Social interactions influence disease spread, information flow and resource allocation across species, yet heterogeneity in social interaction frequency and its fitness consequences are still poorly understood. Additionally, the role of exogenous chemicals, such as non-nutritive plant metabolites that are utilised by several animal species, in shaping social networks remains unclear.
Here, we investigated how non-nutritive plant metabolites impact social interactions and the lifespan of the turnip sawfly, Athalia rosae. Adult sawflies acquire neo-clerodane diterpenoids (‘clerodanoids’) from non-food plants and this can serve as a defence against predation and increase mating success.
We found intraspecific variation in clerodanoids in natural populations and laboratory-reared individuals. Clerodanoids could also be acquired from conspecifics that had prior access to the plant metabolites, which led to increased agonistic social interactions.
Network analysis indicated increased social interactions in sawfly groups where some or all individuals had prior access to clerodanoids, while groups with no prior access had fewer interactions. The frequency of social interactions was influenced by the clerodanoid status of the focal individual and that of other conspecifics.
Finally, we observed a shorter lifespan in adults with prior clerodanoid access when grouped with individuals without prior access, suggesting that social interactions to obtain clerodanoids have fitness costs. Our findings highlight the role of intraspecific variation in the acquisition of non-nutritional plant metabolites in shaping social networks. This variation influences individual fitness and social interactions, thereby shaping the individualised social niche.

1 INTRODUCTION

Social interactions are widespread in animals and lead to the emergence of diverse social networks, from nominally to highly interactive (Frank, 2007; Krause et al., 2015). Such interactions can range from mating to agonistic. A common aspect of networks constructed on social interactions, i.e. animal social networks, is skewness in the number of interactions individuals have (Fisher et al., 2019; Gartland et al., 2022; Krause et al., 2015). Some individuals have frequent social interactions while others have few. Consequently, this variation could have ecological ramifications. For instance, individuals with a higher frequency of interactions may overly affect disease transmission (Lloyd-Smith et al., 2005), which in turn may shape evolution of social systems (Udiani & Fefferman, 2020). More or less social interactions may have associated benefits or costs for an individual (Koto et al., 2023; Ruan & Wu, 2008; Snyder-Mackler et al., 2020). For example, increased agonistic social interactions can lead to injuries or even mortality (Archer, 1988), although such costs are more widely documented in species that have teeth, claws or other armaments (Emlen, 2014; Hardy & Briffa, 2013). Even in unarmed species, there can be costs of frequent social interactions, such as depletion of energy reserves (Briffa & Sneddon, 2007), including reduced lipid or carbohydrate reserves.

Social interactions can depend on various biotic and abiotic factors (Candolin & Wong, 2012; Fisher et al., 2021). One of these biotic factors may be plant–animal associations, but their role in explaining the observed skew in social interactions is little explored. Studies have shown that several specialised plant metabolites are taken up by certain animal species independently of nutrition and stored (sequestered) unmodified or modified, for example, for use in mating or as anti-predation defence (Beran & Petschenka, 2022; Nishida, 2014; Opitz & Müller, 2009). This phenomenon is called pharmacophagy in insects (Boppré, 1984). Remarkably, such non-nutritive plant metabolites or their derivatives can also be acquired from other animals, either conspecifics (Paul et al., 2021; Singh et al., 2022) or heterospecifics (Tea et al., 2021). The uptake of such non-nutritive metabolites from plants or other animals can have direct effects on the behaviour of the individuals (Amano et al., 1999; Conner et al., 2000; Gonzalez et al., 1999). For example, pyrrolizidine alkaloid (PA) pharmacophagy has been shown to impact the behaviour and intraspecific interactions of many Lepidopteran species (Boppré, 1983; Boppré & Monzón, 2023). Insects sequester PAs for chemical defence and sexual communication, with males often using PAs to produce pheromones that enhance mating success. Differential uptake can thus lead to individual-level variation in behaviour, impacting how individuals interact with each other and lead to complex patterns of animal social networks (Krause et al., 2015), where some individuals may have more interactions than others. By impacting social interactions, these sequestered plant metabolites can influence the fitness of the individual animals (Formica et al., 2012; Royle et al., 2012; Silk et al., 2003) and their individualised social niche (Kaiser et al., 2024; Trappes et al., 2022). Moreover, taking up plant metabolites may entail other costs, such as potential toxicity, if the substances are harmful (Kortbeek et al., 2019), or if there are costs of sequestration (Agrawal et al., 2021).

