Evolution of sex chromosomes in Sylvioidea songbirds

Sex chromosomes were discovered more than 100 years ago. They have been studied intensely from a theoretical perspective since then, giving rise to a large body of testable predictions about their evolution from autosomes. A common feature of sex chromosomes is recombination suppression between the sex chromosome copies (X and Y in male heterogametic systems, or Z and W in female heterogametic systems). Without recombination, the sex-limited chromosome (Y or W) is expected to degenerate through the accumulation of deleterious mutations and repeat elements. Over long evolutionary time scales, this degeneration may leave the Y/W chromosomes short and almost completely devoid of functional genes.Using genome sequencing technology, we can now study the full DNA sequence of sex chromosomes. The analysis of sequence data from a wide range of taxonomic groups has revealed that sex chromosomes are more dynamic and variable than previously believed. Several aspects of sex chromosome evolution, however, remain poorly understood, especially relating to the early stages of evolution from autosomes. This is partly because some hypotheses are challenging to test, but also because most well-studied sex chromosome systems are evolutionarily old and biased towards XY systems.In this thesis, I study the evolution of sex chromosomes across Sylvioidea songbirds using genomic data and bioinformatic methodology. All members of this superfamily have a shared “neo-sex chromosome”: a fusion between an autosome (chromosome 4A) and the existing sex chromosomes. The sex chromosomes of birds (ZW) formed in a common ancestor more than 100 million years ago. Since then, the W chromosome has undergone severe degradation and shortening, obscuring almost all traces of their early evolution. Additions of new genetic material through autosome-sex chromosome fusions, however, allow us to study the early stages of sex chromosome evolution.I developed a computational pipeline aimed at discovering and visualizing sex chromosomes. I applied this pipeline to genomic data from species belonging to 13 different Sylvioidea families, and found that four additional autosome-sex chromosome fusions have occurred in different lineages within the group (involving chromosomes 3, 4, 5 and 8). These different fused regions have intermediate to extremely low W degeneration levels, with dosage sensitive and evolutionarily constrained genes being retained to a higher degree than other genes. I also studied the structure of these neo-sex chromosomes, how female gene expression changes in response to W degeneration and how recombination suppression extends along newly added sex chromosome regions. The work in this thesis shows that Sylvioidea songbirds are an ideal system for testing theory relating to sex chromosome evolution, and that bird sex chromosomes are more variable than previously believed

Early life and its implications for astrobiology : a case study from Bitter Springs Chert, Australia

Early life research faces additional challenges than those of the study of later life forms. Due to the de-materialization of the earliest rocks, valuable information about the early Earth is forever lost. Furthermore, early life was small and morphologically basic, effectuating abiotic pseudofossils to infiltrate the fossil record. A central theme is the close connection early life research share with astrobiology, manifested by the notion that early terre-strial life research should be conducted with as much vigilance as potential fossil findings from a remote planet. Both fields benefit from a broad-minded approach as the basic building blocks of life, previously thought to be pre-sent in all life forms, might have room for interchangability. Therefore, the biomarkers traditionally searched for might not reveal the full story of life. Petrography, XRF, SEM and FTIR was applied to rocks from Bitter Springs Formation, Australia, in hope to detect biogenic material. Hydrocarbons were detected in one of the samples thro-ugh FTIR analysis, which is a strong indicator for biogenicity. Many structures were found that are most probably bacterial fossils and oncoid structures.Forskning kring tidigt liv möter svårigheter utöver de som forskning kring senare liv ställs inför. På grund av att de tidigaste bergarterna inte finns bevarade har viktig information om jordens tidiga förhållanden för evigt gått förlorad. Dessutom var de tidigaste livsformerna små och morfologiskt enkla, vilket betyder att abiotiska pseudofossil lätt kan infiltrera fossilarkivet. Ett centralt tema är den nära kopplingen mellan forskning kring tidigt liv och astrobiologi, delvis på grund av att tidigt liv på jorden måste undersökas med samma hårda krav som vi skulle ställa på potentiella fossil från andra planeter. Båda forskningsfälten gagnas av vidsynthet då det är möjligt att de byggstenar vi traditionellt sett kopplat till livsformer kan bytas ut mot andra ämnen. Det är därför möjligt att sökandet efter traditionella biomarkörer inte räcker till för att klarlägga livets fulla historia. Petrografiska undersökningar, XRF, SEM och FTIR applicerades på stuffer från Bitter Springs Formation, Australien, för att se ifall deinnehöll biologiskt material. Kolväten hittades genom FTIR-analys, vilket är en stark bioindikator. Flera strukturer hittades som högst troligtvis är fossila bakterier och oncoider

