Ecology and Evolution of Communication in Social Insects.

Insect life strategies comprise all levels of sociality from solitary to eusocial, in which individuals form persistent groups and divide labor. With increasing social complexity, the need to communicate a greater diversity of messages arose to coordinate division of labor, group cohesion, and concerted actions. Here we summarize the knowledge on prominent messages in social insects that inform about reproduction, group membership, resource locations, and threats and discuss potential evolutionary trajectories of each message in the context of social complexity.

Olfaction is essential for nest recognition in solitary Hymenoptera.

Flying insects are believed to rely primarily on visual cues for orientation, with chemical cues often being overlooked. In the case of solitary bees and wasps, being able to return successfully to their nests and provision their brood cells is paramount for the survival of the species. While vision has been shown to be involved in pinpointing the nest location, our results confirm that olfaction is important in nest recognition. The large diversity in nesting strategies observed among solitary Hymenoptera makes them an excellent model to comparatively study the use of olfactory cues from the nesting individual for nest recognition. We have analyzed the chemical profiles of three nesting bees (Osmia spp.) and one wasp (Sceliphron curvatum) and that of their nest entrances. A striking match in the identified chemicals was revealed between each nest and its occupant. When the chemicals were removed from the nest, a clear behavioral response could be observed for Osmia cornuta. This shows the importance of olfactory cues in complementing visual orientation for precise homing in a solitary species, thereby opening up various promising biological questions in the fields of sensory perception and complementation, or the trade-offs of nest aggregation and associated costs.

The heat is on: reduced detection of floral scents after heatwaves in bumblebees.

Global climate change disrupts key ecological processes and biotic interactions. The recent increase in heatwave frequency and severity prompts the evaluation of physiological processes that ensure the maintenance of vital ecosystem services such as pollination. We used experimental heatwaves to determine how high temperatures affect the bumblebees' ability to detect floral scents. Heatwaves induced strong reductions in antennal responses to floral scents in both tested bumblebee species (Bombus terrestris and Bombus pascuorum). These reductions were generally stronger in workers than in males. Bumblebees showed no consistent pattern of recovery 24 h after heat events. Our results suggest that the projected increased frequency and severity of heatwaves may jeopardize bumblebee-mediated pollination services by disrupting the chemical communication between plants and pollinators. The reduced chemosensitivity can decrease the bumblebees' abilities to locate food sources and lead to declines in colonies and populations.

Species- and sex-specific chemical composition from an internal gland-like tissue of an African frog family.

Intraspecific chemical communication in frogs is understudied and the few published cases are limited to externally visible and male-specific breeding glands. Frogs of the family Odontobatrachidae, a West African endemic complex of five morphologically cryptic species, have large, fatty gland-like strands along their lower mandible. We investigated the general anatomy of this gland-like strand and analysed its chemical composition. We found the strand to be present in males and females of all species. The strand varies in markedness, with well-developed strands usually found in reproductively active individuals. The strands are situated under particularly thin skin sections, the vocal sac in male frogs and a respective area in females. Gas-chromatography/mass spectrometry and multivariate analysis revealed that the strands contain sex- and species-specific chemical profiles, which are consistent across geographically distant populations. The profiles varied between reproductive and non-reproductive individuals. These results indicate that the mandibular strands in the Odontobatrachidae comprise a so far overlooked structure (potentially a gland) that most likely plays a role in the mating and/or breeding behaviour of the five Odontobatrachus species. Our results highlight the relevance of multimodal signalling in anurans, and indicate that chemical communication in frogs may not be restricted to sexually dimorphic, apparent skin glands.

Active around the year: Butterflies and moths adapt their life cycles to a warming world.

Living in a warming world requires adaptations to altered annual temperature regimes. In Europe, spring is starting earlier, and the vegetation period is ending later in the year. These climatic changes are leading not only to shifts in distribution ranges of flora and fauna, but also to phenological shifts. Using long-term observation data of butterflies and moths collected during the past decades across northern Austria, we test for phenological shifts over time and changes in the number of generations. On average, Lepidoptera adults emerged earlier in the year and tended to extend their flight periods in autumn. Many species increased the annual number of generations. These changes were more pronounced at lower altitudes than at higher altitudes, leading to an altered phenological zonation. Our findings indicate that climate change does not only affect community composition but also the life history of insects. Increased activity and reproductive periods might alter Lepidoptera-host plant associations and food webs.

