Escape Traits Research Articles

Water availability and plant-herbivore interactions.

Water is essential to plant growth and drives plant evolution and interactions with other organisms such as herbivores. However, water availability fluctuates, and these fluctuations are intensified by climate change. How plant water availability influences plant-herbivore interactions in the future is an important question in basic and applied ecology. Here we summarize and synthesize the recent discoveries on the impact of water availability on plant antiherbivore defense ecology and the underlying physiological processes. Water deficit tends to enhance plant resistance and escape traits (i.e. early phenology) against herbivory but negatively affects other defense strategies, including indirect defense and tolerance. However, exceptions are sometimes observed in specific plant-herbivore species pairs. We discuss the effect of water availability on species interactions associated with plants and herbivores from individual to community levels and how these interactions drive plant evolution. Although water stress and many other abiotic stresses are predicted to increase in intensity and frequency due to climate change, we identify a significant lack of study on the interactive impact of additional abiotic stressors on water-plant-herbivore interactions. This review summarizes critical knowledge gaps and informs possible future research directions in water-plant-herbivore interactions.

Leaf trait association in relation to herbivore defense, drought resistance, and economics in a tropical invasive plant

Exploring how functional traits vary and covary is important to understand plant responses to environmental change. However, we have limited understanding of the ways multiple functional traits vary and covary within invasive species. We measured 12 leaf traits of an invasive plant Chromolaena odorata, associated with plant or leaf economics, herbivore defense, and drought resistance on 10 introduced populations from Asia and 12 native populations from South and Central America, selected across a broad range of climatic conditions, and grown in a common garden. Species' range and climatic conditions influenced leaf traits, but trait variation across climate space differed between the introduced and native ranges. Traits that confer defense against herbivores and drought resistance were associated with economic strategy, but the patterns differed by range. Plants from introduced populations that were at the fast-return end of the spectrum (high photosynthetic capacity) had high physical defense traits (high trichome density), whereas plants from native populations that were at the fast-return end of the spectrum had high drought escape traits (early leaf senescence and high percentage of withered shoots). Our results indicate that invasive plants can rapidly adapt to novel environmental conditions. Chromolaena odorata showed multiple different functional trait covariation patterns and clines in the native and introduced ranges. Our results emphasize that interaction between multiple traits or functions should be considered when investigating the adaptive evolution of invasive plants.

Multienvironment QTL analysis delineates a major locus associated with homoeologous exchanges for water-use efficiency and seed yield in canola.

Canola varieties exhibit variation in drought avoidance and drought escape traits, reflecting adaptation to water‐deficit environments. Our understanding of underlying genes and their interaction across environments in improving crop productivity is limited. A doubled haploid population was analysed to identify quantitative trait loci (QTL) associated with water‐use efficiency (WUE) related traits. High WUE in the vegetative phase was associated with low seed yield. Based on the resequenced parental genome data, we developed sequence‐capture‐based markers and validated their linkage with carbon isotope discrimination (Δ13C) in an F2 population. RNA sequencing was performed to determine the expression of candidate genes underlying Δ13C QTL. QTL contributing to main and QTL × environment interaction effects for Δ13C and yield were identified. One multiple‐trait QTL for Δ13C, days to flower, plant height, and seed yield was identified on chromosome A09. Interestingly, this QTL region overlapped with a homoeologous exchange (HE) event, suggesting its association with the multiple traits. Transcriptome analysis revealed 121 significantly differentially expressed genes underlying Δ13C QTL on A09 and C09, including in HE regions. Sorting out the negative relationship between vegetative WUE and seed yield is a priority. Genetic and genomic resources and knowledge so developed could improve canola WUE and yield.

Can ‘On-Farm’ Seed Priming and Chitosan Seed Treatments Induce Host Defences in Winter Barley (Hordeum vulgare L.) under Field Conditions?