Interestingly, many animal species show intraspecific variation in the presence and quantity of sequestered plant metabolites (Liu et al., 2023; Mattila et al., 2021; Opitz & Müller, 2009; Speed et al., 2012). Such variation can result from variation in the plant metabolite concentration per se, potential costs related to metabolite acquisition by the animal or factors such as age, sex or immunological status of the individuals (Dimarco & Fordyce, 2017; Massad et al., 2011; Moore et al., 2014; Smilanich et al., 2009; Zvereva & Kozlov, 2015). This raises the question of whether intraspecific variability in sequestered plant metabolites can influence social interactions, and if these metabolites, directly or through modified social interactions, impact fitness indicators such as lifespan. Additionally, the transfer of plant metabolites between individuals is likely to influence the social interactions of both the donor and the recipient (Paul et al., 2021; Singh et al., 2022). However, despite the known impact of sequestered plant metabolites on individual behaviour (Boppré, 1984; Nishida, 2014), our understanding of how these effects translate into broader implications for social interactions remains limited.

To target these open questions, we examined the effect of intraspecific variation in sequestered plant metabolites on social interactions and lifespan in the turnip sawfly, Athalia rosae (Hymenoptera: Tenthredinidae). The adults of A. rosae feed on floral nectar, usually from Apiaceae plants. In addition, they visit non-food plant species such as Ajuga reptans (Lamiaceae), on which they exhibit pharmacophagy by ‘licking’ on the leaf surface and thereby taking up specialised metabolites, neo-clerodane diterpenoids (hereafter called ‘clerodanoids’). These compounds are slightly modified and incorporated into the body surface (Brueggemann et al., 2023). Access to clerodanoids increases their mating success (Amano et al., 1999) and also provides chemical defence against predators (Nishida & Fukami, 1990; Singh et al., 2022). Moreover, individuals can obtain clerodanoids via agonistic interactions from conspecifics that have had access to plant clerodanoids (Paul & Müller, 2021; Singh et al., 2022), by contact with the mouthparts and potential licking, also referred to as ‘nibbling’ (Brueggemann et al., 2023; Paul & Müller, 2021; Singh et al., 2022), but this does not cause any visible wound. Such agonistic interactions may be costly, as suggested by the transcriptional upregulation of metabolic pathways in sawflies that ‘nibbled’ on conspecifics (Paul et al., 2021). This upregulation can demand increased energy and resources, potentially producing toxic byproducts that reduce fitness, as revealed in Drosophila (Misra et al., 2013). Additionally, the uptake of clerodanoids may also directly pose fitness costs, such as a reduced lifespan in A. rosae (Zanchi et al., 2021). However, laboratory cultures of A. rosae are usually maintained without access to clerodanoids, indicating that clerodanoids are not essential for individual survival.

In this study, we initially assessed intraspecific variation in clerodanoid levels within natural A. rosae populations. Subsequently, we investigated how access to clerodanoids, either directly through A. reptans leaves or indirectly via conspecifics, influenced behavioural interactions in laboratory-reared individuals, and analysed their clerodanoid levels. Notably, intraspecific variation in clerodanoid content was observed in both wild-caught and laboratory-reared individuals. To further understand the impact of clerodanoid variation on social interactions, we established treatment groups with different levels of clerodanoid access, using network analysis to quantify individual and group social interaction metrics (Wey et al., 2008). Lastly, we explored the fitness consequences of clerodanoid acquisition by examining its effects on lifespan and metabolic profiles, i.e. lipid and carbohydrate content, employing treatment groups with varying clerodanoid levels. Through these analyses, we elucidated the ecological significance of clerodanoids in shaping social networks and individual fitness in A. rosae populations. We expected intraspecific variation in adult clerodanoid levels. Groups lacking clerodanoid access were expected to exhibit minimal social interactions, whereas asymmetric clerodanoid access would promote increased social interactions. Individuals without direct access were predicted to adjust social interaction frequency based on the clerodanoid status of conspecifics. Furthermore, increased social interactions for clerodanoid acquisition were expected to incur fitness costs, resulting in a reduced lifespan and a greater depletion of lipid and carbohydrate reserves.

2 MATERIALS AND METHODS

2.1 Maintenance of study organism

Adults of A. rosae do not have chewing-biting mouthparts and can only take up nectar or other compounds by ‘licking’ or ‘sucking’. Adults used in the experiments (other than wild-caught adults) were taken from a laboratory stock population that had been established from sawflies collected in and around Bielefeld, Germany, and annually supplemented with field-caught individuals (see Singh et al., 2023 for laboratory rearing details). The individuals were provided with a 2% (v/v) honey-water solution on paper that was refreshed every alternate day. The laboratory population was maintained in multiple mesh cages (each 60 × 60 × 60 cm) at room temperature (15–25°C) with a 16:8 h light:dark cycle and approximately 60% relative humidity.

