Aphid and ladybird beetle abundance depend on the interaction of spatial effects and genotypic diversity

Intraspecific variation and genotypic diversity of host-plants can affect the structure of associated arthropod communities and the dynamics of populations. Similarly, neighboring plants can also affect interactions between host-plants and their associated arthropods. However, most studies on the effects of host-plant genotypes have largely ignored the potential effects of neighboring host-plants on arthropod communities. In this study, we used a common garden experiment to ask how spatial effects of neighboring patches, along with genotype identity and genotypic diversity in tall goldenrod (Solidago altissima), affect the abundances of a common goldenrod herbivore (Uroleucon nigrotuberculatum) and their dominant predator (Harmonia axyridis, a ladybird beetle). Aphid abundance varied 80-fold among genotypes, while ladybird beetle abundance was not affected by genotype identity. Additionally, there were strong effects of neighboring plots: aphid abundance in a focal plot was positively correlated to aphid abundance in nearby plots, suggesting strong spatial patterning in the abundance of aphids. Neither aphid nor ladybird beetle abundance was affected by genotypic diversity. However, focal plot genotypic diversity mediated the strength of the neighborhood effect (i.e., strong effects for genotype polyculture focal plots and weak effects for genotype monoculture focal plots). Our results show that aphids were directly influenced by host-plant genotype identity while ladybird beetles responded mainly to prey abundance, and suggest that genotypic diversity can influence the effects of spatial processes on the plant-herbivore interactions.     

Comparing intra- and inter-specific effects on litter decomposition in an old-field ecosystem

Plant species can differ in the quantity and quality of leaf litter they produce, and many studies have examined whether plant species diversity affects leaf-litter decomposition and nutrient release. A growing number of studies have indicated that intra-specific variation within plant species can also affect key ecosystem processes. However, the relative importance of intra- versus inter-specific variation for the functioning of ecosystems remains poorly known. Here, we investigate the effects of intra-specific variation in a dominant old-field plant species, tall goldenrod (Solidago altissima), and inter-specific variation among goldenrod species on litter quality, decomposition, and nitrogen (N) release. We found that the nutrient concentration of leaf litter varied among genotypes, which translated into ～50% difference in decomposition rates. Variation among other goldenrod species in decomposition rate was more than twice that of genetic variation within S. altissima. Furthermore, by manipulating litterbags to contain 1, 3, 6, or 9 genotypes, we found that S. altissima genotype identity had much stronger effects than did genotypic diversity on leaf-litter quality, decomposition, and N release. Taken together, these results suggest that the order of ecological importance for controlling leaf-litter decomposition and N release dynamics is plant species identity?genotype identity>genotypic diversity.     

Non-Additive Effects of Genotypic Diversity Increase Floral Abundance and Abundance of Floral Visitors

Background

In the emerging field of community and ecosystem genetics, genetic variation and diversity in dominant plant species have been shown to play fundamental roles in maintaining biodiversity and ecosystem function. However, the importance of intraspecific genetic variation and diversity to floral abundance and pollinator visitation has received little attention.

Methodology/Principal Findings

Using an experimental common garden that manipulated genotypic diversity (the number of distinct genotypes per plot) of Solidago altissima, we document that genotypic diversity of a dominant plant can indirectly influence flower visitor abundance. Across two years, we found that 1) plant genotype explained 45% and 92% of the variation in flower visitor abundance in 2007 and 2008, respectively; and 2) plant genotypic diversity had a positive and non-additive effect on floral abundance and the abundance of flower visitors, as plots established with multiple genotypes produced 25% more flowers and received 45% more flower visits than would be expected under an additive model.

Conclusions/Significance

These results provide evidence that declines in genotypic diversity may be an important but little considered factor for understanding plant-pollinator dynamics, with implications for the global decline in pollinators due to reduced plant diversity in both agricultural and natural ecosystems.     

Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness

Recent research suggests that genetic diversity in plant populations can shape the diversity and abundance of consumer communities. We tested this hypothesis in a field experiment by manipulating patches of Evening Primrose ( Oenothera biennis ) to contain one, four or eight plant genotypes. We then surveyed 92 species of naturally colonizing arthropods. Genetically diverse plant patches had 18% more arthropod species, and a greater abundance of omnivorous and predacious arthropods, but not herbivores, compared with monocultures. The effects of genotypic diversity on arthropod communities were due to a combination of interactive and additive effects among genotypes within genetically diverse patches. Greater genetic diversity also led to a selective feedback, as mean genotype fitness was 27% higher in diverse patches than in monocultures. A comparison between our results and the literature reveals that genetic diversity and species diversity can have similar qualitative and quantitative effects on arthropod communities. Our findings also illustrate the benefit of preserving genetic variation to conserve species diversity and interactions within multitrophic communities.     

