chevron down chevron up

PhD Topics 2019

  • Complex trait dissection in conifers. Summary
  • Contribution of transposable elements to adaption during experimental evolution. Summary
  • Detection of adaptive gene introgression. Summary
  • Efficient detection of variants of polygenic adaptation in Drosophila experimental evolution. Summary
  • Evolution of gene expression. Summary
  • Footprints of polygenic adaptation. Summary
  • Functional characterization of adaptive QTLs. Summary
  • Functional characterization of beneficial alleles in Drosophila. Summary
  • Historical demography in horses. Summary
  • Incipient speciation during adaptation to a new environment. Summary
  • Inference of selection parameters using whole genome data. Summary
  • Long term dynamics of transposable element invasions. Summary
  • Microbiome evolution in Drosophila. Summary
  • Multi-measurement experimental evolution: How to combine evidence from different sources? Summary
  • Polygenic adaptation: The roles of pleiotropy and epistasis. Summary
  • Population genomic footprints and drivers of repeated trait shifts during adaptive radiation. Summary
  • Sequence diversity in mammalian Y chromosomes. Summary
  • The genetics of local adaptation in Arabidopsis thaliana. Summary
  • The molecular basis of recurring, multi-trait plant adaptation to substrate. Summary
  • The role of a nascent sex chromosome on interspecific patterns of allele sharing. Summary
  • The sources of variation fueling adaptive radiation after long-distance dispersal. Summary
  • Transposon polymorphism in Arabidopsis thaliana. Summary
  • Within-species consequences of genomic interactions in ecologically important species. Summary


Complex trait dissection in conifers

Principal advisor: Kelly Swarts

Trees are critical components of forest ecosystems but their long generation times make it particularly challenging to adapt to rapidly changing climate. Long generation times also make traditional quantitative genetics approaches for isolating genetic and adaptive (genotype by environment) variation costly and time-intensive. This project focuses on developing a new approach to isolating adaptive variation in natural forest stands using tree-ring information, and then understanding the genetics underlying adaptive variation using genomic approaches. This project involves significant fieldwork sampling trees; a computational or statistical background would be helpful, but is not required.


Contribution of transposable elements to adaption during experimental evolution

Principal advisor: Christian Schlötterer

The insertion of transposable elements affects the pattern of gene expression of neighboring genes. This project addresses the question to what extent transposable elements are mobilized by temperature stress and how mobilized elements contribute to adaptation. The project will have access to two D. melanogaster and three D. simulans populations, which have evolved in replicated experiments for more than 100 generations to hot environments. Using a combination of whole genome sequencing and RNA-Seq data, the impact of TEs will be studied.


Detection of adaptive gene introgression

Principal advisor: Joachim Hermisson

Our previous work focusses on the introgression probability of the beneficial allele and on the hitchhiking probability of single linked deleterious or neutral variants (Uecker et al., 2015). We also developed a method to detect footprints of adaptive introgression from genome-wide polymorphism data (Setter 2018). In a current data-driven project led by K. Stankiewicz and in collaboration with M. Nordborg, these methods are adapted and applied to genome-wide sequence data from Arabidopsis. We plan to complement this project by a model/theory-driven approach with the aim to describe the haplotype structure after adaptive introgression. We will address questions such as: What is the distribution of introgression tract lengths around the beneficial allele for a single successful introgression event? How many distinct pieces of introgressed material do we expect to find – and at which distance to the beneficial allele? How do linked deleterious alleles (which may either hitchhike or not) affect these results? We will use analytical theory based on branching processes (Uecker et al., 2015), and coalescent simulations. Knowledge about the haplotype pattern is relevant, in particular, to distinguish introgression patterns from patterns of long-term balancing selection.

Related literature:

  • Setter D. Footprints of adaptive introgression. PhD thesis (Univ. of Vienna, 2018)
  • Uecker H, Setter D and Hermisson J. Adaptive gene introgression after secondary contact. J. Math. Biol. 70(7), 1523–1580. (2015) doi: 10.1007/s00285-014-0802-y


Efficient detection of variants of polygenic adaptation in Drosophila experimental evolution

