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Cuticular hydrocarbons (CHC) are known to serve as discrimination cues and will trigger defence behaviour in a plethora of eusocial insects. However, little is known how about nestmate recognition ability selects for CHC diversification. In this study we investigate differences in CHC composition of four major honey bee species with respect to the differences in their nesting behavior. In contrast to A. mellifera, A. cerana and A. florea, the giant honey bee A. dorsata prefers to build their nests in aggregations with very small spatial distances between nests, which increases the probability of intrusions. Thus, A. dorsata exhibits a particularly challenging nesting behavior which we hypothesize should be accompanied with an improved nestmate recognition system. Comparative analyses of the worker CHC profiles indicate that A. dorsata workers exhibit a unique and more complex CHC profile than the other three honey bee species. This increased complexity is likely based on a developmental process that retains the capability to synthesize methyl-branched hydrocarbons as adults. Furthermore, two sets of behavioral experiments provide evidence that A. dorsata shows an improved nestmate discrimination ability compared to the phylogenetically ancestral A. florea, which is also open-nesting but does not form nest aggregations. The results of our study suggest that ecological traits like nesting in aggregation might be able to drive CHC profile diversification even in closely related insect species.
Background
Cuticular hydrocarbons (CHC) have been documented to play crucial roles as species- and sex-specific cues in the chemical communication systems of a wide variety of insects. However, whether they are sufficient by themselves as the sole cue triggering sexual behavior as well as preference of con- over heterospecific mating partners is rarely assessed. We conducted behavioral assays in three representative species of parasitoid wasps (Hymenoptera: Pteromalidae) to determine their reliance on CHC as species-specific sexual signaling cues.
Results
We found a surprising degree of either unspecific or insufficient sexual signaling when CHC are singled out as recognition cues. Most strikingly, the cosmopolitan species Nasonia vitripennis, expected to experience enhanced selection pressure to discriminate against other co-occurring parasitoids, did not discriminate against CHC of a partially sympatric species from another genus, Trichomalopsis sarcophagae. Focusing on the latter species, in turn, it became apparent that CHC are even insufficient as the sole cue triggering conspecific sexual behavior, hinting at the requirement of additional, synergistic sexual cues particularly important in this species. Finally, in the phylogenetically and chemically most divergent species Muscidifurax uniraptor, we intriguingly found both CHC-based sexual signaling as well as species discrimination behavior intact although this species is naturally parthenogenetic with sexual reproduction only occurring under laboratory conditions.
Conclusions
Our findings implicate a discrepancy in the reliance on and specificity of CHC as sexual cues in our tested parasitioid wasps. CHC profiles were not sufficient for unambiguous discrimination and preference behavior, as demonstrated by clear cross-attraction between some of our tested wasp genera. Moreover, we could show that only in T. sarcophagae, additional behavioral cues need to be present for triggering natural mating behavior, hinting at an interesting shift in signaling hierarchy in this particular species. This demonstrates the importance of integrating multiple, potentially complementary signaling modalities in future studies for a better understanding of their individual contributions to natural sexual communication behavior.
Background
Brood parasites can exert strong selection pressure on their hosts. Many brood parasites escape their detection by mimicking sensory cues of their hosts. However, there is little evidence whether or not the hosts are able to escape the parasites’ mimicry by changing these cues. We addressed this question by analyzing cuticular hydrocarbon (CHC) profiles of Cerceris and Philanthus wasps and their brood parasites, cuckoo wasps mimicking the CHC profiles of their hosts. Some of these hosts use hydrocarbons to preserve their prey against fungal infestation and thus, they cannot significantly change their CHC composition in response to chemical mimicry by Hedychrum brood parasites.
Results
We found that the CHC overlap between brood parasites and their hosts was lower in case of host wasps not preserving their prey than in case of prey-preserving host wasps, whose CHC evolution is constrained. Furthermore, the CHC profiles in non-preserving host wasps is more strongly diversified in females than in males, thus in the sex that is chemically mimicked by brood parasites.
Conclusion
Our results provide evidence for a chemical arms race between those hosts that are liberated from stabilizing selection on their chemical template and their parasites.
1. Protection against desiccation and chemical communication are two fundamental functions of cuticular hydrocarbons (CHCs) in insects. In the parasitoid jewel wasp Nasonia vitripennis (Walker), characterised by a cosmopolitan distribution through largely different environments, CHCs function as universally recognised female sex pheromones. However, CHC uniformity as basis for sexual recognition may conflict with the desiccation protection function, expected to display considerable flexibility through adaptation to different environmental conditions.
