To defend against predators, insects often modify their morphology, flexibly, to enhance survival and reproductive advantages. Here, we report that predation risks from either isolated predator or predator odor cues, induce a higher proportion of nymphs to developed into long-winged females among the parent generation, as well as among F1 generation offspring. Surprisingly, these previously threatened long-winged adults survived better when attacked by a predator owing to the enhanced agility level gained from risk experience. The long wing, and increased agility level, provide adaptive benefits for SBPHs to escape from predation and so are able to go on to reproduce.
SBPHs responded more strongly to the caged predators (visual + odor risk cues) and predator odor cues, than just the visual cue of the predator. Different risk cues can elicit different levels of responses in prey33,34,35,36. For example, in the case of the Colorado potato beetle, volatile odor cues from the predator stronger reduced the beetle feeding on plants than predator visual and tactile cues35. But a visual cue has been shown to be crucial for insect pollinators detecting and avoiding flowers with predators37. Insect herbivores frequently communicate via chemical odors33,38. Exploiting the odor cue to perceive the presence of predators should have advantages, because the odor cue can be sensed from a long distance and penetrate the blocking effect of foliage or canopy structure39, enabling the prior detection of risks and the preparation of antipredation behaviors.
In densely planted rice paddies, the active foraging behavior of rove beetle may serve as a selective pressure favouring the development in SBPHs of a chemical instead of visual pathway to detect the approach of a rove beetle. However, in the F1 generation, the influence of a predator odor cue on the proportion of winged forms was weaker than that of caged predators, indicating the combined effects of odor and visual cues might be stronger than only an odor cue, suggesting that visual cues cannot be ignored. In our experiments, sealed predator cadavers may have weakened the visual cue of the rove beetles, because the lack of motion did not fully represent the normal visual cue.
SBPHs frequently exhibit wing plasticity in response to population density and food quality28,29. When nymph density is higher, or food has deteriorated, a higher proportion of macropters will arise28,29. The development of the winged form is thought to be a strategy for SBPHs to emigrate from inhospitable environments. However, we assumed, predation risks could also induce the occurrence of the winged form, because long wings might enable SBPHs to escape from predation. As expected, the results presented here show that a higher proportion of long-winged females and their offspring arose when nymphs or adults were previously exposed to predation risk, demonstrating that SBPHs can express morphologically plastic defenses in response to prior predation risk. Additionally, the higher proportion of wing forms was not only due to the increasing number of winged females (see Fig. 1, the number of winged females in “caged rove beetle” treatment was lower), but also the increasing proportion of winged females among female groups (the decreasing numbers and proportions of wingless females, Fig. 1). To date, similar patterns have only been shown in pea aphids, in which when predation risk (foot prints from lady beetles) is higher during the parent generation, a higher proportion of winged morphs arise in the offspring40,41. In our experiments, we tested the risk effects passing from nymphs to adults and from parents to their offspring with combined risk cues, an odor cue or a visual cue, which better reveals the capacity for flexible defense strategies within SBPHs and the nature of predation risks in the perpetual ‘arms race’ against predation. This is the first example of how insects can express both within- generational and transgenerational morphological plasticity as a defense strategy in response to prior predator threat, and we suggest that this phenomenon is likely to occur more widely.
However, SBPHs do not only face a single lethal pressure from their environment as we discussed above. Nymph density, food quality, even the temperatures or photoperiods may play or interplay roles in the induction of wing plasticity in SBPHs28,29. In these situations, the responses of SBPHs may differ from present results, or opposite results can occur. As an example, the growth rates of snails vary depending on snail densities, food supply and the strength of predation risks. Growth rates were higher when snails were reared on high nutrients and in low densities, but decreased steeply as the predation risk increased. Conversely, the growth rate was lower at high densities and with high predation risk, but increased as nutrient availability increased42. As for SBPHs, the proportion of winged adults may be higher if we reared in higher densities combined with high predation risk, or may be lower if the nutrient condition of the rice plants increases (for example, higher fertilizer inputs benefit the development of planthoppers43) and predators are removed. This hypothesis needs to be tested. Further, the rice plant phenotypes (resistant or sensitive phenotypes) are important to the development of planthoppers or leafhoppers44,45,46, and tests of the interactive effects of plant phenotype, plant quality/quantity, nymph density and predation risk on the wing plasticity of SBPHs should provide insights into the evolution of insects within changing environments.
Induced transgenerational defense plasticity as shown in SBPHs may be common in many organisms20,47. It allows parents to transfer their risk experience to offspring and promotes their evolutionary fitness20. When SBPH nymphs are exposed to predation risk, they are likely to develop into long-winged females, because it is an advantageous form for them in the current risk environment. However, such predation risk is variable in time and space, and SBPH parents cannot predict when or whether the predators will disappear. Thus, an appropriate strategy to enhance the survival rate of offspring in an unpredictable environment is to continue producing a higher proportion of long-winged forms. Within-generational and transgenerational plasticity of defense should be a successful adaptive defense strategy for SBPHs, given that rove beetle and other groups of predators such as predatory spiders are abundant all around the year in rice paddies.
