Life stages of an aphid living under similar thermal conditions differ in thermal performance
Graphical abstract
Introduction
Climate change is expected to alter the distribution and phenology of ectotherms including herbivorous insects in the coming decades (Bale et al., 2002, Hoffmann et al., 2013, Kingsolver et al., 2013). An increasing frequency and intensity of extreme temperature events (IPCC, 2013) may be particularly challenging for many ectotherms (Kingsolver et al., 2013, Ma et al., 2015, Overgaard et al., 2014, Vasseur et al., 2014). Small insect herbivores often have short life cycles (Danks, 2006) leading to overlapping generations (Gullan and Cranston, 2005), so any life stage may experience heat stress. As a consequence, the response of these insects to heat stress will likely depend on the thermal sensitivity of all stages (Gilchrist et al., 1997), and population-level effects may vary depending on the distribution of life stages in a population (Zeigler, 2013). This makes it important to understand stage-specific thermal responses (Bowler and Terblanche, 2008, Kingsolver et al., 2011).
Basal tolerance and plastic responses both contribute to the ability of ectotherms to counter heat stress (Fischer and Karl, 2010, Hoffmann et al., 2013). The former represents an inherent and evolved level of tolerance independent of environmental conditions. Plastic responses provide organisms with the capacity to cope with environmental variation within or across generations and involve physiological changes which enhance survival under temperature extremes following exposure to less extreme conditions; it may involve hardening (following exposures of a few hours) or acclimation (longer exposures of days or even weeks) but no genetic changes (Hoffmann et al., 2003). For many species with complex life stages, stage-specific environmental pressures may lead to variation in tolerance responses across life stages; stages which experience chronic stress might be expected to show higher basal tolerance (Sørensen et al., 2001) and life stages exposed to fluctuating conditions might be expected to show increased plastic responses (Rinehart et al., 2006). Overall, less mobile life stages (e.g. egg or pupa) are expected to be more tolerant according to the Bogert effect (Huey et al., 2003, Marais and Chown, 2008), reflecting differences in the microclimate experienced (Kingsolver et al., 2011, Krebs and Loeschcke, 1995) which may change selection pressures for heat tolerance and plasticity (Mitchell et al., 2011).
In contrast to the species with stage-specific features, aphids and many other small hemimetabolous insects do not have an immobile pupal stage, and nymphs resemble adults for which similar thermal conditions might usually be shared (Gullan and Cranston, 2005). In addition, there is a similar heating rate across ontogeny given their small body size (Angilletta, 2009, Huey and Bennett, 1990). Therefore, a similar pattern of selection for heat resistance across stages is expected. Despite some previous studies on aphids focusing on life stage variation in heat tolerance (Ma et al., 2004a, Piyaphongkul et al., 2012) and plastic responses (Harrison and Barlow, 1973, Ju et al., 2011), it is unclear whether these small insects developing incrementally between the juvenile and adult stage show reduced variation for stress tolerance and plastic capacity when compared to hemimetabolous insects.
In addition to affecting fitness directly, heat stress may produce costs associated with plastic thermal responses which have been explored in many species and especially in insects with a complex life history (Krebs and Loeschcke, 1994, Scott et al., 1997, Silbermann and Tatar, 2000). For most studies focusing on the adult stage, reproductive costs after hardening have been confirmed (Krebs and Loeschcke, 1994, Roux et al., 2010, Scott et al., 1997, Zhang et al., 2013). Low costs of hardening may occur across multiple stages given the modularity of metamorphosis insulating later stages from the disturbance in early development (Potter et al., 2011) or compensatory growth counteracting the negative effects of poor early environment (Dmitriew and Rowe, 2007, Orizaola et al., 2010). Consistent with these expectations, there was little impact on fecundity when stress was imposed on the egg stage (Potter et al., 2011, Xing et al., 2014, Xing et al., 2015), or various life stages (Knapp and Nedvěd, 2013, Zani et al., 2005). In the case of P. xylostella, costs increased with stress dosage and proximity of exposure to the adult stage (Zhang et al., 2015) which suggests that repair during metamorphosis and/or compensation may be important in this species. For hemimetabolous insects lacking metamorphosis, the gradual development between nymphs and adult increases the likelihood of impacts of stress imposed on various life stages on adult performance. This raises the question of whether these two types of insects show different cost patterns across stages.
