Background: Drought may become one of the greatest challenges for cereal production under future warming scenarios, and its impact on insect pest outbreaks is still controversial. To address this issue, life-history responses of the English grain aphid, Sitobion avenae (Fabricius), from three areas of different drought levels were compared under three water treatments. Results: Significant differences were identified in developmental time, fecundity and adult weight among S. avenae clones from moist, semiarid and arid areas under all the three water treatments. Semiarid and arid area clones tended to have higher heritability for test life-history traits than moist area clones. We identified significant selection of water- deficit on the developmental time of 1st instar nymphs and adult weight for both semiarid and arid area clones. The impact of intermediate and severe water-stress on S. avenae’s fitness was neutral and negative (e.g., decreased fecundity and weight), respectively. Compared with arid-area clones, moist- and semiarid-area clones showed higher extents of adaptation to the water-deficit level of their respective source environment. Adult weight was identified as a good indicator for S. avenae’s adaptation potential under different water-stress conditions. After their exposure to intermediate water-deficit stress for only five generations, adult weight and fecundity tended to decrease for moist- and semiarid-area clones, but increase for arid-area clones. Conclusions: It is evident from our study that S. avenae clones from moist, semiarid and arid areas have diverged under different water-deficit stress, and such divergence could have a genetic basis. The impact of drought on S. avenae’s fitness showed a water-level dependent pattern. Clones of S. avenae were more likely to become adapted to intermediate water-deficit stress than severe water-deficit stress. After continuous water-deficit stress of only five generations, the adaptation potential of S. avenae tended to decrease for moist and semiarid area clones, but increase for arid area clones. The rapid shift of aphids’ life-history traits and adaptation potential under drought could have significant implications for their evolutionary dynamics and outbreak risks in future climate change scenarios. Keywords: Drought, Water-deficit stress, Global warming, Life-history traits, Genetic divergence, Adaptation potential Background has increased by at least 1.1 °C over the past several dec- Climate change is evident with increasing occurrences of ades till 2007 . The warming trend has been especially weather extremes like heat waves and dry spells around evident in northwestern China, where the frequency of the globe in recent years according to the report of the dry spells has showed an increase of 19% in the 20th cen- Intergovernmental Panel on Climate Change (IPCC) . tury as compared with the previous couple of centuries In China, the annual average atmospheric temperature (1650–1859) . Increasing frequency and intensity of drought from the global warming trend can have significant impacts *Correspondence: email@example.com on plant growth, morphology and physiology . The State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, Shaanxi Province, China changing growth and physiology of plants under drought Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Liu et al. BMC Ecol (2018) 18:17 Page 2 of 15 conditions can in turn have bottom-up effects on the been rare [19, 20]. Thus, S. avenae clones from moist, abundances and outbreaks of insect pests, and such semiarid and arid areas in northwestern China were col- effects depend on many factors such as plant type, herbi - lected and tested in the laboratory. We hypothesize that vore species, feeding guild, and stress intensity and dura- S. avenae clones from these areas have differentiated in tion [5–13]. Drought may also alter the feeding behaviors life-history traits, and the extents of adaptation of these of herbivorous insects [14, 15], as well as omnivorous clones to water-deficit conditions can increase after insects [16, 17]. Due to their sensitivity to plant water exposure to continuous water-deficit stress for a relatively status changes, phloem sap feeders such as aphids are long period of time. The objectives of our study are to: (1) considered as being susceptible to negative impacts of characterize life-history trait (e.g., developmental dura- drought conditions, and their strong responses in life- tion, fecundity and adult weight) differentiation among history to drought are often expected [9, 18, 19]. Thus, these populations under three water-stress treatments; frequent occurrences of extreme events such as drought (2) explore the changing pattern of population differen - in the context of global climate change could alter many tiation after water-stress exposure for five generations of biological parameters (e.g., developmental duration and S. avenae; and (3) evaluate the adaptation potential for S. fecundity) and population dynamics of aphids in agricul- avenae clones under water-deficit conditions both before tural and forest ecosystems [20, 21]. For examples, many and after water-deficit exposure of five generations. studies have explored the effects of drought intensity on aphid population growth in terms of 7–10 d fecundity [9, Results 22, 23]. A few studies have started to focus on changes Comparison of life‑history traits in developmental durations of nymphs and generation Population source, water treatment, clone nested in time for aphids under water-deficit stress [20, 24], as population source, and interactions between the first well as the effects of continuous drought lasted for mul - two factors all showed significant effects on DT5 (the tiple aphid generations . However, the impacts of total developmental time of nymphs), 10 d fecundity drought on plant-aphid interactions and aphid outbreaks and adult weight of S. avenae clones (Table 1). Popula- have been hard to predict [4, 20]. Modified plant physi - tion source accounted for 0.8–4.9% of the total variance ology under drought has been found to have positive, of the abovementioned traits for generation one, whereas negative or neutral consequences on the