1 Introduction

Insect pests population expansion under climate change is one of the major question in modern agriculture and food production, a scenario requiring new monitoring technologies, but also new and modern methods to test the mechanisms behind the rate of expansion and possible management of these pests (Subedi et al. 2023a). Abiotic factors have major influences on insect population dynamics by modifying their reproduction (i.e. no overwintering as eggs in the case of aphids), survival, fecundity, voltinism, host plant and predator interactions and dispersal. Among the abiotic factors, temperature is the most crucial factor affecting insect population flow in different landscapes and ecological regions (Sunil et al. 2023).

Several previous studies have followed the expansion of invasive insects under different abiotic factors (Hartl et al. 2024), but only a few such studies have actually followed the expansion of aphid pests species under climate change (Wu et al. 2020; Subedi et al. 2023). Aphids (Hemiptera: Aphididae) play a major role as major pests of agriculture, horticulture and forestry, both by causing physical damage and transmitting plant pathogenic viruses; their expansion under climate change has not been sufficiently studied until now (Liu et al. 2019; Guo et al. 2017; Zepeda-Paulo and Lavandero 2021). Some important pest aphids such as the corn leaf aphid, Rhopalosiphum maidis (Fitch), a global pest of cereals, especially maize (Zea mays L.) in North America, have been found to increase significantly in terms of its populations in European maize fields during the last five years (Csorba et al. 2021, 2022). Significant population increase and damage were detected in Germany, Poland, Hungary and from 2019 onwards, in Romania (Banat region) (Blackman and Eastop 2000; Emden and Harrington 2007, 2017). Because maize is the major cereal host of the corn leaf aphid, the largest agricultural crop in several European counties, expansion of this pest aphid and the damage it causes is likely to cost billions of Euros before an effective monitoring system and satisfactory control method is developed. Moreover, hitherto, no technologies were– or indeed are– available to control this particular serious pest other than the application of synthetic insecticides and use of hymenopterous parasitoids as biological control agents in European maize fields, as in the USA (Van Emden and Harrington 2017).

Several factors need to be identified in order to help understand the rapid expansion of certain pest aphid species, including the corn leaf aphid, including the effect of microbial symbionts on aphids adaptations. Aphids are closely associated with bacterial symbionts (Douglas 2016). Of these, some are obligate, usually referred to as a primary symbiont, i.e. Buchnera aphidicola. There are also several facultative or secondary species too such as Serratia symbiotica, Wolbachia spp., Hamiltonella defensa, Regiella insecticola, and others, that are harboured and shared between divergent aphid host lineages by undergoing both vertical and horizontal transfer among asexual female (parthenogenetic) aphid matrilines and which might confer additional adaptation mechanisms (Zepeda-Paulo and Lavandero 2021).

Only a few earlier studies have discussed the possibility that these endosymbiotic bacterial communities may well be– or indeed are– involved in the expression of different traits related to aphid adaptations, including tolerance to high and low temperature (Montllor et al. 2002) and host plant adaptation (Tsuchida et al. 2010). Overall, the functional role of these bacterial symbionts can be classified in relation to two main traits: 1) their protective role, traits that may confer advantages to the aphid under specific ecological conditions (high and low temperatures, natural enemies i.e. parasitoids; and 2) their metabolism role, traits that confer advantages in specific nutrients decomposition when this is required after a new host plant invasion, either to an existing host or to a novel one (Douglas 2016).

Previous studies involving heat exposure experiments have revealed the role of B. aphidicola in aphid fitness parameters. Studies that are more detailed show that aphid fecundity decreases due to a mutation suppressing transcriptional response of a gene encoding a small heat shock protein. The absence of this heat shock gene conferred by B. aphidicola seems to explain the heat sensitivity of some aphids (i.e. the black bean aphid, Aphis fabae Scopoli) (Zhang et al. 2019).