Host‐plant genotypic diversity and community genetic interactions mediate aphid spatial distribution

Genetic variation in plants can influence the community structure of associated species, through both direct and indirect interactions. Herbivorous insects are known to feed on a restricted range of plants, and herbivore preference and performance can vary among host plants within a species due to genetically based traits of the plant (e.g., defensive compounds). In a natural system, we expect to find genetic variation within both plant and herbivore communities and we expect this variation to influence species interactions. Using a three‐species plant‐aphid model system, we investigated the effect of genetic diversity on genetic interactions among the community members. Our system involved a host plant (Hordeum vulgare) that was shared by an aphid (Sitobion avenae) and a hemi‐parasitic plant (Rhinanthus minor). We showed that aphids cluster more tightly in a genetically diverse host‐plant community than in a genetic monoculture, with host‐plant genetic diversity explaining up to 24% of the variation in aphid distribution. This is driven by differing preferences of the aphids to the different plant genotypes and their resulting performance on these plants. Within the two host‐plant diversity levels, aphid spatial distribution was influenced by an interaction among the aphid's own genotype, the genotype of a competing aphid, the origin of the parasitic plant population, and the host‐plant genotype. Thus, the overall outcome involves both direct (i.e., host plant to aphid) and indirect (i.e., parasitic plant to aphid) interactions across all these species. These results show that a complex genetic environment influences the distribution of herbivores among host plants. Thus, in genetically diverse systems, interspecific genetic interactions between the host plant and herbivore can influence the population dynamics of the system and could also structure local communities. We suggest that direct and indirect genotypic interactions among species can influence community structure and processes.     

不同邻居物种的基因型多样性对冷蒿生长的影响

植物物种多样性与基因型多样性对群落的结构和功能具有重要的生态作用,近年来植物基因型多样性对植物间相互作用的影响已成为研究者关心的重要科学问题。实验选择退化草原优势种冷蒿(Artemisia frigida)为目标植物,稳定群落建群种羊草(Leymus chinensis)和群落伴生种洽草(Koeleria cristata)为邻居植物,来研究基因型多样性不同的邻居植物对冷蒿生长表现(株高、地上生物量、地下生物量和总生物量)的影响,并通过测量植物相对竞争强度及邻居植物性状变异来进一步探究邻居植物基因型多样性对目标植物影响的内在机制。结果表明:(1)邻居物种为羊草时,基因型多样性对冷蒿的生长表现影响显著,当邻居为6基因型时,冷蒿的株高、地上生物量以及总生物量显著低于单基因型和3基因型时的表现(P0.05),且相对竞争强度高于其他两种处理;而邻居物种为洽草时,基因型多样性对冷蒿所有观测指标以及相对竞争强度的影响均不显著(P0.05)。(2)利用主成分分析法来分析基因型多样性对自身性状变异的影响发现,邻居物种为羊草时,基因型多样性对性状变异响应显著,主要表现为3基因型时,羊草种群的株高、总生物量、地上生物量显著高于单基因型时的表现(P0.05);而邻居物种为洽草时,基因型多样性对性状变异影响不显著(P0.05)。(3)邻居物种为羊草时,羊草总生物量和比叶面积与冷蒿的地上生物量和总生物量呈显著负相关(P0.05);邻居物种为洽草时,洽草各性状与冷蒿性状间无显著相关性(P0.05)。实验结果揭示,基因型多样性对目标植物生长的效应受邻居植物种类的影响,稳定群落建群种羊草高基因型组合能显著抑制冷蒿的生长,这可能与羊草高基因型多样性种群性状变异大且对冷蒿有较高的相对竞争强度有关。所得结果为建群种基因型多样性影响种间相互作用提供了实验证据,为草原的合理利用和保护提供了理论指导。     

Effects of maternal genotypic identity and genetic diversity of the red mangrove Rhizophora mangle on associated soil bacterial communities: A field‐based experiment