performance it explained 3.6–10.1% for generation five. The variance of aphids [18, 22, 25–27]. Therefore, it remains contro - from water treatments constituted 5.1–10.7% and 5.5– versial whether water-deficit stresses can increase aphid 15.4% of the total variance of each trait for generation outbreaks, even though several hypotheses (e.g., ‘plant one and five, respectively. Interactions between popula - stress hypothesis’, ‘plant vigor hypothesis’, and ‘pulsed tion source and water treatment contributed little to the stress hypothesis’) [21, 28, 29] have been suggested to total variance (generation one: 1.0–3.2%; generation five: explain the conflicting results in terms of aphid popula - 0.8–4.2%). Clone (nested in population source) explained tion dynamics under drought. a significant proportion of the total variance for all tested Northwestern China provides a good scenario to traits (generation one: 36.5–42.9%; generation five: 18.1– address this issue. Firstly, drought events have become 36.3%). Clone and population source together accounted more frequent and intense in this part of China in the for 37.3–47.8% of the total variance for each trait at gen- context of the global climate change . Secondly, the eration one, whereas they contributed 27.8–39.9% to the cereal aphid, Sitobion avenae (Fabricius), is the predomi- total at generation five. nant grain pest in northwestern China [31–33], and Significant differences in developmental durations of increasingly severe damage of this aphid to cereal pro- 1st to 4th instar nymphs (DT1 to DT4) and DT5 for S. duction seems to be coincident with the warming trend avenae clones were found among their source areas (i.e., in this part of China [34, 35]. In our previous study, we moist, semiarid and arid) in many cases, and they tended compared life-history responses under well-watered to be prolonged with increasing water-deficit levels in and moderately water-stressed treatments for S. avenae the source areas: (1) At generation one, semiarid area clones from semiarid and moist areas of the Shaanxi clones showed a longer DT1 under intermediate water Province . Since severe drought incidents are increas- stress than moist area clones (Fig. 1a; F = 3.29; df = 2, ingly frequent in northwestern China [20, 30], this study 843; P < 0.05); (2) When tested at generation five, DT2 of is expanded to include arid areas in both Shaanxi and moist area clones was shorter under well-watered condi- Gansu Provinces, and a third water treatment (i.e., severe tions than that of semiarid or arid area clones (Fig. 1b; water stress) is incorporated into the experiment. In addi- F = 58.76; df = 2, 843; P < 0.001), but this pattern was not tion, studies on evolutionary dynamics of plant–insect found in DT3 (Fig. 1c); (3) At generation five, DT4 of arid interactions under relatively long-term water-stress have area clones was longer under well-watered conditions Liu et al. BMC Ecol (2018) 18:17 Page 3 of 15 Table 1 Estimates of variance components for life-history traits of Sitobion avenae populations Traits Generation Variance source df F P % total DT5 1st Source 2 6.4 0.002 0.8 Treatment 2 53.8 < 0.001 6.8 Source × treatment 4 11.5 < 0.001 2.9 Clone (source) 98 5.9 < 0.001 36.5 Error 843 – – 53.0 5th Source 2 65.7 < 0.001 9.7 Treatment 2 39.9 < 0.001 5.9 Source × treatment 4 14.1 < 0.001 4.2 Clone (source) 98 2.5 < 0.001 18.1 Error 843 – – 62.2 10-d Fecundity 1st Source 2 50.8 < 0.001 4.9 Treatment 2 111.8 < 0.001 10.7 Source × treatment 4 5.1 < 0.001 1.0 Clone (source) 98 9.1 < 0.001 42.9 Error 843 – – 40.5 5th Source 2 36.6 < 0.001 3.6 Treatment 2 157.3 < 0.001 15.4 Source × treatment 4 17.7 < 0.001 3.5 Clone (source) 98 7.6 < 0.001 36.3 Error 843 – – 41.3 Adult weight 1st Source 2 27.4 < 0.001 3.2 Treatment 2 43.9 < 0.001 5.1 Source × treatment 4 13.8 < 0.001 3.2 Clone (source) 98 6.9 < 0.001 39.3 Error 843 49.1 5th Source 2 77.3 < 0.001 10.1 Treatment 2 42.0 < 0.001 5.5 Source × treatment 4 3.2 0.012 0.8 Clone (source) 98 4.5 < 0.001 28.7 Error 843 – – 55.0 Main effects of population source (source), water stress treatments (treatment), clone nested in source and interactions are shown; DT5, total developmental time of the nymphal stage; significant effects highlighted in italics than that of moist or semiarid area clones (Fig. 1d; well-watered conditions than under both water-deficit F = 8.61; df = 2, 843; P < 0.001); (4) When tested at gen- treatments (Fig. 1b; F = 7.95; df = 2, 843; P < 0.001); (2) eration five, moist area clones had a shorter DT5 under A longer DT3 was found with increasing water-deficit any water-stress treatment than arid area clones (Fig. 2a; levels for moist area clones when tested at generation F = 65.66; df = 2, 843; P < 0.001). one (Fig. 1c; F = 29.57; df = 2, 843; P < 0.001); (3) At gen- The developmental time of each nymphal instar of S. eration one, moist area clones had a higher DT4 under avenae showed a tendency to increase under treatments the severely stressed treatment compared with the well- with increasing water-deficit stress: (1) At generation watered or intermediately stressed treatment (Fig. 1d; one, semiarid area clones showed a shorter DT2 under F = 3.14; df = 2, 843; P < 0.05); (4) Moist and semiarid area (See figure on next page.) Fig. 1 Comparisons of developmental time for 1st and 5th generation Sitobion avenae clones under three treatments. DT1 to DT4 (a–d), the developmental time of 1st to 4th instar nymphs; WW, well-watered treatment; IS, intermediate water deficit; SS, severe water deficit; data with different uppercase and lowercase letters indicate significant differences (α = 0.05, ANOVA followed by Tukey tests) among treatments for generation one and five, respectively; stars in bars indicate significant differences between generation one and five within a treatment for a particular area (*P < 0.05; **P < 0.01; ***P < 0.001) Liu et al. BMC Ecol (2018) 18:17 Page 4 of 15 Liu et al. BMC Ecol (2018) 18:17 Page 5 of 15 clones showed a higher DT5 with increasing water deficit were found between moist and arid area clones at gen- levels for both generation one (Fig. 2a; F = 53.80; df = 2, eration one, but arid area clones had higher adult weights 843; P < 0.001) and five (F = 