Here we test the hypothesis that life stages of a small hemimetabolous insect experiencing a similar microclimate have similar levels of tolerance to heat stress, by considering basal tolerance and hardening responses in the English grain aphid, Sitobion avenae (Fabricius). During growth period, this species has an anholocyclic life cycle (Fig. S1) with a short life cycle (reach maturity within 1 week) and high reproduction (50–60 offspring per adult) (Asin and Pons, 2001). A mother always deposits nymphs in a ‘group’ which can persist about a week, and even more mobile older and apterous individuals tend to move only a few meters (Dean, 1973) where the microclimate is likely to be similar. The aphids instead spend time and resources processing food to ensure high rates of growth (Dixon, 1998). Therefore, life stages of S. avenae usually experience similar thermal microhabitat during a growing season (Fig. S2), and daily maximum temperatures they experience can be quite high and reach 35 °C (e.g. Fig. S3) which is regarded as stressful for this species (Kieckhefer et al., 1989).
We address the following questions. (1) Do basal thermal tolerances and hardening capacities vary between stages? (2) Is there a relationship between basal thermal tolerance and hardening capacity across stages? (3) Do large reproductive costs of hardening responses occur at the adult stage, and do these depend on stage that has been stressed? We consider two measures of basal tolerance [upper lethal temperature (ULT) and maximum critical temperature (CTmax)] in five stages (1st, 2nd, 3rd and 4th-instar nymphs and newly moulted adult). Furthermore, we investigate hardening effects on CTmax and consider longevity and fecundity to assess costs. The results indicate that basal tolerance, hardening response and costs associated with a brief heat exposure vary with ontogenetic stage. Lower heat resistance and stronger hardening responses were associated, while costs expressed in terms of longevity and fecundity were determined by the period of the hardening rather than the stage exposed.
Section snippets
Stocks and rearing
Stocks and rearing conditions followed Zhao et al. (2014). English grain aphids were collected from a winter wheat field near Beijing (39°48 N, 116°28 E), and were then reared on 10–20 cm tall winter wheat seedlings in screened cages (60 × 60 × 60 cm) at 22 ± 0.5 °C, 50–60% relative humidity, and a photoperiod of 16 L : 8 D. Seedlings were replaced every week. Experiments were undertaken after this stock had been reared under these conditions for 2 years.
Tested insects
Preliminary experiments were performed to determine
Basal heat tolerances of different stages
There was significant variation in ULT50 among stages (Fig. 1 blue bars). The estimated ULT50 values (and 95% confidence intervals) for the 3rd and 4th-instars were 40.4 (40.2, 40.5) °C and 40.4 (40.3, 40.6) °C respectively and markedly higher than for the other stages. The nymphs of 1st and 2nd-instars had the lowest ULT50 which were estimated as 39.4 (39.4, 39.5) and 39.5 (39.4, 39.6) °C, respectively. The ULT50 of adults had an estimated value of 39.8 (39.7, 39.9) °C. Basal CTmax values also
Lack of convergence in basal and hardening tolerance across ontogeny
Instead of the expected convergence in the basal tolerance across life stages, our results indicate lower basal tolerance in younger nymphs, increasing in older nymphs (3rd and 4th-instars) and then decreasing again in adults (Fig. 1). Variation in basal tolerance with age has previously been noted in other aphids (Harrison and Barlow, 1973, Kaakeh and Dutcher, 1993, Ma et al., 2004a). Facultative symbionts are involved in the heat resistance of aphids (Montllor et al., 2002, Oliver et al., 2010
Acknowledgments
We thank Miss Xiu-qin Pei for assistance in completing experiments. This research was supported financially by the National Natural Science Foundation of China (31620103914 and 31272035), the Natural Science Foundation of Shanxi Province (2015011075) and the Foundation in Shanxi Academy of Agricultural Sciences (YBSJJ1512 and yydzx16).
References (65)
- et al.
Hyperthermic aphids: insights into behaviour and mortality
J. Insect Physiol.
(2010) - et al.
Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches
J. Therm. Biol
(2003) - et al.
Resistance to thermal stress in preadult Drosophila buzzatii: variation among populations and changes in relative resistance across life stages
Biol. J. Linn. Soc.
(1995) - et al.
Climate warming may increase aphids' dropping probabilities in response to high temperatures
J. Insect Physiol.
(2012) - et al.
