Biology subjects

Liedvogel, M.

Publications and source records attributed to Liedvogel, M..

17 recordsLinked to original sources

bioRxiv2026

From migrants to residents: Genomic insights into adaptive strategies in European robins (Erithacus rubecula)

Bird migration evolved as an adaptation to seasonally changing habitats. Migratory behaviour can vary within the same species in case of partial migratory behaviour, i.e. one population (or individual) is migratory and another one is resident. Species that exhibit a wide variety of migratory phenotypes provide valuable systems to understand the evolutionary drivers behind different phenotypes and how populations adapt to habitats with distinct seasonality. The European robin (Erithacus rubecula) expresses migratory behaviour in central and northern areas of the species distribution range, whereas populations in the South and on the Macaronesian islands are predominantly resident, providing a suitable system to investigate these questions. We use high coverage whole genome re-sequencing data of 125 European robins to investigate how migration behaviour affects population structure and demography, and how it affects the selection landscape in the genome. Genetic structure in European robins coincides with migratory phenotype and geography and populations are characterised by distinct demographic histories. Our results suggest that both the continental resident population as well as the Macaronesian island populations have derived independently from an ancestral migratory population. Unexpectedly, tests for differential selection revealed extensive positive selection pressure acting across all chromosomes in the resident populations, while selective sweeps are largely absent from migrants. We speculate that this might be an analytical artifact due to mismatching timescales between what population genomics methods can detect and the scale on which migration behaviour likely evolved in the robin. We suggest that future studies on the genomics of migration should more focally account for different time scales on which these processes happen, such as including the wider phylogenomic background of the target species, to capture the full evolutionary history of migratory traits.

evolutionary biology↗

bioRxiv2026

Expression patterns and interaction profiles of heterotrimeric transducin subunits in the retina of the European robin ( Erithacus rubecula )

The heterotrimeric G-protein transducin (Gt) is mediating phototransduction in rod and cone cells of the vertebrate retina, but its expression patterns in migratory songbirds is unknown. We characterised Gt expression in the European robin, a night-migratory songbird known for its light-dependent magnetoreception. One well-supported hypothesis of magnetoreception involves radical-pair formation in the blue light receptor cryptochrome type 4a. The - and {gamma}-subunits of cone specific transducin have been identified as possible interaction partners of cryptochrome 4a. Therefore, we analysed the expression patterns of various G-protein subunits in bird photoreceptors by combining single cell RNA sequencing and immunohistochemistry. Protein-protein interaction was tested by pulldown, co-immunoprecipitation, and NanoBiT luminescence assays. G-protein subunits Gt{beta}1 and Gt{beta}3 are predominantly expressed in rods and cones, and Gt{gamma}T2 was the principal isoform in cones, whereas Gt{gamma}11 was associated with rods. In contrast, we did not detect Gt{gamma}10 expression in either photoreceptor type. Interaction assays demonstrated that all three {beta}{gamma} combinations; {beta}{gamma}T2, {beta}{gamma}10, and {beta}{gamma}11, can associate in vitro. These findings indicate that {beta}{gamma} dimer formation in vivo is likely constrained by the photoreceptor-specific expression of the respective subunits. The absence of Gt{gamma}10 expression in rods and cones does not support a role in photoreceptor-based magnetoreception.

Molecular Biology↗

bioRxiv2026

Rapid and divergent changes in the continental-scale organisation of a short-lived songbird's migratory strategy

It is hard to predict how rapidly songbird migration will change in the Anthropocene. Indeed, since songbird migration is thought to have a strong heritable component, the continental-scale organisation of migratory movement might be seen as fairly inflexible. Perhaps one of the best models for the ecology and evolution of migration is the Eurasian blackcap (Sylvia atricapilla) which, as part of a continent-wide effort to characterise blackcap migratory phenotype, we geolocator-tracked from breeding sites in eastern Poland. Rather than migrating in the expected south-easterly migratory direction, these birds migrated south and south-west - suggesting that blackcaps in the east of their range have switched migratory direction. We sought to investigate the extent of this phenomenon using almost a century of ringing data, which confirmed that blackcaps breeding across the entirety of Eastern Europe have indeed almost completely stopped using their historic eastern flyway. Instead, a shorter-distance west-migrating phenotype has emerged, which we find is consistent with warmer winter temperatures opening up wintering sites at more northerly latitudes in the west. We discuss what drives changes in migratory behaviour over short timescales; and consider what this tells us about how migratory information is inherited.