39.89; df = 2, 843; P < 0.001). than moist area clones under any water treatment when Significant differences in the developmental time of tested at generation five. At generation one, semiarid S. avenae clones were identified after their exposure to area clones tended to have higher adult weights than arid intermediate water-deficit stress for five generations. area clones under the three water treatments, but little Compared with generation one, DT1 of semiarid area differences were found between them at generation five. clones was prolonged under severe water stress at gener- When tested at generation one, moist area clones under ation five (Fig. 1a; F = 16.00; df = 1, 149; P < 0.001). Simi- intermediate water stress had a higher weight than under larly, DT3 increased under intermediate water stress for severe water stress (F = 43.93; df = 2, 843; P < 0.001). At semiarid area clones at generation five (Fig. 1c; F = 9.03; both generations, weights of semiarid area clones under df = 1, 149; P < 0.01), and DT4 was extended at generation the well-watered or intermediately stressed treatment five for semiarid (Fig. 1d; F = 19.94; df = 1, 149; P < 0.001) were higher than those under the severely stressed treat- and arid (F = 22.95; df = 1, 201; P < 0.001) area clones ment (F = 42.01; df = 2, 843; P < 0.001). For both genera- under severe water stress. In comparison to generation tion one and five, arid area clones showed a higher weight one, DT5 also increased at generation five for semi - under well-watered conditions than under severe water arid (Fig. 2a; F = 12.01; df = 1, 149; P < 0.001) and arid stress. Compared with generation one, moist and semi- (F = 8.34; df = 1, 201; P < 0.01) area clones under severe arid area clones showed a lower weight under all three water stress. Thus, the developmental times of S. avenae water stress treatments at generation five (e.g., moist clones tended to increase after their water-deficit expo - area clones under well-watered conditions, F = 11.79; sure for only five generations. df = 1, 180; P < 0.001). However, arid area clones showed At generation one, moist area clones tended to have a a higher weight at generation five than at generation one higher 10-d fecundity than semiarid or arid area clones under well-watered (F = 4.19; df = 1, 203; P < 0.05) and under any of the water treatments (Fig. 2b; F = 50.76; intermediately stressed (F = 14.09; df = 1, 201; P < 0.001) df = 2, 843; P < 0.001). They showed a lower fecundity treatments. than semiarid or arid area clones at generation five under all water treatments except severe water stress (F = 36.59; Differences in broad‑sense heritability of life‑history traits df = 2, 843; P < 0.001). Fecundities of moist area clones Compared with generation one, the life-history trait under well-watered and intermediately stressed condi- heritability of S. avenae clones from moist areas tions were higher than those under severely stressed con- increased at generation five for DT1, DT3, fecundity ditions for both generation one (F = 111.84; df = 2, 843; and weight, but decreased for DT2 and DT4 (Table 2). P < 0.001) and five (F = 157.31; df = 2, 843; P < 0.001), and When tested at generation one, semiarid area clones the same patterns were found for semiarid and arid area showed significant heritabilities for all tested traits clones. Compared with generation one, moist and semi- but DT4. Compared with generation one, these clones arid area clones showed a decrease in fecundity at gen- showed decreased heritabilitiy for DT2 and DT3, but eration five in all cases except for semiarid area clones increased heritability for DT4 at generation five. Sig- under intermediately stressed conditions, whereas arid nificant heritabilities for arid area clones were iden- area clones showed an increase in fecundity under severe tified in DT1, DT5, fecundity and weight at both water stress at generation five (F = 9.79; df = 1, 201; generations. Overall, S. avenae clones of semiarid and P < 0.01). arid areas tended to have more life-history traits with For both generation one (Fig. 2c; F = 27.44; df = 2, 843; significant heritabilities than those of moist areas. P < 0.001) and five (F = 77.30; df = 2, 843; P < 0.001), moist After their exposure to five generations of water-def- area clones tended to have lower adult weights than icit stress, the heritability of certain life-history traits semiarid area clones under all water treatments except tended to increase for moist area clones, but decrease severe water stress. Little differences in adult weight for semiarid area clones. (See figure on next page.) Fig. 2 Comparisons of DT5, fecundity and adult weight for different Sitobion avenae clones under three treatments. DT5, (a); 10-d fecundity, (b) ; adult weight, (c); DT5, total duration of the nymphal stage; WW, well-watered treatment; IS, intermediate water deficit; SS, severe water deficit; data with different uppercase and lowercase letters indicate significant differences (α = 0.05, ANOVA followed by Tukey tests) among treatments for generation one and five, respectively; stars in bars indicate significant differences between generation one and five within a treatment for a particular area (*P < 0.05; **P < 0.01; ***P < 0.001) Liu et al. BMC Ecol (2018) 18:17 Page 6 of 15 Liu et al. BMC Ecol (2018) 18:17 Page 7 of 15 Table 2 Broad-sense heritability for life-history traits of Sitobion avenae clones from moist, semiarid and arid areas Traits Moist area clones under WW Semiarid area clones under IS Arid area clones under SS G1 G5 G1 G5 G1 G5 DT1 0.333 0.402* 0.467** 0.396* 0.400* 0.426* DT2 0.500* 0.300 0.571** 0.212 0.333 0.376 DT3 0.200 0.401* 0.452* 0.337 0.403* 0.327 DT4 0.500* 0.189 0.316 0.560** 0.200 0.441* DT5 0.353 0.356 0.644** 0.571** 0.429* 0.452* Fecundity 0.014 0.501** 0.592** 0.522** 0.751*** 0.745*** Weight 0.018 0.468** 0.738*** 0.568** 0.590** 0.455* DT1–DT4 the developmental time of 1st to 4th instar nymphs, DT5 the total developmental time of nymphs, WW well-watered treatment, IS intermediate water stress, SS severe water stress, G1 generation one, G5 generation five; the statistical significance of broad-sense heritabilities evaluated with likelihood-ratio tests (LRTs); *P < 