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Schrader, L.

Publications and source records attributed to Schrader, L..

13 recordsLinked to original sources

Population genomics of the inquiline social parasite Acromyrmex insinuator and its leaf-cutting ant hosts A. echinatior and A. octospinosus reveals cryptic differentiation and reduced efficiency of selection in the parasite

Inquiline social parasites usurp colonies of closely related host ants to exploit their social resources. They are almost invariably rare, patchily distributed and difficult to study. Here we build on almost 25 years of Panamanian fieldwork on the social parasite Acromyrmex insinuator and its A. echinatior and A. octospinosus hosts, to perform a population genomic analysis to test hypotheses that have been suggested to shape the evolution of inquiline social parasites: 1. Do these parasites indeed have extremely reduced effective population size? 2. Does extant genetic variation at coding and non-coding sites carry signatures of erosion of adaptive potential? 3. Has A. insinuator become fully reproductively isolated from its sympatric hosts and how closely related are its primary and secondary host? We show that the two host species are completely distinct and that genetic diversity and effective population size of the social parasite are dramatically reduced despite ongoing but very minor recent gene flow between the parasite and its primary host A. echinatior. We also demonstrate that non-synonymous codon-sites evolved at rates nearly indistinguishable from synonymous codon-sites. This indicates a significant reduction in the efficiency of natural selection consistent with inquiline social parasite lineages generally being evolutionarily short-lived. We finally uncover clear sub-structure in the parasite population, with two genetically distinct lineages occurring in sympatry in the Panama Canal Zone, and with significant differences in their likelihood of exploiting the secondary host A. octospinosus and the primary host from which they segregated sympatrically ca. 1 MYA.

genomics↗

High-throughput phenomics of global ant biodiversity

The big data era in biology is underway, but the study of organismal form has been slow to capitalize on advances in imaging and computation. Modern imaging can digitize whole organisms, but low throughput has limited the effort to document morphological diversity. Within the open science initiative Antscan, we applied high-throughput synchrotron X-ray microtomography to capture phenotypes across a diverse and ecologically dominant insect group -- ants. We provide 2193 whole-body 3D ant datasets from 792 species to broadly cover the ant phylogeny with a global scope, also pairing phenomic data with genome sequencing projects. Scans acquired with standardized parameters facilitate automated analysis and free access to data can broaden the audience and incentivize methods development. Antscan presents a scalable approach to create libraries of diverse anatomies, heralding a new era of studies on the evolution, structure, and function of organismal phenotypes.

zoology↗

Epigenetic reprogramming by 5-aza-dC alters gene methylation and suppresses aggression in founding queens of the California harvester ant Pogonomyrmex californicus.

Epigenetic mechanisms are increasingly recognized as key drivers of phenotypic plasticity in social insects, where the caste and function of an individual is usually not determined by its genotype. These mechanisms may also regulate variation in social behavior or interactions and ultimately social organization. We experimentally manipulated genome-wide DNA methylation in founding queens of Pogonomyrmex californicus using the DNA methylation inhibitor decitabine (5-aza-20-deoxycytidine), to investigate the effect of DNA demethylation on aggressive interactions during colony founding in P. californicus, leading either to colonies with single (i.e., monogyny) or multiple queens (i.e., polygyny). Genome-wide methylation profiling showed widespread gene hypomethylation in treated queens, including those encoding the DNA methyltransferases DNMT1 and DNMT3. Furthermore, treated queens exhibited significantly reduced aggression in queen-queen interactions compared to untreated ones. Interestingly, genes linked to energy metabolism showed increased methylation in aggressive founding queens compared to non-aggressive queens. Our results highlight a potential epigenetic basis for behavioral and social variation, contributing to the understanding of social niche polymorphism in ants.

animal behavior and cognition↗

The impact of a fatty acid synthase gene in regulating a complex multifunctional trait essential for survival and sexual communication