Principal advisor: Andreas Futschik

In recent E&R experiments with Drosophila, some loci show an initial strong increase in allele frequency followed by a period where allele frequencies remain fairly constant. Such a plateauing pattern of allele frequency change may occur for different reasons but does not fit into a selective sweep framework (Orozco-terWengel et al., 2012). The same pattern has also been observed with other organisms. Indeed, using experimental data from outcrossed yeast populations, Kosheleva and Desai (2018) observed a diminishing strength of selection at the individual locus level while fitness is still increasing. They found evidence that this observed pattern results from recombination acting on a large number of weakly selected sites, with subsets of them initially in linkage disequilibrium. Their underlying (close to infinitesimal) model involving highly polygenic adaptation may in principle apply also to similar patterns found in Drosophila. Without fitness measurements there are also alternative explanations for a diminishing strength of selection at the locus level, such as a smaller number of unlinked loci both with weak and strong additive effects that are selected until a trait optimum is reached. Large, initially selected, blocks could then also be explained by hitchhiking on beneficial haplotypes. Epistasis or loci at which there is some form of heterozygote advantage may also lead to plateauing. A first goal is to find out whether it is possible to distinguish between these scenarios based on a typical experimental setup with Drosophila when fitness measurements are not available. Suitable summary statistics will be needed for this purpose, whose distributions differ between the scenarios. In Hermisson and Pennings (2017), footprints of rapid adaptation are discussed. Under the scenario proposed by the authors, summary statistics should also capture the pattern of decay of LD, and could possibly be derived from the dynamics of the correlation patterns of the allele frequency changes. Another approach would be to use machine learning based on a large number of simulated data to come up with suitable summary statistics. The software packages SLiM and MimicrEE are suitable for producing individual based simulation data in our context. Because yeast and Drosophila differ in many respects, we also plan to explore which experimental design parameters (in particular: population size, number of generations, number of replicates, number of sequencing time points, number of founding haplotypes) are needed to distinguish between the discussed scenarios.

Related literature:

  • Hermisson J and Pennings PS. Soft sweeps and beyond: understanding the patterns and probabilities of selection footprints under rapid adaptation. Methods Ecol. Evol. 8(6), 700–716. (2017) doi: 10.1111/2041-210X.12808
  • Kosheleva K and Desai MM. Recombination alters the dynamics of adaptation on standing variation in laboratory yeast populations. Mol. Biol. Evol. 35(1), 180–201. (2018) doi: 10.1093/molbev/msx278
  • Orozco-terWengel P, Kapun M, Nolte V, Kofler R, Flatt T and Schlötterer C. Adaptation of Drosophila to a novel laboratory environment reveals temporally heterogeneous trajectories of selected alleles. Mol. Ecol. 21(20), 4931–4941. (2012) doi: 10.1111/j.1365-294X.2012.05673.x


Evolution of gene expression

Principal advisor: Christian Schlötterer

While variation in gene expression is a major source of phenotypic diversity, our understanding of the processes driving changes in gene expression are still poorly understood. With the new sequencing technologies it will be possible to address many important questions about the evolution of gene expression.

The successful candidate will be part of a team of scientists studying adaptation of experimental Drosophila populations to temperature stress. She/he can build on several highly replicated Drosophila populations that have evolved under various temperature regimes.  We are planning to address the importance of plasticity in gene expression for adaptation to novel temperature regimes and how expression differences translate into fitness.

Related literature:

  • Jaksic, A.M., and Schlötterer, C. (2016). The interplay of temperature and genotype on patterns of alternative splicing in Drosophila melanogaster. Genetics 204, 315-325.
  • Chen, J., Nolte, V., and Schlötterer, C. (2015a). Temperature stress mediates decanalization and dominance of gene expression in Drosophila melanogaster. PLoS Genetics 11, e1004883. 10.1371
  • Chen, J., Nolte, V., and Schlötterer, C. (2015b). Temperature related reaction norms of gene expression: regulatory architecture and functional implications. Molecular Biology and Evolution 32, 2393-2402.