Enhancing host defences through induced resistance, disease tolerance, and/or escape, in combination with current disease management regimes may be a valuable strategy to reduce pesticide use. Since both ‘on-farm’ seed priming (OSP) and chitosan priming (CHP) have been reported to confer varying levels of host defence, this study sought to investigate their potential to deliver disease control as a strategy for sustainable management of foliar pathogens in winter barley. Field experiments were conducted to determine the effects of OSP and CHP at two different field sites using three different cultivars under fungicide/non-fungicide regimes. Overall, no evidence was found to suggest that CHP or OSP can induce effective resistance in temperate field conditions. However, these field trials enabled the identification of candidate traits to deliver disease tolerance (and escape) for the primary and secondary spread of powdery mildew, i.e., large canopies and rapid stem elongation respectively. Thus, these seed treatments may deliver disease tolerance and escape traits, but these benefits are dependent upon successful establishment and vigour first. The integration of seed treatments into sustainable crop protection may be better undertaken with spring crops or in semi-arid agriculture where the added vigour at emergence can help compensate for negative environmental interactions.

Evaluating grazing response strategies in winter annuals: A multi‐trait approach

Abstract Plants minimize fitness losses through grazing by three fundamental strategies: tolerance, avoidance and escape. Annual species have been traditionally assumed to escape grazing through their short life cycle and seed dormancy; however, their grazing response strategies remain almost unexplored. How traits and their coordination affect species' grazing responses, and whether the generalized grazing model, which posits convergent filtering by grazing and drought, is applicable to this ecologically and economically important species group thus remain unclear. We used a trait‐based approach to evaluate grazing response strategies of winter annuals from the Middle East. Across 23 species, we examined the coordination of 16 traits hypothesized to be relevant for grazing responses, and linked them to species' fecundity responses, as proxy for fitness responses, to simulated grazing in controlled conditions, to species' abundance responses to grazing in the field and to species' distribution along a large‐scale rainfall gradient. Winter annuals exhibited both grazing escape and to a lesser extent tolerance indicated by (a) independent coordination of escape and tolerance traits, and (b) maintenance of higher fecundity in species with more pronounced escape or tolerance traits under simulated grazing. In the natural habitat, species with a more pronounced escape but not tolerance strategy maintained higher abundance under grazing in dry habitats, indicating convergent favouring of escape by both grazing and drought. However, this finding at the local scale was not mirrored by a strategy shift along a large‐scale rainfall gradient. Synthesis. The convergent favouring of escape traits by grazing and drought in annuals is consistent with the generalized grazing model. This model, which has been developed for perennials based on the avoidance strategy, can thus be extended to annuals based on escape, a finding that should facilitate projecting consequences of global change in drylands dominated by annuals.

Selection on escape performance during ecological speciation driven by predation

Despite the many study systems in which predation has played a major role in phenotypic diversification and speciation, the underlying selective regimes imposed by different predator assemblages have rarely been quantified. We did so for the damselfly genus Enallagma which strongly diverged in antipredator traits when the ancestral species occupying lakes containing fish (hereafter fish lakes) repeatedly invaded fishless lakes with dragonfly larvae as top predators (hereafter dragonfly lakes). In two selection experiments in field enclosures we quantified the selection on two key escape traits of two fish-lake Enallagma species associated with survival selection by fish in the ancestral fish lakes and by dragonfly predators in the invaded fishless, dragonfly lakes. In accordance with the different hunting modes, fish imposed selection for a decreased swimming propensity while dragonfly larvae imposed selection for increased swimming speed in one of the two species. In two complementary quantitative genetic rearing experiments, we found relatively low but significant broad-sense heritabilities for both escape traits. Integrating these estimates for the selection coefficients and the heritabilities suggests that the evolutionary increase in swimming speed associated with the habitat shift may have occurred rapidly. Our study suggests that the phenotypic evolution of ecologically important traits related to habitat shifts may occur at an ecological timescale.

Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding

This paper reviews current knowledge about genes for resistance to Septoria tritici blotch (STB) of wheat, caused by Zymoseptoria tritici (formerly Mycosphaerella graminicola). These genes can be placed into two classes, although a few may have characteristics of both classes. Qualitative resistance is controlled by genes which control large fractions of genetic variation, 21 of which have been discovered and mapped so far. Most of them have been shown to be genotype-specific, being effective against the minority of Z. tritici isolates which are avirulent, and Stb6 has been shown to control a gene-for-gene relationship. Most qualitative resistances are unlikely to be durable and some formerly effective genes have been overcome by the evolution of pathogen virulence. Quantitative resistance is generally controlled by genes with small-to-moderate effects on STB. They have generally weaker specificity than qualitative genes and have provided more durable resistance. 89 genome regions carrying quantitative trait loci (QTL) or meta-QTL have been identified to date. Some QTL have been mapped at or near loci of qualitative genes, especially Stb6, which is present in several sources of resistance. Another gene of particular interest is Stb16q, which has been effective against all Z. tritici isolates tested so far. In addition to resistance, the susceptibility of wheat cultivars to STB can also be reduced by disease escape traits, some of which may be undesirable in breeding. The fundamental requirements for breeding for STB-resistance are genetic diversity for resistance in wheat germplasm and a field trial site at which STB epidemics occur regularly and effective selection can be conducted for resistance combined with other desirable traits. If these are in place, knowledge of resistance genes can be applied to improving control of STB.

High night temperature induces contrasting responses for spikelet fertility, spikelet tissue temperature, flowering characteristics and grain quality in rice.

Climate change is increasing night temperature (NT) more than day temperature (DT) in rice-growing areas. Effects of combinations of NT (24-35°C) from microsporogenesis to anthesis at one or more DT (30 or 35°C) at anthesis on rice spikelet fertility, temperature within spikelets, flowering pattern, grain weight per panicle, amylose content and gel consistency were investigated in contrasting rice cultivars under controlled environments. Cultivars differed in spikelet fertility response to high NT, with higher fertility associated with cooler spikelets (P<0.01). Flowering dynamics were altered by high NT and a novel high temperature tolerance complementary mechanism, shorter flower open duration in cv. N22, was identified. High NT reduced spikelet fertility, grain weight per panicle, amylose content and gel consistency, whereas high DT reduced only gel consistency. Night temperature >27°C was estimated to reduce grain weight. Generally, high NT was more damaging to grain weight and selected grain quality traits than high DT, with little or no interaction between them. The critical tolerance and escape traits identified, i.e. spikelet cooling, relatively high spikelet fertility, earlier start and peak time of anthesis and shorter spikelet anthesis duration can aid plant breeding programs targeting resilience in warmer climates.

Tests for the joint evolution of mating system and drought escape in Mimulus

Self-fertilizing taxa are often found at the range margins of their progenitors, where sub-optimal habitats may select for alternative physiological strategies. The extent to which self-fertilization is favoured directly vs. arising indirectly through correlations with other adaptive life history traits is unclear. Trait responses to selection depend on genetic variation and covariation, as well as phenotypic and genetic responses to altered environmental conditions. We tested predictions of the hypothesis that self-fertilization in Mimulus arises through direct selection on physiological and developmental traits that allow seasonal drought escape. Phenotypic selection on mating system and drought escape traits was estimated in field populations of M. guttatus. In addition, trait phenotype and phenotypic selection were compared between experimental wet and dry soil in two greenhouse populations each of M. guttatus and M. nasutus. Finally, genetic variation and covariation for traits were compared between wet and dry soil treatments in a greenhouse population of M. guttatus. Consistent with predictions, selection for early flowering was generally stronger than for mating system traits, and selection for early flowering was stronger in dry soil. Inconsistent with predictions, selection for water-use efficiency was largely absent; selection for large flowers was stronger than for drought escape in the field; and most drought escape and mating system traits were not genetically correlated. A positive genetic correlation between flowering time and flower size, which opposed the adaptive contour, emerged only in wet soil, suggesting that variation in water availability may maintain variation in these traits. Plastic responses to soil moisture treatments supported the idea that taxonomic divergence could have been facilitated by plasticity in flowering time and selfing. The hypothesis that plant mating systems may evolve indirectly via selection on correlated life history characteristics is plausible and warrants increased attention.