The genetic basis of multi-functional traits shaped by both natural and sexual selection remains poorly understood. In insects, cuticular hydrocarbons (CHCs) are an excellent example of such traits, providing protection against different micro-climatic conditions while simultaneously encoding cues predominantly used in sexual signaling. The fatty acid synthase (fas) gene family has been implied as an important cornerstone in initiating and maintaining CHC functionality, whereas their exact biosynthetic and regulatory mechanisms have remained poorly understood. Here, we characterize a single fatty acid synthase gene (fas3) impacting the main CHC functions in the parasitoid wasp model organism Nasonia vitripennis. Knockdown of fas3 significantly decreases wasp survival under desiccation stress while also completely depleting sexual attractiveness of female wasps, where this trait naturally functions as sex pheromone. Transcriptomic analyses revealed that fas3 regulates other fas and CHC-associated genes, as well as key biosynthetic pathway hubs. We also identified striking sex-specific expression differences in fas3 across individual developmental stages, suggesting divergent functional roles of this gene in males and females. These findings largely advance our knowledge on the multi-functionality of fas genes in governing survival and sexual signaling and underscore their relevance for future studies on metabolomics, ecological adaptation, and sexual communication. Author SummaryTraits that serve both adaptive and reproductive functions--such as those involved in survival and mating success--are often complex, and their genetic foundations remain poorly understood. In insects, chemical compounds on the outer cuticle represent a prime example: they help prevent desiccation and act as key sexual signals. In this study, we investigate the gene fas3, a member of the fatty acid synthase family, in the parasitoid wasp Nasonia vitripennis, whose knockdown drastically reduces these surface chemicals. Consequently, both of their natural functionalities, namely enhancement of survival in dry conditions and female sexual attractiveness, are severely impaired. Transcriptomic analysis further revealed that fas3 also regulates multiple other genes, including those in further major biosynthetic pathways. Our findings shed light on how a single gene can coordinate the expression of multifunctional traits, contributing to both ecological adaptation and sexual communication.

genetics↗

Adaptive evolution of odorant receptors is associated with elaborations of social organization in ants

Cooperation in social insect colonies depends on complex chemical communication, requiring a large array of chemosensory receptors. Ant odorant receptors (ORs) were dramatically expanded compared to other insects, most notably in the "9-exon" subfamily, which was implicated in responding to cuticular hydrocarbons, a major class of signalling compounds. These observations indicate adaptive evolution of olfactory functions, but this process was never studied in the context of the evolution of specific sociobiological traits. The Global Ant Genomics Alliance has compiled 163 high-quality ant genomes, enabling detailed study of OR evolution in unprecedented detail. Analysing 55,068 ORs across the phylogeny, we tested for association between sociobiological traits and adaptive evolution of ORs, including gene duplication and adaptive sequence evolution. We identified strong enrichment of positive selection on 9-exon ORs in the ancestor of the formicoid clade, which evolved larger colonies and greater reproductive division of labour. This result indicates a key role of chemical communication in the early evolution of complex social organization. We also observed enrichment of positive selection on 9-exon ORs associated with the recent evolution of continuous worker polymorphism in multiple lineages. Surprisingly, the evolution of other sociobiological traits was associated with reduced positive selection on ORs. These results suggest that worker polymorphism involves more extensive adaptation of chemical communication compared to other aspects of ant sociobiology. By analysing the most comprehensive OR dataset to date, we provide new insights into the specific context in which ORs played a major role in the elaboration of social traits in ants.

evolutionary biology↗

Castes and developmental stages of the harvester ant P. californicus differ in genome-wide and gene specific DNA methylation

DNA methylation in social insects has been proposed as a key mechanism underlying both reproductive and non-reproductive caste determination by regulating gene expression in response to environmental cues. So far, studies on DNA methylation in social insects have yielded mixed results, with some studies finding no effect on caste determination or worker behaviour while others have reported such effects. In order to link DNA methylation to either process one first needs to show variation in DNA methylation between castes and developmental stages. This study determined cytosin methylation in a CpG context (CmpG) in the harvester ant Pogonomyrmex californicus using ONT (Oxford Nanopore Sequencing) sequencing in larvae, pupae, workers and queens, moreover we compared accuracy of methylation with the gold standard WGBS (Whole Genome Bisulfite Sequencing). Methylation sites were highly correlated between WGBS and ONT (r2=0.8). Overall, the P. californicus genome showed low levels of methylation (3%) which is comparable to what has been found in other Hymenopterans. DNA methylation was significantly increased in gene bodies and in particular exons and showed a significant decrease at the transcription start site and promotor region. Introns, intergenic regions and transposable elements have the lowest levels of DNA methylation. Gene body methylation was positively correlated with gene expression in queens, which is in accordance with other studies and the opposite of what is found in vertebrate studies. Both castes and developmental stages showed significant variation and differences in gene body methylation frequencies. Furthermore, castes and stages which have a high metabolic rate (queens and pupae) show higher DNA methylation, suggesting plasticity and an active role of DNA methylation in gene regulation and in extension caste regulation.