Cuticular Hydrocarbon Profiles of Himalayan Bumble Bees (Hymenoptera: Bombus Latreille) are Species-Specific and Show Elevational Variation.

Bumble bees are important pollinators in natural environments and agricultural farmlands, and they are in particular adapted to harsh environments like high mountain habitats. In these environments, animals are exposed to low temperature and face the risk of desiccation. The Eastern Himalayas are one of the recognized biodiversity hotspots worldwide. The area covers subtropical rainforest with warm temperature and high precipitation as well as high mountain ranges with peaks reaching up to 7,000 m, shaping a diverse floral and faunal community at the different elevational zones. To identify possible adaptation strategies, we investigated the cuticular hydrocarbon profiles of four bumble bee species occurring at different elevational ranges in Arunachal Pradesh, the northeastern most state in India. At 17 locations along an elevational gradient, we collected workers of two species from lower elevations (B. albopleuralis and B. breviceps; ~ 100 m - 3,000 m asl) and two species from higher elevations (B. prshewalskyi and B. mirus; ~ 2,800 m - 4,500 m asl). The CHC profiles of all four species showed a significant degree of variation in the composition of hydrocarbons, indicating species specificity. We also found clear correlation with elevation. The weighted mean chain length of the hydrocarbons significantly differed between the low and high elevation species, and the proportion of saturated hydrocarbons in CHC profiles significantly increased with the elevational range of the bumble bee species. Our results indicate that bumble bees living at high elevations reduce the risk of water loss by adapting their CHC composition on their cuticle, a phenomenon that has also been found in other insects like ants and fruit flies.

The de novo genome of the Black-necked Snakefly (Venustoraphidia nigricollis Albarda, 1891): A resource to study the evolution of living fossils.

Snakeflies (Raphidioptera) are the smallest order of holometabolous insects that have kept their distinct and name-giving appearance since the Mesozoic, probably since the Jurassic, and possibly even since their emergence in the Carboniferous, more than 300 million years ago. Despite their interesting nature and numerous publications on their morphology, taxonomy, systematics, and biogeography, snakeflies have never received much attention from the general public, and only a few studies were devoted to their molecular biology. Due to this lack of molecular data, it is therefore unknown, if the conserved morphological nature of these living fossils translates to conserved genomic structures. Here, we present the first genome of the species and of the entire order of Raphidioptera. The final genome assembly has a total length of 669 Mbp and reached a high continuity with an N50 of 5.07 Mbp. Further quality controls also indicate a high completeness and no meaningful contamination. The newly generated data was used in a large-scaled phylogenetic analysis of snakeflies using shared orthologous sequences. Quartet score and gene concordance analyses revealed high amounts of conflicting signals within this group that might speak for substantial incomplete lineage sorting and introgression after their presumed re-radiation after the asteroid impact 66 million years ago. Overall, this reference genome will be a door-opening dataset for many future research applications, and we demonstrated its utility in a phylogenetic analysis that provides new insights into the evolution of this group of living fossils.

Improving Agri-environmental Schemes: Suggestions from Farmers and Nature Managers in a Central European Region.