Of the studies performed to date, the presence of S. symbiotica in ant populations has been investigated, especially on species with mutualistic interactions with aphids although the diversity of strains was found to be similar within the gut of aphids and ants since ants feed on the honeydew of aphids (Renoz et al. 2019). It has also been reported that S. symbiotica is involved in defense against heat stress and potentially in aphid nutrition, being capable of producing proteases such as metalloproteases, which may facilitate aphid development, help in plant protein digestion, as well as suppressing plant defenses (Skaljac et al. 2019). Other studies have further revealed that both obligate and facultative symbiont strains are e transmitted maternally (Montllor et al. 2002).

The endosymbiont Wolbachia was first detected in aphids (e.g. in Cinara cedri Mimeur) by Gómez-Valero et al. in 2004a and reported to have importance in the prevalence and persistence of asexual lineages. Later studies showed that Wolbachia is one of the most frequently found microorganisms in aphids, i.e. in 82 species (Zytynska and Weisser 2016), these symbiotic relationships protecting aphids and other arthropods against several pathogens and abiotic stresses (Oliver et al. 2003; Gómez-Valero et al., 2004a).

The role of the other facultative endosymbionts such as Hamiltonella defensa and Regiella insecticola in aphid adaptation to abiotic and biotic factors should be reconsidered. Studies report that the presence of Hamiltonella serves as a defense against hymenopterous parasitoid wasps (braconids) by inhibiting the development of wasp larvae inside the body of their aphid host e.g. the pea aphid, Acyrthosiphon pisum Harris (Oliver et al. 2005). In contrast,, aphids infested with R. insecticola were observed to be more predated and did not improve defenses against ladybird (Coleoptera: Coccinellidae) predators; also such -infected aphids showed increased performance on wheat, while the opposite was true on barley (Ramírez-Cáceres et al. 2019).

1.1 Objectives of the present study

In light of the various factors outlined above, in the present study three central questions, important both from a fundamental as well as potentially an applied point of view (i.e. aphid pest control), were posited: (1) Do corn leaf aphid populations expand significantly along a gradient of 200,000 square kilometer, which includes different maize management systems and climatic regions?; (2) Do the aforementioned factors, especially climatic conditions, influence corn leaf aphid endosymbiotic (both obligate and facultative) bacterial community composition? If so, (3) can these factors be correlated with rapid corn leaf aphid distribution and population increase with time, as currently observed in many European agroecosystems?

2 Materials and methods

2.1 Study area and sampling methods of corn leaf aphids

Maize is the largest cash crop in Romania, with an average yield of 18.6 million tonnes per annum (p.a), making the country the ninth largest maize producer in the world (Șimon et al. 2023).

In our study, a comprehensive field assessment of corn leaf aphid colonies and sampling were performed in Romania during a four-year period (2020-23) and involving the most important agricultural regions in the country. The variation of corn leaf aphid population density were followed starting from the 2020 vegetative propagation season, and 16 maize plots inside eight fields were periodically visited, and aphid populations assessed from the four climate areas. As aphid populations started to increase, comprehensive field collection was begun with aphids collected from the same eight fields (and two plots inside each one, so 16 plots in total) during the same time period (June and July) when all plots were in flowering stages R2 to R3.