genomics↗

Queen loss fails to elicit physiological and transcriptional responses in workers of the invasive garden ant Lasius neglectus

Insect colonies with morphologically distinct castes have been called superorganisms because their queens and workers are functionally analogous to the germline and soma in metazoan bodies. In the haplodiploid ants, workers typically lost the sperm storage organ but retained ovaries so they can lay unfertilized eggs. Worker reproduction often occurs after queen loss and is accompanied by a number of physiological changes. However, in some evolutionarily derived ants, workers have become functionally sterile and in many of these species colonies contain multiple queens and can readily raise replacement queens - a syndrome characteristic for invasive ants. We hypothesized that the combination of full worker sterility and regular queen replacement should have eliminated important aspects of the physiological interdependence between queens and workers. We tested this hypothesis by analysing fat body gene expression and worker resistance to oxidative stress in colonies of the invasive ant Lasius neglectus with and without queens. We found age-related transcriptional shifts between young and old queens and young and old workers, suggesting rapid ageing in all castes. However, the removal of any queens in controlled experiments failed to elicit changes in the transcriptional activity and oxidative stress resistance of workers, consistent with our hypothesis. The invasive syndrome of this ant may thus have led to a somatic work force that evolved to be physiologically independent of queen presence.

evolutionary biology↗

The role of cuticular hydrocarbons in intraspecific aggression in the invasive ant Cardiocondyla obscurior

Cuticular hydrocarbons (CHCs) are important cues for nestmate discrimination and intraspecific aggression in ants. In invasive ants, diminished CHC profile diversity is suspected to contribute to the ecological and evolutionary success of populations by reducing intraspecific aggression between colonies. The ant Cardiocondyla obscurior has successfully colonized habitats around the world, reaching high local population densities. However, despite being invasive, colonies still react aggressively against each other, especially in interactions with non-nestmate alate queens. Here, we study whether CHCs are relevant for antagonistic interactions in this species, by combining behavioral experiments with gas-chromatography coupled with mass spectrometry (GC-MS). We show that queen and worker CHC profiles show pronounced quantitative as well as qualitative differences, that queens with depleted CHC profiles receive virtually no aggression from non-nestmates, and that aggression levels are positively correlated with the naturally occurring CHC profile differences between colonies. These findings provide first empirical evidence for a role of CHCs and chemical diversity in antagonistic behaviors against foreign queens in this species. They further suggest that invasive populations of C. obscurior are multicolonial and polydomous.

animal behavior and cognition↗

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 signaling. CHC profiles can consist of dozens of different compounds and are considered a prime example for a complex trait. 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. Taking advantage of the wasps haplo-diploid sex determination and cross-species fertility, we mapped 91 quantitative trait loci (QTL) explaining variation of a total of 43 CHCs in F2 hybrid males from interspecific crosses between three Nasonia species. To identify candidate genes, we localized orthologs of CHC biosynthesis-related genes in the Nasonia genomes. By doing so, 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 on chromosome 1 close to the centromere, 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 both Nasonia CHC profiles and many other Hymenoptera. Our study considerably extends our knowledge on the so far little-known genetic and genomic architecture governing biosynthesis and variation of this fundamental compound class, establishing a model for methyl-branched alkane genetics in the Hymenoptera in general.

genetics↗

Genomic architecture and evolutionary dynamics of a social niche polymorphism in the California harvester ant, Pogonomyrmex californicus