Whole-genome analysis across 10 songbird families within Sylvioidea reveals a novel autosome-sex chromosome fusion

Sex chromosomes in birds have long been considered to be extremely stable. However, this notion has lately been challenged by findings of independent autosome-sex chromosome fusions within songbirds, several of which occur within a single clade, the superfamily Sylvioidea. To understand what ecological and evolutionary processes drive changes in sex chromosome systems, we need complete descriptions of sex chromosome diversity across taxonomic groups. Here, we characterize the sex chromosome systems across Sylvioidea using whole-genome data of species representatives of 10 different families, including two published and eight new genomes. We describe a novel fusion in the family Cisticolidae (represented by Cisticola juncidis) involving a part of chromosome 4. We also confirm the previously identified fusion between chromosome Z and a part of chromosome 4A in all 10 families and show that fusions involving parts of chromosomes 3 and 5 are not found outside the families where they were first discovered (Alaudidae and Panuridae). These findings add to the complexity of the sex chromosome system in Sylvioidea, where four independent autosome-sex chromosome fusions have now been identified

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

Background: 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. Results: Here we present findZX, an automated Snakemake-based computational pipeline for detecting and visualizing sex chromosomes through differences in genome coverage and heterozygosity between any number of males and females. A main feature of the pipeline is the option to perform a genome coordinate liftover to a reference genome of another species. This 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, and fish), with sex chromosome systems of different ages, sizes, and levels of differentiation. We also demonstrate that the liftover method is robust over large phylogenetic distances (> 80 million years of evolution). Conclusions: With findZX we provide an easy-to-use and highly effective tool for identification of sex chromosomes. The pipeline is compatible with both Linux and MacOS systems, and scalable to suit different computational platforms

Assessment of phylogenetic approaches to study the timing of recombination cessation on sex chromosomes

The evolution of sex chromosomes is hypothesized to be punctuated by consecutive recombination cessation events, forming “evolutionary strata” that ceased to recombine at different time points. The demarcation of evolutionary strata is often assessed by estimates of the timing of recombination cessation (tRC) along the sex chromosomes, commonly inferred from the level of synonymous divergence or with species phylogenies at gametologous (X-Y or Z-W) sequence data. However, drift and selection affect sequences unpredictably and introduce uncertainty when inferring tRC. Here, we assess two alternative phylogenetic approaches to estimate tRC; (i) the expected likelihood weight (ELW) approach that finds the most likely topology among a set of hypothetical topologies and (ii) the BEAST approach that estimates tRC with specified calibration priors on a reference species topology. By using Z and W gametologs of an old and a young evolutionary stratum on the neo-sex chromosome of Sylvioidea songbirds, we show that the ELW and BEAST approaches yield similar tRC estimates, and that both outperform two frequently applied approaches utilizing synonymous substitution rates (dS) and maximum likelihood (ML) trees, respectively. Moreover, we demonstrate that both ELW and BEAST provide more precise tRC estimates when sequences of multiple species are included in the analyses

Why Do Sex Chromosomes Stop Recombining?