Since about 2 million ha of maize is cultivated in Romania annually, the eight maize fields were selected along a large geographic gradient of 200,000 square kilometers, taking into consideration two main aspects, each representing the Romanian and the European maize cultivation systems. These were the geographic locations, and maize management systems, with climatic zones were defined according to Marcu and Borz (2013) (Marcu and Borz 2013). Accordingly, corn leaf aphid infested maize fields ranging from south, south-western and east-western Romania (Timiș, Olt, Călărași, Brăila sitest) were sampled from both wet-warm and wet-temperate climate regions of maize cultivation and high size and input management systems (abbreviated as HIFw = high input fields and wet warm climate and HIFt = high input fields and wet temperate climate, respectively), together representing some 60% of the total Romanian maize production p.a. Fields from eastern and mid-western parts of Romania (Iași, Cluj) with a temperate continental climate and medium size and input maize management systems (abbreviated as MIF = medium impact fields), represented about 20% of Romanian maize production p a. Lastly, fields from Central-Romania (Brașov, Harghita) with cool continental climate regions between mountainous areas and low area and input management maize systems (abbreviated as LIF = low impact fields), also represented about 20% of Romanian maize production p.a. (Fig. 1). All fields and plots were managed using seed treatments, fertilizers and insecticides against corn rootworm beetle, Diabrotica virgifera LeConte (Coleoptera: Chryomelidae) in conventional management regimes (Table 1).

Fig. 1
figure 1

Locations of maize cultivation and corn leaf aphid sample collections in Romanian maize management in relation to field size systems and climate conditions

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Table 1 Management plan for sample areas in different maize fields in Romania. Each treatment has been presented in the order of application during the crop vegetation period
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The infestation rate during the four-year assessment were made in each field and plot by choosing 50 plants per plot (16 plots inside the 8 fields) in a transect of 10 × 5 m from the margin to the field interior and the presence of the aphids colonies were searched for. If all 50 plants had colonies, the infestation was determined as severe, if up to 25 plants, as high, while if only ten plants were colonised, as low (Fig. 2).

Fig. 2
figure 2

The rate of infestation and severe infestation of corn leaf aphids in the visited 16 maize fields between 2020–2023

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Inside each of the eight fields, two smaller similar plots were defined and sampled from. Aphids were collected from maize plants inside these smaller plots to minimize the possible effects of field margins, and the same sampling method was used in all sites. Asexual wingless (apterous) aphids were searched for inside the colonies, choosing ten maize plants per smaller plots. From each colony, first instar aphid nymphs (five from each colony / plant) were collected and stored in 0.5 mL Eppendorf tubes containing 99% ethanol prior to DNA analysis. Because at the beginning of the study, not all the sites were infected, the rate of infestation in each of the 16 plots was assessed by searching for the colonies. If a colony was detected, samples were collected, but also the start of any plant infections were noted and used in the results. The increased infestation rate from 2021, and especially in 2022 and 2023, enabled thorough sampling (all sites and plots having aphid colonies), all samples collected being used for genetic analyses. From each sample of ten plants (i.e. with an aphid colony per small plot sampled as earlier stated and the procedure replicated biweekly three-times each year in June and July), five samples were selected and used for symbiont genetic assessment. In such cases, a number of 20 samples per three collection dates in 2020 (n = 60), 30 in 2021(n = 90), 65 in 2021 (n = 195) and 80 in 2023 (n = 240) were analyzed genetically In total, 585 corn leaf aphid samples were analyzed, but because there was no continuous infestation in 2020, only data from 2021 to 2023 (525 samples) were tested statistically from the eight maize fields and four climate areas.

2.2 Bacterial symbionts identification and bioinformatics assessments

Amplified partial sequences of the 16 S rRNA gene from aphid DNA extracts were performed using primer pairs designed for the hypervariable regions of the genes V2-4-8 and V3-6, 7–9. The resulting PCR products targeting specific regions of the 16 S rRNA gene were purified with Agencourt AMPure beads (Beckman Coulter™). Subsequently, libraries were constructed using the Ion Plus Fragment Library kit (Applied Biosystems) and their concentration determined with the Ion Universal Library Quantitation kit (Cat no. A26217). Template preparation was completed using the ION PGM Hi-Q View OT2 kit-400, followed by sequencing of the amplicon libraries on a 318-chip using the Ion Torrent PGM system (Figure S1).

