Terrestrial biodiversity is dominated by plants and the herbivores that consume them, and they are one of the major conduits of energy flow up to higher trophic levels. Here, we address the processes that have generated the spectacular diversity of flowering plants (>300,000 species) and insect herbivores (likely >1 million species). Long-standing macroevolutionary hypotheses have postulated that reciprocal evolution of adaptations and subsequent bursts of speciation have given rise to much of this biodiversity. We critically evaluate various predictions based on this coevolutionary theory. Phylogenetic reconstruction of ancestral states has revealed evidence for escalation in the potency or variety of plant lineages' chemical defenses; however, escalation of defense has been moderated by tradeoffs and alternative strategies (e.g., tolerance or defense by biotic agents). There is still surprisingly scant evidence that novel defense traits reduce herbivory and that such evolutionary novelty spurs diversification. Consistent with the coevolutionary hypothesis, there is some evidence that diversification of herbivores has lagged behind, but has nevertheless been temporally correlated with that of their host-plant clades, indicating colonization and radiation of insects on diversifying plants. However, there is still limited support for the role of host-plant shifts in insect diversification. Finally, a frontier area of research, and a general conclusion of our review, is that community ecology and the long-term evolutionary history of plant and insect diversification are inexorably intertwined.

https://www.pnas.org/content/pnas/106/43/18054.full.pdf

Macroevolution and the biological diversity of plants and herbivores

Summary
1. Induced resistance is now widely accepted as a potent and widespread ecological force although several pieces of the story remain very poorly known. Theory predicts that induced defences should be favoured in variable environments especially when plants can use cues to reliably predict future conditions; however, this idea has not been seriously evaluated for plants.

2. Theory also predicts that plastic, induced defences should be favoured over permanent, constitutive defences if defences are costly and not always needed. This hypothesis has received considerable attention and limited support; resource allocation costs have been difficult to detect although ecological costs of defence may be more common. Recently, priming has emerged as a mechanism that may further reduce costs. Primed plants do not immediately produce the gene products associated with induced resistance but later respond more rapidly and strongly to severe or repeated attacks. It remains to be determined how common priming is.

3. Much of what we know about induced resistance is from the herbivore’s point of view. Induced resistance will be beneficial from the plant’s point of view if herbivores avoid induced plants, but the behavioural responses of herbivores to induced plant variation are still poorly studied.

4. Recent progress in understanding the detailed spatial and temporal extent of induced resistance has improved our appreciation of the phenomenon. Although some induced responses are systemic throughout entire plant individuals, many others have been found to be localized to damaged tissues. Plant vascular architecture and transpiration rates greatly constrain the distribution of vascular cues. Some plants rely on volatile cues that are active over relatively short distances and may be subject to eavesdropping by other plants, herbivores, and carnivores. Similarly, the temporal duration of induced responses may have important consequences on effectiveness although limited information is available concerning lag times before induction and relaxation times following induction.

5. Limited spatial and temporal scales of induced responses make plants more variable from the herbivore’s point of view. Recent work suggests that plant heterogeneity may be difficult for herbivores to cope with although this hypothesis awaits further empirical testing.

https://besjournals.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-2435.2010.01789.x

The ecology and evolution of induced resistance against herbivores

The subdiscipline of 'community phylogenetics' is rapidly growing and influencing thinking regarding community assembly. In particular, phylogenetic dispersion of co-occurring species within a community is commonly used as a proxy to identify which community assembly processes may have structured a particular community: phylogenetic clustering as a proxy for abiotic assembly, that is habitat filtering, and phylogenetic overdispersion as a proxy for biotic assembly, notably competition. We challenge this approach by highlighting (typically) implicit assumptions that are, in reality, only weakly supported, including (i) phylogenetic dispersion reflects trait dispersion; (ii) a given ecological function can be performed only by a single trait state or combination of trait states; (iii) trait similarity causes enhanced competition; (iv) competition causes species exclusion; (v) communities are at equilibrium with processes of assembly having been completed; (vi) assembly through habitat filtering decreases in importance if assembly through competition increases, such that the relative balance of the two can be thus quantified by a single parameter; and (vii) observed phylogenetic dispersion is driven predominantly by local and present-day processes. Moreover, technical sophistication of the phylogenetic-patterns-as-proxy approach trades off against sophistication in alternative, potentially more pertinent approaches to directly observe or manipulate assembly processes. Despite concerns about using phylogenetic dispersion as a proxy for community assembly processes, we suggest there are underappreciated benefits of quantifying the phylogenetic structure of communities, including (i) understanding how coexistence leads to the macroevolutionary diversification of habitat lineage-pools (i.e. phylogenetic-patterns-as-result approach); and (ii) understanding the macroevolutionary contingency of habitat lineage-pools and how it affects present-day species coexistence in local communities (i.e. phylogenetic-patterns-as-cause approach). We conclude that phylogenetic patterns may be little useful as proxy of community assembly. However, such patterns can prove useful to identify and test novel hypotheses on (i) how local coexistence may control macroevolution of the habitat lineage-pool, for example through competition among close relatives triggering displacement and diversification of characters, and (ii) how macroevolution within the habitat lineage-pool may control local coexistence of related species, for example through origin of close relatives that can potentially enter in competition. 2015 British Ecological Society.

