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Hansson, B.

Publications and source records attributed to Hansson, B..

18 recordsLinked to original sources

Evolutionary dynamics of sex chromosomes and candidate sex-determining genes across the beetle phylogeny

The evolutionary dynamics of beetle sex chromosomes remain poorly understood. Using synteny analyses of 163 chromosome-level genome assemblies, we examine sex chromosome evolution across the beetle phylogeny. Beetles retain a highly conserved ancestral X chromosome region, even in superfamilies with extensive autosomal rearrangements and in species with enlarged neo-X chromosomes formed by fusions of autosomal segments. In contrast, Y chromosomes vary greatly in presence, size and gene content, driven by degeneration of ancestral regions and addition of neo-Y segments in some species. Neo-X and neo-Y chromosomes frequently occur and generally evolve independently, highlighting a flexible neo-sex chromosome dynamics. We identify putative sex-determining genes and propose a novel candidate, the highly conserved and sexually differentially expressed X-linked gene ELAV-like. Our results uncover conserved X elements, fragile Y chromosomes, and independent neo-X and neo-Y formation across 300 million years of beetle genome evolution.

genomics↗

PhaseWY: A pipeline for haplotype phasing, sex chromosome identification and extraction of sex-limited sequences

Sex chromosomes are central to many ecological and evolutionary processes. Evidence has accumulated that sex chromosome systems vary extensively in age, turnover and transitions, motivating renewed efforts to study the diversity of sex chromosome systems across the tree of life. However, successful genomic detection of sex chromosomes depends on several factors, including the size and divergence time, background genetic diversity, and the number of sequenced females and males. In addition, technical challenges associated with sequencing and analysing the sex-limited Y/W chromosome remain. Here, we present PhaseWY, an automated Snakemake pipeline that uses whole-genome sequencing data from multiple female and male individuals to identify sex-chromosomal regions and extract the corresponding Y/W sequences. PhaseWY (i) detects sex differences in alignment depth, (ii) applies read-based and statistical haplotype phasing, (iii) identifies sex-linked regions using haplotype clustering, and (iv) subsets autosomal, X/Z- and Y/W-linked variants for downstream analyses. We applied PhaseWY to simulated data to benchmark factors influencing sex-linkage detection and successful extraction of Y/W-linked variants. To demonstrate its practical utility, we further applied PhaseWY to the neo-sex chromosome system in Alauda larks (Alaudidae) and performed a range of downstream analyses demonstrating the scope of applications of the PhaseWY output. We conclude that PhaseWY provides an easy-to-use and reproducible tool for population-genomic analyses in non-model organisms, with particular importance for advancing our understanding of sex-chromosome evolution.

bioinformatics↗

From divergence to contact: demographic history and genomic context shape introgression across independent damselfly hybrid zones

Hybridisation outcomes often vary across space and time, yet the relative roles of demographic history and genomic architecture in shaping introgression remain unclear. Here, we investigate three replicated hybrid zones between the damselflies Ischnura elegans and Ischnura graellsii across Spain to test whether genomic introgression patterns are repeatable across independently formed zones. Using genome-wide data, we combined demographic modelling, genomic cline, and functional annotation of introgressed loci. Demographic inference supported three independent secondary contact events of different ages: The South-east zone forming first ([~]207 years ago), followed by the North-west ([~]73.5 years) and North-central ([~]33 years) hybrid zones. Despite similar cline steepness across autosomes, asymmetric gene flow from I. graellsii into I. elegans was observed, with a low overlap of introgressed loci between zones. These loci were mainly associated with broad regulatory and transport-related functions in both hybrid zones, indicating repeatability at the level of gene function rather than gene identity. In contrast, the X chromosome showed steeper clines, suggesting strong intrinsic genomic constraints. Together, demographic history explains geographic heterogeneity in introgression, whereas chromosome architecture imposes consistent constraints. These findings highlight how replicated hybrid zones can disentangle contingent versus repeatable genomic responses during early stages of speciation with gene flow.

evolutionary biology↗

Hybridization outcomes reflect context-dependent reproductive isolation in two damselfly hybrid zones