0.05; **P < 0.01; ***P < 0.001 Adaptation index and its correlation with test life‑history to generation one, S. avenae clones of all the three areas traits presented no significant changes in adaptation indices at At generation one, S. avenae clones from both moist generation five (F = 1.28; df = 1, 161; P = 0.26). and semiarid areas showed higher adaptation indices At generation one, the adaptation indices of moist than those from arid areas (Fig. 3; F = 26.61; df = 2, 35; area clones correlated only with weight among all P < 0.001), but no significant differences in adaptation test life-history traits (Table 3; r = 0.7009, P < 0.001). indices were found between moist and semiarid area When tested at generation five, adaptation indices of clones. At generation five, the adaptation index of moist these clones correlated to DT4 (r = − 0.3623, P < 0.05), area clones was lower than that of semiarid area clones, prin3 (the third factor of PCA) (r = − 0.3893, P < 0.05) but higher than that of arid area clones. In comparison and weight (r = 0.4957, P < 0.01). At generation one, Fig. 3 Adaptation indices of 1st and 5th generation clones of Sitobion avenae from three areas. X > 0, X = 0, and X < 0 means better, equal, and ad ad ad worse performances, respectively, for S. avenae clones under the original water level (e.g., well-watered for moist area clones), compared with those under alternative water levels (e.g., intermediately or severely stressed for moist area clones) Liu et al. BMC Ecol (2018) 18:17 Page 8 of 15 semiarid area clones showed positive correlations clones at generation five (Table 4). Under intermedi- between adaptation indices and weight (r = 0.4409, ate water stress, selection differentials of semiarid area P < 0.05), but negative correlations between adapta- clones were positive for DT1 and adult weight, but neg- tion indices and prin2 (r = − 0.3680, P < 0.05). At gen- ative for DT3 at generation five. The selection gradients eration five, the extent of adaptation for semiarid area for these clones were significantly positive or negative clones was negatively correlated to DT3 (r = − 0.5710, for all traits but DT1. Severe water stress showed rela- P < 0.001), but it was positively correlated to weight tively little selection for life-history traits of arid area (r = 0.6895, P < 0.001). The adaptation index for arid clones at generation five, and significant selection coef - area clones was significantly correlated with DT2 ficients included the differential of adult weight, and (r = − 0.3215, P < 0.05), DT5 (r = − 0.3464, P < 0.05), the gradients of DT1 and adult weight. weight (r = 0.7850, P < 0.001), prin2 (r = − 0.3575, P < 0.05) and prin3 (r = -0.3568, P < 0.05) at generation Discussion one, but it was only correlated with adult weight at gen- Divergence and adaptation of S. avenae clones eration five (r = 0.6763, P < 0.001). In this study, significant differences in developmen - tal time, 10-d fecundity and adult weight were found among S. avenae clones from moist, semiarid and arid Selection coefficients for life‑history traits areas under any of the three water treatments at gen- Under well-watered conditions, moist area clones of S. eration one of these clones. For examples, at generation avenae showed significant differentials for DT5 (nega - one, arid area clones of S. avenae had significantly lower tive) and weight (positive), and the only significant fecundities than moist area clones under any of the three selection gradient was found for adult weight of these water treatments, and they also had lower adult weight Table 3 Correlations between habitat adaptation indices and life-history traits for Sitobion avenae clones from three areas Traits Moist areas Semiarid areas Arid areas G1 G5 G1 G5 G1 G5 DT1 − 0.1865 − 0.0152 − 0.0585 0.2929 − 0.2271 − 0.1717 DT2 − 0.1885 − 0.1076 0.0471 0.2287 − 0.3215* 0.2524 DT3 − 0.1707 0.0489 − 0.2031 -0.5710*** 0.0866 − 0.0568 DT4 0.2304 − 0.3623* 0.0892 0.0755 -0.2007 − 0.1650 DT5 − 0.1423 − 0.2500 − 0.0704 -0.0378 -0.3464* − 0.0874 Adult weight 0.7009*** 0.4957** 0.4409* 0.6895*** 0.7850*** 0.6763*** Prin1 − 0.0134 0.1795 − 0.2606 − 0.1798 0.1584 − 0.0301 Prin2 − 0.0311 0.1020 − 0.3680* − 0.0156 − 0.3575* 0.0213 Prin3 0.1402 − 0.3893* − 0.0414 − 0.2761 − 0.3568* − 0.0850 DT1–DT4 the developmental time of 1st to 4th instar nymphs, DT5 the total developmental time of nymphs, G1 1st generation, G5 5th generation; prin1 to prin3, the first three principal components extracted in PCA; *P < 0.05; **P < 0.01; ***P < 0.001 Table 4 Selection differentials and gradients for life-history traits of 5th generation Sitobion avenae clones under water- stress Traits Moist area clones under WW Semiarid area clones under IS Arid area clones under SS Differential Gradient Differential Gradient Differential Gradient DT1 − 0.1153 − 0.0767 0.2413* 0.0492 − 0.1183 − 0.1634* DT2 − 0.0476 − 0.1061 − 0.0674 − 0.3119*** 0.1604 0.1133 DT3 − 0.0215 − 0.0654 − 0.2610* − 0.2764** − 0.0233 0.1138 DT4 − 0.1534 − 0.1620 0.0539 − 0.1801* − 0.0702 0.0271 DT5 − 0.2048* − 0.1462 − 0.0430 − 0.2228** − 0.0272 0.0459 Weight 0.4737*** 0.4548*** 0.6801*** 0.7346*** 0.6839*** 0.6888*** DT1–DT4 the developmental time of 1st to 4th instar nymphs, DT5 the total developmental time of nymphs, WW well-watered treatment, IS intermediate water stress, SS severe water stress; *P < 0.05; **P < 0.01; ***P < 0.001 Liu et al. BMC Ecol (2018) 18:17 Page 9 of 15 than semiarid area clones under well-watered and inter- from arid areas. This makes sense since severe water mediately stressed conditions. DT1 and DT4, but not stress in arid areas can cause relatively more extinc- DT2 or DT3, tended to be prolonged with increasing tion events of local aphid clones that obliterate locally water-deficit stress, and this was especially apparent for adapted gene pools , and the extinction-recoloni- moist and semiarid area clones. These results indicated zation cycles can be unfavorable to the occurrence of that S. avenae clones from the three areas had evidently local adaptation for arid area clones. Compared with arid diverged response to water-deficit stress. In addition to area clones, semiarid area clones presented higher adult 10-d fecundity, various