animal behavior and cognition↗

bioRxiv2026

The road to nowhere: geolocation-by-genotype traces large-scale yellow-browed warbler vagrancy to central Siberia

Vagrant animals - individuals found far outside their normal range - offer powerful natural experiments for understanding migratory mechanisms. The yellow-browed warbler (Phylloscopus inornatus) provides perhaps the best-yet example, typically migrating from Siberia to South/Southeast Asia yet found in increasingly large numbers in Western Europe. This represents a strikingly unresolved evolutionary puzzle: why do so many migrants consistently move in almost the complete wrong direction? A critical first step toward solving this enigma is determining where these birds come from. If vagrants came from the proximal western range edge this would imply simple disorientation, whilst a more easterly origin could imply large-scale reverse misorientation. Here, we develop a geolocation-by-genotype algorithm for low-coverage whole-genome resequencing data collected from feathers. Our method identifies spatially informative SNPs; clusters them to account for covariance in allele frequency through space; and employs a bootstrapped maximum-likelihood framework to estimate spatial origin with uncertainty. Applied to more than 80 European-caught birds, our results place their origin in central Siberia (118{degrees}E; 89-134{degrees}E [95% CI]); over 2000km east of the western range edge. These results suggest mass misorientation in a near-reverse direction, and highlight the yellow-browed warbler as an exceptional system for probing the mechanism, ontogeny and evolution of migration.

animal behavior and cognition↗

bioRxiv2025

Migration patterns and hybridization within the Asian stonechat complex in response to a major geographical barrier

Long-distance avian migration is thought to be under strong natural selection. Facing geographical barriers, migrants display various patterns considered to be adaptive. For example, they may detour along either side around the barrier or cross it, requiring specialized behavioral adaptations. Variations within closely related taxa are excellent sources for understanding the evolutionary background of migration and how barriers are shaping migration routes. In Asia, some species are assumed to have a migratory divide in response to the major geographical barrier, the Qinghai-Tibet Plateau (QTP), including the stonechat taxa (Siberian Stonechat Saxicola maurus maurus and Amur Stonechat S. stejnegeri). As they detour along either side of the QTP, these taxa are believed to disfavor a crossing over the highland. However, the more southernly distributed Tibetan Stonechat (S. m. przewalskii) breeds on the QTP, suggesting adaptation to high elevation. To investigate migration patterns and the potentially associated genetic differences, we studied migration routes and population genetics of four populations around the assumed migratory divide in Russia and Mongolia, and of one from the QTP in China. Our results confirmed the existence of a migratory divide between maurus and stejnegeri, albeit with extensive hybridization. We observed both the hypothesized western and eastern routes, but also found individuals employing intermediate routes crossing the QTP, of which two-thirds were clear hybrids. Meanwhile, przewalskii followed a highland-crossing route and was genetically differentiated from maurus and stejnegeri. The diverse migration routes among Asian stonechats show differential responses towards the geographical barrier. The intermediate route may be associated with hybridization, and its conditional viability may facilitate gene flow between maurus and stejnegeri. The Asian stonechat complex thus offers great opportunities for novel research of the genetics and evolution of migration. The specific evolutionary background associated with inhabiting and crossing the QTP can offer new perspectives in this field. Teaser textMigratory divides can arise in birds because alternative routes around migratory barriers would select for behaviors to restrict hybridization. Hybrids of parental types that employ alternative routes are hypothesized to embark on intermediate routes that would expose them to suboptimal conditions, resulting in post-zygotic reproductive isolation. However, this hypothesis is challenged when a sister taxon actually breeds on the geographical barrier. This is the case in the Asian stonechat complex that breeds near or on the Qinghai-Tibet Plateau (QTP), the roof of the world. We demonstrated a migratory divide in central Siberia to Mongolia for race maurus and stejnegeri, yet showed also evidence for extensive hybridization. Hybrids migrated along a newly discovered intermediate route, seemingly viable and overlaps with the migration trajectory of race przewalskii over the eastern part of the QTP. The Asian migratory divide relative to the QTP thus provided new insights to the evolution of landbird migration.

