Biology subjects

Babik, W.

Publications and source records attributed to Babik, W..

11 recordsLinked to original sources

bioRxiv2025

A key regulator of missing-self innate immunity is polymorphic and under diversifying selection

Host-parasite co-evolution drives the diversification of host immune genes involved in the recognition of pathogen antigens and molecular patterns. In contrast, the immune genes involved in self-recognition and inhibition of immune responses against self-cells (missing-self immunity) are expected to be evolutionarily constrained. However, many pathogens, such as the Lyme disease agent Borrelia, hijack these genes to evade the immune system and may therefore select for their diversification. How these contrasting but concurrent selective forces shape the evolution of missing-self regulators is not clearly understood. To fill this gap, we investigated polymorphism and molecular signatures of selection acting on a missing-self regulator, the Complement Factor H (CFH), in bank vole populations, which are an important wild reservoir for Borrelia. We then compared the geographic structuring in the CFH domain interacting with Borrelia (CCP 20) against a genomic background represented by RAD-seq markers. We found signals of positive and diversifying selection at CCP 20, suggesting that CFH evolved in response to pressures from pathogens. Additionally, we found other innate immunity genes within the alternative complement pathway, which is regulated by CFH, under diversifying selection, highlighting its involvement in host-parasite coevolution. This study demonstrates that an innate missing-self sensor in a wild vertebrate is under diversifying selection, likely driven by pathogens.

evolutionary biology↗

bioRxiv2025

Dynamics of complex genomic regions in giant genomes: MHC evolution in newts

Major Histocompatibility Complex (MHC) molecules are central to vertebrate adaptive immunity and MHC genes serve are key models in evolutionary genomics, offering insight into birth-and-death evolution, gene duplication, and the maintenance of genetic diversity. However, the organization and evolution of the MHC in species with giant genomes, such as salamanders, remain poorly understood. Here, we use comparative genomics, ontogenetic, tissue expression and polymorphism data across seven newt species to investigate MHC evolution in this group. Contrary to earlier suggestions of a massively expanded MHC in salamanders, we find that the core MHC region remains relatively compact, demonstrating that genome gigantism does not scale proportionally in this region. Our finding also challenges the model of coevolution between a single classical MHC-Ia gene and antigen processing genes (APGs), revealing instead several polymorphic and highly expressed putative MHC-Ia located at varying distances from the APGs. MHC-I genes exhibit lineage-specific duplications and signs of concerted evolution, resulting in poorly resolved phylogenies. In contrast, MHC-II genes are more conserved and exhibit extensive trans-species polymorphism. Expression and polymorphism patterns identify putative nonclassical MHC-Ib genes, likely repeatedly derived from MHC-Ia genes--paralleling patterns seen in mammals, but contrasting with the situation in fish and Xenopus frogs. In all seven species, some MHC-Ib genes show high relative expression during the larval stage but not at adulthood, suggesting a role in larval immunity. Our results underscore the importance of salamanders for understanding the evolution of complex regions in giant genomes and the architecture of the tetrapod MHC.

genomics↗

bioRxiv2025

Selection inference in a complex genomic landscape: the role of inversions in the spruce bark beetle