reproductive parameters (e.g., weight under intermediate water stress at generation net reproductive rate, lifetime fecundity, and reproduc- one. This indicates that semiarid area clones should have tive time) presented significant differences between higher adaptation potential under moderate water stress moist and semiarid area clones of S. avenae under inter- than arid area clones, since adult weight is shown to be mediate water stress in our previous study , provid- the best indicator of adaptation potential of S. avenae ing more evidence of population differentiation between clones in this study. Such results add another line of evi- both areas. Although non-genetic environmental effects dence that the occurrence of local adaptation is common (e.g., maternal effects and phenotypic plasticity) could for this aphid [34, 37]. The identified changes in adapta - contribute to the abovementioned differences in S. ave - tion potential of S. avenae clones from the three areas at nae’s life-history characters, such confounding effects generation one suggest that some genotypes of this aphid were minimized through rearing all test aphid clones in might have become adapted to particular drought condi- common laboratory conditions for two to three genera- tions in the field. Further studies with multiple microsat - tions before the initiation of our experiments [36, 37]. ellites are required to confirm this, especially for those S. u Th s, the identified differences among S. avenae clones avenae clones from moist and semiarid areas. from the three areas with different drought levels could have a genetic basis. Indeed, 18.1–42.9% of the total vari- Eec ff ts of relatively longer‑term water‑deficit exposure ation for test life-history characters of S. avenae clones In the present study, S. avenae clones of moist, semi- was explained by clone (nested in source) alone in the arid and arid areas all showed rapid changes in life-his- ANOVA, showing substantial genotypic effects. In our tory characters after they were kept under intermediate previous study, clone also explained an apparently high water-deficit stress for only five generations. In compari - proportion (i.e., 35.79–83.22%) of the total variance for son to generation one, moist area clones of generation each life-history trait (e.g., fecundity, reproductive time, five showed a significant decrease in the total develop - and adult lifespan) . In addition, S. avenae clones mental time of nymphs under intermediate and severe from semiarid and arid areas at generation one tended to water stress, indicating a benefit for these clones after have higher heritability (meaning higher possibility of off - exposure to water-deficit stress for five generations. spring inheritance) for test life-history traits than those Despite this benefit, these clones had declined fecundity from moist areas in this study. This provides another line and adult weight at generation five under any of the water of evidence that a significant proportion of the life-his - treatments, and the adaptation extent of these clones to tory differentiation among S. avenae populations from well-watered conditions did not change at generation areas of different drought levels can be attributed to five. This suggests that some of these clones might have genetic factors. Thus, genetic divergence among S. ave - adapted to moist conditions in their source area after nae clones from the three areas could have occurred. long-term exposure in the field. Compared with gen - The potential genetic divergence among S. avenae eration one, semiarid area clones of generation five had clones from moist, semiarid and arid areas also means increased developmental time of nymphs under severe that these clones may experience substantial selective water stress, reduced fecundity under well-watered and pressure under drought in the field. Indeed, we found severely stressed conditions, and reduced adult weight consistently negative selection of intermediate water under all three water treatments, showing significantly stress on DT4 for semiarid area clones in the current and negative impact of water-deficit stress that lasted for previous study , and consistently positive selection of only five generations. However, the adaptation extent of well-watered and intermediately stressed conditions on these clones to intermediate water stress showed no sig- daily fecundity of different S. avenae clones from moist nificant changes between generation one and five. This and semiarid areas in the previous study . Therefore, makes sense since these clones may have been subjected it is not unexpected in this study that S. avenae clones to intermediately water-stressed conditions in nature for from moist and semiarid areas showed relatively higher a long time. Compared with generation one, arid area extent of adaptation to the water-stress level of their clones of generation five presented increased fecundity respective source environment in comparison to those under severe water stress. Similar to S. avenae clones of Liu et al. BMC Ecol (2018) 18:17 Page 10 of 15 other areas, their experience of intermediate water stress increasing outbreaks of cereal aphids (e.g., S. avenae) on for only five generations was not sufficient to alter the wheat in China [34, 35]. In this study, we did find that adaptation extent of these clones to severe water stress. the adaptation potential of arid-area S. avenae clones although consistent and positive selection of water-defi - was enhanced after their continuous exposure to inter- cit stress on adult weight was identified for these clones. mediate water-deficit stress for only five generations, Overall, after their exposure to intermediate water-deficit suggesting a rapid shift of this aphid’s adaptation poten- stress for only five generations, adult weight and fecun - tial under drought. Based on our current results, we sus- dity tended to decrease for moist- and semiarid-area pect that there are only a small percentage of S. avenae clones, but increase for arid-area clones, suggesting genotypes in our samples that have become adapted to rapid shifts in vital life-history characters and adaptation particular drought conditions. It is possible that