evolutionary biology↗

bioRxiv2025

Shifting balancing selection on a chromosomal inversion in island populations

Chromosomal inversions often underlie local adaptation and differentiation between populations. However, little is known about how selection acting on a balanced inversion shifts in different environments in the context of demographic events. Here, we combine population genomic approaches with extensive simulations to show that split events of island populations shifted a parameter of balancing selection on a polymorphic inversion. In Eurasian blackcaps (Sylvia atricapilla), an 8 Mb-long inversion has been maintained polymorphic in most populations across the species distribution range by long-term balancing selection. The frequency of this inversion is consistently lower in island resident and continental resident populations compared to behaviourally ancestral continental migrant populations. Inference of population history shows that at least four groups of residents, specifically one continental population and three sets of populations on different island systems, originate from independent and simultaneous split events from one ancestral population. Such a demographic history indicates that the consistent reduction in the inversion frequency among these independent resident populations is unlikely due to shared stochastic events. Approximate Bayesian computation (ABC) applied to simulations of balancing selection under the blackcap demography indicates that the optimal frequency of the inversion in the regime of negative frequency-dependent selection, a type of balancing selection, became lower in island populations. These results highlight how parallel shifts in selection parameters in similar environments can contribute to genetic differentiation among populations at inversion loci.

evolutionary biology↗

bioRxiv2025

Cryptochrome 4b protein is likely irrelevant for the radical pair based magnetoreception in the European robin

Avian cryptochrome 4 (Cry4) protein is a putative magnetosensitive molecule facilitating precise long-distance navigation in migratory birds. Two splice variants of Cry4 were reported in European robin (Erithacus rubecula), namely ErCry4a and ErCry4b. It is known that ErCry4a protein exhibits electron transfer between the flavin adenine dinucleotide (FAD) cofactor and tryptophan residues that generates magnetically sensitive radical pairs for magnetoreception. However, little is known about the ErCry4b isoform. We therefore characterized the properties of ErCry4b to see whether it fulfills prerequisites to be a radical pair magnetic sensor molecule. Our results show that ErCry4b protein does not bind FAD in vitro. Computational structure simulations revealed that the FAD non-binding in ErCry4b is likely due to protein structure dynamics. Furthermore, ErCry4b protein abundance in the robin retina, cerebellum and liver is below the detection limit of immunoprecipitation assays coupled with mass spectrometry. Meanwhile, transcript analyses show that ErCRY4b mRNA abundance is 10 times less than ErCRY4b in the retina. In conclusion, ErCry4b does not fulfill the prerequisites to be a radical pair based magnetic sensing molecule due to the lack of FAD binding, and it might not even be expressed as a functional protein in the European robin.

biochemistry↗

bioRxiv2024

High-recombining genomic regions affect demography inference

Inference of population history of non-model species is important in evolutionary and conser- vation biology. Multiple methods of population genomics, including those to infer population history, are based on the ancestral recombination graph (ARG). These methods use observed mutations to model local genealogies changing along chromosomes. Breakpoints at which genealogies change effectively represent the positions of historical recombination events. How- ever, inference of underlying genealogies is difficult in regions with high recombination rate relative to mutation rate. This is because genealogies cover genomic intervals that are too short to accommodate sufficiently many mutations informative of the structure of the un- derlying genealogies. Despite the prevalence of high-recombining genomic regions in some non-model organisms, such as birds, its effect on ARG-based demography inference has not been well studied. Here, we use population genomics simulations to investigate the impact of high-recombining regions on ARG-based demography inference. We demonstrate that inference of effective population size and the time of population split events is systematically affected when high-recombining regions cover wide breadths of the chromosomes. We also show that excluding high-recombining genomic regions can practically mitigate this effect. Finally, we confirm the relevance of our findings in empirical analysis by contrasting demography inferences applied for a bird species, the Eurasian blackcap (Sylvia atricapilla), using different parts of the genome with high and low recombination rates. Our results suggest that demography inference using ARG-based methods should be carried out with caution when applied in species whose reference genomes contain long stretches of high-recombining regions.

