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Privman, E.

Publications and source records attributed to Privman, E..

16 recordsLinked to original sources

Large-scale genomic rearrangements are a potential explanation for reproductive isolation in the Pogonomyrmex dependent-lineage system

Genetic variation is the raw material for evolution. One source of variation is chromosomal rearrangements, which can bring genes together and form genetic linkage. Rearrangements can also suppress recombination and gene flow, as in the case of sex chromosome evolution. We conducted the first population genomic study of the red harvester ant Pogonomyrmex barbatus to investigate genomic rearrangements that differentiate the lineages J1 and J2 in the "dependent-lineage system" (also known as "social hybridogenesis"). In this unusual reproductive system, males and females from different lineages mate to create hybrids, yet these hybrids develop into sterile offspring (workers), and so the two lineages remain reproductively isolated. We sequenced high-quality reference genomes for the two lineages to search for a potential explanation of the suppression of gene flow between them. Comparison of the two genome assemblies revealed multiple large-scale genomic rearrangements, all of which occurred in the J1 lineage. The rearrangements formed some of the largest J1 chromosomes, including the largest scaffold in the assembly that was formed by at least two translocation events and additional intra-chromosomal rearrangements. The translocations brought together 118 odorant receptor (OR) genes on this rearranged chromosome, 44 of which are 9-exon ORs, which are implicated in chemical communication in ants. We also identified an enrichment of transposable elements in a large synteny gap between the translocated segments. The discovery of multiple translocations that formed large rearranged chromosomes provides a potential explanation for the reproductive isolation between the pair of dependent lineages in this system, and opens the way for the study of the molecular genetic basis of an intriguing evolutionary phenomenon in these and in other ant lineages.

evolutionary biology↗

Shifts in demography in changing ecological conditions in a dependent-lineage population of harvester ant colonies

Environmental stress can influence population dynamics and shift selection pressures. We considered the demographic effects since 2011 of intensifying drought in a J1/J2 dependent-lineage population, monitored since 1988, of the red harvester ant, Pogonomyrmex barbatus. A queen must mate with males of both dependent lineages to found a viable colony; mating with the same lineage results in a gyne, while mating with the other lineage results in a worker. We used reduced representation genomic sequencing of workers from 407 colonies, ages 1-3, mostly sampled in 2021-23, to determine colony lineage, identify sets of colonies with the same mitotype, and estimate kinship between mother-daughter pairs. We found that the rare lineage J1 became even more rare, from 39% in 2011 to 25% in 2023. This creates pressure on J1 to produce more sperm or more males to allow the population to persist. We compared survival and numbers of offspring produced in the two lineages and in sets of colonies with the same mitotypes, using census data. Survival and fecundity were similar among 5 J1 and 6 J2 mitotype groups, showing no evidence for selection favoring any mitotype. We identified 62 mother-daughter colony pairs. These included 14 grandmother-triplets, with most grandmothers found in J2, suggesting that some families dominate each mitotype group. Within the 62 mother-daughter pairs, those from J1 tended to live longer than J2 colonies, maintaining a low but constant fecundity rate, while J2 colonies showed the highest fecundity at ages 11-17. Our results suggest that increasingly harsh ecological conditions are shaping population dynamics more rapidly than selection for phenotypic traits that could facilitate adaptation.

evolutionary biology↗

Genomic architecture of species-specific sex pheromone variation and mate choice

Speciation often begins with subtle changes in sexual communication and mate choice, yet the genetic basis of these early reproductive barriers remains largely unresolved. Here, we dissect the chemical and genomic architecture underlying species-specific female cuticular sex pheromones and their role in mate choice in two closely related parasitoid wasp species. Using high-resolution quantitative trait locus (QTL) mapping, fine-scale chemical profiling, and behavioral assays on hybrid populations, we identify three methyl-branched alkanes as key pheromonal compounds that strongly predict male mating preferences. QTL explaining their species-specific variation partially co-localize with genomic regions enriched for candidate genes involved in cuticular hydrocarbon biosynthesis, including cytochrome P450 enzymes and fatty acid synthases. These findings suggest a potential mechanistic link between the variation in these gene clusters and species-specific chemical signaling. Further comparative analyses reveal hitherto unrecognized sex-specific regulatory effects, cytoplasmic influences, and complex genomic interactions shaping the variation in these pheromonal profiles. This study is among the first to connect individual pheromone compounds with mate choice and their underlying genomic basis in a haplodiploid system, offering a rare glimpse into how chemical divergence can reinforce behavioral isolation and potentially drive early speciation.

evolutionary biology↗

Testing for positive selection in multi-copy gene families using a reconciliation approach