these potential of this aphid under continuous water-deficit adapted clones will spread quickly in the future with the stress for a relatively longer term. This could have sig - increasing pace of the climate warming trend as currently nificant implications for evolutionary dynamics and out - present and less-adapted ones die out. Therefore, we cau - break risks of aphids in future climate change scenarios. tion against the perception of declining aphid outbreaks under future warming scenarios . There’s an urgent Aphid outbreak risks in the context of global warming need to determine the number of S. avenae genotypes In comparison to well-watered conditions, severe water that have become adapted to drought, as well as the pace stress of this study led to decreased fecundity for S. ave- of their evolution and underlying mechanisms. In addi- nae clones of all three areas, as well as declined adult tion, other ecological factors (e.g., natural enemies, tem- weight for all clones except those from moist areas. perature extremes, CO , aphid genotypes, phenotypic Therefore, severe water stress could have the potential plasticity and secondary endosymbionts) could interact to lower the abundance and outbreak risk of S. avenae with water-deficit stress to show complicated impacts populations under future warming scenarios. However, on aphid outbreaks in the context of global warming [39, compared with well-watered environments, intermediate 45–47]. For example, the differential responses of S. ave - water stress showed neutral effects (in terms of fecundity nae nymphal instars in developmental durations shown and weight) on S. avenae clones in nearly all the cases, in this study could significantly affect parasitism rates and the only exception was that it increased the adult under water-deficit stress. Further studies in the above - weight of moist area clones at generation one. One expla- mentioned aspects will make it more practical to predict nation for the identified water-level dependent pattern is future outbreaks and changing dynamics of aphids under differential life-history trait plasticity of S. avenae clones different climate change scenarios. under variable water-deficit conditions, since phenotypic plasticity of vital characters in this aphid has been shown Conclusions to evolve as a by-product of adaptation to certain envi- We identified both adaptive and non-adaptive changes in ronments . Therefore, the potential risk of S. avenae developmental time, fecundity and adult weight among S. outbreaks can vary depending on the drought level in a avenae clones from moist, semiarid and arid areas under particular area under different future warming scenarios. all the three water treatments, providing substantial evi- Predicted climate change can cause increasing inten- dence of population divergence under drought for this sity and frequency of drought events in many parts of aphid. Based on analyses of life-history trait variance and the world, which may have significant consequences for heritability, the population divergence of this aphid could outbreaks of insect pests . Because of their signifi - have a genetic basis. Clones of S. avenae from moist and cance in various agricultural systems and sensitivity to semiarid areas showed a relatively higher extent of adap- water availability [4, 20, 32], aphids’ response to drought tation to the water-stress level of their respective source has received considerable attention. In some cases, environment in comparison to those from arid areas. drought has shown little or negative effects on aphids After their exposure to intermediate water-deficit stress [22–24, 40]. This agrees with our results in this study for five generations, the fecundity and adult weight of that severe water stress could lower the adaptability and S. avenae clones tended to increase for arid areas, but abundance of S. avenae populations. However, popula- decrease for moist and semiarid areas, indicating that tions of quite a few aphid species [e.g., Diuraphis noxia significant shifts in vital life-history characters of this (Kurdjumov), Rhopalosiphum maidis (Fitch), Schizaphis aphid can occur under future warming scenarios. The graminum (Rondani)), and Brevicoryne brassicae L.] impact of intermediate and severe water-deficit stress on showed enhanced performance and increased outbreaks the fitness S. avenae was neutral and negative, respec - under drought [41–43]. This is consistent with the find - tively. However, we did find that the adaptation poten - ing that the climate change trend appears to have caused tial of arid-area S. avenae clones could be enhanced after Liu et al. BMC Ecol (2018) 18:17 Page 11 of 15 their continuous exposure to intermediate water-deficit relative humidity 65 ± 5%, and photoperiod 16:8 (L:D) h. stress for only five generations. Collectively, our data sug - Prior to the experiment, all test aphid clones were reared gest that there should be only low numbers of S. avenae on well-watered plants for at least 2–3 generations in the genotypes in our samples that have become adapted to same laboratory conditions mentioned above, since such particular drought conditions, and these adapted clones treatments could minimize confounding environmental could spread quickly in the future with the increasing effects . pace of the climate warming trend. Therefore, predic - After that, aphid clones from each location were ran- tion of aphid outbreaks under future warming scenarios domly selected for use in the following tests. For two of is much more complicated than expected. Future studies the locations in arid areas (i.e., Yulin and Shanglang), rel- on the number, distribution and evolution of drought- atively more samples (i.e., over 40) were collected at each adapted aphid genotypes will provide insight into the location, and 15 clones per location were then selected. genetic structuring and evolutionary ecology of aphid For all the other locations, over 20 clones per location populations under drought, which can make it more were collected in the field, and 10 clones per location practical to predict aphid outbreak risks in the context of were selected. u Th s, a total of 100 clones of different global warming. areas