Pair of species with multiple hybrid zones provide powerful systems to examine how reproductive isolation and reinforcement may depend on ecological and demographic contexts. We conducted a comparative analysis of two hybrid zones between Ischnura elegans and Ischnura graellsii in North-central (NC) and North-western (NW) Spain to evaluate how differences in reproductive barriers shape patterns of hybridization and admixture. First, we quantified five prezygotic barriers in the NC hybrid zone--where no barrier estimates previously existed--and compared them with published data from the NW hybrid zone. Second, we conducted genomic analyses using 5,702 SNPs to assess genetic structure, differentiation, and diversity between species; and 381 SNPs with species-specific alleles to characterize hybrid classes and introgression across both regions. Reproductive isolation was strongly context dependent. Mechanical reinforcement acted in the same cross direction in both hybrid zones, but the NC hybrid zone also showed stronger gametic (fertility) isolation. Consequently, total prezygotic isolation was higher in the NC hybrid zone. These differences were also observed genomically: the NC hybrid zone exhibited limited and largely unidirectional introgression, whereas the NW hybrid zone showed more extensive admixture, bidirectional gene flow, and reduced interspecific differentiation, consistent with a longer or more sustained history of hybridization. Our results demonstrate that hybridization outcomes can differ markedly between hybrid zones involving the same pair of species, underscoring the importance of evaluating spatial variation in reproductive barriers and introgression to assess the presence, asymmetry, and repeatability of reinforcement, as well as the microevolutionary processes shaping hybrid zone structure.

evolutionary biology↗

Genomic erosion through the lens of comparative genomics

Loss of genetic diversity threatens species survival, yet the dynamics of such loss and species responses thereof can vary widely depending on their evolutionary histories, life-history traits and demographic trajectories. Comparative genomics offers a powerful framework to explore the dynamics of genomic erosion across species. Here, we analysed the genomes of three species -- the Mauritius parakeet, the Mauritius kestrel, and the pink pigeon -- that experienced extreme and well-documented population bottlenecks. We compared them to 36 species spanning the avian phylogeny, with varied IUCN Red List statuses to investigate the genomic consequences of their demographic collapses. For each species, we assessed nucleotide diversity, genetic load, and runs of homozygosity (ROH), alongside genome synteny and transposable elements. We found a negative correlation between nucleotide diversity and ROH, but neither metric was a good predictor of the species Red List status. Rather, the population effective to census size ratio showed a strong correlation to Red List status. Moreover, species with larger historical effective population sizes showed greater heterozygosity but carried a higher heterozygous load, highlighting the importance of historical demography to assess species vulnerability to genomic erosion. We found significant differences in homozygous load between taxonomic groups of our target species, possibly due to differences in life-history traits and demographic histories. Genome structure analyses revealed differences in transposable elements and genomic rearrangements between groups, suggesting their potential role in shaping genome architecture and adaptive potential across species. Our findings underscore the value of multispecies comparisons in understanding the evolutionary dynamics of genomic erosion and its relevance for biodiversity conservation.

genomics↗

Signatures of genomic adaptation to Cuckoo brood parasitism in Reed Warbler hosts across Europe

Behaviour is a fundamental defence mechanism for animals facing enemies, yet its plasticity makes finding associated genomic evidence for coevolution challenging. As a solution, we apply landscape genomics methods more typically deployed with abiotic variables to a coevolutionary model system: Reed Warblers (Acrocephalus scirpaceus) and their Cuckoo (Cuculus canorus) brood parasites. Using continental sampling of genome-wide data from hosts breeding under varying brood parasitism rates, we reveal that gene flow varies among populations, and, controlling for variation due to environmental differences, identify genomic regions and putative genes that differ with exposure to brood parasitism. Therefore, our results suggest that variable host responses to selection are possible, even by highly mobile and connected populations, supporting long-held assumptions that behavioural defences may reflect genomic adaptation despite their plasticity. Further studies, including those linking genetic variation to individual-level behaviours involved in parental responses to brood parasitism, are required to confirm a genetic basis to specific coevolutionary adaptations, and to test for other biotic or abiotic variables potentially confounding with local parasitism rate.