Social insects vary considerably in their social organization both between and within species. In the California harvester ant, Pogonomyrmex californicus (Buckley 1867), colonies are commonly founded and headed by a single queen (haplometrosis, primary monogyny). However, in some populations in California (USA), unrelated queens cooperate not only during founding (pleometrosis) but throughout the life of the colony (primary polygyny). The genetic architecture and evolutionary dynamics of this complex social niche polymorphism (haplometrosis vs pleometrosis) have remained unknown. Here, we provide a first analysis of its genomic basis and evolutionary history using population genomics comparing individuals from a haplometrotic population to those from a pleometrotic population. We discovered a recently evolved (< 200 k years), 8 Mb non-recombining region segregating with the observed social niche polymorphism. This region shares several characteristics with supergenes underlying social polymorphisms in other socially polymorphic ant species. However, we also find remarkable differences from previously described social supergenes. Particularly, four additional genomic regions not in linkage with the supergene show signatures of a selective sweep in the pleometrotic population. Within these regions, we find for example genes crucial for epigenetic regulation via histone modification (chameau) and DNA methylation (Dnmt1). These results suggest that social morph in this species is a polygenic trait involving a potential young supergene. Further studies targeting haplo- and pleometrotic individuals from a single population are however required to conclusively resolve whether these genetic differences underlie the alternative social phenotypes or have emerged through genetic drift.

evolutionary biology↗

High-Quality Genome Assembly and Annotation of the California Harvester Ant Pogonomyrmex californicus (Buckley, 1867)

The harvester ant genus Pogonomyrmex is endemic to arid and semiarid habitats and deserts of North and South America and California harvester ant Pogonomyrmex californicus is the most widely distributed Pogonomyrmex species in the North America. P. californicus colonies are usually monogynous, i.e. a colony has one queen. However, in a few populations in California, primary polygyny evolved, i.e. several queens cooperate in colony founding after their mating flights and continue to coexist in mature colonies. Here, we present high quality genome assembly and annotation of P. californicus. The size of the assembly is 241 Mb, which is in good agreement with previously estimated genome size and we were able to annotate 17,889 genes in total, including 15,688 protein-coding ones with BUSCO completeness at the 95% level. This high quality genome will pave the way for investigations of the genomic underpinnings of social polymorphism in queen number, regulation of aggression, and the evolution of adaptations to dry habitats in P. californicus.

genomics↗

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

BackgroundParasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biocontrol, and infecting aphids requires overcoming both aphid defenses and their defensive endosymbionts. ResultsWe present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp), highly syntenic, and the most AT-rich reported thus far for any arthropod (GC content: 25.8% and 23.8%). This nucleotide bias is accompanied by skewed codon usage, and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and age-specific energy demands. We identify expansions of F-box/Leucine-rich-repeat proteins, suggesting that diversification in this gene family may be associated with their broad host range or with countering defenses from aphids endosymbionts. The absence of some immune genes (Toll and Imd pathways) resembles similar losses in their aphid hosts, highlighting the potential impact of symbiosis on both aphids and their parasitoids. ConclusionsThese findings are of fundamental interest for insect evolution and beyond. This will provide a strong foundation for further functional studies including coevolution with respect to their hosts, the basis of successful infection, and biocontrol. Both genomes are available at https://bipaa.genouest.org.

genomics↗

The transcription factor Shox2 shapes thalamocortical neuron firing properties by regulation of key ion channels

Thalamocortical neurons (TCNs) transmit information about sensory stimuli from the thalamus to the cortex. In response to different physiological states and demands TCNs can fire in tonic and/or phasic burst modes. These firing properties of TCNs are supported by precisely timed inhibitory synaptic inputs from the thalamic reticular nucleus and intrinsic currents, including T-type Ca2+ and HCN currents. These intrinsic currents are mediated by Cav3.1 and HCN channel subunits, and alterations in expression or modulation of these channels can have dramatic implications on thalamus function. The factors that regulate these currents controlling the firing patterns important for integration of the sensory stimuli and the consequences resulting from the disruption of these firing patterns are not well understood. Shox2 is a transcription factor known to be important for pacemaker activity in the heart. We show here that Shox2 is also expressed in adult mouse thalamus. We hypothesized that genes regulated by Shox2s transcriptional activity may be important for physiological properties of TCNs. In this study, we used RNA sequencing on control and Shox2 knockout mice to determine Shox2-affected genes and revealed a network of ion channel genes important for neuronal firing properties. Quantitative PCR confirmed that expression of Hcn2, 4 and Cav3.1 genes were affected by Shox2 KO. Western blotting showed expression of the proteins for these channels was decreased in the thalamus, and electrophysiological recordings showed that Shox2 KO impacted the firing and synaptic properties of TCNs. Finally, behavioral studies revealed that Shox2 expression in TCNs play a role in somatosensory function and object recognition memory. Overall, these results reveal Shox2 as a transcription factor important for TCN firing properties and thalamic function.

neuroscience↗