It is commonly assumed that sex chromosomes evolve recombination suppression because selection favours linkage between sex-determining and sexually antagonistic genes. However, although the role of sexual antagonism during sex chromosome evolution has attained strong support from theory, experimental and observational evidence is rare or equivocal. Here, we highlight alternative, often neglected, hypotheses for recombination suppression on sex chromosomes, which invoke meiotic drive, heterozygote advantage, and genetic drift, respectively. We contrast the hypotheses, the situations when they are likely to be of importance, and outline why it is surprisingly difficult to test them. Lastly, we discuss future research directions (including modelling, population genomics, comparative approaches, and experiments) to disentangle the different hypotheses of sex chromosome evolution

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

Recombination strongly impacts sequence evolution by affecting the extent of linkage and the efficiency of selection. Here, we study recombination over the Z chromosome in great reed warblers (Acrocephalus arundinaceus) using pedigree-based linkage mapping. This species has extended Z and W chromosomes (“neo-sex chromosomes”) formed by a fusion between a part of chromosome 4A and the ancestral sex chromosomes, which provides a unique opportunity to assess recombination and sequence evolution in sex-linked regions of different ages. We assembled an 87.54 Mbp and 90.19 cM large Z with a small pseudoautosomal region (0.89 Mbp) at one end and the fused Chr4A-part at the other end of the chromosome. A prominent feature in our data was an extreme variation in male recombination rate along Z with high values at both chromosome ends, but an apparent lack of recombination over a substantial central section, covering 78% of the chromosome. The nonrecombining region showed a drastic loss of genetic diversity and accumulation of repeats compared to the recombining parts. Thus, our data emphasize a key role of recombination in affecting local levels of polymorphism. Nonetheless, the evolutionary rate of genes (dN/dS) did not differ between high and low recombining regions, suggesting that the efficiency of selection on protein-coding sequences can be maintained also at very low levels of recombination. Finally, the Chr4A-derived part showed a similar recombination rate as the part of the ancestral Z that did recombine, but its sequence characteristics reflected both its previous autosomal, and current Z-linked, recombination patterns

A novel neo-sex chromosome in Sylvietta brachyura (Macrosphenidae) adds to the extraordinary avian sex chromosome diversity among Sylvioidea songbirds

We report the discovery of a novel neo-sex chromosome in an African warbler, Sylvietta brachyura (northern crombec; Macrosphenidae). This species is part of the Sylvioidea superfamily, where four separate autosome–sex chromosome translocation events have previously been discovered via comparative genomics of 11 of the 22 families in this clade. Our discovery here resulted from analyses of genomic data of single species-representatives from three additional Sylvioidea families (Macrosphenidae, Pycnonotidae and Leiothrichidae). In all three species, we confirmed the translocation of a part of chromosome 4A to the sex chromosomes, which originated basally in Sylvioidea. In S. brachyura, we found that a part of chromosome 8 has been translocated to the sex chromosomes, forming a unique neo-sex chromosome in this lineage. Furthermore, the non-recombining part of 4A in S. brachyura is smaller than in other Sylvioidea species, which suggests that recombination continued along this region after the fusion event in the Sylvioidea ancestor. These findings reveal additional sex chromosome diversity among the Sylvioidea, where five separate translocation events are now confirmed

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

Abstract Recombination strongly impacts sequence evolution by affecting the extent of linkage and the efficiency of selection. Here, we study recombination over the Z chromosome in great reed warblers (Acrocephalus arundinaceus) using pedigree-based linkage mapping. This species has extended Z and W chromosomes (“neo-sex chromosomes”) formed by a fusion between a part of chromosome 4A and the ancestral sex chromosomes, which provides a unique opportunity to assess recombination and sequence evolution in sex-linked regions of different ages. We assembled an 87.54 Mbp and 90.19 cM large Z with a small pseudoautosomal region (0.89 Mbp) at one end and the fused Chr4A-part at the other end of the chromosome. A prominent feature in our data was an extreme variation in male recombination rate along Z with high values at both chromosome ends, but an apparent lack of recombination over a substantial central section, covering 78% of the chromosome. The nonrecombining region showed a drastic loss of genetic diversity and accumulation of repeats compared to the recombining parts. Thus, our data emphasize a key role of recombination in affecting local levels of polymorphism. Nonetheless, the evolutionary rate of genes (dN/dS) did not differ between high and low recombining regions, suggesting that the efficiency of selection on protein-coding sequences can be maintained also at very low levels of recombination. Finally, the Chr4A-derived part showed a similar recombination rate as the part of the ancestral Z that did recombine, but its sequence characteristics reflected both its previous autosomal, and current Z-linked, recombination patterns