Agri-environmental schemes (AES) are important policy instruments within the Common Agricultural Policy (CAP) of the European Union for environmental protection. Due to the voluntary nature of AES, their attractiveness to farmers and stakeholders involved in nature management and protection (nature managers) is essential for high participation levels. This study aims to assess farmers' and nature managers' ideas to improve agri-environmental schemes. We analyzed suggestions of 825 farmers and 118 nature managers for improvements of AES collected in a large-scale survey in Bavaria, Germany. A content analysis was applied to categorize and compare suggestions by farmers (differentiated into two groups through a cluster analysis) and nature managers. The results reveal that stakeholders were highly willing to share ideas and made detailed suggestions for improvements and individual measures. They were aware of the importance of protecting nature and promoting biodiversity in agricultural landscapes and acknowledged the necessity of (financial) support programs. Farmers placed more emphasis on the practicability and profitability of measures on arable land, while nature managers tended to propose policy-related ideas focusing on nature protection, biodiversity, and specific species. Among farmers, suggestions differed with farm characteristics such as the operation mode (full-time, part-time). These findings can support the design of future AES, accounting for different background situations and thereby increasing acceptability. This includes considering perspectives from different stakeholder groups and creating regionally adapted programs with varying levels of flexibility and practicability.

Metabolomics evaluation of the photochemical impact of violet-blue light (405 nm) on ex vivo platelet concentrates.

INTRODUCTION: Microbicidal violet-blue light in the visible spectrum (405 nm) has been under evaluation for pathogen inactivation in ex vivo human plasma and platelets (PLTs) stored in plasma. Results to date have demonstrated that several blood-borne infectious disease-causing pathogens can be successfully reduced to significantly low levels in the light-treated plasma and PLTs. METHOD: In order to evaluate whether the microbicidal 405 nm light is safe for the treatment of PLT concentrates for pathogen inactivation, LC/MS-based metabolomics analyses were performed to evaluate the overall impact of 405 nm violet-blue light treatment on ex vivo PLT concentrates suspended in plasma and on plasma itself, and to identify metabolome changes in intra-platelet and extra-cellular medium (i.e., plasma). RESULTS: The metabolomics data identified that platelet activating factors (PAFs), agonists and prostaglandins, which can influence PLT basic functions such as integrity, activation, and aggregation potential were unaltered, suggesting that 405 nm light illumination is safe regarding PLT basic functions. Distinct increases in hydroxyl fatty acids and aldehydes, as well as decreases in antioxidant metabolites indicated that reactive oxygen species (ROS) were generated at high levels after only one hour of exposure to 405 nm light. Distinctly changed endogenous photosensitizer metabolites after 1 h of light exposure provided good evidence that 405 nm light was an effective microbicide acting through ROS mechanism and no external additive photosensitizers were required.

Enhancing the structural diversity between forest patches-A concept and real-world experiment to study biodiversity, multifunctionality and forest resilience across spatial scales.

Intensification of land use by humans has led to a homogenization of landscapes and decreasing resilience of ecosystems globally due to a loss of biodiversity, including the majority of forests. Biodiversity-ecosystem functioning (BEF) research has provided compelling evidence for a positive effect of biodiversity on ecosystem functions and services at the local (α-diversity) scale, but we largely lack empirical evidence on how the loss of between-patch ß-diversity affects biodiversity and multifunctionality at the landscape scale (γ-diversity). Here, we present a novel concept and experimental framework for elucidating BEF patterns at α-, ß-, and γ-scales in real landscapes at a forest management-relevant scale. We examine this framework using 22 temperate broadleaf production forests, dominated by Fagus sylvatica. In 11 of these forests, we manipulated the structure between forest patches by increasing variation in canopy cover and deadwood. We hypothesized that an increase in landscape heterogeneity would enhance the ß-diversity of different trophic levels, as well as the ß-functionality of various ecosystem functions. We will develop a new statistical framework for BEF studies extending across scales and incorporating biodiversity measures from taxonomic to functional to phylogenetic diversity using Hill numbers. We will further expand the Hill number concept to multifunctionality allowing the decomposition of γ-multifunctionality into α- and ß-components. Combining this analytic framework with our experimental data will allow us to test how an increase in between patch heterogeneity affects biodiversity and multifunctionality across spatial scales and trophic levels to help inform and improve forest resilience under climate change. Such an integrative concept for biodiversity and functionality, including spatial scales and multiple aspects of diversity and multifunctionality as well as physical and environmental structure in forests, will go far beyond the current widely applied approach in forestry to increase resilience of future forests through the manipulation of tree species composition.

Global change drives phenological and spatial shifts in Central European longhorn beetles (Coleoptera, Cerambycidae) during the past 150 years.