evolutionary biology↗

bioRxiv2023

The unexpected consequences of predictor error in ecological model selection

1O_LIThe ability to select statistical models based on how well they fit an empirical dataset is a central tenet of modern bioscience. How well this works, though, depends on how goodness-of-fit is measured. Likelihood and its derivatives (e.g. AIC) are popular and powerful tools when measuring goodness-of-fit, though inherently make assumptions about the data. One such assumption is absence of error on the x-axis (i.e. no error in the predictor). This, however, is often not correct and deviations from this assumption are often hard (or impossible) to measure. C_LIO_LIHere, we show that, when predictor error is present, goodness-of-fit as perceived using likelihood will increase with decreases in sample size, effect size, predictor error and predictor variance. This results in predictors with increased effect size, predictor variance or predictor error being punished. As a consequence, we suggest that larger effect sizes are biased against in likelihood-based model comparison. Of note: (i) this problem is exacerbated in datasets with larger samples sizes and a broader range of predictor values - typically considered desirable biological data collection; and (ii) the magnitude of this effect is non-trivial given that proxy error (caused by using correlates of a predictor rather than the predictor itself) can lead to unexpectedly high amounts of error. C_LIO_LIWe investigate the effects of our findings in an empirical dataset of wood anemone (Anemone nemorosa) first flowering date regressed against temperature. Our results show that the proxy error caused by using air temperature rather than ground temperature results in a {triangleup}AIC of around 3. We also demonstrate potential consequences for model selection procedures with autocorrelation (e.g. sliding window approaches). Via simulation we show that in the presence of predictor error AIC will favour autocorrelated, lower effect size predictors (such as those found on the edges of predictive windows), rather than the a priori specified true window. C_LIO_LIOur results suggest significant and far-reaching implications for biological inference with model selection for much of todays ecology using observational data under non-experimental conditions. We assert that no obvious, globally-applicable solution to this problem exists; and propose that quantifying predictor error is key in accurate ecological model selection going forward. C_LI

ecology↗

bioRxiv2023

Structural genomic variation and migratory behavior in wild songbirds

Structural variants (SVs) are a major source of genetic variation, but accurate descriptions in natural populations and connections with phenotypic traits remain scarce. We integrated advances in genomic sequencing and animal tracking to begin filling this knowledge gap in the Eurasian blackcap. Specifically, we (i) characterized the genome-wide distribution, frequency and overall fitness effects of SVs using haplotype-resolved assemblies for 79 birds, and (ii) used these SVs to study the genetics of seasonal migration. We detected >15K SVs. Many SVs overlapped repetitive regions and exhibited evidence of purifying selection suggesting they have overall deleterious effects on fitness. We used estimates of genomic differentiation to identify SVs exhibiting evidence of selection in blackcaps with different migratory strategies. Insertions and deletions dominated these SVs and were associated with genes that are either directly (e.g., regulatory motifs that maintain circadian rhythms) or indirectly (e.g., through immune response) related to migration. We also broke migration down into individual traits (direction, distance and timing) using existing tracking data and tested if genetic variation at the SVs we identified could account for phenotypic variation at these traits. This was only the case for one trait - direction - and one specific SV (a deletion on chromosome 27) accounted for much of this variation. Our results highlight the evolutionary importance of SVs in natural populations and provide insight into the genetic basis of seasonal migration.

evolutionary biology↗

bioRxiv2023

Evidence for adaptive evolution towards high magnetic sensitivity of potential magnetoreceptor in songbirds

Migratory birds possess remarkable accuracy in orientation and navigation, which involves various compass systems including the magnetic compass. Identifying the primary magnetosensor remains a fundamental open question. Cryptochromes (Cry) have been shown to be magnetically sensitive, specifically Cry4 shows enhanced magnetic sensitivity in migratory songbirds compared to resident species. Here, we investigate cryptochromes and their potential involvement in magnetoreception in a phylogenetic framework, integrating molecular evolutionary analyses with protein dynamics modeling. We base our analysis on 363 bird genomes and associate different selection regimes with migratory behaviour. We show that Cry4 is characterized by strong positive selection and high variability, typical characteristics of sensor proteins. We identify key sites that likely facilitated the evolution of a highly optimized sensory protein for night time compass orientation in songbirds and a potential functional shift or specialisation. Additionally, we show that Cry4 was lost in hummingbirds, parrots and Tyranni (Suboscines) and thus identified a natural comparative gene knockout, which can be used to test the function of Cry4 in birds. In contrast, the other two cryptochromes Cry1 and Cry2, were highly conserved in all species, indicating basal, non-sensory functions. Our results strengthen the hypothesised role of Cry4 as sensor protein in (night)-migratory songbirds.