evolutionary biology↗

Male-biased recombination at chromosome ends in a songbird revealed by precisely mapping crossover positions

Recombination plays a crucial role in evolution by generating novel haplotypes and disrupting linkage between genes, thereby enhancing the efficiency of selection. Here, we analyse the genomes of twelve great reed warblers (Acrocephalus arundinaceus) in a three-generation pedigree to identify precise crossover positions along the chromosomes. We located more than 200 crossovers and found that these were highly concentrated towards the telomeric ends of the chromosomes. While the number of recombination events was similar between the sexes, the crossovers were located significantly closer to the ends of paternal compared to maternal chromosomes. The frequency of crossovers was similar between intergenic and genic regions, but within genes, they occurred more frequently in exons than in introns. In conclusion, our study of the great reed warbler revealed substantial variation in crossover frequencies within chromosomes, with a distinct bias towards the sub-telomeric regions, particularly on the paternal side. These findings emphasise the importance of thoroughly screening the entire length of chromosomes to characterise the recombination landscape and uncover potential sex-biases in recombination. Article summaryThe genetic exchange between the paternal and maternal chromosomes during meiosis - recombination - plays a crucial role in evolution by generating new haplotypes that natural selection can act upon. By analysing genomic data of a three-generation family of great reed warblers, we detected precise locations of approximately 200 recombination events in the genome of these birds. This unveiled a prominent sex-bias with recombination occurring more often towards chromosome ends in males than in females.

evolutionary biology↗

Testing the predictions of reinforcement: long-term empirical data from a damselfly mosaic hybrid zone

Theoretical work suggests that reinforcement can cause the strengthening of prezygotic isolation in sympatry by mitigating the costs of maladaptive hybridization. However, only a handful of studies have tested all predictions of this theory in natural populations. We investigated reinforcement in a mosaic hybrid zone of the damselflies Ischnura elegans and I. graellsii. Firstly, we tested if the conditions of reinforcement were fulfilled by quantifying whether hybridization was costly, and prezygotic isolation was strengthening in sympatry compared with in allopatry. Secondly, we investigated three specific predictions of reinforcement: rarer female effect, presence of concordant prezygotic and postzygotic isolation asymmetries in sympatry, and greater premating asymmetries associated with weaker postzygotic isolation in sympatry. We found that reinforcement has strengthened mechanical isolation in one cross direction between species in sympatry. Our study details a case of reinforcement and heterospecific gene flow causing opposite effects between reciprocal heterospecific crosses and describes a natural model in which reproductive isolation is built by the simultaneous effects of reinforcement, the lock-and-key model, Bateson-Dobzhansky-Muller incompatibilities and Haldanes rule.

evolutionary biology↗

Sensing volatiles throughout the body: Geographic and tissue-specific olfactory receptor expression in the fig wasp Ceratosolen fusciceps

An essential adaptive strategy in insects is the evolution of olfactory receptors (ORs) to recognize important volatile environmental chemical cues. Our model species, Ceratosolen fusciceps, a specialist wasp pollinator of Ficus racemosa, likely possesses an OR repertoire that allows it to distinguish fig-specific volatiles in highly variable environments. Using a newly assembled genome-guided transcriptome, we annotated 63 ORs in the species and reconstructed the phylogeny of Ceratosolen ORs in conjunction with other hymenopteran species. Expression analysis showed that though ORs were mainly expressed in the antennae, 20 percent were also expressed in non-antennal tissues such as the head, thorax, abdomen, legs, wings, and ovipositor. Specific upregulated expression was observed in OR30C in the head and OR60C in the wings. We identified OR expression from all major body parts of C. fusciceps, suggesting novel roles of ORs throughout the body. Further examination of OR expression of C. fusciceps in widely separated geographical locations, i.e., south (urban) and northeast (rural) India, revealed distinct OR expression levels in different locations. This discrepancy likely parallels the observed variation in fig volatiles between these regions and provides new insights into the evolution of insect ORs and their expression across geographical locations and tissues.

genomics↗

RecView: an interactive R application for viewing and locating recombination positions using pedigree data