2. We compared male and female CHC profiles of N. vitripennis across a wide latitudinal gradient in Europe and correlated their CHC variation with climatic factors associated with desiccation. Additionally, we tested male mate discrimination behaviour between populations to detect potential variations in female sexual attractiveness.
3. Results did not conform to the general expectation that longer, straight‐chain CHCs occur in higher proportions in warmer and drier climates. Instead, unexpected environmental correlations of intermediate chain‐length CHCs (C31) were found exclusively in females, potentially reflecting the different life histories of the sexes in N. vitripennis.
4. Furthermore, we found no indication of population‐specific male mate preference, confirming the stability of female sexual attractiveness, likely conveyed through their CHC profiles. C31 mono‐ and C33 di‐methyl‐branched alkanes were consistently and most strongly associated with sexual dimorphism, suggesting their potential role in encoding the female‐specific sexual signalling function.
5. Our study sheds light on how both adaptive flexibility and conserved sexual attractiveness can potentially be integrated and encoded in CHC profiles of N. vitripennis females across a wide distribution range in Europe.
The recently observed consistent loss of β-diversity across ecosystems indicates increasingly homogeneous communities in patches of landscapes, mainly caused by increasing land-use intensity. Biodiversity is related to numerous ecosystem functions and stability. Therefore, decreasing β-diversity is also expected to reduce multifunctionality. To assess the impact of homogenization and to develop guidelines to reverse its potentially negative effects, we combine expertise from forest science, ecology, remote sensing, chemical ecology and statistics in a collaborative and experimental β-diversity approach. Specifically, we will address the question whether the Enhancement of Structural Beta Complexity (ESBC) in forests by silviculture or natural disturbances will increase biodiversity and multifunctionality in formerly homogeneously structured production forests. Our approach will identify potential mechanisms behind observed homogenization-diversity-relationships and show how these translate into effects on multifunctionality. At eleven forest sites throughout Germany, we selected two districts as two types of small ‘forest landscapes’. In one of these two districts, we established ESBC treatments (nine differently treated 50x50 m patches with a focus on canopy cover and deadwood features). In the second, the control district, we will establish nine patches without ESBC. By a comprehensive sampling, we will monitor 18 taxonomic groups and measure 21 ecosystem functions, including key functions in temperate forests, on all patches. The statistical framework will allow a comprehensive biodiversity assessment by quantifying the different aspects of multitrophic biodiversity (taxonomical, functional and phylogenetic diversity) on different levels of biodiversity (α-, β-, γ-diversity). To combine overall diversity, we will apply the concept of multidiversity across the 18 taxa. We will use and develop new approaches for quantification and partitioning of multifunctionality at α- and β- scales. Overall, our study will herald a new research avenue, namely by experimentally describing the link between β-diversity and multifunctionality. Furthermore, we will help to develop guidelines for improved silvicultural concepts and concepts for management of natural disturbances in temperate forests reversing past homogenization effects.
Insect brood parasites have evolved a variety of strategies to avoid being detected by their hosts. Few previous studies on cuckoo wasps (Hymenoptera: Chrysididae), which are natural enemies of solitary wasps and bees, have shown that chemical mimicry, i.e., the biosynthesis of cuticular hydrocarbons (CHC) that match the host profile, evolved in several species. However, mimicry was not detected in all investigated host-parasite pairs. The effect of host range as a second factor that may play a role in evolution of mimicry has been neglected, since all previous studies were carried out on host specialists and at nesting sites where only one host species occurred. Here we studied the cuckoo wasp Parnopes grandior, which attacks many digger wasp species of the genus Bembix (Hymenoptera: Crabronidae). Given its weak host specialization, P. grandior may either locally adapt by increasing mimicry precision to only one of the sympatric hosts or it may evolve chemical insignificance by reducing the CHC profile complexity and/or CHCs amounts. At a study site harbouring three host species, we found evidence for a weak but appreciable chemical deception strategy in P. grandior. Indeed, the CHC profile of P. grandior was more similar to all sympatric Bembix species than to a non-host wasp species belonging to the same tribe as Bembix. Furthermore, P. grandior CHC profile was equally distant to all the hosts' CHC profiles, thus not pointing towards local adaptation of the CHC profile to one of the hosts' profile. We conducted behavioural assays suggesting that such weak mimicry is sufficient to reduce host aggression, even in absence of an insignificance strategy, which was not detected. Hence, we finally concluded that host range may indeed play a role in shaping the level of chemical mimicry in cuckoo wasps.