2.2 Chemical analysis for clerodanoid content of wild-caught sawflies

To collect initial information on potential variation in clerodanoid content in A. rosae in nature, in total 18 female and eight male adults were collected in the wild at three locations (Data S1). For analysis of clerodanoid amounts, the insects were individually frozen, lyophilised, homogenised and extracted twice for 10 min in ethyl acetate (LC–MS grade; VWR, Leuven, Belgium), using ultrasonication. After centrifugation (Centrifuge 5415 R, Eppendorf, Germany) for 5 min at 16912 x g, supernatants were dried and resolved in 100 μL of methanol with mefenemic acid (Sigma-Aldrich GmbH, Taufkirchen, Germany) as internal standard. Samples were filtered with syringe filters (PTFE membrane, pore size 0.2 μm; Phenomenex, USA) and analysed using an ultra-high performance liquid chromatograph (Dionex UltiMate 3000; Thermo Fisher Scientific, San José, CA, USA) equipped with a Kinetex XB-C18 column (1.7 μm, 150 × 2.1 mm, with guard column; Phenomenex) kept at 45°C, coupled to a quadrupole time of flight mass spectrometer (compact; Bruker Daltonics, Bremen, Germany) in negative electrospray ionisation mode, following Brueggemann et al. (2023). Samples were separated with a gradient from 0.1% formic acid (p.a., eluent additive for LC–MS, ~98%; Sigma-Aldrich) in deionised water (eluent A) to 0.1% formic acid in acetonitrile (LC–MS grade, Fisher Scientific, Loughborough, UK; eluent B) at a flow rate of 0.5 mL/min, starting eluent B at 2%, increasing to 30% within 20 min, and then to 75% within 9 min, followed by column cleaning and equilibration. The settings for the MS mode were capillary voltage 3000 V, end plate offset 500 V, nebuliser (N₂) pressure 3 bar, dry gas (N₂, 275°C) flow 12 L/min, quadrupole ion energy 4 eV and collision energy 7 eV. Line spectra were captured at 6 Hz, with a range of 50–1300 m/z. For recalibration of the m/z axis, a Na(HCOO)-solution was injected prior to each sample. Blanks without animal material were prepared in the same way and measured under the same conditions. Mass axis recalibration and peak picking with the T-ReX 3D algorithm including spectral background subtraction were performed in Metaboscape 2021b (Bruker Daltonics), with an intensity threshold of 1000 counts and minimum peak length of nine spectra. The allowed ion types for bucket generation were: [M-H]⁻, [M-H₂O-H]⁻, [M + Cl]⁻, [M + HCOOH-H]⁻, [M + CH₃COOH-H]⁻ and [2M-H]⁻. From each bucket only the feature with the highest intensity was used. We focused on two metabolites which are likely taken up from A. reptans and metabolised by the sawflies (Brueggemann et al., 2023), putative clerodanoid 1 eluting at 16.3 min (m/z 529.229 [M + HCOOH-H]⁻) and putative clerodanoid 2 eluting at 18.2 min (m/z 527.214 [M + HCOOH-H]⁻), with the monoisotopic masses of 484.231 Da (proposed sum formula C₂₄H₃₆O₁₀) and 482.214 Da (C₂₄H₃₄O₁₀), respectively. Peak intensities of these target metabolites were related to the peak intensity of mefenemic acid for semi-quantitative analysis.

We found intraspecific variation in clerodanoids in natural A. rosae populations. Both females and males varied in the amount of putative clerodanoid 1 and clerodanoid 2 across the three locations from which they were collected (Figure 1). In five individuals no putative clerodanoid 1, and in two individuals no putative clerodanoid 2 could be detected, while the others had relatively high quantities.

Details are in the caption following the image — **FIGURE 1**
Open in figure viewer PowerPoint

Bar chart to show intraspecific variation in peak intensities of putative clerodanoid 1 (grey) and clerodanoid 2 (white) per individual in wild-caught male (n = 8) and female (n = 18) *Athalia rosae* sawflies from three locations. Note that no male was collected from location 2.