were used in this study. Methods Water‑deficit stress treatments Aphid collection and colony establishment Well-watered and intermediately water-stressed treat- Following Zhao et al.  and Bai et al. , arid, semi- ments were carried out as described previously in . arid, and moist areas were defined as those with a mean The severely water-stressed treatment was added in annual precipitation up to 200 mm or less, 200–800 mm, this study, so three water stress treatments were con- and 800 mm or more, respectively. From May to July ducted. Each pot of single wheat seedlings (T. aestivum 2014, aphid populations were collected from three loca- cv. Aikang 58) with 35 g (dry weight) of growing sub- tions for each area (Fig. 4). At least 20 wingless adults strate in the well-watered, intermediate water-deficit, (considered as independent clones) were collected and severe water-deficit treatments was provided every from each location. We followed the sampling protocol 3 d by approximately 10, 7, and 5 ml of water, respec- described in  in order to minimize the likelihood of tively. We used both soil and leaf water potentials to collecting the same clones at a particular location. In the maintain targeted levels of physiological water stress in abovementioned three areas, S. avenae is usually abun- test plants . Soil moisture was determined with a ten- dant on cereal crops from April to June of each year. At siometer (TEN30, Top Instrument, Hangzhou, China). the three locations in arid areas, the mean trimonthly The soil water potentials for the three treatments were rainfall of Jan to March, Apr to June, Jul to Sept and Oct maintained at a range of − 0.02 to − 0.01 MPa, − 0.035 to Dec is about 5, 31, 71 and 9 mm, respectively, based to − 0.02 MPa and lower than − 0.045 MPa, respectively. on data collected from 1951 to 2008 . The respective Water potentials were also measured in plant leaves using trimonthly rainfall in this order is about 21, 95, 240, and the Chardakov method in . The corresponding water 32 mm for semiarid areas, and it is about 47, 252, 501, potentials of wheat leaves in the three treatments were and 113 mm for moist areas . The collected aphid is kept at a range of 0 to − 0.2 MPa, − 0.2 to − 0.6 MPa not an endangered or protected species, and no special and − 0.6 to − 0.8 MPa, respectively (for information on permits have been required for sample collections at all dynamics of leaf water potential, see Additional file 1). the sites mentioned above. Targeted water conditions in test pots were maintained These collected clones from each location were then by checking soil water potential and the weights of plants reared in segregated colonies. All aphid colonies were with growing media twice a week. established on seedlings (stage 11 to 16 at the Zadoks scale ) of wheat (Triticum aestivum L. cv. Aikang 58) Life history data collection in 200 ml plastic pots (7 cm in diameter), containing turfy The experiment was initially replicated six times per soil mixed with vermiculite and perlite (4:3:1, v/v/v). The clone, but three replicates were conducted in the late wheat cultivar ‘Aikang 58’ is selected for use in our study batch of the experiment due to logistic problems. Thus, because of easy manipulations in the laboratory, and it is three or six replicates were conducted for each clone widely planted in China. Each plant with aphids on it was under each treatment. The life-history tests were con well covered with a transparent plastic cylinder (6.5 cm ducted as detailed previously in [19, 20, 32]. Briefly, in diameter, 15 cm in height, and a 60 mesh net on top). each pot of wheat seedlings at the one- to two-leaves Aphid colonies were maintained in growth chambers stage (11–12 at the Zadoks scale ) received one under the following conditions: temperature 22 ± 1 °C, Liu et al. BMC Ecol (2018) 18:17 Page 12 of 15 o o Fig. 4 A map of locations for Sitobion avenae sampling. Arid area: Yulin Co., 38 19′48″ N, 109 43′25″ E; Shanglang Town of Mingqin Co., 38°35′48″ o o o N, 103°06′17″ E; Xiaotian Town of of Mingqin Co., 38°36′40″ N, 103°07′18″ E; semiarid area: Yanlian Co., 35 41′29″ N, 109 16′13″ E; Yaozhou Co., 34 o o o 53′38″ N, 108 58′18″ E; Fuxian Co., 35 45′33″ N, 109 11′26″ E; moist area: Longting Town of Yangxian Co., 33°12′43″ N, 107°38′30″ E; Jinshui Town of o o Yangxian Co., 33°16′20″ N, 107°47′45″ E; Chenggu Co., 33 07′50″ N, 107 16′49″ E apterous adult of S. avenae clones. Wheat seedlings to as DT5 hereafter), 10-d fecundities (total number were inspected under room temperatures (about 22 °C) of offspring produced in 10 d after the onset of repro - two to three hours later, and all aphid individuals on a duction), and adult weight (for newly emerged adults test plant were removed except one newborn nymph. less than 1 d old) were tabulated. The test plants were The test aphid clones were kept in growth chambers replenished every 2 weeks. Using this procedure, the with the abovementioned conditions. They were then baseline generation-one life-history data for S. avenae monitored until 10 d after the beginning of reproduc- clones of different areas were recorded. In our pre - tion for each test aphid individual. Molting, mortality liminary experiments, S. avenae clones did not survive and reproductive events were recorded daily, and the under severe water stress after two or three genera- weight of newly molted adults under each treatment tions, but they survived well under intermediate water was also measured. As detailed previously in , stress. Therefore, test S. avenae clones of moist, semi - developmental durations of 1st, 2nd, 3rd & 4th nym- arid and arid areas were maintained under intermediate phal instars (referred to as DT1 to DT4 hereafter), total water stress (instead of severe water stress) continu- developmental durations of the nymphal stage (referred ously for five generations. After that, these clones of Liu et al. BMC Ecol (2018) 18:17 Page 13 of 15 generation five were subjected to the abovementioned and life-history bioassays under three water stress treat- (FS − MPFS) (FI − MPFI ) (FW − MPFW ) ments, and their life-history data were then collected. X = − − ad MFAP MFSAP MFMP Statistical analyses Three-way nested analyses of