Recombination generates new haplotypes and disconnects linked genes thereby increasing the efficiency of selection and the adaptive potential. Quantifying the recombination landscape, i.e., the recombination rate variation along chromosomes, is important for understanding how evolutionary processes such as selection and drift are acting on genes and chromosomes. Here, we present RecView, an interactive R application, designed to view and locate recombination positions along chromosomes using whole-genome genotype data of a three-generation pedigree. RecView visualises the grandparent-of-origin of all informative alleles along each chromosome of the offspring in the pedigree. It also infers putative recombination positions with two algorithms, one based on change in the proportion of the alleles with specific grandparent-of-origin, and one on the degree of continuity of alleles with the same grandparent-of-origin, along the chromosome. Putative recombination positions are given in base pairs together with an estimated error based on the local density of informative alleles. We demonstrate the applicability of RecView using sequencing data of one 120 Mb-large chromosome of one offspring (and its four grandparents and two parents) of a passerine bird, the great reed warbler (Acrocephalus arundinaceus). On this chromosome, we detected five recombination events, three on the paternal chromosome and two on the maternal chromosome with both algorithms. To evaluate how sensitive the analysis is for SNP density, we downsampled our data to 10% of the original dataset. In conclusion, we provide an easy-to-use and highly effective application for viewing and locating recombination positions along chromosomes in small pedigrees. RecView and test data are available on GitHub (https://github.com/HKyleZhang/RecView.git).

genomics↗

Genomic signatures of isolation, hybridization, and selection during speciation of island finches

Sister species occurring sympatrically on islands are rare and offer unique opportunities to understand how speciation can proceed in the face of gene flow. The Sao Tome grosbeak is a massive-billed, giant finch endemic to the island of Sao Tome in the Gulf of Guinea, where it has diverged from its co-occurring sister species the Principe seedeater, an average-sized finch that also inhabits two neighbouring islands. Here, we show that the grosbeak carries a large number of unique alleles different from all three Principe seedeater populations, but also shares many alleles with the sympatric Sao Tome population of the seedeater, a genomic signature signifying divergence in isolation as well as subsequent introgressive hybridization. Furthermore, genomic segments that remain unique to the grosbeak are situated close to genes, including genes that determine bill morphology, suggesting the preservation of adaptive variation through natural selection during divergence with gene flow. This study reveals a complex speciation process whereby genetic drift, introgression, and selection during periods of isolation and secondary contact all have shaped the diverging genomes of these sympatric island endemic finches. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=60 SRC="FIGDIR/small/474904v1_ufig1.gif" ALT="Figure 1"> View larger version (41K): org.highwire.dtl.DTLVardef@5b18a5org.highwire.dtl.DTLVardef@af0c4forg.highwire.dtl.DTLVardef@512a60org.highwire.dtl.DTLVardef@b51c61_HPS_FORMAT_FIGEXP M_FIG C_FIG

evolutionary biology↗

Restricted X chromosome introgression and support for Haldane's rule in hybridizing damselflies

Contemporary hybrid zones act as natural laboratories for the investigation of species boundaries and allow to shed light on the little understood roles of sex chromosomes in species divergence. Sex chromosomes are considered to function as a hotspot of genetic divergence between species; indicated by less genomic introgression compared to autosomes during hybridisation. Moreover, they are thought to contribute to Haldanes rule which states that hybrids of the heterogametic sex are more likely to be inviable or sterile. To test these hypotheses, we used contemporary hybrid zones of Ischnura elegans, a damselfly species that has been expanding its range into the northern and western regions of Spain, leading to chronic hybridization with its sister species Ischnura graellsii. We analysed genome-wide SNPs in the Spanish I. elegans and I. graellsii hybrid zone and found (i) that the X chromosome shows less genomic introgression compared to autosomes and (ii) that males are underrepresented among admixed individuals as predicted by Haldanes rule. This is the first study in Odonata that suggests a role of the X chromosome in reproductive isolation. Moreover, our data adds to the few studies on species with X0 sex determination system and contradicts the hypothesis that the absence of a Y chromosome causes exceptions to Haldanes rule.