2.3 Experiment 1: Effect of direct and indirect clerodanoid acquisition on social interactions

We investigated the effects of no clerodanoid access (C−), indirect clerodanoid access from a conspecific (C+ from conspecific), or direct clerodanoid access from a plant (C+ from plant) by females on social interactions with C− males. For logistical reasons, we focused on varying the treatment for females only, as chemical access in female A. rosae has a more pronounced impact on behavioural interactions (Amano et al., 1999; Paul & Müller, 2021). Note that ‘C+ from conspecific’ has been previously referred to as AC+ (Paul et al., 2021; Singh et al., 2022). For the ‘C+ from plant’ treatment, freshly eclosed females were each provided with an A. reptans leaf disc (~1 cm²) for 48 h, while ‘C+ from conspecific’ treatment females were kept with a C+ conspecific (2–4 days old female that had previously contact to A. reptans) for 48 h. Males (6–10 days post-eclosion) were kept individually in Petri dishes for 48 h prior to the assays. The males were mated to a non-focal C− female (~3 days old) 24 h prior to the experiment to avoid any differences arising due to first mating, as observed in other species (Torres-Vila & Jennions, 2005). For the behavioural assays, one female was set up with one male in a clean Petri dish (5.5 cm diameter) and recorded (Sony HDR-CX410VE camcorder, AVCHD—1920 × 1080—25 fps) for 25 min (16 replicates per treatment combination). One to two replicates of each treatment were set up simultaneously in a trial. An observer scored the number of occurrences of agonistic behaviours (see Paul & Müller, 2021 for detailed behavioural descriptions), and mating behaviour (number of mating, latency until first mating) in each movie replicate using the software BORIS v7.13.9 (Friard & Gamba, 2016), being blind to the treatment of the replicate (see Data S2 for sample behaviour video clips). Agonistic interactions included behaviours involving physical contact, such as front limb battling with the use of front legs, fighting utilising all limbs and full-body movement, and ‘nibbling’ where the attacker's mouthparts make contact with the defender's body. We hypothesised that some agonistic behaviours, such as front limb battling and fighting, may not necessarily result in clerodanoid acquisition, and may instead serve as defensive behaviours to fend off conspecifics or prevent them from ‘nibbling’. We expected that C− individuals would attempt to obtain clerodanoids from C+ individuals through ‘nibbling’. In response, C+ individuals may either be passive or engage in aggressive behaviours, such as fighting, with these responses potentially influenced by factors such as energy and body size (Briffa, 2008). Thus, instead of focusing on the mechanisms of clerodanoid acquisition, we examined the impact of clerodanoid acquisition on social interactions by analysing both agonistic and mating behaviours. After the behavioural assays, five females from each treatment were chosen randomly, frozen and analysed for their clerodanoid content as done for the wild-caught adults.

2.4 Experiment 2: Effect of intraspecific variation in clerodanoids on social networks

We found intraspecific variation in clerodanoid content in both wild-caught and lab-reared sawflies (see above and Section 3). To test the effect of clerodanoid acquisition status on social networks, we set up three group types of two males and two females each, in which either no individual had prior access to clerodanoids (C− group, symmetric), only one female and one male had prior access to clerodanoids (mixed group, asymmetric) or all individuals had prior access to clerodanoids from A. reptans leaves (C+ group, symmetric). We set up 15 replicates per group type. Two hours before the behavioural assay, each individual was colour-marked (green, red, white or yellow; Uni POSCA marker pens, Japan) on its thorax and wings to enable identification during behaviour scoring. The colours were alternated between sexes and treatments across replicates to avoid any colour effects. In each trial, one to two replicates per group type were set up simultaneously in Petri dishes and recorded for 25 min. Agonistic and mating interactions of each individual in a movie replicate were scored by an observer while being blind to the treatment, as in experiment 1.

For the social network analysis, we analysed group as well as individual measures of the network. Therefore, we constructed an undirected weighted network for the social interactions (sum of agonistic and mating interactions) in each replicate. We calculated the network weights as the total number of interactions between each pair of individuals (dyad). We normalised the weights at the replicate level and at the dyadic level in each replicate, by dividing by the maximum number of interactions across all replicates and all dyads, respectively. At the group level, we calculated the density of social interactions in each replicate, as follows:

\mathrm{Density}=\frac{\mathrm{sum}\ \mathrm{of}\ \mathrm{weights}}{\left[\mathrm{number}\ \mathrm{of}\ \mathrm{vertices}\times \left(\mathrm{number}\ \mathrm{of}\ \mathrm{vertices}-1\right)\right]\times 0.5},

where vertices is the number of individuals in a replicate. Moreover, at the group level, we counted the number of distinct dyads that exhibited social interactions in each replicate. At the individual level, we calculated the strength (Barrat et al., 2004) and harmonic centrality (Marchiori & Latora, 2000). The strength is a measure of how strongly an individual is directly connected to other individuals in the network. Harmonic centrality calculates the ‘average’ distance of an individual to the other individuals in the network. We used harmonic centrality as we had disconnected networks in some replicates.

2.5 Experiment 3: Costs of direct and indirect clerodanoid acquisition on lifespan, lipid and carbohydrate content

To examine the fitness costs of clerodanoid acquisition and its effects on metabolism, we measured the lifespan and lipid and carbohydrate content of individuals from different groups. Similar to experiment 2, freshly eclosed A. rosae adults were colour-marked and assigned to C− or C+, offering the latter A. reptans leaves for 48 h. The adults were then used to construct three group types consisting of two males and two females, as in experiment 2 (C− group, mixed group and C+ group). We set up 10 replicates per group type. After 4 days of being in a group, the adults were separated and one male and one female were taken to assess survivorship while the other male and female were taken to measure their lipid and carbohydrate content. Note that some individuals died during the 4-day group period; however, they were included in the survivorship/metabolic trait analysis.