Loss of plant biodiversity can result in reduced abundance and diversity of associated species with implications for ecosystem functioning. In ecosystems low in plant species diversity, such as Neotropical mangrove forests, it is thought that genetic diversity within the dominant plant species could play an important role in shaping associated communities. Here, we used a manipulative field experiment to study the effects of maternal genotypic identity and genetic diversity of the red mangrove Rhizophora mangle on the composition and richness of associated soil bacterial communities. Using terminal restriction fragment length polymorphism (T‐RFLP) community fingerprinting, we found that bacterial community composition differed among R. mangle maternal genotypes but not with genetic diversity. Bacterial taxa richness, total soil nitrogen, and total soil carbon were not significantly affected by maternal genotypic identity or genetic diversity of R. mangle. Our findings show that genotype selection in reforestation projects could influence soil bacterial community composition. Further research is needed to determine what impact these bacterial community differences might have on ecosystem processes, such as carbon and nitrogen cycling.     

Effects of genotype identity and diversity on the invasiveness and invasibility of plant populations

Genetic diversity within species is a potentially important, but poorly studied, determinant of plant community dynamics. Here we report experiments testing the influence of genotype identity and genotypic diversity both on the invasibility of a foundation, matrix-forming species (Kentucky bluegrass, Poa pratensis), and on the invasiveness of a colonizing species (dandelion, Taraxacum officinale). Genotypes of Kentucky bluegrass in monoculture showed significant variation in productivity and resistance to dandelion invasion, but the productivity and invasion resistance of genotypic mixtures were not significantly different from those of genotypic monocultures. Indirect evidence suggested temporal shifts in the genotypic composition of mixtures. Dandelion genotypes in monoculture showed striking and significant variation in productivity and seed production, but there was no significant tendency for these variables in mixtures to deviate from null expectations based on monocultures. However, productivity and seed production of dandelion mixtures were consistently greater than those of the two least productive genotypes, and statistically indistinguishable from those of the three most productive genotypes, suggesting the possibility of greater invasiveness of genotypically diverse populations in the long run due to dominance by highly productive genotypes. In both experiments, the identity of genotypes was far more important than genetic diversity per se.     

Ample genetic variation but no evidence for genotype specificity in an all‐parthenogenetic host–parasitoid interaction

Antagonistic coevolution between hosts and parasites can result in negative frequency‐dependent selection and may thus be an important mechanism maintaining genetic variation in populations. Negative frequency‐dependence emerges readily if interactions between hosts and parasites are genotype‐specific such that no host genotype is most resistant to all parasite genotypes, and no parasite genotype is most infective on all hosts. Although there is increasing evidence for genotype specificity in interactions between hosts and pathogens or microparasites, the picture is less clear for insect host–parasitoid interactions. Here, we addressed this question in the black bean aphid (Aphis fabae) and its most important parasitoid Lysiphlebus fabarum. Because both antagonists are capable of parthenogenetic reproduction, this system allows for powerful tests of genotype × genotype interactions. Our test consisted of exposing multiple host clones to different parthenogenetic lines of parasitoids in all combinations, and this experiment was repeated with animals from four different sites. All aphids were free of endosymbiotic bacteria known to increase resistance to parasitoids. We observed ample genetic variation for host resistance and parasitoid infectivity, but there was no significant host clone × parasitoid line interaction, and this result was consistent across the four sites. Thus, there is no evidence for genotype specificity in the interaction between A. fabae and L. fabarum, suggesting that the observed variation is based on rather general mechanisms of defence and attack.     

Plant genotype and induced responses affect resistance to herbivores on evening primrose (Oenothera biennis)

Abstract. 1. Although both genotype and induced responses affect a plant's resistance to herbivores, little is known about their relative and interactive effects. This study examined how plant genotype of a native plant (Oenothera biennis) and induced plant responses to herbivory affect resistance to, and interactions among, several herbivores. 2. In a field experiment, genetic and environmental variation among habitats led to variation in the amount of early season damage and plant quality. The pattern of variation in early season infestation by spittlebugs (Philaenus spumarius, a piercing–sucking herbivore) negatively correlated with oviposition preference by a later feeding specialist weevil (Tyloderma foveolatum, a leaf‐chewer). 3. To determine if plant genotype and induced responses to herbivory might be responsible for these field patterns, we performed no‐choice and choice bioassays using four genotypes of O. biennis that varied in resistance. Plants were induced by either spittlebugs or weevils and assays measured the responses of the same specialist weevil as well as a generalist caterpillar (Spodoptera exigua). 4. Resistance to adult weevils was largely unaffected by plant genotype, while they experienced induced resistance following damage by conspecific weevils in no‐choice assays. Caterpillars were more strongly affected by plant genotype than induced responses in both no‐choice and choice assays, but they also fed less and experienced higher mortality on plants previously damaged by weevils. In contrast to the pattern suggested by the field experiment, spittlebugs did consistently induce resistance against either weevils or caterpillars in the bioassay experiment. 5. These results support recent findings that show herbivore species can compete via induced plant responses. Additionally, a quantitative review of the literature demonstrates that plant genotype tends to be more important than interspecific competition among herbivores (plant‐mediated or otherwise) in affecting herbivore preference and performance.     