evolutionary biology↗

bioRxiv2022

Comparative analysis of genome-scale, base-resolution DNA methylation profiles across 580 animal species

Methylation of cytosines is the prototypic epigenetic modification of the DNA. It has been implicated in various regulatory mechanisms throughout the animal kingdom and particularly in vertebrates. We mapped DNA methylation in 580 animal species (535 vertebrates, 45 invertebrates), resulting in 2443 genome-scale, base-resolution DNA methylation profiles of primary tissue samples from various organs. Reference-genome independent analysis of this comprehensive dataset quantified the association of DNA methylation with the underlying genomic DNA sequence throughout vertebrate evolution. We observed a broadly conserved link with two major transitions - once in the first vertebrates and again with the emergence of reptiles. Cross-species comparisons focusing on individual organs supported a deeply conserved association of DNA methylation with tissue type, and cross-mapping analysis of DNA methylation at gene promoters revealed evolutionary changes for orthologous genes with conserved DNA methylation patterns. In summary, this study establishes a large resource of vertebrate and invertebrate DNA methylomes, it showcases the power of reference-free epigenome analysis in species for which no reference genomes are available, and it contributes an epigenetic perspective to the study of vertebrate evolution.

genomics↗

bioRxiv2022

bi-axial orientation could explain range expansion in a migratory songbird

The likelihood of a new migratory route evolving is a function of the associated fitness payoff, and the probability that the route arises in the first place. Cross-breeding studies suggest that young birds migrate in a direction intermediate between their parents, though this would seemingly not explain how highly divergent migratory trajectories arise in apparently sympatric populations. It has been suggested that diametrically opposed reverse migratory trajectories might be surprisingly common, and if such routes were heritable it follows that they could underlie the rapid evolution of divergent migratory trajectories. Here, we used Eurasian blackcap (Sylvia atricapilla; blackcap) ringing recoveries and geolocator trajectories to investigate whether a recently-evolved northwards autumn migratory route could be explained by the reversal of each individuals expected southwards migratory direction. We found that northwards migrants were recovered closer to the sites specified by a precise axis reversal than would be expected by chance, consistent with the rapid evolution of new migratory routes via bi-axial variation in orientation. We suggest that the surprisingly high probability of axis reversal might allow birds to expand their wintering ranges rapidly, and hence propose that understanding how direction is encoded is crucial when characterising the genetic basis of migratory direction and how this relates to route evolution.

zoology↗

bioRxiv2022

Population-specific association of Clock gene polymorphism with annual cycle timing in stonechats

Timing is essential for survival and reproduction of organisms across the tree of life. The core circadian clock gene Clk has been implicated in annual timing and shows highly conserved sequence homology across vertebrates except for one variable region of poly Glutamine repeats. Clk genotype varies in some species with latitude, seasonal timing and migration. However, findings are inconsistent, difficult to disentangle from environmental responses, and biased towards high latitudes. Here we combine field data with a common-garden set up to study associations of Clk with latitude, migration and annual-cycle timing within the stonechat species complex with trans-equatorial distribution range. Including 950 individuals from nine populations with diverse migratory strategies. Gene diversity was lowest in resident African and Canary Island populations and increased with latitude, independently of migration distance. Repeat length and annual-cycle timing was linked in a population-specific way. Specifically, equatorial African stonechats showed delayed timing with longer repeat length for all annual-cycle stages. Our data suggest that at low latitudes with constant photoperiod, Clk genotype might orchestrate a range of consistent, individual chronotypes. In contrast, the influence of Clk on annual-cycle timing at higher latitudes might be mediated by its interactions with genes involved in (circadian) photoperiodic pathways.