Temperature increases and land-use changes induce altered annual activity periods of arthropods. However, sufficiently resolved long-term data sets (> 100 years) are mostly missing. We use a data set of longhorn beetle records (71 species) collected in Luxembourg 1864-2014. Increase of annual temperatures was significantly correlated with an earlier annual appearance. Forty-four species present before and after 1980 appeared on average 8.2 days earlier in the year in the more recent period. Since 1950, the estimated shift was 0.26 days per year. Increase of temperature in spring (March-June) preponed the first appearance of beetles by on average 9.6 days per 1 °C. We found significant changes in the composition of beetle communities, with a net gain in species richness during the last 40 years. Eleven species recorded only after 1997 were characterized by comparatively early annual appearance. Smaller beetles tended to appear earlier in the year in comparison to large-bodied species. Shifts in phenology did not correlate with species Red List status. As also demonstrated by our data, climate change in general affects insect phenologies and changes species composition. However, land-use change has taken place in parallel with climate change. Both aspects of global change are influencing the changes in longhorn beetle occurrences in Luxemburg in their combination. This might be most clearly reflected in the strong decrease of species with continental climate niches dwelling in old-growth deciduous forests that apparently are threatened by the loss of these habitats and increasing spring temperatures.

The Alarm Pheromone and Alarm Response of the Clonal Raider Ant.

Ants communicate via an arsenal of different pheromones produced in a variety of exocrine glands. For example, ants release alarm pheromones in response to danger to alert their nestmates and to trigger behavioral alarm responses. Here we characterize the alarm pheromone and the alarm response of the clonal raider ant Ooceraea biroi, a species that is amenable to laboratory studies but for which no pheromones have been identified. During an alarm response, ants quickly become unsettled, leave their nest pile, and are sometimes initially attracted to the source of alarm, but ultimately move away from it. We find that the alarm pheromone is released from the head of the ant and identify the putative alarm pheromone as a blend of two compounds found in the head, 4-methyl-3-heptanone and 4-methyl-3-heptanol. These compounds are sufficient to induce alarm behavior alone and in combination. They elicit similar, though slightly different behavioral features of the alarm response, with 4-methyl-3-heptanone being immediately repulsive and 4-methyl-3-heptanol being initially attractive before causing ants to move away. The behavioral response to these compounds in combination is dose-dependent, with ants becoming unsettled and attracted to the source of alarm pheromone at low concentrations and repulsed at high concentrations. While 4-methyl-3-heptanone and 4-methyl-3-heptanol are known alarm pheromones in other more distantly related ant species, this is the first report of the chemical identity of a pheromone in O. biroi, and the first alarm pheromone identified in the genus Ooceraea. Identification of a pheromone that triggers a robust, consistent, and conserved behavior, like the alarm pheromone, provides an avenue to dissect the behavioral and neuronal mechanisms underpinning chemical communication.

Teaching the Modeling of Human-Environment Systems: Acknowledging Complexity with an Agent-Based Model.

Agent-based modeling is a promising tool for familiarizing students with complex systems as well as programming skills. Human-environment systems, for instance, entail complex interdependencies that need to be considered when modeling these systems. This complexity is often neglected in teaching modeling approaches. For a heterogeneous group of master's students at a German university, we pre-built an agent-based model. In class, this was used to teach modeling impacts of land use policies and markets on ecosystem services. As part of the course, the students had to perform small research projects with the model in groups of two. This study aims to evaluate how well students could deal with the complexity involved in the model based on their group work outcomes. Chosen indicators were, e.g., the appropriateness of their research goals, the suitability of the methods applied, and how well they acknowledged the limitations. Our study results revealed that teaching complex systems does not need to be done with too simplistic models. Most students, even with little background in modeling and programming, were able to deal with the complex model setup, conduct small research projects, and have a thoughtful discussion on the limitations involved. With adequate theoretical input during lectures, we recommend using models that do not hide the complexity of the systems but foster a realistic simplification of the interactions. Supplementary Information: The online version contains supplementary material available at 10.1007/s10956-022-10022-z.