Multi-copy gene families evolve through dynamic processes of duplication, loss, and sequence divergence, often exhibiting complex paralogy and orthology relationships that complicate the detection of adaptive evolution. Traditional dN/dS-based positive selection analyses are typically limited to single-copy genes, overlooking most of the adaptive signal in multi-copy families. We present a novel pipeline that integrates existing tools to map branch-specific positive selection events from gene trees onto species phylogenies. Our approach incorporates a normalization procedure that corrects for biases caused by variable branch lengths, reducing false enrichment signals on longer branches. Applied to the odorant receptor repertoires of ants, the framework successfully identified branches of the species tree enriched for positive selection, revealing clade-specific adaptive patterns obscured by conventional methods. This reconciliation-based strategy enables detection of adaptive hotspots in complex gene families, providing a versatile tool for linking molecular evolution to species-level diversification.

bioinformatics↗

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↗

Genetic basis of cuticular hydrocarbon variation in the desert ant

Cuticluar hydrocarbons (CHCs) are a ubiquitous component of insect cuticles that are used for a wide range of chemical signaling functions, especially recognition. Recognition and other signals are vital for the maintenance of insularity and cooperation in social insect colonies. Therefore, we expect natural selection on the composition and variabitlity of social insect CHC profiles. Selection on these signals may result in the evolution of genetic polymorphism affecting variation in CHC profiles. Here we tested for a genetic basis of CHC variation in the desert ant Cataglyphis niger. We applied a genomic mapping appraoch to a cohort of brothers from the same nest to reduce noise from environmental effects and achieve a clear statistical signal for association between the variation of CHCs and quantitative trait loci (QTL). This analysis identified 19 QTLs associated with 8 out of the 31 CHCs identified, and one QTL associated with total CHC quantity. These QTLs are located on 11 different chromosomes, including two cases where QTLs of different CHCs overlap. Each QTL explains between 13-25% of the variation in a specific CHC. We highlight several candidate genes in the QTLs identified, including fatty acid elongase and reductase genes. Our results reveal a polygenic genomic architecture underlying CHC variation in a population of the desert ant and open new research avenues into the genetic basis and evolution of chemical signaling in social insects.

ecology↗

Repeated evolution of supergenes on an ancient social chromosome

Supergenes are non-recombining chromosomal regions that code for complex polymorphic traits. Advances in population genomics have uncovered supergenes associated with diverse traits, ranging from butterfly wing patterns to floral morphs. In ants, two supergenes on non-homologous "social chromosomes" in Solenopsis and Formica are associated with social polymorphism, with either single queen (monogyne) or multiple queens (polygyne) colonies. We discovered a new supergene associated with similar polymorphism in the desert ant Cataglyphis niger. Despite Cataglyphis being more closely related to Formica than Solenopsis, its social chromosome is homologous to that of Solenopsis, with conservation of synteny in gene content and order. This suggests that the social chromosome is ancient, dating back to the common ancestor of Solenopsis and Cataglyphis, at least 90 million years ago. Low sequence divergence between supergene haplotypes in both Solenopsis and Cataglyphis suggests that the two supergenes evolved recently and independently in the two divergent lineages on this ancient social chromosome. Comparative analysis of hymenopteran genomes further revealed a bee chromosome homologous to the ants social chromosome. The ant social chromosome contains the largest set of genes that are conserved as a linkage group across ant and bee genomes. This conserved gene set is enriched for olfactory functions, most notably a large number of odorant-binding proteins. The conservation of this gene set suggests that this chromosome plays an important role in social behavior across social Hymenoptera. We propose that the conserved gene set in the social chromosome was repeatedly used as a pre-adapted toolkit for the evolution of social traits in general, and specifically in the evolution of polygyne social structure in ants.

evolutionary biology↗

Genomic architecture of nestmate recognition cues in the desert ant

Nestmate recognition is the basis for cooperation within social insect colonies. Quantitative variation in cuticle hydrocarbons (CHCs) is used for nestmate recognition in ants and other social insects. We carried out a Genome Wide Association Study (GWAS) of CHCs in the desert ant Cataglyphis niger by sampling 47 colonies, fully sequencing six workers from each colony, and measuring the relative amounts of their CHCs. Under the Gestalt colony odour model, social interactions between nestmates, in which CHCs are being transferred and mixed, are essential in creating a uniform colony CHC profile. Therefore, we carried out a second GWAS between the colonies and their uniform Gestalt odour by averaging nestmate genotypes and comparing them to their averaged CHC amounts. Our results are in line with the Gestalt model. Together, the two analyses identified 99 candidate QTLs associated with 18 of the CHCs. Thirteen clusters of two to four QTLs located within 10cM from each other were identified, seven of which contained QTLs from both analyses. We conclude that nestmate recognition cues are a complex quantitative colony-level trait with a significant genetic component to their phenotypic variation and a highly polygenic architecture.

ecology↗

Statistical analysis and simulation allowing simultaneously positive, negative, and no crossover interference in multilocus recombination data