Footprints of polygenic adaptation

Principal advisor: Joachim Hermisson

The standard model in molecular population genetics assumes that selection on a phenotypic trait leads to simple directional selection on its genetic basis. This leads to (hard or soft) selective sweeps as a footprint of selection in DNA polymorphism data. In contrast, polygenic adaptation refers to a scenario where phenotypic adaptation results from a collective change in the allele frequencies at many underlying genes (e.g., Boyle and Pritchard, 2017). If selection on single loci is constrained by epistatic interaction with its genetic background, allele frequency trajectories (and resulting footprints) differ strongly from the sweep paradigm. Empirical evidence indicates that this may often be the case. Literature on polygenic adaptation assumes a deterministic model for allele frequency changes (Chevin and Hospital, 2008; Jain and Stephan, 2017). However, our previous results (Hermisson and Pennings, 2017; Höllinger et al., 2018 in prep.) show that genetic drift is crucial for the pattern. In Höllinger et al. (2018 in prep.), we have developed an analytical approach to address this problem based on Yule branching processes. In the next funding period, we will apply this approach to various selection scenarios on quantitative traits, including spatially and temporally heterogeneous selection (“moving optimum”, see Jones et al. 2014, Matuszewski et al. 2015) and truncation selection. Based on these results, we will develop statistical frameworks to detect footprints of polygenic adaptation from replicated evolution experiments.

Related literature:

  • Boyle EA, Li YI and Pritchard JK. An expanded view of complex traits: From polygenic to omnigenic. Cell. (2017) doi: 10.1016/j.cell.2017.05.038Boyle EA, Li YI and Pritchard JK. An expanded view of complex traits: From polygenic to omnigenic. Cell. (2017) doi: 10.1016/j.cell.2017.05.038
  • Chevin LM and Hospital F. Selective sweep at a quantitative trait locus in the presence of background genetic variation. Genetics 180(3), 1645–1660. (2008) doi: 10.1534/genetics.108.093351
  • Hermisson J and Pennings PS. Soft sweeps and beyond: understanding the patterns and probabilities of selection footprints under rapid adaptation. Methods Ecol. Evol. 8(6), 700–716. (2017) doi: 10.1111/2041-210X.12808
  • Höllinger I, Pennings PS, Hermisson J: Polygenic adaptation: From sweeps to subtle frequency shifts. bioRxiv 450759. (2018) doi: 10.1101/450759
  • Jain K and Stephan W. Rapid adaptation of a polygenic trait after a sudden environmental shift. Genetics 206(1), 389–406. (2017) doi: 10.1534/genetics.116.196972
  • Jones AG, Bürger R and Arnold SJ. Epistasis and natural selection shape the mutational architecture of complex traits. Nat. Commun. 5, 3709. (2014) doi: 10.1038/ncomms4709
  • Matuszewski S, Hermisson J and Kopp M. Catch me if you can: Adaptation from standing genetic variation to a moving phenotypic optimum. Genetics 200(4), 1255–1274. (2015) doi: 10.1534/genetics.115.178574


Functional characterization of adaptive QTLs

Principal advisor: Christian Schlötterer

It is widely accepted that most adaptive traits are encoded by many loci, each with a relatively small effect. Hence, in many cases the identification of such loci by population genetic tests is difficult, if not impossible. In an experimental evolution framework with replicated populations it is, however, possible to identify and characterize adaptive QTLs. Based on the analysis of D. simulans populations, which have evolved for more than 100 generations in a novel temperature environment, the PhD student will identify selected loci. After fine-mapping, the selected loci will be functionally characterized using CRISPR/Cas9 mediated transgenesis in combination with state of the art high-throughput phenotyping (RNA-Seq, translatomics and metabolomics).


Functional characterization of beneficial alleles in Drosophila

Principal advisors: Kirsten-André Senti, Christian Schlötterer

One of the most amazing feats in biology is how natural selection enabled the adaption of species to different natural environments. Yet even a single Drosophila species thrives in diverse climates as equatorial Africa or Europe. From the natural variation within such species, we can – in principle - learn how evolution has shaped environmental adaption. Yet until recently finding the link between phenotype and genotype was a rare and difficult undertaking (1). However, today’s next generation sequencing offers an unprecedented view on the genetic variability. Combining phenotypic analyses with sequencing, Genome Wide Association Studies (GWAS) for instance enabled the identification of beneficial human alleles that protect against diseases (2).

Using paradigms such as starvation resistance and adaption to different temperatures, we have performed both GWAS as well as experimental evolution in combination with whole-genome re-sequencing of natural Drosophila populations (3). These experiments have established a number naturally occurring alleles that are associated with either increased survival under starvation stress or improved adaption to warmer or colder climates.

To validate these associations, we aim to employ the powerful CRISPR/Cas9 mediated genome engineering to functionally test if these natural gene variants indeed provide fitness advantages in well-controlled experimental settings. First, this project will establish a stable genome modification platform for natural Drosophila strains. Secondly, it will provide genetic and functional proof for beneficial adaptive alleles. Finally and in conjunction with our previous work, this approach will uncover those biological mechanisms that evolution tinkered with during adaption of natural populations.

