects varied across plant organs and depended on how resistance was measured. However, domestication had no consistent effects on the specific plant defence traits underlying resistance, including secondary metabolites and physical feeding barriers. The values of these traits sometimes increased and sometimes decreased during domestication. Consistent negative effects of domestication were observed only when defence traits were measured in reproductive organs or in the plant organ that was harvested. These results highlight the complexity of evolution under domestication and the need for an improved theoretical understanding of the mechanisms through which agronomic selection can influence the species interactions that impact both the yield and sustainability of our food systems. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’.

Evidence for the Adaptive Significance of Secondary Compounds in Vertebrate-Dispersed Fruits

Although the primary function of fleshy fruits is to attract seed dispersers, many ripe fruits contain toxic secondary compounds. A number of hypotheses have been proposed to explain this evolutionary paradox, most of which describe the potential adaptive role that secondary compounds may play in seed dispersal. However, some authors have argued that fruit secondary compounds may be nonadaptive and instead explain their occurrence as a pleiotropic consequence of selection for defense of leaves and other tissues. We address these alternative evolutionary hypotheses through a comparative examination of iridoid glycosides in the leaves, unripe fruits, and ripe fruits of Lonicera × bella (Belle’s bush honeysuckle), combined with an examination of fruit damage and removal in natural populations. We provide several lines of evidence that fruit secondary compounds cannot be explained solely as a consequence of foliar defense, including higher concentrations and more individual compounds in fruits compared to leaves and a negative relationship between iridoid glycoside concentration and fruit damage. However, we also show that the compositions and concentrations of secondary compounds in leaves and fruits are not entirely independent, emphasizing that selection in different plant parts is intrinsically linked. We conclude that the adaptive significance of chemical traits is best considered in a whole-plant context that includes fruit-frugivore interactions.

Iridoid and secoiridoid glycosides in a hybrid complex of bush honeysuckles (Lonicera spp., Caprifolicaceae): implications for evolutionary ecology and invasion biology.

Interspecific hybridization among non-native plant species can generate genotypes that are more reproductively successful in the introduced habitat than either parent. One important mechanism that may serve as a stimulus for the evolution of invasiveness in hybrids is increased variation in secondary metabolite chemistry, but still very little is known about patterns of chemical trait introgression in plant hybrid zones. This study examined the occurrence of iridoid and secoiridoid glycosides (IGs), an important group of plant defense compounds, in three species of honeysuckle, Lonicera morrowii A. Gray, Lonicera tatarica L., and their hybrid Lonicera×bella Zabel. (Caprifoliaceae), all of which are considered invasive in various parts of North America. Hybrid genotypes had a diversity of IGs inherited from both parent species, as well as one component not detected in either parent. All three species were similar in that overall concentrations of IGs were significantly higher in fruits than in leaves, and several compounds that were major components of fruits were never found in leaves. However, specific patterns of quantitative distribution among leaves, unripe fruits, and ripe fruits differed among the three species, with a relatively higher allocation to fruits in the hybrid species than for either parent. These patterns likely have important consequences for plant interactions with antagonistic herbivores and pathogens as well as mutualistic seed dispersers, and thus the potential invasiveness of hybrid and parental species in their introduced range. Methods established here for quantitative analysis of IGs will allow for the exploration of many compelling research questions related to the evolutionary ecology and invasion biology of these and other related species in the genus Lonicera.

The eco-evolutionary impacts of domestication and agricultural practices on wild species

Agriculture is a dominant evolutionary force that drives the evolution of both domesticated and wild species. However, the various mechanisms of agriculture-induced evolution and their socio-ecological consequences are not often synthetically discussed. Here, we explore how agricultural practices and evolutionary changes in domesticated species cause evolution in wild species. We do so by examining three processes by which agriculture drives evolution. First, differences in the traits of domesticated species, compared with their wild ancestors, alter the selective environment and create opportunities for wild species to specialize. Second, selection caused by agricultural practices, including both those meant to maximize productivity and those meant to control pest species, can lead to pest adaptation. Third, agriculture can cause non-selective changes in patterns of gene flow in wild species. We review evidence for these processes and then discuss their ecological and sociological impacts. We finish by identifying important knowledge gaps and future directions related to the eco-evolutionary impacts of agriculture including their extent, how to prevent the detrimental evolution of wild species, and finally, how to use evolution to minimize the ecological impacts of agriculture. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’.