Understanding the genetic basis of adaptation is a key objective in evolutionary biology. Although advances in genomic selection scans have greatly improved our ability to detect signatures of adaptation, distinguishing true signals from false positives remains challenging. This task is particularly difficult in regions of reduced recombination, such as polymorphic inversions. In this study, we examine the genome-wide landscape of selection in the European spruce bark beetle (Ips typographus), Europes most destructive forest pest, which has one of the most complex inversion-associated recombination landscapes known. Using simulation-based analyses and whole-genome resequencing data from 312 individuals across 23 populations, we applied two complementary selection scan methods (nSL and {Lambda}) to assess how inversions influence the detection of adaptive signals. Simulations revealed that the two selection scan methods differ in their susceptibility to false-positive signals within inversions and that partitioning data by inversion genotype (i.e., homozygote classes) can substantially reduce these errors. Consistent with the results of our simulations, our empirical data showed that inversions are highly enriched for selection signals when all inversion genotypes are analyzed but are depleted when only homozygotes are considered. This demonstrates that focusing on homozygote genotypes allows for a more precise identification of putative selection targets and haplotype-specific signals, as it overcomes the confounding effects of suppressed recombination in heterokaryotypic individuals. In contrast, the detection of selection in collinear regions was largely unaffected by the presence of inversions. Our findings highlight that inversions may play an important role in shaping adaptation, underscoring the need to account for species-specific genomic architecture when interpreting signals from selection scans. Author summaryDetecting the genetic basis of adaptation is one of the main goals in evolutionary biology. However, it is often difficult to tell whether selection signals identified by genome scans truly reflect natural selection signatures or are simply artefacts of genome structure. In this study, we examined how polymorphic inversions affect the detection of selection in the European spruce bark beetle, one of Europes most destructive forest pests. First, we assessed two selection scan methods using simulation approach. Second, we tested the influence of polymorphic inversion on the selection inference using genome-wide data from 23 beetle populations. We showed that inversions can create false signals of selection when all individuals are analyzed together but by separating individuals according to their inversion genotypes, we were able to distinguish potential adaptive regions from false positives. Our results demonstrate that accounting for genomic architecture is crucial for identifying selection signatures and provide practical guidelines for studying species with inversion-rich genomes.

evolutionary biology↗

bioRxiv2024

Identification of Y-chromosome turnover in newts fails to support a sex chromosome origin for the Triturus balanced lethal system

Non-recombining regions of the genome often have profound effects on evolution, resulting in phenomena such as sex chromosomes and supergenes. Amongst the strangest examples are balanced lethal systems, such as that found in newts of the genus Triturus. These systems halve reproductive output, and the evolution of such a deleterious trait is difficult to explain. For Triturus an intriguing model proposes that the balanced lethal system evolved from an ancestral Y-chromosome. To test this hypothesis, we identify the Y-chromosome of Triturus and verify whether it, or the balanced lethal system, is homologous to the Y-chromosome of its sister genus Lissotriton, which does not possess the balanced lethal system. We identify a set of candidate Y-linked markers in T. ivanbureschi and place them on a high-density linkage map that we construct with 7,233 RADseq markers. We validate male specificity of the markers across the genus, and then place both the Triturus and Lissotriton Y-linked regions within previously constructed target capture linkage maps that include genes linked to the balanced lethal system. We observe that neither the Triturus balanced lethal system, nor the Triturus Y-chromosome are homologous to the Lissotriton Y-chromosome. This is the first molecular evidence of a transition between Y-chromosome systems within salamanders. However, unless additional sex chromosome turnover events are involved, our data does not support a sex chromosome origin of the balanced lethal system.

evolutionary biology↗

bioRxiv2024

Genomic evidence suggests the balanced lethal system in Triturus newts originated in an instantaneous speciation event.

Triturus newts are afflicted by a balanced lethal system causing the spontaneous death of half of their offspring. How could such a maladaptive trait evolve? We construct genetic maps for Triturus and its sister genus Lissotriton, identifying genes involved in the balanced lethal system. Triturus chromosome 1 has diverged into two versions, which each carry a single massive deletion that is compensated for by duplication of the same region in the alternate version - indicating that the balanced lethal system arose instantaneously, in a single macromutation. Simulations show that, counterintuitively, the deleterious nature of the rearranged chromosomes protects them against competition with the ancestral arrangement via reproductive isolation. We conclude that the origin of the Triturus balanced lethal system also led to instantaneous speciation.