Crossover interference (COI) is a widespread feature of homologous meiotic recombination. It can be quantified by the classical coefficient of coincidence (CoC) `but this characteristic is highly variable and specific to the pair of chromosomal intervals considered. Several models were proposed to characterize COI on a chromosome-wise level. In the gamma model, the strength of interference is characterized by a shape parameter{nu} , while the gamma-sprinkled two-pathway model (GS) accounts for both interference-dependent and independent crossover (CO) events by fitting a mixture of gamma distributions with v>1 and v=1, correspondingly, and mixture proportions 1-p and p. In reality, COI can vary along chromosomes resulting in low compliance of the fitted model to real data. Additional inconsistency can be caused by common neglecting of possible negative COI in the model, earlier reported for several organisms. In this work, we propose an extension of the GS-model to take possible negative COI into account. We propose a way for data simulation and parameter estimation for such situations.

bioinformatics↗

Optimising ddRAD sequencing for population genomic studies with ddgRADer

Double-digest Restriction-site Associated DNA sequencing (ddRADseq) is widely used to generate genomic data for non-model organisms in evolutionary and ecological studies. Along with affordable paired-end sequencing, this method makes population genomic analyses more accessible. However, multiple factors should be considered when designing a ddRADseq experiment, which can be challenging for new users. The generated data often suffer from substantial read overlaps and adaptor contamination, severely reducing sequencing efficiency and at times affecting data quality. Here, we analyse diverse datasets from the literature and carry out controlled experiments to understand the effects of enzyme choice and size selection on sequencing efficiency. The empirical data reveal that size selection is imprecise and has limited efficacy. In certain scenarios, a substantial proportion of short fragments pass below the lower size-selection cut-off resulting in low sequencing efficiency. However, enzyme choice can considerably mitigate inadvertent inclusion of these shorter fragments. A simple model based on these experiments is implemented to predict the number of genomic fragments generated after digestion and size selection, number of SNPs genotyped, number of samples that can be multiplexed, and the expected sequencing efficiency. We developed ddgRADer - http://ddgrader.haifa.ac.il/ - a user-friendly webtool that aids ddRADseq experimental design while optimising sequencing efficiency. This tool can also be used for single enzyme protocols such as Genotyping-by-Sequencing (GBS). Given user-defined study goals, ddgRADer recommends enzyme pairs and allows users to compare and choose enzymes and size-selection criteria. ddgRADer improves the accessibility and ease of designing ddRADseq experiments and increases the probability of success of the first population genomic study conducted in labs with no prior experience in genomics.

genomics↗

Differences in Long-Chained Cuticular Hydrocarbons between Males and Gynes in Cataglyphis Desert Ants

Cuticualar hydrocarbons play an important role in chemical communication in social insects, serving, among other things, as nestmate, gender, dominance and fertility recognition cues. In ants, however, very little is known about the precopulatory signals cuticular hydrocarbons carry. These signals may serve as affecting sex pheromones and aphrodisiacs or as reliable signals for idiosyncratic traits, which indirectly affect sexual selection. In this study, we examined, for the first time, in the Cataglyphis genus, sex-specific variability in cuticular hydrocarbons. We focused on a species that exhibits split sex-ratio and found significant quantitative differences between virgin queens and their potential mates. In an analyses of both absolute amounts and relative amounts, we found different compounds to be significantly displayed on gynes and drones, suggesting absolute and relative amounts may carry different signals influencing mating behavior and mate choice. We discuss the possible signals advertised by the non-polar fraction of these hydrocarbon profiles.

ecology↗

Incipient species or social polymorphism? Diversity in the desert ant Cataglyphis

Species are the fundamental units upon which evolutionary research is based. In insects, due to the high level of hybridization, the delimitation of such species can be challenging. The genus Cataglyphis presents a high level of diversification, making it an excellent model with which to study evolutionary paths. Israel appears to be a \"hot spot\" for recent speciation in this genus. Although previous studies have described multiple species of Cataglyphis in Israel, a recent genetic study has questioned the existence of some of these historically described species. The present study focuses on an apparent species complex that is distinguishable by its mitochondrial DNA (and therefore named mitotypes) but not by its nuclear DNA. Using a multi-method approach (genetics, chemistry and behavior), we show that these mitotypes also differ in their social structures and are readily distinguishable by their cuticular hydrocarbons profiles. While the different mitotypes are in general allopatric, at our study site they all coexist but nonetheless maintain the observed differences between them. This raises many evolutionary questions: Are these incipient species that have diverged with gene flow, or is this a case of social and chemical polymorphism that is maintained within a single species.

evolutionary biology↗

Comparative study of population genomic approaches for mapping colony-level traits