Smaller adult fish size in warmer water is not explained by elevated metabolism.

Fish and other ectotherms living in warmer waters often grow faster as juveniles, mature earlier, but become smaller adults. Known as the temperature-size rule (TSR), this pattern is commonly attributed to higher metabolism in warmer waters, leaving fewer resources for growth. An alternative explanation focuses on growth and reproduction trade-offs across temperatures. We tested these hypotheses by measuring growth, maturation, metabolism and reproductive allocation from zebrafish populations kept at 26 and 30°C across six generations. Zebrafish growth and maturation followed TSR expectations but were not explained by baseline metabolic rate, which converged between temperature treatments after a few generations. Rather, we found that females at 30°C allocated more to reproduction, especially when maturing at the smallest sizes. We show that elevated temperatures do not necessarily increase baseline metabolism if sufficient acclimation is allowed and call for an urgent revision of modelling assumptions used to predict population and ecosystem responses to warming.

Genetic and genomic architecture of species-specific cuticular hydrocarbon variation in parasitoid wasps.

Cuticular hydrocarbons (CHCs) serve two fundamental functions in insects: protection against desiccation and chemical signalling. How the interaction of genes shapes CHC profiles, which are essential for insect survival, adaptation and reproductive success, is still poorly understood. Here we investigate the genetic and genomic basis of CHC biosynthesis and variation in parasitoid wasps of the genus Nasonia. We mapped 91 quantitative trait loci (QTL) explaining the variation of a total of 43 CHCs in F2 hybrid males from interspecific crosses between three Nasonia species. To identify candidate genes, we localized orthologues of CHC biosynthesis-related genes in the Nasonia genomes. We discovered multiple genomic regions where the location of QTL coincides with the location of CHC biosynthesis-related candidate genes. Most conspicuously, on a region close to the centromere of chromosome 1, multiple CHC biosynthesis-related candidate genes co-localize with several QTL explaining variation in methyl-branched alkanes. The genetic underpinnings behind this compound class are not well understood so far, despite their high potential for encoding chemical information as well as their prevalence in hymenopteran CHC profiles. Our study considerably extends our knowledge on the genetic architecture governing this important compound class, establishing a model for methyl-branched alkane genetics in the Hymenoptera in general.

Climate, immigration and speciation shape terrestrial and aquatic biodiversity in the European Alps.

Quaternary climate fluctuations can affect speciation in regional biodiversity assembly in two non-mutually exclusive ways: a glacial species pump, where isolation in glacial refugia accelerates allopatric speciation, and adaptive radiation in underused adaptive zones during ice-free periods. We detected biogeographic and genetic signatures associated with both mechanisms in the assembly of the biota of the European Alps. Age distributions of endemic and widespread species within aquatic and terrestrial taxa (amphipods, fishes, amphibians, butterflies and flowering plants) revealed that endemic fish evolved only in lakes, are highly sympatric, and mainly of Holocene age, consistent with adaptive radiation. Endemic amphipods are ancient, suggesting preglacial radiation with limited range expansion and local Pleistocene survival, perhaps facilitated by a groundwater-dwelling lifestyle. Terrestrial endemics are mostly of Pleistocene age and are thus more consistent with the glacial species pump. The lack of evidence for Holocene adaptive radiation in the terrestrial biome is consistent with faster recolonization through range expansion of these taxa after glacial retreats. More stable and less seasonal ecological conditions in lakes during the Holocene may also have contributed to Holocene speciation in lakes. The high proportion of young, endemic species makes the Alpine biota vulnerable to climate change, but the mechanisms and consequences of species loss will likely differ between biomes because of their distinct evolutionary histories.

Immune challenges increase network centrality in a queenless ant.