evolutionary biology↗

bioRxiv2024

Sex-specific recombination landscape in a species with holocentric chromosomes

The rate and chromosomal positioning of meiotic recombination significantly affects the distribution of the genetic diversity in eukaryotic genomes. Many studies have revealed sex-specific recombination patterns, with male recombination typically biased toward chromosome ends, while female recombination is more evenly distributed along chromosomes, or concentrated in pericentromeric region. It has been proposed that such patterns in females may counteract meiotic drive caused by selfish genetic elements near centromeres and should not occur in species devoid of clearly defined centromeres, but evidence for this expectation is scarce. Here, we constructed a sex-specific genetic map of a species with holocentric chromosomes, the bulb mite (Rhizoglyphus robini), a model organism for sexual selection studies with heritable alternative male reproductive phenotypes. We found a similar recombination landscape in both males and females, with a consistent pattern of increased rates towards both chromosome ends, and a higher recombination rate in females than in males. Recombination rate was positively correlated with repeat density and negatively with gene density. Our results are consistent with the meiotic drive hypothesis and suggest that the evolution of recombination patterns is closely linked to chromosome features.

genomics↗

bioRxiv2023

Complex genomic landscape of inversion polymorphism in Europe's most destructive forest pest

In many species, polymorphic inversions underlie complex phenotypic polymorphisms and facilitate local adaptation in the face of gene flow. Multiple polymorphic inversions can co-occur in a genome, but the prevalence, evolutionary significance, and limits to complexity of genomic inversion landscapes remain poorly understood. Here, we examine genome-wide variation in one of Europes most destructive forest pests, the spruce bark beetle Ips typographus, scan for polymorphic inversions, and test whether inversions are involved in key adaptations in this species. We analyzed 240 individuals from 18 populations across the species European range and, using a whole-genome resequencing approach, identified 27 polymorphic inversions covering approximately 28% of the genome. The inversions vary in size and in levels of intra-inversion recombination, are highly polymorphic across the species range, and often overlap, forming a complex genomic architecture. We test several mechanisms, including directional selection, overdominance and associative overdominance that can contribute to the maintenance of inversion polymorphisms in the genome. We show that the heterogeneous inversion landscape is likely maintained by the combined action of several evolutionary forces and that inversions are enriched in odorant receptor genes encoding key elements of recognition pathways for host plants, mates, and symbiotic fungi. Our results indicate that the genome of this major forest pest of growing social, political, and economic importance harbors one of the most complex inversion landscapes described to date posing a question about limits of genomic architecture complexity.

evolutionary biology↗

bioRxiv2023

Exploring the impact of read clustering thresholds on RADseq-based systematics: an empirical example from European amphibians.

Restriction site-Associated DNA sequencing (RADseq) has great potential for genome-wide systematics studies of non-model organisms. However, accurately assembling RADseq reads into orthologous loci remains a major challenge in the absence of a reference genome. Traditional assembly pipelines cluster putative orthologous sequences based on a user-defined clustering threshold. Because improper clustering of orthologs is expected to affect results in downstream analyses, it is crucial to design pipelines for empirically optimizing the clustering threshold. While this issue has been largely discussed from a population genomics perspective, it remains understudied in the context of phylogenomics and coalescent species delimitation. To address this issue, we generated RADseq assemblies of representatives of the amphibian genera Discoglossus, Rana, Lissotriton and Triturus using a wide range of clustering thresholds. Particularly, we studied the effects of the intra-sample Clustering Threshold (iCT) and between-sample Clustering Threshold (bCT) separately, as both are expected to differ in multi-species data sets. The obtained assemblies were used for downstream inference of concatenation-based phylogenies, and multi-species coalescent species trees and species delimitation. The results were evaluated in the light of a reference genome-wide phylogeny calculated from newly generated Hybrid-Enrichment markers, as well as extensive background knowledge on the species systematics. Overall, our analyses show that the inferred topologies and their resolution are resilient to changes of the iCT and bCT, regardless of the analytical method employed. Except for some extreme clustering thresholds, all assemblies yielded identical, well-supported inter-species relationships that were mostly congruent with those inferred from the reference Hybrid-Enrichment data set. Similarly, coalescent species delimitation was consistent among similarity threshold values. However, we identified a strong effect of the bCT on the branch lengths of concatenation and species trees, with higher bCTs yielding trees with shorter branches, which might be a pitfall for downstream inferences of evolutionary rates. Our results suggest that the choice of assembly parameters for RADseq data in the context of shallow phylogenomics might be less challenging than previously thought. Finally, we propose a pipeline for empirical optimization of the iCT and bCT, implemented in optiRADCT, a series of scripts readily usable for future RADseq studies.