Species living in sympatry and sharing a similar niche often express parallel phenotypes as a response to similar selection pressures. The degree of parallelism within underlying genomic levels is often unexplored, but can give insight into the mechanisms of natural selection and adaptation. Here, we use multi‐dimensional genomic associations to assess the basis of local and climate adaptation in two sympatric, cryptic Crematogaster levior ant species along a climate gradient. Additionally, we investigate the genomic basis of chemical communication in both species. Communication in insects is mainly mediated by cuticular hydrocarbons (CHCs), which also protect against water loss and, hence, are subject to changes via environmental acclimation or adaptation. The combination of environmental and chemical association analyses based on genome‐wide Pool‐Seq data allowed us to identify single nucleotide polymorphisms (SNPs) associated with climate and with chemical differences. Within species, CHC changes as a response to climate seem to be driven by phenotypic plasticity, since there is no overlap between climate‐ and CHC‐associated SNPs. The only exception is the odorant receptor OR22c, which may be a candidate for population‐specific CHC recognition in one of the species. Within both species, climate is significantly correlated with CHC differences, as well as to allele frequency differences. However, associated candidate SNPs, genes and functions are largely species‐specific and we find evidence for minimal parallel evolution only on the level of genomic regions (J = 0.04). This highlights that even closely related species may follow divergent evolutionary trajectories when expressing similar adaptive phenotypes.
Cryptic species and hidden ecological interactions of halictine bees along an elevational gradient
(2021)
Changes of abiotic and biotic conditions along elevational gradients represent serious challenges to organisms which may promote the turnover of species, traits and biotic interaction partners. Here, we used molecular methods to study cuticular hydrocarbon (CHC) profiles, biotic interactions and phylogenetic relationships of halictid bees of the genus Lasioglossum along a 2,900 m elevational gradient at Mt. Kilimanjaro, Tanzania. We detected a strong species turnover of morphologically indistinguishable taxa with phylogenetically clustered cryptic species at high elevations, changes in CHC profiles, pollen resource diversity, and a turnover in the gut and body surface microbiome of bees. At high elevations, increased proportions of saturated compounds in CHC profiles indicate physiological adaptations to prevent desiccation. More specialized diets with higher proportions of low‐quality Asteraceae pollen imply constraints in the availability of food resources. Interactive effects of climatic conditions on gut and surface microbiomes, CHC profiles, and pollen diet suggest complex feedbacks among abiotic conditions, ecological interactions, physiological adaptations, and phylogenetic constraints as drivers of halictid bee communities at Mt. Kilimanjaro.
In social groups, infections have the potential to spread rapidly and cause disease outbreaks. Here, we show that in a social insect, the ant Lasius neglectus, the negative consequences of fungal infections (Metarhizium brunneum) can be mitigated by employing an efficient multicomponent behaviour, termed destructive disinfection, which prevents further spread of the disease through the colony. Ants specifically target infected pupae during the pathogens non-contagious incubation period, utilising chemical 'sickness cues' emitted by pupae. They then remove the pupal cocoon, perforate its cuticle and administer antimicrobial poison, which enters the body and prevents pathogen replication from the inside out. Like the immune system of a metazoan body that specifically targets and eliminates infected cells, ants destroy infected brood to stop the pathogen completing its lifecycle, thus protecting the rest of the colony. Hence, in an analogous fashion, the same principles of disease defence apply at different levels of biological organisation.
1. The potential for competition is highest among species in close association. Despite net benefits for both parties, mutualisms can involve costs, including food competition. This might be true for the two neotropical ants Camponotus femoratus and Crematogaster levior, which share the same nest in a presumably mutualistic association (parabiosis).
2. While each nest involves one Crematogaster and one Camponotus partner, both taxa were recently found to comprise two cryptic species that show no partner preferences and seem ecologically similar. Since these cryptic species often occur in close sympatry, they might need to partition their niches to avoid competitive exclusion.
3. Here, we investigated first, is there interference competition between parabiotic Camponotus and Crematogaster, and do they prefer different food sources under competition? And second, is there trophic niche partitioning between the cryptic species of either genus?
4. Using cafeteria experiments, neutral lipid fatty acid and stable isotope analyses, we found evidence for interference competition, but also trophic niche partitioning between Camponotus and Crematogaster. Both preferred protein‐ and carbohydrate‐rich baits, but at protein‐rich baits Ca. femoratus displaced Cr. levior over time, suggesting a potential discovery‐dominance trade‐off between parabiotic partners. Only limited evidence was found for trophic differentiation between the cryptic species of each genus.
5. Although we cannot exclude differentiation in other niche dimensions, we argue that neutral dynamics might mediate the coexistence of cryptic species. This model system is highly suitable for further studies of the maintenance of species diversity and the role of mutualisms in promoting species coexistence.