The higher mortality of SBPH nymphs when they experience predation risk, has been broadly addressed before24,48,49. Reduced food intake during risk periods may contribute to this poorer survival outcome, because insects are likely to alter their feeding behavior50,51, or shift from a high-risk host to a safer, but nutritionally inferior, one52, when they detect the presence of predators. However, we did not observe an apparent behavior change in threatened nymphs in our experiments, even those going on to be macropters, compared to the non-threatened ones. For example, changing feeding location, non-feeding related motility, an increase in jump frequency, etc. did not occur in threatened nymphs. Thus, behavior plasticity seems not to be invoked to explain this phenomenon. However, considering the food consumption of sap-sucking SBPHs is difficult to determine, experiments employing electrical penetration graph (EPG) techniques should be conducted to quantify the amounts of sap consumption during risk periods53. This will help to explain whether the higher mortality is due to a change of feeding behavior (less food intake). Furthermore, some obscure internal physiological plasticity may also cause the higher mortality of SBPH nymphs at risk. For example, increased oxidative damage and decreased assimilation efficiency during the risk period may weaken the survival success of SBPH nymphs. Unfortunately, few studies have verified this assumption, although it has been shown that different assimilation efficiencies may arise under predation risk17, or oxidative damage may be induced by predation risk resulting in a slower growth rate54 and decreased escape performance55.
SBPHs exhibit sexual differences in both with- and trans- generational morphological plasticity in relation to defense, i.e., threatened nymphs/parents are more likely to develop into long-winged females, due to the different vulnerability of females and males to predation. This predation difference is particularly acute between short-winged females and males, given that the proportion of short-winged females is lower than that seen in control settings (Fig. 1), and we assume the level of vulnerability may depend on their body size and reproductive role. The body sizes of short-winged females are larger than those of long-winged females or males, causing them to be more vulnerable to predation because they are more highly preferred targets for predator. Also, the short-winged female needs to stay and deposit eggs in the bare rice stem, which increases the time window of exposure to predators while, by contrast, long-winged males are slim and are not required to lay eggs, and so should be not be heavily predated. It follows that short-winged females should be more vulnerable to predation than long-winged females or males. Hence, in SHPBs, increasing the proportion of long-wing females in a population creates greater opportunities to migrate to predator-free habitats for reproduction, while at the same time reducing their vulnerability to predation. We hypothesize that the sexual difference in responses should be adaptive, and might be inheritable if predation pressure frequently favors the long-winged forms among populations over multiple generations.
Results presented here also show that previously threatened long-winged offspring survived better than previosuly non-threatened ones when attacked by P. fuscipes. Studies suggest prey-altered morphology in response to predation risks should confer a survival advantage (fitness gained), i.e., a better-developed defensive structure13,24, or refuge in having a larger size that increase survival success57. However, wings themselves are without protective functions for SBPHs, as seen in pea aphids41. Thus, we setup behavioral experiments to reveal how threatened long-winged adults may increase their survival when attacked by a predator. Results show threatened long- winged offspring (but not parents) are more active, and respond more quickly, than unthreatened ones, i.e., a higher number of attacks are needed for P. fuscipes to capture a previously threatened long-winged offspring than one that has not been threatened before. We suggest the increased agility level is not because of the long wing itself, but due to the enhanced muscle strength in the legs of long-winged adults, because in our observation, long-winged adults avoid attack mainly by jumping but not by flight, probably because a jump needs less reaction time than flight.
We only observed transgenerational plasticity of induced behavioral defense in SBPHs. This generational difference (within- and trans-generational) in behavioral defense in SBPHs may reflect potential carry-over effects from parents. To our knowledge, the generational difference in defense has rarely been shown in insects, though in pea aphids a fluctuating expression of transgenerational defensive traits (long wing) over generations when predation risk was present or absent has been reported58. We also expect there will be cumulative effects59 accumulated by SBPHs from the parent generation to the F1 generation. However, we are not certain whether these effects exist in our experiments. To determine this, experiments examining defensive traits across multigeneration should be conducted.
However, if predation risk increases the number of agile, long-winged SBPH adults, which are of benefit in respect of dispersal, migration, and thus spreading rice viruses, the application of P. fuscipes in biological control appears ultimately to weaken the control effectiveness. Also, a study with field experiments found that predatory ladybugs increase the number of dispersed aphid nymphs, especially in plants with lower resistance. However, surprising results show that the higher number of dispersed aphid nymphs will not necessarily translate into population growth because dispersed aphids are weak (less food intake) and more easily predated by predators60. Thus, the benefits of anti-predator defense in aphids will, over time, translate into negative developmental costs that suppress the aphid population. As for SBPHs, threatened long-winged females perform well in dispersal and defense, but worse in development and reproduction. Recent experiments reveal that previously threatened long-winged females have a longevity that is three days shorter, and produces about 60 fewer eggs per female, than non-threatened long-winged females (unpublished data). Consequently, these negative effects would eventually translate into lower population growth rates within SBPHs. Thus, the introduction of the predation risk from P. fuscipes to control SBPHs is workable, since field experiments in controlling western flower thrips and grasshoppers by exposure to predation risk have been successful49,61, and the main purpose of biological control is to suppress the pest population beneath the relevant economic threshold, and reduce plant mass loss without necessarily eliminating the pest altogether.
This study advances the importance of predation risk on the induction of flexible anti-predation defenses in insect parents and their offspring, uncovers the mediating mechanisms, shows how this anti-predation defense expresses differently between sexes, and further explores the adaptation significance of these defense traits for insects exposed to unpredictable environments. These findings should prove important for predicting SBPH migration or dispersal, conducting effective pest control, and better understanding prey-predator interactions. However, future work should examine the effects of predation risks from other groups of predators or parasites on the physiological and behavioral plasticity of SBPHs.
Source: Ecology - nature.com