Chemical ecology of fruit defence: synergistic and antagonistic interactions among amides from Piper

Summary 1. Although ripe, fleshy fruits function primarily to attract seed dispersers, they must also be defended against diverse communities of seed predators and pathogens. For some plants, the concentration and diversity of secondary metabolites in fruits can exceed that of leaves and other plant parts, but little is known about the functional significance of the suites of compounds found in fruits. Fruit secondary metabolites may function in defence, or they may play a variety of other roles in seed development and dispersal. 2. In this study, we conducted a series of experiments to test the effects of amides, a highly diverse class of secondary metabolites found in Piper fruits, on a variety of antagonistic fruit pests, including an insect seed predator (Sibaria englemani, Pentatomidae) and three unidentified species of fungi isolated from ripe Piper reticulatum (Piperaceae) fruits. We tested the effects of amide-rich extracts from unripe and ripe fruits of P. reticulatum and the effects of two pure compounds, piperine and piplartine, presented alone and in combination. 3. Amide-rich extracts from unripe and ripe fruits had no effect on insect feeding preferences, but strong negative effects on fungal growth rates. A comparison of the relative bioactivity of unripe and ripe fruit extracts, controlling for concentration, showed that the specific composition of compounds in unripe fruits provides a more effective defence than that of ripe fruits against two of the three fungal species tested. 4. Pure amides had variable effects on insect feeding preferences and strong negative effects on fungal growth rates. Tests of the bioactivity of two pure amides, presented alone and in combination, showed that the same two compounds can interact either synergistically or antagonistically in mixtures depending on the particular consumer involved. 5. Together, these results suggest that the secondary metabolites in fruits may be a key characteristic contributing to fruit defence and plant reproductive success. Specifically, our results emphasize: (i) the potential for slight changes in the composition of mixtures to alter the efficacy of defence; and (ii) the potential for complex interactions among compounds in mixtures that can alter the bioactivity of secondary metabolites differentially among different consumers.

Patterns of Secondary Metabolite Allocation to Fruits and Seeds in Piper reticulatum

Little is known about the evolution, diversity, and functional significance of secondary metabolites in reproductive plant parts, particularly fruits and seeds of plants in natural ecosystems. We compared the concentration and diversity of amides among six tissue types of Piper reticulatum: leaves, roots, flowers, unripe fruit pulp, ripe fruit pulp, and seeds. This represents the first detailed description of amides in P. reticulatum, and we identified 10 major and 3 minor compounds using GC/MS and NMR analysis. We also detected 30 additional unidentified minor amide components, many of which were restricted to one or a few plant parts. Seeds had the highest concentrations and the highest diversity of amides. Fruit pulp had intermediate concentrations and diversity that decreased with ripening. Leaves and roots had intermediate concentrations, but the lowest chemical diversity. In addition, to investigate the potential importance of amide concentration and diversity in plant defense, we measured leaf herbivory and seed damage in natural populations, and examined the relationships between amide occurrence and plant damage. We found no correlations between leaf damage and amide diversity or concentration, and no correlation between seed damage and amide concentration. The only relationship we detected was a negative correlation between seed damage and amide diversity. Together, our results provide evidence that there are strong selection pressures for fruit and seed defense independent of selection in vegetative tissues, and suggest a key role for chemical diversity in fruit-frugivore interactions.