The sequence reads obtained were filtered by the Ion Reporter PGM software to eliminate polyclonal and low-quality reads. The resulting sequencing data were analyzed using Quantitative Insights Into Microbial Ecology (QIIME). Operational Taxonomic Units (OTUs) of the 16 S rRNA gene were defined at a threshold of ≥ 97% sequence homology to calculate downstream diversity measures. Classification of all reads was performed utilizing reference datasets (Curated Greengenes v13.5; Curated MicroSEQ(R) 16 S Reference Library v2013.1).

2.3 Data analysis

The community composition of the most frequent bacterial symbionts for each aphid colony and site were analyzed by year and 16 plots separately. The data were paired by year, and because there were generally only low infestations by aphids in the plots, the frequency of the bacterial endosymbionts were only compared between plots with infections. Because within fields and years (i.e. HIFw Timis and years) there were no differences found in terms of symbiotic bacterial community composition and frequency in those plots where colonies were discovered, and also no differences between collection periods, these samples were pooled after genetic analysis, and clumped together for statistical analyses. Alignment of all bacterial genetic sequences was performed using ClustalW, and the results visualized in EMPeror (Vázquez-Baeza et al. 2013). Non-metric multidimensional scaling (NMDS) based on beta diversity analysis using 3-D principal coordinates analysis was then performed involving the Bray–Curtis dissimilarity index. This was followed by bacterial community classifications in terms of family, genus and species level using data from 2021 to 2023, when all sites were infested), and the most dominant bacterial taxa from each community were presented at these three levels. Hence at family level, the 15 most frequent endosymbiont taxa were analyzed and presented, while at genus and species level, the 20 most frequent taxa.

Principal Coordinate Analyses (PCoA) was used to test the effect of climate conditions and site on bacterial symbionts abundances at species level for the eight maize fields, where locations were considered as main components and endosymbiont species abundances as variables. In the following analyses, heat-map matrices were constructed to compare bacterial symbionts abundances between sites. In this approach, blue colours of matrices represent low abundance and red high abundances. For this analysis, the most frequent 14 endosymbiont species were used for a better representation in a heat-map matrix. Bray-Curtis similarity indices were computed and cluster analyses used to compare the composition of bacterial endosymbionts species in the eight sites. Data analyses and visualization were made using the computer program PAST 4.02. (https://past.en.lo4d.com/windows).

To improve the reliability of the statistics performed using PCoA, heat map and Bray-Curtis analyses, complete data from 2021to 2023 were used. Correlations between the infestation rate of the maize fields visited between 2020 and 2023 (when all fields had aphid colonies), and the frequency of the most abundant endosymbionts (2021to 2023) were compared using linear relation factors.

3 Results

An increasing number of the infested maize fields were detected from 2020 onwards, when only four fields were infested at low level with corn leaf aphids, and thereafter an increasing tendency was observed until 2024, when all maize fields and inside them all plots assessed were infested. Severe infestation (almost each plant starting from the field margins) with well-developed aphid colonies and concomitant crop damage were detected in each eight fields and 16 plots (Fig. 2).

The community composition analyses of the aphid bacterial endosymbionts clearly represent a snapshot of the frequency of the microbiomes at the level of family, genus and species. At family level, the 15 taxa represent 95% of the total families identified; high size plots with a wet warm continental climate (HIFw) were clearly dominated by endosymbiont taxa Enterobacteriaceae followed by Anaplasmataceae (Figure S2A). High size plots with wet temperate climate (HIFt) were likewise dominated by Enterobacteriaceae; however here endosymbionts belonging to the following taxa, Microbacteriaceae, Moraxellaceae, Vibrionaceae, Pseudomonadaceae and Sphingomonadaceae were also frequent at sites from Braila (Figure S2B). Medium size and input fields at temperate continental climate (MIF) had higher bacterial symbiont diversity with dominance of Enterobacteriaceae, Pseudomonadaceae, Moraxellaceae and Vibrionaceae (Figure S2C). Corn leaf aphid microbial symbionts at low size and input field with cool continental climate (LIF) were similar with those from HIFw, and dominated by Enterobacteriaceae followed by Anaplasmataceae (Figure S2D).