Lipid and carbohydrate contents were determined for each individual using a method adapted from Cuff et al. (2021). Individuals were isolated in Eppendorf tubes (2 mL) and frozen at −80°C, lyophilised for 48 h and weighed. Afterwards, each individual was soaked in 0.5 mL of a 1:12 chloroform:methanol solution for 24 h. From the supernatant 250 μL was collected for lipid analysis, followed by additional soaking of the adult in 0.25 mL of 1:12 chloroform:methanol to remove residual lipids for later carbohydrate analysis. The solvent with residuals was discarded. Lipid analysis was conducted with 50 μL of supernatant in a 96-well plate to which 10 μL of concentrated sulfuric acid was added. The plate was covered with a lid, heated in a lab oven (Heraeus UT12; Kendro Laboratory Products, Germany) at 100°C for 10 min and then 240 μL of 0.2 mg/mL vanillin in phosphoric acid was added to each well, followed by photometric analysis at 490 nm. A dilution series of cricket oil (Acheta Cricket Oil; Thailand Unique) in 1:12 chloroform:methanol was measured on the same plate for calibration. For carbohydrate analysis, the remaining individuals were homogenised with glass beads, treated with 0.5 mL of 0.1 M NaOH, incubated in a shaker (250 rpm for 30 min at 80°C) and subsequently allowed to stand at room temperature for 16 h. Carbohydrate analysis was conducted with 40 μL of the supernatant in a 96-well plate, adding 160 μL of anthrone reagent, and heating the plate covered with a lid at 92°C in a lab oven (Heraeus UT12; Kendro Laboratory Products) for 10 min, before photometric analysis at 620 nm. A dilution series of 1:1 trehalose:glycogen (trehalose: 98%, Roth; glycogen: AppliChem) in water was measured on the same plate for calibration of carbohydrates. Body lipid and carbohydrate content were determined as percentage relative to dry body mass.

We also conducted a similar experiment constructing pairs of females with no access, asymmetric access or symmetric access to clerodanoids (see Data S1), which allowed us to confirm that our effects of direct and indirect clerodanoid acquisition on lifespan (see Section 3) were not stemming only from increased mating interactions in mixed and C+ groups but also from increased agonistic interactions in these group types.

2.6 Statistical analyses

All statistical analyses were conducted using R version 4.2.1 (R Core Team, 2022). We used Poisson-distributed generalised linear mixed models (GLMM) with trial as a random effect to assess the effect of female treatment on agonistic and mating interactions in experiment 1 (package ‘lme4’ version 1.1-30, package ‘lmerTest’ version 3.1-3; Bates et al., 2015; Kuznetsova et al., 2017). Effect of female treatment on mating latency was examined using a linear mixed model (LMM) with trial as a random effect. Differences in clerodanoid 1 and 2 among treatment groups were assessed using Kruskal–Wallis tests followed by Dunn tests with Holm correction (‘FSA’ package version 0.9.4, Ogle et al., 2023). In experiment 2, we ran LMMs for density and binomial GLMMs for the number of dyads with social interactions, with group type as a fixed effect and trial as a random effect. Effect of group type, sex and their interaction on individual-level network measures were analysed separately for C− and C+ sawflies using Poisson-distributed GLMMs for strength and LMMs for harmonic centrality (‘igraph’ package version 1.5.1, Csárdi et al., 2023), with replicate ID and trial as random effect. For experiment 3, individuals were classified based on both their individual and group treatments, yielding four composite treatment categories: ‘C− from C− group’, ‘C− from mixed group’, ‘C+ from mixed group’ and ‘C+ from C+ group’. LMM were used to assess the impact of sex, composite treatment, and their interaction on lifespan, lipid and carbohydrate content, with replicate ID as random effect. Model validity was confirmed by examining residual distributions. If the interaction terms were non-significant, they were dropped to test the significance of the lower-order terms. Post hoc analyses were conducted using the ‘multcomp’ package version 1.4-20 (Hothorn et al., 2008) for LMMs and GLMMs.

3 RESULTS

3.1 Clerodanoid uptake affects sawfly behaviour, with varying levels detected in lab-reared sawflies (experiment 1)

There was a significant effect of female treatment on number of agonistic interaction occurrences (χ² = 48.56, df = 2, p < 0.001, Figure 2A), but not on mating occurrences (χ² = 1.76, df = 2, p = 0.41, Figure 2B). C− and ‘C+ from conspecific’ treatment females had significantly fewer agonistic interactions than ‘C+ from plant’ treatment females (Data S4a). There was a significant effect of female treatment on mating latency (χ² = 9.90, df = 2, p = 0.007, Figure 2C) with C− females having a significantly longer latency until mating than ‘C+ from plant’ females, while ‘C+ from conspecific’ females showed an intermediate mating latency (Data S4b).

There was a significant difference between C−, ‘C+ from conspecific’ and ‘C+ from plant’ females in the amount of clerodanoid 1 (χ² = 8.11, df = 2, p = 0.017, Figure 2D) and clerodanoid 2 (χ² = 8.10, df = 2, p = 0.017, Figure 2E). No clerodanoids were detected in C− females, while there was intraspecific variation in clerodanoids in both ‘C+ from conspecific’ and ‘C+ from plant’ females, which did not differ significantly from each other (Data S4c,d).