Related literature:

  • (1) Sawyer L.A. et al., (1997) Natural variation in a Drosophila clock gene and temperature compensation. Science 278, 5346, 2117-2120
  • (2) Harper A.R. et al. (2015) Protective alleles and modifier variants in human health and disease. Nature Reviews Genetics, doi:10.1038/nrg4017
  • (3) Schlötterer C. et al. (2015) Combining experimental evolution with next-generation sequencing: a powerful tool to study adaptation from standing genetic variation. Heredity 114, 431-440


Historical demography in horses

Principal advisor: Barbara Wallner

The male specific region on the Y chromosome is a powerful tool to study population histories, in particular in comparison with the female-specific mtDNA. Horses provide a particularly striking example for different demographic patterns of the two sexes. The high mtDNA diversity, with coalescence times clearly pre-dating the species’ domestication, contrasts a very recent Y chromosome, derived from a common ancestor roughly 1000 years ago. Due to extensive human intervention, contemporary horse populations are genetically distinct from 5,500 year old early domestics. However, neither time frames nor the impact of historic radiations that influenced the horse genomic landscape are clearly defined yet. We recently showed that the strong male-focused import of horses from the Orient during the past 500 years eradicated Y chromosomal sequence diversity in Central Europe. The shallow contemporary horse Y chromosome phylogeny is in contrast to the polymorphic Y observed in ancient horses. Asian and rural breeds from other parts of the world experienced breeding histories different from strongly selected European breeds. Therefore they provide the opportunity to uncover historic signatures that have been erased in intensively bred populations. This project aims to draw a picture about historic radiations in horses by studying comprehensive MSY and mtDNA phylogenies from a worldwide population sample. The disclosure of the full spectrum of male and female lineages sampled today should uncover the impact of human cultures have and had on the horse genome. A student working on this project will first infer the distribution of already described Y and mtDNA haplogroups by genotyping followed by de novo variant ascertainment via Next Generation Sequencing. The inclusion of ancient samples should augment the view on past Y-chromosomal haplotype trajectories and build a backbone for tracing the origin of present lineages.

Related literature:

  • Felkel S, Vogl C, Rigler D, Jagannathan V, Leeb T, Fries R, Neuditschko M, Rieder S, Velie B, Lindgren G, Rubin C-J, Schlötterer C, Rattei T, Brem G and Wallner B. Asian horses deepen the MSY phylogeny. Anim. Genet. 49(1), 90–93. (2018) doi: 10.1111/age.12635
  • Wallner B, Palmieri N, Vogl C, Rigler D, Bozlak E, Druml T, Jagannathan V, Leeb T, Fries R, Tetens J, Thaller G, Metzger J, Distl O, Lindgren G, Rubin CJ, Andersson L, Schaefer R, … Brem G. Y chromosome uncovers the recent oriental origin of modern stallions. Curr. Biol. 27(13), 2029–2035.e5. (2017) doi: 10.1016/j.cub.2017.05.086


Incipient speciation during adaptation to a new environment

Principal advisor: Christian Schlötterer

The emergence of new species is one of the most fundamental questions in biology, that is still not fully resolved. This project builds on the observation that flies which evolved for less than 200 generations in a novel environment are less likely to mate with flies from the ancestral population. In combination with the diverged gene expression of genes involved in sexual selection, these data suggest that the evolved flies are becoming reproductively isolated. The project will use state of the art phenotyping, including video-based behavioral assays, CHC and gene expression analyses and metabolomics to study this case of incipient speciation and shed light on the process of reproductive isolation occurring on time scales shorter than 200 generations.


Inference of selection parameters using whole genome data

Principal advisor: Claus Vogl

We will extend existing models to allow for exact inference of directional selection (or equivalently GC-biased gene conversion) in addition to mutation and drift using allele frequency spectra. Even short introns and fourfold degenerate sites, the best candidates for neutrally evolving nucleotide sites, show deviation from neutrality but can be described by the nearly neutral theory. A model with directional selection (or equivalently GC-biased gene conversion) with a scaled selection strength of about one, however fits the data (Vogl and Bergman, 2015; and unpublished data analyses). So far, we assumed mutation-selection-drift equilibrium for maximum marginal likelihood inference (Vogl and Bergman, 2015). To this end, we developed a model, where a single mutation segregates in a moderately sized sample (Bergman et al., 2018). This model is identical to a first order Taylor series expansion for small scaled mutation rates of the general mutation-drift model. We extended this model to splitting populations and non-equilibrium scenarios using orthogonal polynomials and now propose to incorporate also directional selection in this framework. We will apply the method to data from cosmopolitan and sub-Saharan African Drosophila populations to infer concurrently mutation, selection, and population demography.