evolutionary biology↗

FindZX: an automated pipeline for detecting and visualising sex chromosomes using whole-genome sequencing data

Sex chromosomes have evolved numerous times, as revealed by recent genomic studies. However, large gaps in our knowledge of sex chromosome diversity across the tree of life remain. Filling these gaps, through the study of novel species, is crucial for improved understanding of why and how sex chromosomes evolve. Characterization of sex chromosomes in already well-studied organisms is also important to avoid misinterpretations of population genomic patterns caused by undetected sex chromosome variation. Here we present findZX, an automated Snakemake-based computational pipeline for detecting and visualizing sex chromosomes through differences in genome coverage and heterozygosity between males and females. FindZX is user-friendly and scalable to suit different computational platforms and works with any number of male and female samples. An option to perform a genome coordinate lift-over to a reference genome of another species allows users to inspect sex-linked regions over larger contiguous chromosome regions, while also providing important between-species synteny information. To demonstrate its effectiveness, we applied findZX to publicly available genomic data from species belonging to widely different taxonomic groups (mammals, birds, reptiles, fish, and insects), with sex chromosome systems of different ages, sizes, and levels of differentiation. We also demonstrate that the lift-over method is robust over large phylogenetic distances (>80 million years of evolution).

bioinformatics↗

Extreme variation in recombination rate and genetic variation along the Sylvioidea neo-sex chromosome

In the majority of bird species, recombination between the sex chromosome pairs in heterogametic females (ZW) is restricted to a small pseudoautosomal region (PAR), whereas recombination is ongoing along the entire Z chromosome in the homogametic males (ZZ). Recombination has a strong impact on the sequence evolution by affecting the extent of linkage, level of genetic diversity and efficacy of selection. Species within the Sylvioidea superfamily are unique among birds in having extended Z and W chromosomes ("neo-sex chromosomes") formed by a fusion between the ancestral sex chromosomes and a part of chromosome 4A. So far the recombination landscape of the Sylvioidea neo-sex chromosomes remains unknown, despite its importance for understanding sequence evolution. Here, we use linkage mapping in a multi-generation pedigree to assemble, and assess the recombination rate along the entire Z chromosome of one Sylvioidea species, the great reed warbler (Acrocephalus arundinaceus). This resulted in an 87.54 Mbp and 90.19 cM large Z including the ancestral-Z, where the small PAR (0.89 Mbp) is located, and the added-Z. A striking result was an extreme variation in recombination rate along the Z in male great reed warblers with high rates at both telomeric ends, but an apparent lack of recombination over a substantial central section, covering 77% of the chromosome. This region showed a drastic loss of nucleotide diversity and accumulation of repeats compared to the highly recombining regions. Nonetheless, the evolutionary rate of genes (measured by dN/dS) did not differ between these regions, suggesting that the efficacy of selection on protein-coding sequences is not reduced by lack of recombination.

genetics↗

Genomics of an avian neo-sex chromosome reveals the evolutionary dynamics of recombination suppression and sex-linked genes

How the avian sex chromosomes first evolved from autosomes remains elusive as 100 million years (Myr) of divergence and degeneration obscure their evolutionary history. Sylvioidea songbirds is an emerging model for understanding avian sex chromosome evolution because a unique chromosome fusion event [~]24 Myr ago has formed enlarged "neo-sex chromosomes" consisting of an added (new) and an ancestral (old) part. Here, we report the female genome (ZW) of one Sylvioidea species, the great reed warbler (Acrocephalus arundinaceus). We confirm that the added region has been translocated to both Z and W, and show that the added-W part has been heavily reorganised within itself and with the ancestral-W. Next, we show that recombination between Z and W continued after the fusion event, and that recombination suppression took [~]10 Myr to be completed and arose locally and non-linearly along the sex chromosomes. This pattern is inconsistent with that of large inversions and instead suggests gradual and mosaic recombination suppression. We find that the added-W mirrors the ancestral-W in terms of repeat accumulation, loss of genetic variation, and gene degeneration. Lastly, we show that genes being maintained on W are slowly evolving and dosage sensitive, and that highly conserved genes across broad taxonomic groups, regardless of sex-linkage, evolve slower on both Z and W. This study reveals complex expansion of recombination suppression along avian sex chromosomes, and that the evolutionary trajectory of sex-linked genes is highly predictable and governed partly by sex-linkage per se, partly by their functional properties.