3.2 Intraspecific variation in clerodanoid access modulates social networks (experiment 2)

The group types varied in their social networks, with the C− group having fewer interactions than the mixed and the C+ group (Figure 3A). Our results showed that there was a significant effect of group type on density (χ² = 27.98, df = 2, p < 0.001, Figure 3B) and number of dyads with social interactions (χ² = 41.29, df = 2, p < 0.001, Figure 3C). Mixed groups had a significantly higher density and more dyads that had interacted than C− and C+ groups (Data S5a,b).

For C− sawflies, there was a significant effect of group type (χ² = 63.55, df = 1, p < 0.001) on strength (Figure 4A) such that C− sawflies in mixed groups had a higher strength, i.e., had more social interactions, than adults in C− groups (Data S6a). In contrast, there was a significant effect of sex (χ² = 25.14, df = 1, p < 0.001) on strength of interactions (Figure 4B) for C+ sawflies, with males having a lower strength than females across mixed and C+ groups (Data S6a). For harmonic centrality, there was a significant effect of group type (χ² = 6.88, df = 1, p = 0.008) in C− sawflies (Figure 4C), such that those in mixed groups had higher harmonic centrality values. There was no significant effect of any predictor variable on harmonic centrality in C+ sawflies (Figure 4D; Data S6b).

3.3 C+ from mixed group adults have a shorter lifespan but no effect on lipid and carbohydrate content (experiment 3)

For lifespan, there was a significant effect of composite treatment (χ² = 18.74, df = 3, p < 0.001) such that ‘C+ from mixed group’ sawflies had a shorter lifespan than ‘C− from C− group’, ‘C− from mixed group’ and ‘C+ from C+ group’ (Figure 5A; Data S7a and S8). Additionally, sex (χ² = 12.52, df = 1, p < 0.001) had a significant effect on lifespan with males having a shorter lifespan than females. There was no significant effect of sex, composite treatment or their interaction on body lipid content (Data S7b). Only sex had a significant effect on body carbohydrate content (χ² = 13.09, df = 1, p < 0.001; Data S7c), with females having higher carbohydrate content than males. We obtained qualitatively similar results for the effect of direct and indirect clerodanoid acquisition on lifespan using female pairs (see Data S3).

4 DISCUSSION

We observed variation in clerodanoid amounts in wild-caught A. rosae adults of both sexes and from all locations. A capture release study had shown that most A. rosae adults could be recaptured from within 100 m of their release, suggesting limited dispersal in this species (Nagasaka, 1992). Thus, our field populations were likely separated, indicating that intraspecific variation in sequestered compounds may be common in natural populations of herbivorous insects that are able to sequester plant metabolites. Moreover, we observed intraspecific variation in clerodanoid amounts of lab-reared sawflies with both direct (via plant leaves) and indirect (from conspecifics) access to clerodanoids, similar to previous studies (Singh et al., 2022; Paul et al., 2021). Such intraspecific variation in sequestered plant chemicals in animals is widely observed (Opitz & Müller, 2009; Speed et al., 2012). While this variation may result from environmental stochasticity, e.g., variation in metabolite concentrations across plants, it could also have an evolutionary basis, e.g., some individuals of an animal species may be chemically defended while others are not (Brower et al., 1970; Speed et al., 2012). Our study shows that intraspecific variation in sequestered plant chemicals can impact social networks and have fitness consequences in sawflies.

The presence and quantity of clerodanoids can be considered as important parts of the chemical phenotype of individuals, which could play a key role in shaping the individualised niche, as has been argued for plants (Müller & Junker, 2022). While effects of food plants on the phenotype and behaviour of herbivorous individuals are widely documented (Geiselhardt et al., 2012; Jarrett & Miller, 2024; Müller & Müller, 2017; Singh et al., 2020), we showed here that plant chemicals sequestered from plants that do not serve as food plants can also modulate social interactions. Our results demonstrated that social networks comprising mixed groups exhibited the highest density and number of interacting dyads, followed by C+ groups. The asymmetric access to clerodanoids in mixed groups may lead to an increase in social interactions, potentially due to C− trying to obtain clerodanoids from C+ individuals. Moreover, C− individuals in mixed groups could acquire clerodanoids from C+ individuals, which may then increase their social interactions, as it will change their clerodanoid acquisition status. Individuals in C− groups had the least density and number of interacting dyads, suggesting that when all individuals lack clerodanoids, they have only few intra-and inter-sex social interactions. The higher centrality values of C− sawflies in mixed groups indicated that they had more connections to other individuals in the network. This could have resulted, for example, from C− individuals trying to obtain clerodanoids from other individuals, leading to more interactions.