Aphid and host‐plant genotype × genotype interactions under elevated CO2

1. Elevated CO₂ can alter plant physiology and morphology, and these changes are expected to impact diet quality for insect herbivores. While the plastic responses of insect herbivores have been well studied, less is known about the propensity of insects to adapt to such changes. Genetic variation in insect responses to elevated CO₂ and genetic interactions between insects and their host plants may exist and provide the necessary raw material for adaptation. 2. We used clonal lines of Rhopalosiphum padi (L.) aphids to examine genotype‐specific responses to elevated CO₂. We used the host plant Schedonorus arundinaceus (tall fescue; Schreb), which is capable of asexual reproduction, to investigate host plant genotype‐specific effects and possible host plant‐by‐insect genotype interactions. The abundance and density of three R. padi genotypes on three tall fescue genotypes under three concentrations of CO₂ (ambient, 700, and 1000 ppm) in a controlled greenhouse environment were examined. 3. Aphid abundance decreased in the 700 ppm CO₂ concentration, but increased in the 1000 ppm concentration relative to ambient. The effect of CO₂ on aphid density was dependent on host plant genotype; the density of aphids in high CO₂ decreased for two plant genotypes but was unchanged in one. No interaction between aphid genotype and elevated CO₂ was found, nor did we find significant genotype‐by‐genotype interactions. 4. This study suggests that the density of R. padi aphids feeding on tall fescue may decrease under elevated CO₂ for some plant genotypes. The likely impact of genotype‐specific responses on future changes in the genetic structure of plant and insect populations is discussed.     

Disparate effects of plant genotypic diversity on foliage and litter arthropod communities

Intraspecific diversity can influence the structure of associated communities, though whether litter-based and foliage-based arthropod communities respond to intraspecific diversity in similar ways remains unclear. In this study, we compared the effects of host-plant genotype and genotypic diversity of the perennial plant, Solidago altissima, on the arthropod community associated with living plant tissue (foliage-based community) and microarthropods associated with leaf litter (litter-based community). We found that variation among host-plant genotypes had strong effects on the diversity and composition of foliage-based arthropods, but only weak effects on litter-based microarthropods. Furthermore, host-plant genotypic diversity was positively related to the abundance and diversity of foliage-based arthropods, and within the herbivore and predator trophic levels. In contrast, there were minimal effects of plant genotypic diversity on litter-based microarthropods in any trophic level. Our study illustrates that incorporating communities associated with living foliage and senesced litter into studies of community genetics can lead to very different conclusions about the importance of intraspecific diversity than when only foliage-based community responses are considered in isolation. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Ant–aphid interactions on Asclepias syriaca are mediated by plant genotype and caterpillar damage

The means by which plant genotypes influence species interactions and arthropod community structure remain poorly understood. One potential, but largely unstudied mechanism is that occurring through plant genetic variation in induced responses to herbivory. Here we test whether induced responses to leaf damage and genotypic variation for induction in Asclepias syriaca influence interactions among Formica podzolica ants, the ant‐tended aphid Aphis asclepiadis, and the untended aphid Myzocallis asclepiadis. In so doing, we assess genetic variation in plant‐mediated interactions among different herbivore guilds. We conducted a three‐way factorial field experiment manipulating plant genotype, leaf damage by specialist monarch caterpillars Danaus plexippus, and ant presence, and documented effects on aphid and ant abundances. Leaf damage increased Aphis abundance in both the presence and absence of ants and Myzocallis abundance under ant exclusion. In the presence of ants, leaf damage decreased Myzocallis abundance, likely due to effects on ant–Myzocallis interactions; ants showed a positive association with Myzocallis, leaf damage increased the strength of this association (425% more ants per aphid), and this in turn fed back to suppress Myzocallis abundance. Yet, these aggregate effects of leaf damage on Myzocallis and ants were underlain by substantial variation among milkweed geno types, with leaf damage inducing lower aphid and ant abundances on some genotypes, but higher abundances on others. As a consequence, a substantial fraction of the variation in leaf damage effects on ants (R² =0.42) was explained by milkweed genetic variation in the strength and sign of leaf damage effects on Myzocallis. Although plant genetic variation influenced Aphis abundance, this did not translate into genetic variation in ant abundance, and leaf damage did not influence Aphis–ant interactions. Overall, we show that variation in induced responses to herbivory is a relevant condition by which plant genotype influences interactions in plant‐centered arthropod communities and provide novel results of effects on the third trophic level.     