evolutionary biology↗

Non-random association of MHC-I alleles in favor of high diversity haplotypes in wild songbirds revealed by computer-assisted MHC haplotype inference using the R package MHCtools

Major histocompatibility complex (MHC) genes play a central role for pathogen recognition by the adaptive immune system. The MHC genes are often duplicated and tightly linked within a small genomic region. This structural organization suggests that natural selection acts on the combined property of multiple MHC gene copies in segregating haplotypes, rather than on single MHC genes. This may have important implications for analyses of patterns of selection on MHC genes. Here, we present a computer-assisted protocol to infer segregating MHC haplotypes from family data, based on functions in the R package MHCtools. We employed this method to identify 107 unique MHC class I (MHC-I) haplotypes in 116 families of wild great reed warblers (Acrocephalus arundinaceus). In our data, the MHC-I genes were tightly linked in haplotypes and inherited as single units, with only two observed recombination events among 334 offspring. We found substantial variation in the number of different MHC-I alleles per haplotype, and the divergence between alleles in MHC-I haplotypes was significantly higher than between randomly assigned alleles in simulated haplotypes. This suggests that selection has favored non-random associations of divergent MHC-I alleles in haplotypes to increase the range of pathogens that can be recognized by the adaptive immune system. Further studies of selection on MHC haplotypes in natural populations is an interesting avenue for future research. Moreover, inference and analysis of MHC haplotypes offers important insights into the structural organization of MHC genes, and may improve the accuracy of the MHC region in de novo genome assemblies.

evolutionary biology↗

Genomics of expanded avian sex chromosomes shows that certain chromosomes are predisposed towards sex-linkage in vertebrates

Sex chromosomes have evolved from the same autosomes multiple times across vertebrates, suggesting that certain genomic regions are predisposed towards sex-linkage. However, to test this hypothesis detailed studies of independently originated sex-linked regions and their gene content are needed. Here we address this problem through comparative genomics of birds where multiple chromosomes appear to have formed neo-sex chromosomes: larks (Alaudidae; Sylvioidea). We detected the largest known avian sex chromosome (195.3 Mbp) and show that it originates from fusions between (parts of) four avian chromosomes (Z, 3, 4A and 5). We found evidence of five evolutionary strata where recombination has been suppressed at different time points, and that these time points correlate with the level of Z-W gametolog differentiation. We show that there is extensive homology to sex chromosomes in other vertebrate lineages: three of the fused chromosomes (Z, 4A, 5) have independently evolved into sex chromosomes in fish (Z), turtles (Z, 5), lizards (Z, 4A) and mammals (Z, 4A). Moreover, we found that the fourth chromosome, chromosome 3, was significantly enriched for genes with predicted sex-specific functions. These results support a key role of chromosome content in the evolution of sex chromosomes in vertebrates.

evolutionary biology↗

The making of an olfactory specialist

The evolution of animal behaviour is poorly understood. Despite numerous correlations of behavioural and nervous system divergence, demonstration of the genetic basis of interspecific behavioural differences remains rare. Here we develop a novel neurogenetic model, Drosophila sechellia, a close cousin of D. melanogaster that displays profound behavioural changes linked to its extreme host fruit specialisation. Through calcium imaging, we identify olfactory pathways detecting host volatiles. Mutational analysis indicates roles for individual receptors in long- and short-range attraction. Cross-species allele transfer demonstrates that differential tuning of one receptor is important for species-specific behaviour. We identify the molecular determinants of this functional change, and characterise their behavioural significance and evolutionary origin. Circuit tracing reveals that receptor adaptations are accompanied by increased sensory pooling onto interneurons and novel central projection patterns. This work links molecular and neuronal changes to behavioural divergence and defines a powerful model for investigating nervous system evolution and speciation.

neuroscience↗