Social insect colonies exhibit colony-level phenotypes such as social immunity and task coordination, which are the sum of individual phenotypes. Mapping the genetic basis of such phenotypes requires associating the colony-level phenotype with the genotypes in the colony. In this paper, we examine alternative approaches to DNA extraction, library construction and sequencing for genome wide association (GWAS) studies of colony-level traits. We evaluate the accuracy of allele frequency estimation in sequencing a pool of individuals (pool-seq) from each colony in either whole-genome sequencing or reduced representation genomic sequencing. Based on empirical measurement of the experimental noise in sequencing DNA pools, we show that whole-genome pool-seq is more accurate than reduced representation pool-seq. We evaluate the power of the alternative approaches for detecting quantitative trait loci (QTL) of colony-level traits by using simulations that account for an environmental effect on the phenotype. Our results can inform experimental designs and enable optimizing the power of GWAS depending on budget, availability of samples and research goals. We conclude that for a given budget, sequencing un-normalized pools of individuals from each colony achieves greater QTL detection power.

bioinformatics↗

Split sex-ratio and variability in aggressive behavior in the ant Cataglyphis niger

In social insects, non-nestmates interactions are typically agonistic and many factors may influence the degree of exhibited aggression. Two of these factors are the physical proximity between nests and the chemical dissimilarity between colonies chemical signatures. We studied a population sample of 43 colonies of Cataglyphis niger ants distributed along a transect of [~]4KM. This geographic distribution allowed us to examine correlations of aggression levels with physical and chemical distances. Ants were collected before mating season, when sexuals (unmated gynes and drones) could be found in nests. In our sample, colonies had either gynes or drones but never both. The presence of sexuals, therefore, was another factor we took into account in our behavioral analyses. Workers from nests with sexuals were more aggressive towards conspecifics than workers from nests where sexuals were absent. We also found those workers to be more vigorously active towards colonies with greater chemical distances, while workers from nests without sexuals were indifferent to chemical distances. We therefore concluded that ants are able to detect differences in chemical dissimilarity, but their aggression levels are mainly determined by other mechanisms. A possible additional mechanism is associative learning and long term memory of the chemical signatures of neighboring colonies. Such learning is supported by our finding that aggression is higher towards neighboring nests, which is in line with the previously reported nasty neighbour effect in Cataglyphis ants. These results suggest that previous experience and learning of neural templates representing neighbors chemical cues is a stronger component than chemical dissimilarity in the mechanisms which determine aggression towards conspecifics in this species. We discuss possible explanations for the observed effect of the presence of sexuals on agonistic behavior and responsiveness to chemical distances.

evolutionary biology↗

Molecular evolution of juvenile hormone esterase-like proteins in a socially exchanged fluid

Socially exchanged fluids are a direct means for organisms to influence conspecifics. When orally feeding larval offspring via trophallaxis, Camponotus floridanus ant workers were shown to transfer Juvenile Hormone (JH), a key developmental regulator, as well as paralogs of JH esterase (JHE), an enzyme that hydrolyzes JH. We combine proteomic, phylogenetic and selection analyses to investigate the evolution of this esterase subfamily. We show that Camponotus JHE-like proteins have sustained multiple duplications, positive selection, and changed localization to become abundantly and selectively present in trophallactic fluid. To assess their potential role in larval development, we fed workers a JHE-specific inhibitor to introduce it into the trophallactic network. This increased the proportion larvae reared to metamorphosis by these workers, similar to supplementation with JH. Together these findings suggest that JHE-like proteins have evolved new roles in inter-individual regulation of larval development in Camponotus.

evolutionary biology↗

Taxon sampling unequally affects individual nodes in a phylogenetic tree: consequences for model gene tree construction in SwissTree

Medium to large phylogenetic gene trees constructed from datasets of different species density and taxonomic range are rarely topologically consistent because of missing phylogenetic signal, non-phylogenetic signal and error. In this study, we first use simulations to show that taxon sampling unequally affects nodes in a gene tree, which likely contributes to controversial conclusions from taxon sampling experiments and contradicting species phylogenies such as for the boreoeutherians. Hence, because it is unlikely that a large gene tree can be reconstructed correctly based on a single optimized dataset, we take a two-step approach for the construction of model gene trees. First, stable and unstable clades are identified by comparing phylogenetic trees inferred from multiple datasets and data types (nucleotide, amino acid, codon) from the same gene family. Subsequently, data subsets are optimized for the analysis of individual uncertain clades. Results are summarized in form of a model tree that illustrates the evolutionary relationship of gene loci. A case study shows how a seemingly complex gene phylogeny becomes increasingly consistent with the reference species tree by attentive taxon sampling and subtree analysis. The procedure is progressively introduced to SwissTree (http://swisstree.vital-it.ch), a resource of high confidence model gene (locus) trees. Finally we demonstrate the usefulness of SwissTree for orthology benchmarking.

bioinformatics↗