The social interactions of the individuals depended not only on their own clerodanoid acquisition status but also on that of other conspecifics in the group. For example, C− individuals had a higher number of social interactions in mixed than in C− groups (see Figure 4A,C), suggesting that even for the same clerodanoid-holding status, an individual may have low or high frequencies of social interactions, depending on the group composition. Similar effects of conspecifics on an individual's behaviour has been shown in an aquatic insect, Notonecta irrorata, where the propensity to disperse depended on the behavioural type of conspecifics present (Kitchen & Chalcraft, 2020). Indeed, studies across various animal species have shown that the behaviour of a focal individual can be shaped by both internal factors, such as personality traits, and external factors, such as social context and interactions with conspecifics (Webster & Ward, 2011). Given the intraspecific variation in clerodanoid content that we observed in wild-caught individuals of A. rosae, we expect social interactions in natural populations to range from low, for example, if no A. reptans plants are around from which clerodanoids can be sequestered, to high, when some insects could sequester clerodanoids, leading to a skewed distribution of social interaction frequency.

Social interactions may accrue over time, and influence fitness of individuals through different ways, such as injury or mortality resulting from agonistic interactions, variation in mating frequency or disease progression (Alwash & Levine, 2019; Dawson et al., 2018; Guo & Dukas, 2020; Stroeymeyt et al., 2018). We observed a reduced lifespan in C+ adults from mixed groups. In experiment 1, we saw that C+ females paired with C− males had the most agonistic interactions. Similarly, in mixed groups, we found more frequent interactions than in C− or C+ groups, suggesting that access to clerodanoids increases social interactions with more individuals interacting. Thus, we can expect that C+ adults in mixed groups had more social, especially agonistic, interactions with their conspecifics that may have ‘nibbled’ (or attempted to do so) on the C+ individual to get access to clerodanoids. These increased agonistic interactions may have led to a decreased lifespan for C+ adults in mixed groups. Also, in female pairs that could not have had mating events, there was a reduced lifespan for C+ individuals from asymmetric access pairs. Together, this suggests that social interactions, especially agonistic, to obtain clerodanoids may have fitness costs in terms of lifespan.

Costs of aggression have also been shown in the fruit fly, Drosophila melanogaster, where flies that engaged in aggressive behaviour had a reduced survival despite not showing any differences in wing damage from no-aggression treatment flies (Guo & Dukas, 2020). This particular study hypothesised that such costs could arise from physiological and metabolic changes triggered by stress and aggressive conflicts. Indeed, a previous study (Paul et al., 2021) demonstrated transcriptional upregulation of metabolic pathway genes in A. rosae C− sawflies that ‘nibbled’ on C+ conspecifics (both males), indicating potential costs associated with aggressive interactions. However, the transcriptome of the male that was ‘nibbled’ upon was not examined. Given that the interactions were solely between these two males (C− and C+) in that study, it is assumed that metabolic upregulation occurred due to increased agonistic contests within the pair, potentially affecting both individuals (Paul et al., 2021). However, we found no significant impact on body lipid and carbohydrate content in the present study. Moreover, while there was no visible damage to the sawflies, injuries not visible to us may have occurred in the C+ individuals from the mixed group type that could lead to a reduced lifespan. Finally, our experiment did not indicate any direct lifespan costs from the sequestration of clerodanoids from plants, as C− individuals from both the C− group type and mixed group type did not differ significantly in lifespan from C+ individuals from the C+ group type for either sex. However, there may be other costs, such as reduced reproductive output, that we have not measured.

In A. rosae, clerodanoids are known to serve as defence against predation (Singh et al., 2022) and also increase mating success (Amano et al., 1999). In other species, sequestered plant metabolites can also provide direct benefits for the offspring (Eisner et al., 2000; Eisner & Meinwald, 1995; Gonzalez et al., 1999). However, at least under controlled laboratory conditions, no significant effects of parental clerodanoid status on offspring were found in A. rosae (Paul et al., 2022). Thus, while clerodanoid acquisition may be associated with benefits for the adults, there may be a trade-off with costs in terms of a reduced lifespan due to agonistic interactions. This in turn may maintain intraspecific variation in clerodanoids in natural populations of A. rosae. Understanding the effects of variation in these sequestered plant metabolites is essential, as their ecological effects can scale up from the individual level to influence factors that shape animal social interaction networks. Moreover, while the impact of animals taking up plant specialised metabolites on plant fitness remains unclear, there may be some effects. For instance, adults of certain Lepidopteran species engage in pharmacophagy, consuming PAs by scratching plant parts such as leaves, flowers or buds with their tarsi (Boppré, 1983; Boppré & Monzón, 2023; Tea et al., 2021). This behaviour could potentially damage plant tissues and impact fitness, though this possibility has yet to be thoroughly explored.