A test of the accuracy of operative temperature thermometers for studies of small ectotherms
J. Therm. Biol
(1996) Thermal Adaptation: A Theoretical and Empirical Synthesis
(2009)- et al.
Effect of high temperature on the growth and reproduction of corn aphids (Homoptera: Aphididae) and implications for their population dynamics on the northeastern Iberian peninsula
Environ. Entomol.
(2001) - et al.
Herbivory in global climate change research: direct effects of rising temperature on insect herbivores
Glob. Change Biol.
(2002) - et al.
Insect thermal tolerance: what is the role of ontogeny, ageing and senescence?
Biol. Rev.
(2008) - et al.
Experimental evidence for physiological costs underlying the trade-off between reproduction and survival
Funct. Ecol.
(2010)
Short life cycles in insects and mites
Can. Entomol.
Aphid colonization of spring cereals
Ann. Appl. Biol.
Physiology of heat sensitivity
Aphid Ecology: An Optimization Approach
Effects of early resource limitation and compensatory growth on lifetime fitness in the ladybird beetle (Harmonia axyridis)
J. Evol. Biol.
Exploring plastic and genetic responses to temperature variation using copper butterflies
Clim. Res.
Thermal sensitivity of Drosophila melanogaster: evolutionary responses of adults and eggs to laboratory natural selection at different temperatures
Physiol. Zool.
The Insects: An Outline of Entomology
Survival of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae), at extreme temperatures
Can. Entomol.
Upper thermal limits in terrestrial ectotherms: how constrained are they?
Funct. Ecol.
Physiological adjustments to fluctuating thermal environments: an ecological and evolutionary perspective
Behavioral drive versus behavioral inertia in evolution: a null model approach
Am. Nat.
Summary for policymakers
Effects of heat shock, heat exposure pattern, and heat hardening on survival of the sycamore lace bug, Corythucha ciliata
Entomol. Exp. Appl.
Survival of yellow pecan aphids and black pecan aphids (Homoptera: Aphididae) at different temperature regimes
Environ. Entomol.
Hardening capacity in the Drosophila melanogaster species group is constrained by basal thermotolerance
Funct. Ecol.
Effects of constant and fluctuating temperatures on developmental rates and demographic statistics of the English grain aphid (Homoptera: Aphididae)
Ann. Entomol. Soc. Am.
Complex life cycles and the responses of insects to climate change
Integr. Comp. Biol.
Heat stress and the fitness consequences of climate change for terrestrial ectotherms
Funct. Ecol.
Gender and timing during ontogeny matter: effects of a temporary high temperature on survival, body size and colouration in Harmonia axyridis
PLoS One
Costs and benefits of activation of the heat-shock response in Drosophila melanogaster
Funct. Ecol.
The combined effects of bacterial symbionts and aging on life history traits in the pea aphid, Acyrthosiphon pisum
Appl. Environ. Microbiol.
Cited by (46)
Interspecific differences in thermal tolerance landscape explain aphid community abundance under climate change
2023, Journal of Thermal BiologyHeat-avoidance behavior associates with thermal sensitivity rather than tolerance in aphid assemblages
2023, Journal of Thermal BiologyStill standing: The heat protection delivered by a facultative symbiont to its aphid host is resilient to repeated thermal stress
2023, Current Research in Insect ScienceEffect of short-term heat stress on life table parameters of green peach aphid [Myzus persicae (Sulzer) (Hemiptera: Aphididae)]
2022, Journal of King Saud University - ScienceCitation Excerpt :Higher temperatures are expected to have stage-specific impacts on insects. The impacts of high temperatures can also differ throughout generation in the insects with very basic life cycles, such as true bugs and scale insects (Zhao et al., 2017). Additionally, high-temperature effects observed in earlier life span can be transmitted to subsequent phases and between generations.
Geographic dispersion of invasive crop pests: the role of basal, plastic climate stress tolerance and other complementary traits in the tropics
2022, Current Opinion in Insect ScienceCitation Excerpt :The actual stress tolerance comprises basal and plastic tolerance. Basal represents an inherent tolerance independent of environmental conditions [20]. Whereas plasticity copes with environmental variation to enhance survival under extreme environments following exposure to suboptimal conditions, involving hardening (exposing for a few minutes to hours) or acclimation (exposing for days or even weeks) but with no genetic changes [20,21••].