At the genus level, the 20 endosymbiont taxa represented > 90% of the total taxa identified. HIFw were clearly dominated by endosymbionts belonging to the genus Serratia, followed by Wolbachia and Buchnera (Figure S3A), whereas both HIFt and MIF were dominated by Buchnera at high frequency, followed by Serratia, Wolbachia and Shigella at a lower frequency (Figure S3B, C). The microbial symbiont composition of LIF were again very similar to HIFw and were dominated by a high frequency of Serratia, but a much lower frequency of Buchnera. At HIFw, the frequency of Wolbachia was higher than that of Buchnera (Figure S3D).

The same general trends were detected at the species level. Thus, Serratia symbiotica dominated HIFw and LIF (fields under extreme climate conditions), whereas in contrast, S. marcescens and S. ureilytica were detected, whilst a low frequency of Buchnera and high frequency of Wolbachis under HIFw conditions were again observed (Fig. 3A, D). The clear domination of B. aphidicola and a much lower frequency of S. symbiotica were seen under both HIFt and MIF conditions. Lastly, the presence of Sigella spp, and Vibrio spp., in this instance V. metschnikovii, V. atlanticus and V. parahaemolyticus) were noted (Fig. 3B, C).

Fig. 3
figure 3

Corn leaf aphid endosymbiont bacterial frequency at species level under different maize management systems and climate conditions. High size and input fields under wet warm climate (A), High size and input fields under wet temperate climate (B), Medium size and input fields under temperate continental climate (C), and Low size and input fields under cool continental climate (D). Only the most frequent 20 endosymbiont species are presented

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The Principal Coordinate Analyses revealed the effect of climate conditions on corn leaf aphid microbial endosymbionts distribution. The climate as factor determined > 88% of the endosymbionts distributions recorded, which in effect means that site effects were so dominant that no other factors were comparable, and no similar strong effect on endosymbionts distributions were detected (Fig. 4A). Heat map analyses also revealed that the abundance of the facultative endosymbionts S. symbiotica and Wolbachia were highest under LIF followed by HIFw conditions. The abundance of the obligate B. aphidicola was lower under LIF conditions, and was followed by HIFt (Fig. 4B). Bray-Curtis cluster analyses revealed leaf corn aphid endosymbiont taxa and frequency distributions to be similar between HIFw and LIF, as well as between MIF and HIFt (Fig. 4C).

Fig. 4
figure 4

(A). The Principal Coordinate effect of climate conditions on corn leaf aphid microbial symbionts distribution; (B) Heat map of the abundance of the most frequent 14 bacterial species under different management and climate conditions; and (C). Bray-Curtis similarity and cluster analyses of bacterial endosymbionts between the eight sites

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Lastly, highly significant positive linear correlations (P > 0.01) were detected between the infestation rate (number of infected maize fields) and increasing abundance of S. symbiotica and Wolbachia under HIFw and LIF conditions, while their abundances under HIFt and MIF slowly decreased during the assessment period. The opposite trend was detected with B. aphidicola; this obligate endosymbiont was present, but its abundance decreased with the increasing rate of the maize field infection between 2021 and 2023 (Fig. 5A, B, C, D).

Fig. 5
figure 5

(A). Correlations between the infestation rate of the visited maize fields between 2020 and 2023, and the frequency of the most abundant endosymbionts in these years. Infestation rate by year (number of fields) frequency of (B), B. aphidicola (C), S. symbiotica and (D), Wolbachia between 2021-23

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4 Discussion

In the present study, a comprehensive assessment of the population density and the endosymbiotic bacterial species variation of corn leaf aphids was performed. From this, it was found that a clear increase in aphid population density and increase in some endosymbionts were detectable during the four-year study period.