Related literature:

  • Bergman J, Schrempf D, Kosiol C and Vogl C. Inference in population genetics using forward and backward, discrete and continuous time processes. J. Theor. Biol. 439, 166–180. (2018) doi: 10.1016/j.jtbi.2017.12.008
  • Vogl C and Bergman J. Inference of directional selection and mutation parameters assuming equilibrium. Theor. Popul. Biol. 106, 71–82. (2015) doi: 10.1016/j.tpb.2015.10.003

Long term dynamics of transposable element invasions

Principal advisor: Robert Kofler

The activity of transposable elements (TEs) is suppressed by small RNAs, the so-called piRNAs (Brennecke et al., 2007; Gunawardane et al., 2007). These piRNAs are generated at distinct genomic loci, the piRNA clusters (Malone et al., 2009). It is assumed that a TE invasion proceeds until insertions in piRNA clusters occur, which suppress the activity of the TE (Bergman et al., 2006; Kofler et al., 2018).

This project will use computer simulations to evaluate the predicted TE dynamics of the “trap model”. One prediction is that several distinct piRNA cluster insertions silencing a particular TE are segregating in a population just after the invasion is being controlled by the piRNA defense. In small populations, cluster insertions may be lost by drift in some individuals, resulting in a reactivation of the invading TE. We will compare the invasion dynamics for different population sizes to evaluate the extent of TE reactivation. Another scenario is the combination of the trap model with negative selection. Ectopic recombination among TEs causes negative selection against TE insertions, including cluster insertions. We will test the hypothesis that this negative selection can reactivate TEs by loss of cluster insertions. A further prediction of the “trap model” is that cluster insertions eventually become fixed by genetic drift, resulting in a permanent TE silencing. We will estimate the time required for fixation of such cluster insertions and thus determine the period of time for which a residual activity of a TE can be expected. The results of the computer simulations will be compared to data from recent P-element invasions in natural and laboratory Drosophila populations.

Related literature:

  • Bergman CM, Quesneville H, Anxolabéhère D and Ashburner M. Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome. Genome Biol. 7(11), R112. (2006) doi: 10.1186/gb-2006-7-11-r112
  • Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R and Hannon GJ. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128(6), 1089–1103. (2007) doi: 10.1016/j.cell.2007.01.043
  • Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H and Siomi MC. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 315(5818), 1587–1590. (2007) doi: 10.1126/science.1140494
  • Kofler R, Senti K-A, Nolte V, Tobler R and Schlötterer C. Molecular dissection of a natural transposable element invasion. Genome Res. gr.228627.117. (2018) doi: 10.1101/gr.228627.117
  • Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, Sachidanandam R and Hannon GJ. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137(3), 522–535. (2009) doi: 10.1016/j.cell.2009.03.040

Microbiome evolution in Drosophila

Principal advisor: Christian Schlötterer

The microbiome is a complex community of microorganisms which has a major influence on its host. While it has been shown that the composition of the microbiome is affected by many factors (e.g.:  diet), long-term transgenerational studies of microbiome dynamics are rare. Drosophila provides an excellent model to study microbiome evolution, because the microbiome is simple consisting of only a moderate number of taxa. In combination with the short generation time of Drosophila, it is possible to follow the evolution of the Drosophila microbiome across many generations.

This project will take advantage of many Drosophila populations, which have been evolving for more than 150 generations together with their associated microbiome. Using a combination of state-of-the-art metagenomics and targeted analysis of individual strains of ancestral and evolved microbiomes this project with provide unprecedented insights into the evolution of the microbiome.


Multi-measurement experimental evolution: How to combine evidence from different sources?