variance (nested ANOVA) The S. avenae clones with higher values of X should ad were used to analyze the abovementioned life-history have higher extent of adaptation to the water-deficit level traits in SAS . We analyzed the fixed effect of ‘popula - of their source area (i.e., moist, semiarid and arid). The tion source’ (i.e., moist, semi-arid and arid areas), ‘treat- Pearson’s correlations between adaptation indices and ment’ (i.e., well watered, intermediately water-stressed, life-history traits of S. avenae clones were determined by and severely water-stressed), and their interactions, as using the PROC CORR procedure in SAS . The prin - well as the random effect of ‘clone’ nested in ‘source’. cipal component analysis (PCA; PROC PRINCOMP in Treatment means were separated by using Tukey tests SAS) was conducted with vital life-history traits (includ- following significant ANOVA (α = 0.05). When needed, ing DT1-DT5, and adult weight) after raw data were log- data were log transformed to meet the assumptions of transformed. The factor weightings of each replicate from normality and homoscedasticity in the analyses. the PCA were calculated, and they were used as compos- As detailed previously in , 10-d fecundity was ite life-history factors (i.e., prin1 to prin3) in correlation used as a fitness surrogate in this study. Based on fitness analyses. parameters, an index was developed to evaluate extents Our life-history tests use clonal aphid lines, and this of plant specialization (or habitat adaptation) for insect experimental design allows us to assess the total variance clones or populations [36, 54]. Similarly, we can deter- of a particular life-history character (V ), which includes mine the adaptation index (X ) for S. avenae clones inter-clone components V (i.e., the broad-sense genetic ad G from different source areas by testing them under water variance) and intra-clone components V (i.e., environ- levels of source and alternative environments. If adapted mental variance) . Variance estimates for life-history to the source water environment, an aphid clone will characters were obtained with the restricted maximum have higher fecundity than the average fecundity of the likelihood method by using the software VCE 6.0.2 . population under the source water level, and it will show Broad-sense heritabilities (H = V /V ) were then calcu- G P higher mean fecundity under the source water level than lated as described previously in . The statistical sig - under alternative water levels. X of an aphid clone rep- nificance of broad-sense heritabilities was evaluated with ad resents the difference between its fecundities under the likelihood-ratio tests (LRTs) following Carter et al. . source water level and those under alternative water lev- In order to evaluate the strength of selection under els. Thus, X can reflect the extents of adaptation to the different test environments (i.e., the water-stressed and ad source water environment for the clone involved. X val- well-watered conditions), both differentials and gradients ad ues of moist area clones were evaluated by using the fol- of selection were evaluated by utilizing the PROC REG lowing equation (modified from [36, 54]): procedure in SAS as described in detail previously in . Briefly, lifetime fecundity of S. avenae female adults (FW − MPFW ) (FI − MPFI ) (FS − MPFS) was considered as the fitness estimate, and relative fit - X = − − ad MFMP MFSAP MFAP ness of a particular aphid clone was evaluated by dividing the clone’s lifetime fecundity by the average of all clones FW, fitness under the well-watered treatment; MPFW, under each treatment. Standardized selection differen - mean population fitness under the well-watered treat - tials and gradients were calculated by using simple and ment; MFMP, mean fitness of the moist area population; multiple linear regressions, respectively (for more details, FI, fitness under the intermediate water stress; MPFI, see [57, 58]). mean population fitness under intermediate water stress; Additional file MFSAP, mean fitness of the semiarid area population; FS, fitness under severe water stress; MPFS, mean popula - Additional file 1. Dynamics (from day 1 to day 15) of leaf water potential tion fitness under severe water stress; MFAP, mean fit - (SE) in wheat seedlings under three water treatments. ness of the arid area population. Similarly, X values of semiarid and arid area clones of ad S. avenae were respectively determined using: Abbreviations st th DT1-DT4: the developmental time of 1 to 4 instar nymphs; DT5: total developmental time of the nymphal stage; WW: well-watered treatment; IS: (FI − MPFI ) (FW − MPFW ) (FS − MPFS) X = − − ad intermediate water stress; SS: severe water stress; G1: generation one; G5: MFSAP MFMP MFAP generation five; X : adaptation index. ad Liu et al. BMC Ecol (2018) 18:17 Page 14 of 15 Authors’ contributions 8. Cornelissen T, Fernandes GW, Vasconcellos-Neto J. Size does matter: DL and PD conceived and designed research. PD, SL, SSA, ZS, and XS per- variation in herbivory between and within plants and the plant vigor formed research and collected data. DL and PD analyzed data. 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Wang causes contrasting responses in lepidopteran herbivores. Oikos. (Northwest A&F University, China). We would like to thank S. Seybold (USDA 2011;120:1732–40. Forest Service) and Y. Chen (University of California, Davis) for their critical 13. Han P, et al. Does plant cultivar difference modify the bottom-up comments on previous versions of this manuscript. effects of resource limitation on plant–herbivorous insect interactions? J Chem Ecol. 2016;42:1293–303. Competing interests 14. Bisigato AJ, Saín CL, Campanella MV, Cheli GH. Leaf traits, water stress, The authors declare that they have no competing interests. and insect herbivory: Is food selection a hierarchical process? Arthro- pod Plant Interact. 2015;9:477–85. Availability of data and materials 15. Bestete LR, Torres JB, Silva RBB, Silva-Torres CSA. Water stress and kaolin All data used in this study are included in the article and its supplementary spray affect herbivorous insects’ success on cotton. 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