Previous studies have also reported that the primary symbionts Buchnera as well as a few facultative species (Seratia, Wolbachia) dominate corn leaf aphid communities (Csorba et al. 2022); however, variations in the abundance of these symbionts between crops, environmental factors and management can be more clearly explained. Moreover, our findings are the first to report correlations between environmental factors (climate change) and variation in endosymbionts harboured by corn leaf aphids infesting the same host plant (maize). These correlations also explain the exponential increase of severe infestation rate of this aphid species, which might have significances in aphid pest control. The presence of the obligate endosymbiont B. aphidicola has been definitively observed, and high variations in its frequency between fields from different climate conditions detected. This obligate endosymbiont is generally required for the survival of aphids and provides essential amino acids that are rare in their phloem sap diet (Shigenobu et al. 2000), as well as having a role in aphids heat tolerance (Zhang et al. 2019; Majeed et al. 2022).

Earlier researches have revealed that if a novel symbiont is found that physically replaces B. aphidicola (here in Geopemphigus aphids), and as such no longer adequately provided the essential functions to their hosts, the host may acquire additional symbiont species or even replace the old symbionts with new ones (Chong and Moran 2018). This change in endosymbionts was previously observed within the tribe Cerataphidini (subfamily Hormaphidinae) (Nováková et al. 2013; Wegierek et al. 2017). The Cerataphidini (and Geopemphigus) are adapted to warm climate conditions and because B. aphidicola is sensitive to both high and low temperatures, it is possible that aphids living in extreme climates are forced to acquire new, facultative endosymbionts that are tolerant of heat and cold (Chong and Moran 2018). In this study, the first evidence of the decrease of B. aphidicola abundance and increase in that of other, facultative endosymbionts has been demonstrated over a large geographic area, and four climatic conditions, which hence may explain the rapid expansion of the corn leaf aphid populations as observed do to the climate change.

The relative high abundance of the facultative endosymbiont Serratia symbiotica in both HIFw and LIF is also new evidence of the aphid’s extreme climate adaptation mechanism. S. symbiotica is involved in defense against heat and potentially in aphid nutrition. In our study, S. symbiotica was dominant in HIFw, but also in LIF with cold climates. An earlier study describing the endosymbiotic bacterial diversity of two oligophagous aphids, Melanaphis sacchari (Zehntner) and Neophyllaphis podocarpi Takahashi, related with climate conditions, revealed that altitude was negatively correlated with the symbiont richness; even so, several facultative symbionts such as Serratia spp. were detected in high abundance and it was hence concluded that these symbionts protected pea aphids, A. pisum, from heat stress (in both directions) by regulating the aphid metabolome (Xu et al. 2021).

In this study, another Serratia species, S. marcescens, was also detected, but in lower frequency in HIFw, LIF as well as in MIF conditions. To our knowledge, there has hitherto been no previously published evidence of a clear effect of this symbiont on aphid adaptation. In previous studies, this opportunist symbiont has been isolated from rice roots and stems (Gyaneshwar et al. 2001). Also, it was shown that S. marcescens is highly resistant and can survive by utilizing a large variety of nutrients (Sleigh 1983). This property gives it the ability to survive under extreme conditions, and it can thus confer positive effects to its host, so its role in corn leaf aphid adaptations under extreme conditions is highly probable. Accordingly, additional studies are needed to confirm as well as elucidate the role of S. marcescens as a facultative endosymbiont of aphids.

Another Serratia species found in low density was S. ureilytica under LIF conditions; its presence can be explained due to the use of organic fertilizer, since this particular species can metabolize urea as a source of nitrogen (Bhadra et al. 2005). Again, as with the aforementioned Serratia species, its role in corn leaf aphid adaptation requires more research.