https://besjournals.onlinelibrary.wiley.com/doi/pdf/10.1111/1365-2435.12425

Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better)

'Summary'	733	
I.	'Introduction'	733	
II.	'PSM variation in time: ontogeny, phenology and induced defences'	734	
III.	'PSM variation through space: the role of environment'	735	
IV.	'Genes and biosynthetic pathways underlying PSM variation'	735	
V.	'Mechanisms for diversification of PSMs'	735	
VI.	'Examples of diversity from specific biosynthetic pathways'	737	
VII.	'How and why is chemical diversity maintained?'	739	
VIII.	'Evolvability of PSM variation'	740	
IX.	'Evolutionary strategies and diversity in plant chemical defence'	742	
X.	'Conclusions and future directions'	744	
 	'Acknowledgements'	745	
 	References	745	


Summary
Plant secondary metabolites (PSMs) are ubiquitous in plants and play many ecological roles. Each compound can vary in presence and/or quantity, and the composition of the mixture of chemicals can vary, such that chemodiversity can be partitioned within and among individuals. Plant ontogeny and environmental and genetic variation are recognized as sources of chemical variation, but recent advances in understanding the molecular basis of variation may allow the future deployment of isogenic mutants to test the specific adaptive function of variation in PSMs. An important consequence of high intraspecific variation is the capacity to evolve rapidly. It is becoming increasingly clear that trait variance linked to both macro- and micro-environmental variation can also evolve and may respond more strongly to selection than mean trait values. This research, which is in its infancy in plants, highlights what could be a missing piece of the picture of PSM evolution. PSM polymorphisms are probably maintained by multiple selective forces acting across many spatial and temporal scales, but convincing examples that recognize the diversity of plant population structures are rare. We describe how diversity can be inherently beneficial for plants and suggest fruitful avenues for future research to untangle the causes and consequences of intraspecific variation.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.12526

Explaining intraspecific diversity in plant secondary metabolites in an ecological context.

Arthropod-resistant crops provide significant ecological and economic benefits to global agriculture. Incompatible interactions involving resistant plants and avirulent pest arthropods are mediated by constitutively produced and arthropod-induced plant proteins and defense allelochemicals synthesized by resistance gene products. Cloning and molecular mapping have identified the Mi-1.2 and Vat arthropod resistance genes as CC-NBS-LRR (coiled coil-nucleotide binding site-leucine rich repeat) subfamily NBS-LRR resistance proteins, as well as several resistance gene analogs. Genetic linkage mapping has identified more than 100 plant resistance gene loci and linked molecular markers used in cultivar development. Rice and sorghum arthropod-resistant cultivars and, to a lesser extent, raspberry and wheat cultivars are components of integrated pest management (IPM) programs in Asia, Australia, Europe, and North America. Nevertheless, arthropod resistance in most food and fiber crops has not been integrated due primarily to the application of synthetic insecticides. Plant and arthropod genomics provide many opportunities to more efficiently develop arthropod-resistant plants, but integration of resistant cultivars into IPM programs will succeed only through interdisciplinary collaboration.

Molecular Bases of Plant Resistance to Arthropods

Tolerance and resistance are two different plant defense strategies against herbivores. Empirical evidence in natural populations reveals that individual plants allocate resources simultaneously to both strategies, thus plants exhibit a mixed pattern of defense. In this review we examine the conditions that promote the evolutionary stability of mixed defense strategies in the light of available empirical and theoretical evidence. Given that plant tolerance and resistance are heritable and subject to environmentally dependent selection and genetic constraints, the joint evolution of tolerance and resistance is analyzed, with consideration of multiple species interactions and the plant mating system. The existence of mixed defense strategies in plants makes it necessary to re-explore the coevolutionary process between plants and herbivores, which centered historically on resistance as the only defensive mechanism. In addition, we recognize briefly the potential use of plant tolerance for pest management. Finally, we highlight unresolved issues for future development in this field of evolutionary ecology.

Juan N

Papers

The Evolution of Resistance and Tolerance to Herbivores