Contributions of disease resistance and escape to the control of septoria tritici blotch of wheat

The contributions of disease escape and disease resistance to the responses of wheat to septoria tritici leaf blotch (STB) were analysed in a set of 226 lines, including modern cultivars, breeding lines and their progenitors dating back to the origin of scientific wheat breeding. Field trials were located in the important wheat‐growing region of eastern England and were subject to natural infection by Mycosphaerella graminicola. STB scores were related to disease‐escape traits, notably height, leaf spacing, leaf morphology and heading date, and to the presence of known Stb resistance genes and isolate‐specific resistances. The Stb6 resistance gene was associated with a reduction of 19% in the level of STB in the complete set of 226 lines and with a 33% reduction in a subset of 139 lines of semidwarf stature. Greater plant height was strongly associated with reduced STB in the full set of lines, but only weakly in the semidwarf lines. Shorter leaf length was also associated with reduced STB, but, in contrast to earlier reports, lines with more prostrate leaves had more STB on average, probably because they tended to have longer leaves. Several lines, notably cvs Pastiche and Exsept, had low mean levels of STB which could not be explained by either escape traits or specific resistance genes, implying that they have unknown genes for partial resistance to STB.

To avoid or deter: interactions among defensive and escape strategies in sabellid worms

Numerous studies demonstrate how sessile marine organisms utilize chemical, structural, and nutritional deterrents to persist in predator-rich environments. Little is known, however, about how mobile, more behaviorally complex species minimize predation by integrating avoidance and deterrence strategies. We investigated this using sabellid polychaete worms from the Caribbean and temperate western Atlantic. Sabellids extend their feather-like radioles beyond their protective tubes for feeding and respiration; the body remains inside the tube and the radioles retract when threatened. We used co-occurring consumers to determine the palatability of radioles and bodies for each of the eight species tested. In addition, we examined chemical or structural traits affecting palatability and evaluated predator escape traits, such as tube strength, speed of radiole retraction, completeness of retraction, and sensitivity to a nearby disturbance. All species had unpalatable radioles that were chemically or structurally defended, but only two species had unpalatable bodies. Thus, most species allocated defenses to tissues that were most exposed to predation. The two species with chemically defended bodies, Bispira brunnea and Bispira variegata, relied less on behavioral escapes than the other species. Their tubes were weak, they did not retract until disturbances were very close, and B. brunnea retracted slowly and incompletely even when touched. Other species generally had stronger tubes and/or retracted when disturbances were farther away. This trade-off of deterrence versus escape even occurred within a single species when populations differed in palatability. Populations of B.variegata from North Carolina and Georgia were chemically deterrent to both temperate and tropical consumers, while populations from Panama and Florida were palatable. The more palatable Panama population retracted in response to distant movement, while the unpalatable North Carolina population did not retract until nearly touched. Thus, most species utilize a combination of predator avoidance and deterrence strategies, but more deterrent populations of species utilized avoidance less.

Rapid evolution of escape ability in Trinidadian guppies (Poecilia reticulata).

Predators are widely assumed to create selection that shapes the evolution of prey escape abilities. However, this assumption is difficult to test directly due to the challenge of recording both predation and its evolutionary consequences in the wild. We examined these events by studying natural and experimental populations of Trinidadian guppies, Poecilia reticulata, which occur in distinct high-predation and low-predation environments within streams. Importantly, in the last two decades several populations of guppies have been experimentally introduced from one type of predatory environment into the other, allowing measurements of the consequences of change. We used this system to test two hypotheses: First, that changes in predatory environments create phenotypic selection favoring changes in escape ability of guppies, and second, that this selection can result in rapid evolution. For the first test we compared escape ability of wild caught guppies from high- versus low-predation environments by measuring survival rates during staged encounters with a major predator, the pike cichlid Crenicichla alta. We used guppies from three streams, comparing two within-stream pairs of natural populations and three within-stream pairs of an introduced population versus its natural source population. In every comparison, guppies from the high-predation population showed higher survival. These multiple, parallel divergences in guppy survival phenotype suggest that predatory environment does create selection of escape ability. We tested our second hypothesis by rearing guppies in common garden conditions in the laboratory, then repeating the earlier experiments using the F2 generation. As before, each comparison resulted in higher survival of guppies descended from the high-predation populations, demonstrating that population differences in escape ability have a genetic basis. These results also show that escape ability can evolve very rapidly in nature, that is, within 26-36 generations in the introduced populations. Interestingly, we found rapid evolutionary loss of escape ability in populations introduced into low-predation environments, suggesting that steep fitness trade-offs may influence the evolution of escape traits.