Belowground interactions shift the relative importance of direct and indirect genetic effects

Intraspecific genetic variation can affect decomposition, nutrient cycling, and interactions between plants and their associated belowground communities. However, the effects of genetic variation on ecosystems can also be indirect, meaning that genes in a focal plant may affect ecosystems by altering the phenotype of interacting (i.e., neighboring) individuals. We manipulated genotype identity, species identity, and the possibility of belowground interactions between neighboring Solidago plants. We hypothesized that, because our plants were nitrogen (N) limited, the most important interactions between focal and neighbor plants would occur belowground. More specifically, we hypothesized that the genotypic identity of a plant's neighbor would have a larger effect on belowground biomass than on aboveground biomass, but only when neighboring plants were allowed to interact belowground. We detected species‐ and genotype‐level variation for aboveground biomass and ramet production. We also found that belowground biomass and ramet production depended on the interaction of neighbor genotype identity and the presence or absence of belowground interactions. Additionally, we found that interspecific indirect genetic effects (IIGEs; changes in focal plant traits due to the genotype identity of a heterospecific neighbor) had a greater effect size on belowground biomass than did focal genotype; however, this effect only held in pots that allowed belowground interactions. These results expand the types of natural processes that can be attributed to genotypes by showing that, under certain conditions, a plant's phenotype can be strongly determined by the expression of genes in its neighbor. By showing that IIGEs are dependent upon plants being able to interact belowground, our results also provide a first step for thinking about how genotype‐based, belowground interactions influence the evolutionary outcomes of plant‐neighbor interactions.     

Covariation and composition of arthropod species across plant genotypes of evening primrose, Oenothera biennis

Genetic variation in plants has broad implications for both the ecology and evolution of species interactions. We addressed how a diverse community of arthropod species covary in abundance among plant genotypes of a native herbaceous plant ( Oenothera biennis ), and if these effects scale-up to shape the composition, diversity, and total abundance of arthropods over the entire lifetime of plants (two years). In a field experiment, we replicated 14 plant genotypes of O. biennis across five field habitats and studied the arthropod communities that naturally colonized plants. Genetic variation in O. biennis affected the abundance of 45% of the eleven common species in 2002, and 75% of sixteen common species in 2003. We examined the strength of correlations in mean abundance of arthropod species among plant genotypes and found that species responded independently to variation among genotypes in the first year of the study, whereas species formed positively covarying clusters of taxa in the second year (r_mean=0.35). The strength of these correlations did not consistently correspond to either taxonomy or functional attributes of the different species. The effects of plant genetic variation on the abundance and covariation of multiple arthropod species was associated with cascading effects on higher levels of community organization, as plant genotype and habitat interacted to affect the species composition, diversity, and total abundance of arthropods in both 2002 and 2003, though the specific effects varied across years. Our results suggest that plants may employ generalized resistance strategies effective against multiple herbivores, but such strategies are unlikely to be effective against entire functional groups of species. Moreover, we show that genotypic variation in plants is an important ecological factor that affects multiple levels of community organization, but the effects of plant genotype vary in both space and time.     

Species and genotype diversity drive community and ecosystem properties in experimental microcosms

Species diversity is important to ecosystems because of the increased probability of including species that are strong interactors and/or because multiple-species communities are more efficient at using resources due to synergisms and resource partitioning. Genetic diversity also contributes to ecosystem function through effects on primary productivity, community structure and resilience, and modulating energy and nutrient fluxes. Lacking are studies investigating the relationship between ecosystem function and diversity where hierarchical levels of biological diversity are systematically varied during experimentation. In this experiment, we manipulated both species and genotypic diversity of two Daphnia species in microcosms initially seeded with Chlamydomonas and measured community- and ecosystem-level properties to determine which level of diversity was most important for explaining variation in the property. Our results show that species diversity alters bacterial community composition while high genotypic diversity reduces bacterial richness and primary productivity. In addition, the highest levels of genotypic and species richness appear to increase community and ecosystem stability. These findings reveal that species and genotypic diversity are significant drivers of community and ecosystem properties and stability.     