The facultative endosymbiont Wolbachia spp. was present in high frequency only under HIFw and LIF conditions. The presence of this particular endosymbiont was first reported by Gómez-Valero et al. (2004a) in Cinara cedri Mimeur aphids (Gómez-Valero et al., 2004b), and who also found that harbouring of this particular endosymbiont increased the prevalence of asexual lineages in the host. The role of Wolbachia is however diverse, previous studies reporting that it can also protect aphids (and other arthropods) against several pathogens and abiotic (extreme heat and cold) stresses (Brownlie et al. 2009; Iturbe-Ormaetxe et al. 2011). Wolbachia has also been reported as important for other arthropods (e.g. bed bugs, parasitic wasps and collembolan species), having a role in egg development (Hosokawa et al. 2010), as well as improving the fecundity of the female insect host (Ou et al. 2023). In our previous research involving preliminary exploration of corn leaf aphid symbiont diversity, Wolbachia was not only present in large-scale field corn crops under warm climate but also under colder conditions, so taken together with the findings of the present study, it is clear that the microorganism apparently has an important role in the thermal adaptation of corn leaf aphid.

The presence of the Shigella flexneri under HIFw, HIFt and MIF conditions was also detected. Shigella species are known to infect non-human primates such as the rhesus macaque, Macaca mulatta (Zimmermann) (Lee et al. 2011). Shigella has also been detected at different levels inside leaf samples of the mouse-ear cress plant, Arabidopsis thaliana (L.) Heynh., and is considered to act as an agent actively damaging plant cells (Jo et al. 2019). Its presence in aphids as a secondary symbiont was recorded in the present study, but also for the first time in our previous study with oak aphid symbionts (MS under preparation). Shigella is probably harbored by, and transferred via, plant cells, but further assessment is required to test its possible effect/s on aphid adaptations.

The presence of Vibrio species can be correlated with maize fields irrigations, in some cases (HIFt and HIFw fields) from rivers, and this particular microorganism is well known to be a sediment inhabiting bacterial species (Huang et al., n.d.). They are probably transmitted to aphids via plant phloem, but their role in aphid adaptations is as yet unconfirmed. In addition, whilst the presence of the other bacterial species found at low frequency cannot at present be associated with corn leaf aphid adaptations (e.g. Massilia at HIFw, Kluyvera at HIFt, Cardiobacterium at MIF or Sphingomonas at LIF), this possibility, as with Shigella mentioned above, requires further investigations and assessment.

In conclusion, we demonstrate for the first time that along a large geographic area and range of climatic conditions, a strong relationship exists between the decrease of the obligate endosymbiont B. aphidicola, and the increase of facultative endosymbionts S. symbiotica and Wolbachia spp. and the increase in corn leaf aphid populations, which we suggest explains this aphid pest’s rapid expansion with concomitant damage in Europe. We also conclude that only the primary symbiont Buchnera and facultative symbionts Serratia and Wolbachis seemingly have a direct effect on aphid adaptations related to climate conditions and management systems. These findings are potentially important for future programmes to combat this aphid pest in maize fields via integrated pest management (IPM) scenarios.

Earlier studies have demonstrated that other factors could also influence the expansion of aphids. In the case of cereal aphids, the factors most strongly associated with the population dynamics have been found to be fertilizer input and mean winter temperature (Wang et al. 2015). In addition, other factors like tillage systems and biodiversity changes as well as different soil management and environmental factors must be considered when trying to tease apart which factors are indeed critical in the rise of corn leaf infestation of maize in Europe and further studies are needed to understand these complex interactions.

As no directed control as yet exists in European maize fields against corn leaf aphid, whereas more than ten synthetic pesticides are available in the USA to combat this pest, before using these compounds (which are all neurotoxins), the effect of symbionts on the distribution and abundance of this aphid species should be considered, and the possibility of using biochemical agents against their symbionts tested. Such a methodological approach will allow more effective methods of control to be developed, thereby providing better long term and environmentally-friendly solutions for controlling this economically important pest of maize under conditions of climate change, as are indeed currently ongoing world-wide.