AUTHOR CONTRIBUTIONS

Conceptualization and experimental design: Pragya Singh. Data collection: Yasmina Saidi for experiment 2, Steven Janz for experiment 3, Steven Janz, Pragya Singh and Leon Brueggemann for experiment 4. Chemical analysis: Leon Brueggemann. Data validation and analysis: Pragya Singh and Gaurav Baruah for network analysis, Pragya Singh for other experiments. Data visualisation: Pragya Singh. Writing original draft: Pragya Singh, Caroline Müller. Reviewing and editing: Pragya Singh, Caroline Müller, Leon Brueggemann, Gaurav Baruah. Funding acquisition: Caroline Müller.

ACKNOWLEDGEMENTS

This study was funded by the German Research Foundation (DFG) as part of the SFB TRR 212 (NC³), project number 396777467 (granted to CM). We thank Karin Djendouci for her help in conducting the experiments and Rohit Sasidharan for help with collecting sawflies. Open Access funding enabled and organized by Projekt DEAL.

CONFLICT OF INTEREST STATEMENT

The authors have no conflict of interest to declare.

ETHICS STATEMENT

This study complies with the current laws of Germany on the use of invertebrates in research.

Open Research

DATA AVAILABILITY STATEMENT

The datasets are available on the Zenodo repository (https://doi.org/10.5281/zenodo.10969832; Singh et al., 2024).

Supporting Information

Filename

Description

jane14189-sup-0001-DataS1-S8.zipZip archive, 37.8 MB

Data S1. Locations of wild-caught Athalia rosae adults.

Data S2. Video clips showing different behaviours between a male (smaller) and a female (larger) Athalia rosae individual.

Data S3. Experiment to confirm the costs of direct and indirect clerodanoid acquistion on lifespan in female Athalia rosae sawflies.

Data S4. Results of post-hoc analyses from examining the effect of female treatment on the (a) number of agonistic interactions, (b) mating latency, (c) (putative) clerodanoid 1 and (d) clerodanoid 2 in experiment 1.

Data S5. Result of post-hoc analyses for examining the effect of group type on (a) density and (b) number of dyads/pairs with social interactions in social networks in experiment 2.

Data S6. Effect of predictor variables on individual social network parameters of (a) strength and (b) harmonic centrality in sawfly treatment of C− and C+.

Data S7. Effects of predictor variables on lifespan, lipid content (%) and carbohydrate content (%) in A. rosae adults.

Data S8. Result of post-hoc analyses for examining the effects of treatment on lifespan in A. rosae adults.

Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.

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Plant metabolites modulate social networks and lifespan in a sawfly

Abstract

1 INTRODUCTION

2 MATERIALS AND METHODS

2.1 Maintenance of study organism

2.2 Chemical analysis for clerodanoid content of wild-caught sawflies

2.3 Experiment 1: Effect of direct and indirect clerodanoid acquisition on social interactions

2.4 Experiment 2: Effect of intraspecific variation in clerodanoids on social networks

2.5 Experiment 3: Costs of direct and indirect clerodanoid acquisition on lifespan, lipid and carbohydrate content

2.6 Statistical analyses

3 RESULTS

3.1 Clerodanoid uptake affects sawfly behaviour, with varying levels detected in lab-reared sawflies (experiment 1)

3.2 Intraspecific variation in clerodanoid access modulates social networks (experiment 2)

3.3 C+ from mixed group adults have a shorter lifespan but no effect on lipid and carbohydrate content (experiment 3)

4 DISCUSSION

AUTHOR CONTRIBUTIONS

ACKNOWLEDGEMENTS

CONFLICT OF INTEREST STATEMENT

ETHICS STATEMENT

Open Research

DATA AVAILABILITY STATEMENT

Supporting Information

REFERENCES

Figures

References

Information

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Plant metabolites modulate social networks and lifespan in a sawfly

Abstract

1 INTRODUCTION

2 MATERIALS AND METHODS

2.1 Maintenance of study organism

2.2 Chemical analysis for clerodanoid content of wild-caught sawflies

2.3 Experiment 1: Effect of direct and indirect clerodanoid acquisition on social interactions

2.4 Experiment 2: Effect of intraspecific variation in clerodanoids on social networks

2.5 Experiment 3: Costs of direct and indirect clerodanoid acquisition on lifespan, lipid and carbohydrate content

2.6 Statistical analyses

3 RESULTS

3.1 Clerodanoid uptake affects sawfly behaviour, with varying levels detected in lab-reared sawflies (experiment 1)

3.2 Intraspecific variation in clerodanoid access modulates social networks (experiment 2)

3.3 C+ from mixed group adults have a shorter lifespan but no effect on lipid and carbohydrate content (experiment 3)

4 DISCUSSION

AUTHOR CONTRIBUTIONS

ACKNOWLEDGEMENTS

CONFLICT OF INTEREST STATEMENT

ETHICS STATEMENT

Open Research

DATA AVAILABILITY STATEMENT

Supporting Information

REFERENCES

Figures

References

Related

Information

Journal list menu

Tools

Follow journal