Social animals display a wide range of behavioural defences against infectious diseases, some of which increase social contacts with infectious individuals (e.g. mutual grooming), while others decrease them (e.g. social exclusion). These defences often rely on the detection of infectious individuals, but this can be achieved in several ways that are difficult to differentiate. Here, we combine non-pathogenic immune challenges with automated tracking in colonies of the clonal raider ant to ask whether ants can detect the immune status of their social partners and to quantify their behavioural responses to this perceived infection risk. We first show that a key behavioural response elicited by live pathogens (allogrooming) can be qualitatively recapitulated by immune challenges alone. Automated scoring of interactions between all colony members reveals that this behavioural response increases the network centrality of immune-challenged individuals through a general increase in physical contacts. These results show that ants can detect the immune status of their nest-mates and respond with a general 'caring' strategy, rather than avoidance, towards social partners that are perceived to be infectious. Finally, we find no evidence that changes in cuticular hydrocarbon profiles drive these behavioural effects.

Little parallelism in genomic signatures of local adaptation in two sympatric, cryptic sister species.

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.

Biogeography of Italy revisited: genetic lineages confirm major phylogeographic patterns and a pre-Pleistocene origin of its biota.

Warm-adapted species survived the cold stages of the past glacial-interglacial cycles in southern European peninsulas and recolonized major parts of Central and Northern Europe in the wake of postglacial warming. However, many of the genetic lineages which differentiated within these refugia predate even the Pleistocene. One of these refugia is the Italian Peninsula with its surrounding islands. In this meta-analysis, we compiled phylogeographic patterns of multiple species across this region. We transformed existing geographic information on 78 animal and plant species (with a total of 471 genetic lineages) within 17 predefined areas into presence/absence matrices. We elaborated three matrices: (i) only old lineages exclusively distinguished by deep splits, (ii) only young lineages distinguished by shallow (i.e. recent) splits, and (iii) presence/absence of the respective species. To infer biogeographic relationships between the predefined areas, we performed bootstrapped neighbour joining cluster analyses on these three matrices. In addition, we reviewed the geological history of Italy to identify causes of the observed biogeographic patterns. We found Sardinia and Corsica to be biogeographically closely linked with each other, and that they diverge strongly from all other regions. Sicily also diverges strongly from all other regions, while the intra-island differentiation was comparatively low. On the Italian mainland, Calabria exhibited the most pronounced biogeographic differentiation, often with several lineages present, resulting from old vicariance events within the region. Furthermore, southern Apulia and the Po Plain with adjoining areas of northern peninsular Italy displayed considerable distinctiveness. Admixture prevailed in the areas between these three regions. The ancient isolation of Sicily, as well as Sardinia plus Corsica, resulted in endemic lineages with only moderate recent exchange with adjacent mainland regions. Pronounced diversification occurs within the Italian Peninsula. The complex tectonic activities, such as shifting (micro)plates, submergence of major parts of peninsular Italy with the genesis of numerous Pliocene islands, in combination with the climatic cycles during the Pleistocene have most likely generated the current biogeographic pattern of species. Immigrations from the Balkan Peninsula into northern Italy partly accounted for the distinctiveness of this region.

Evaluation of the Performance of Lipidyzer Platform and Its Application in the Lipidomics Analysis in Mouse Heart and Liver.

Lipids play important roles in cell signaling, energy storage, and as major structural components of cell membranes. To date, little work has been conducted to show the extent of tissue specificity of lipid compositions. Here, the recently acquired Lipidyzer platform was employed in this pilot study: (i) to assess the performance of the Lipidyzer platform, (ii) to explore lipid profiles in liver and cardiac tissue in mice, (iii) to examine sex-specific differences in lipids in the liver tissue, and (iv) to evaluate biological variances in lipidomes present in animals. In total, 787 lipid species from 13 lipid classes were measured in the liver and heart. Lipidomics data from the Lipidyzer platform were very reproducible with the coefficient of variations of the quality control (QC) samples, ∼10%. The total concentration of the cholesterol esters (CE) lipid class, and specifically CE(16:1) and CE(18:1) species, showed sex differences in the liver. Cardiac tissue had higher levels of phospholipids containing docosahexaenoic acid, which could be related to heart health status and function. Our results demonstrate the usefulness of the Lipidyzer platform in identifying differences in lipid profile at the tissue level and between male and female mice in specific tissues.