Genotypic diversity of an invasive plant species promotes litter decomposition and associated processes

Following studies that showed negative effects of species loss on ecosystem functioning, newer studies have started to investigate if similar consequences could result from reductions of genetic diversity within species. We tested the influence of genotypic richness and dissimilarity (plots containing one, three, six or 12 genotypes) in stands of the invasive plant Solidago canadensis in China on the decomposition of its leaf litter and associated soil animals over five monthly time intervals. We found that the logarithm of genotypic richness was positively linearly related to mass loss of C, N and P from the litter and to richness and abundance of soil animals on the litter samples. The mixing proportion of litter from two sites, but not genotypic dissimilarity of mixtures, had additional effects on measured variables. The litter diversity effects on soil animals were particularly strong under the most stressful conditions of hot weather in July: at this time richness and abundance of soil animals were higher in 12-genotype litter mixtures than even in the highest corresponding one-genotype litter. The litter diversity effects on decomposition were in part mediated by soil animals: the abundance of Acarina, when used as covariate in the analysis, fully explained the litter diversity effects on mass loss of N and P. Overall, our study shows that high genotypic richness of S. canadensis leaf litter positively affects richness and abundance of soil animals, which in turn accelerate litter decomposition and P release from litter.     

Effects of tree species diversity and genotypic diversity on leafminers and parasitoids in a tropical forest plantation

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Interspecific plant functional variation prevails over intraspecific variation in driving spider beta diversity

1. Non-trophic interactions between plants and animals can affect community structure and species trait composition. However, it is unclear how changes in intra- and interspecific morphological traits of plant species affect non-trophic interactions at a metacommunity scale. Additionally, whether plant evolutionary history determines taxonomic and functional diversity of plant-dwelling predators is an open question. 2. To address these gaps, this study used a published dataset with spiders dwelling exclusively on bromeliads to investigate if: (i) intra- and interspecific variability in host plant morphological traits affects spider taxonomic and functional diversity; and (ii) bromeliad trait evolution determines present-day patterns of spider trait diversity. 3. Spider and bromeliad traits were measured, and a new statistical framework was used to quantify the response of spider beta diversity to intra- and interspecific variation in bromeliad traits. In addition, bromeliad traits were decomposed across its phylogenetic tree to check whether the current variation in morphological traits of bromeliads is a result of either ancestral or recent diversification. 4. Bromeliad intraspecific variation did not affect spiders, but leaf length variation between bromeliad species had a positive effect on spider functional beta diversity. Interestingly, the most ancestral split between two subfamilies explained most of the variation in bromeliad species, which suggests that spider functional diversity could represent an outcome of bromeliad evolutionary history. 5. Overall, the results of this study suggest that interactions between plants and organisms that do not feed directly on their tissues could be shaped by plant evolutionary history, which in turn suggests that non-trophic interactions can be maintained over time.     

Complex genotype interactions influence social fitness during the developmental phase of the social amoeba Dictyostelium discoideum

When individuals interact, phenotypic variation can be partitioned into direct genetic effects (DGEs) of the individuals’ own genotypes, indirect genetic effects (IGEs) of their social partners’ genotypes and epistatic interactions between the genotypes of interacting individuals (‘genotype‐by‐genotype (G×G) epistasis’). These components can all play important roles in evolutionary processes, but few empirical studies have examined their importance. The social amoeba Dictyostelium discoideum provides an ideal system to measure these effects during social interactions and development. When starved, free‐living amoebae aggregate and differentiate into a multicellular fruiting body with a dead stalk that holds aloft viable spores. By measuring interactions among a set of natural strains, we quantify DGEs, IGEs and G×G epistasis affecting spore formation. We find that DGEs explain most of the phenotypic variance (57.6%) whereas IGEs explain a smaller (13.3%) but highly significant component. Interestingly, G×G epistasis explains nearly a quarter of the variance (23.0%), highlighting the complex nature of genotype interactions. These results demonstrate the large impact that social interactions can have on development and suggest that social effects should play an important role in developmental evolution in this system.