Fruit secondary compounds mediate the retention time of seeds in the guts of Neotropical fruit bats

Plants often recruit frugivorous animals to transport their seeds; however, gut passage can have varying effects on plant fitness depending on the physical and chemical treatment of the seed, the distance seeds are transported, and the specific site of deposition. One way in which plants can mediate the effects of gut passage on fitness is by producing fruit secondary compounds that influence gut-retention time (GRT). Using frugivorous bats (Carollia perspicillata: Phyllostomidae) and Neotropical plants in the genus Piper, we compared GRT of seeds among five plant species (Piper colonense, Piper peltatum, Piper reticulatum, Piper sancti-felicis, and Piper silvivagum) and investigated the role of fruit amides (piperine, piplartine and whole fruit amide extracts from P. reticulatum) in mediating GRT. Our results showed interspecific differences in GRT; P. reticulatum seeds passed most slowly, while P. silvivagum and P. colonense seeds passed most rapidly. Piplartine and P. reticulatum amide extracts decreased GRT, while piperine had no effect. In addition, we examined the effects of GRT on seed germination success and speed in laboratory conditions. For germination success, the effects were species specific; germination success increased with GRT for P. peltatum but not for other species. GRT did not influence germination speed in any of the species examined. Plant secondary compounds have primarily been studied in the context of their defensive role against herbivores and pathogens, but may also play a key role in mediating seed dispersal interactions.

Comparative Herbivory Rates and Secondary Metabolite Profiles in the Leaves of Native and Non-Native Lonicera Species

Non-native plants introduced to new habitats can have significant ecological impact. In many cases, even though they interact with the same community of potential herbivores as their new native competitors, they regularly receive less damage. Plants produce secondary metabolites in their leaves that serve a range of defensive functions, including resistance to herbivores and pathogens. Abiotic factors such as nutrient availability can influence the expression of defensive traits, with some species exhibiting increased chemical defense in low-nutrient conditions. Plants in the genus Lonicera are known to produce a diverse array of these secondary metabolites, yet non-native Lonicera species sustain lower amounts of herbivore damage than co-occurring native Lonicera species in North America. In this study, we searched for evidence of biochemical novelty in non-native species, and quantified its association with resistance to herbivores. In order to achieve this, we evaluated the phenolic and iridoid glycoside profiles in leaves of native and non-native Lonicera species grown under high and low fertilization treatments in a common garden. We then related these profiles to naturally occurring herbivore damage on whole plants in the garden. Herbivore damage was greater on native Lonicera, and chemical profiles and concentrations of selected putative defense compounds varied by species. Geographic origin was an inconsistent predictor of chemical variation in detected phenolics and iridoid glycosides (IGs). Overall, fertilization did not affect herbivore damage or measures of phenolics or IGs, but there were some fertilization effects within species. While we cannot conclude that non-natives were more chemically novel than native Lonicera species, chemical defense profiles and concentrations of specific compounds varied by species. Reduced attraction or deterrence of oviposition, specific direct resistance traits, or a combination of both may contribute to reduced herbivory and competitive advantages for non-native Lonicera in North America.

Leaf herbivory imposes fitness costs mediated by hummingbird and insect pollinators

Plant responses induced by herbivore damage can provide fitness benefits, but can also have important costs due to altered interactions with mutualist pollinators. We examined the effects of plant responses to herbivory in a hummingbird-pollinated distylous shrub, Palicourea angustifolia. Through a series of field experiments we investigated whether damage from foliar herbivores leads to a reduction in fruit set, influences floral visitation, or alters floral traits that may influence pollinator preference or pollinator efficiency. Foliar herbivory by a generalist grasshopper led to reduced fruit set in branches that were directly damaged as well as in adjacent undamaged branches on the same plant. Furthermore, herbivory resulted in reduced floral visitation from two common hummingbird species and two bee species. An investigation into the potential mechanisms behind reduced floral visitation in induced plants showed that foliar herbivore damage resulted in shorter styles and lower nectar volumes. This reduction in style length could reduce pollen deposition between different floral morphs that is required for optimal pollination in a distylous plant. We did not detect any differences in the volatile blends released by damaged and undamaged branches, suggesting that foliar herbivore-induced changes in floral morphology and rewards, and not volatile blends, are the primary mechanism mediating changes in visitation. Our results provide novel mechanisms for how plant responses induced by foliar herbivores can lead to ecological costs.