genetics↗

bioRxiv2021

Recombination suppression and selection affect local ancestries in genomes of a migratory songbird

Genetic variation of the entire genome represents population structure, yet individual loci can show distinct patterns. Such deviations identified through genome scans have often been attributed to effects of selection instead of randomness. This interpretation assumes that long enough genomic intervals average out randomness in underlying genealogies, which represent local genetic ancestries. However, an alternative explanation to distinct patterns has not been fully addressed: too few genealogies to average out the effect of randomness. Specifically, distinct patterns of genetic variation may be due to reduced local recombination rate, which reduces the number of genealogies in a genomic window. Here, we associate distinct patterns of local genetic variation with reduced recombination rates in a songbird, the Eurasian blackcap (Sylvia atricapilla), using genome sequences and recombination maps. We find that distinct patterns of local genetic variation reflect haplotype structure at low-recombining regions either shared in most populations or found only in a few populations. At the former species-wide low-recombining regions, genetic variation depicts conspicuous haplotypes segregating in multiple populations. At the latter population-specific low-recombining regions, genetic variation represents variance among cryptic haplotypes within the low-recombining populations. With simulations, we confirm that these distinct patterns of haplotype structure evolve due to reduced recombination rate, on which the effects of selection can be overlaid. Our results highlight that distinct patterns of genetic variation can emerge through evolution of reduced local recombination rate. Recombination landscape as an evolvable trait therefore plays an important role determining the heterogeneous distribution of genetic variation along the genome.

evolutionary biology↗

bioRxiv2017

Comparative analysis examining patterns of genomic differentiation across multiple episodes of population divergence in birds

Heterogeneous patterns of genomic differentiation are commonly documented between closely related populations and there is considerable interest in identifying factors that contribute to their formation. These factors could include genomic features (e.g., areas of low recombination) that promote processes like linked selection (positive or purifying selection that affects linked neutral sites) at specific genomic regions. Examinations of repeatable patterns of differentiation across population pairs can provide insight into the role of these factors. Birds are well suited for this work, as genome structure is conserved across this group. Accordingly, we re-estimated relative (FST) and absolute (dXY) differentiation between eight sister pairs of birds that span a broad taxonomic range using a common pipeline. Across pairs, there were modest but significant correlations in window-based estimates of differentiation (up to 3% of variation explained for FST and 26% for dXY), supporting a role for processes at conserved genomic features in generating heterogeneous patterns of differentiation. This suggestion was reinforced by linear models identifying several genomic features (e.g., gene densities) as significant predictors of FST and dXY repeatability. FST repeatability was higher among pairs that were further along the speciation continuum (i.e., more reproductively isolated), suggesting that early stages of speciation may be dominated by positive selection that is different between pairs and replaced by processes acting according to shared genomic features as speciation proceeds.

genomics↗

bioRxiv2017

Correlated patterns of genetic diversity and differentiation across an avian family

Comparative studies of genomic differentiation among independent lineages can provide insights into aspects of the speciation process, such as the relative importance of selection and drift in shaping genomic landscapes, the role of genomic regions of high differentiation, and the prevalence of convergent molecular evolution. We investigated patterns of genetic diversity and divergence in stonechats (genus Saxicola), a widely distributed avian species complex with phenotypic variation in plumage, morphology, and migratory behavior, to ask whether similar genomic regions are important in the evolution of independent, but closely related, taxa. We used whole-genome pooled sequencing of 262 individuals from 5 taxa and found that patterns of genetic diversity and divergence are highly similar among different stonechat taxa. We then asked if these patterns remain correlated at deeper evolutionary scales and found that homologous genomic regions have become differentiated in stonechats and the closely related Ficedula flycatchers. Such correlation across a range of evolutionary divergence and among phylogenetically independent comparisons suggests that similar processes may be driving the differentiation of these independently evolving lineages, which in turn may be the result of intrinsic properties of particular genomic regions (e.g., areas of low recombination). Consequently, studies employing genome scans to search for areas important in reproductive isolation should account for corresponding regions of differentiation, as these regions may not necessarily represent speciation islands or facilitate local adaptation.

genomics↗