evolutionary biology↗

bioRxiv2023

Inconsistent estimates of hybridization frequency in newts revealed by SNPs and microsatellites

Hybridization between the European smooth and palmate newts has recurrently been mentioned in the literature. The only two studies that attempted to quantify the frequency of hybridization and gene admixture between these two species came to strikingly opposite conclusions. According to Arntzen et al (1998, 42 allozymes), hybrids are rare in nature and introgression negligible, while according to Johanet et al (2011, 6 microsatellites), introgressive hybridization is significant and widespread across the shared distribution range. To clarify this question, we implemented high-throughput SNP genotyping with diagnostic biallelic SNPs on 965 specimens sampled across Europe. Our results are in line with Arntzen et al, since only two F1 hybrids were identified in two distinct French localities, and no further hybrid generations or backcrosses. Moreover, reanalysis of 78 of the samples previously studied by Johanet et al. (2011) using our SNPs panel could not reproduce their results, suggesting that microsatellite-based inference overestimated the hybridization frequency between these two species. Since we did not detect methodological issues with the analyses of Johanet et al., our results suggest that SNP approaches outperform microsatellite-based assessments of hybridization frequency, and that conclusions previously published on this topic with a small number of microsatellite loci should be taken with caution, and ideally be repeated with an increased genomic coverage.

genetics↗

bioRxiv2019

Pervasive introgression of MHC genes in newt hybrid zones

Variation in the vertebrate major histocompatibility complex (MHC) genes is crucial for fighting pathogen assault. Because new alleles confer a selective advantage, MHC should readily introgress between species, even under limited hybridization. Using replicated transects through two hybrid zones between strongly reproductively isolated newts, we demonstrated recent and ongoing MHC introgression. Its extent correlated with the age of contact. In the older zone, MHC similarity between species within transects exceeded that of between transects within species, implying pervasive introgression - a massive exchange of MHC genes, not limited to specific variants. In simulations, the observed pattern emerged under the combined action of balancing selection and hybridization, but not when these processes acted separately. Thus, massive introgression at advanced stages of divergence can introduce novel and restore previously lost MHC variation, boosting the adaptive potential of hybridizing taxa. In consequence, MHC genes may be the last to stop introgressing between incipient species.

evolutionary biology↗

bioRxiv2016

Isolation and Gene Flow in a Speciation Continuum in Newts

Because reproductive isolation often evolves gradually, differentiating lineages may retain the potential for genetic exchange for prolonged periods, providing an opportunity to quantify and understand the fundamental role of gene flow during speciation. Here we delimit taxa, reconstruct the phylogeny and infer gene flow in newts of the Lissotriton vulgaris species complex based on 74 nuclear markers sampled from 127 localities. We demonstrate that distinct lineages along the speciation continuum in newts exchange nontrivial amounts of genes, affecting their evolutionary trajectories. By integrating a wide array of methods, we delimit nine taxa and show that two principle factors have driven their genetic differentiation: time since the last common ancestor determining levels of shared ancestral polymorphism, and shifts in geographic distributions determining the extent of secondary contact. Post-divergence gene flow, indicative of evolutionary non-independence, has been most extensive between sister and non-sister taxa in Central Europe, while four southern European lineages have acquired the population genetic hallmarks of independent species (L. graecus, L. kosswigi, L. lantzi, L. schmidtleri). We obtained strong statistical support for widespread mtDNA introgression, previously suggested by discordance between mtDNA phylogeny and morphology. Our study suggests that long-term evolution in structured populations that may periodically exchange genes may be common: although some of these populations may become extinct or fuse, others will acquire complete reproductive isolation and will carry signatures of this complex history in their genomes.

evolutionary biology↗