Principal advisor: Andreas Futschik

A typical Evolve and resequence (E&R) experiment involves replicate populations for which allele frequency changes are measured. Common methods to test for selection are either applied to each population separately or assume a consistent signal across replicates. However, inconsistent signals are frequently encountered across replicates. Methods that assume consistent allele frequency changes are then not very efficient. It is therefore of interest to develop new approaches that can combine evidence from different replicates and provide good power both for consistent and inconsistent signals. As a starting point, we will use the omnibus test developed by Futschik et al. (2018) which is based on independent p-values. This test provides good power no matter for how many tests k (≥1) the null hypothesis is false. An advantage of the method is its modularity, i.e., p-values from any statistical test can be taken as input, provided they are uniformly distributed under the null model. We intend to extend this approach in several directions: For instance, (i) by considering a whole time series of measurements simultaneously; (ii) by considering spatial response patterns along the chromosome, and taking into account linkage and haplotype structure; (iii) by simultaneous consideration of gene sets (as defined e.g., by GO-categories) to obtain the combined evidence for a GO-category; and (iv) by simultaneously considering different types of –omics data for genes that show a signal of selection in at least one of these categories while still controlling for multiple testing. Finally, as measurements at the single-cell level are currently becoming available, we intend to combine the evidence across cells to determine the genes that exhibit a response in at least some of the cells. Our intended method will not dilute sparse signals by averaging across all cells.

Related literature:

  • Futschik A, Taus T and Zehetmayer S. An omnibus test for the global null hypothesis. Stat. Methods Med. Res. (2018) arXiv: 1709.00960


Polygenic adaptation: The roles of pleiotropy and epistasis

Principal advisor: Reinhard Bürger

Many traits important for ecological adaptation are quantitative traits, i.e., traits, such as body size, that vary continuously and can be measured on a scale. Typically, they are determined by contributions from many genetic loci. Often these loci also affect other traits, i.e., they have pleiotropic effects, and alleles exhibit dominance. Loci may also interact with each other, a phenomenon called epistasis. The aim of this project is to study the evolutionary dynamics of gene and genotype frequencies while the trait is adapting to a new optimum, i.e., after an environmental shift. Pleiotropy may be modeled, for instance, by deleterious effects on fitness but also by direct effects on other traits under selection. Problems of the following kind will be tackled. How many loci show a response? What is the magnitude of response at individual loci? In particular, do plateaus in the response occur, i.e., are complete or incomplete sweeps more common? What is the role of epistasis, dominance, and pleiotropy? How much variation of the response among replicates is expected? How does the response depend on initial frequencies (standing variation vs. new mutations), on the magnitude of allelic effects, and on population size. In the deterministic case, when population size is very large, the corresponding models are formulated as systems of nonlinear difference or differential equations. Otherwise, they are framed in terms of stochastic processes, in particular, branching processes and diffusion processes (depending on the question that shall be answered). The models will be studied by mathematical techniques from dynamical systems and by individual-based computer simulations.


Population genomic footprints and drivers of repeated trait shifts during adaptive radiation

Principal advisor: Christian Lexer

Species radiations have thus far been studied primarily from a macro-evolutionary perspective within a phylogenetic framework. Novel genomic tools now allow population geneticists to identify the major sources of genetic variation that fuel evolutionary radiations, as exemplified by recent high-profile work on cichlids, tropical butterflies, and flowering plants. In this project, you will address the genomic substrate and population genetic drivers of diversification in a highly species-rich clade of Bromeliaceae, the pineapple family, a group that benefits from several existing and emerging chromosome-level genome assemblies (e.g. Ming et al., 2015 Nat Genet 47). Numerous enigmatic adaptive traits or ´key innovations´ segregate in the family, including different photosynthetic pathways (C3 vs. CAM) and pollination syndromes (humming birds / bats / insects). Focused on a particularly species-rich and phenotypically variable clade of tillandsioid bromeliads (Tillandsia biflora complex), you will use a combination of whole genome resequencing, target capture sequencing, and transcriptomics to address (1) the role of repeated evolution vs wide-spread interspecific gene flow in generating patterns of trait shifts seen in phylogenetic trees, (2) the roles of adaptive protein evolution, regulatory evolution, and gene duplication in providing the genomic substrate for adaptive radiation.


Sequence diversity in mammalian Y chromosomes

Principal advisor: Barbara Wallner

Y chromosomes are much more dynamic than previously assumed. In flies, the number of Y-linked genes varies substantially between species with many genes on Y chromosomes, being recruited secondarily from autosomes and the X chromosome. Mammalian Y chromosomes also show strong lineage specific evolution, but transfers from other chromosomes are not well documented. So far our understanding of the evolutionary dynamics of gene persistence and loss on the mammalian Y chromosome is mainly based on studies in primate lineages. The divergence times of several domestic species groups is similar to human and apes, providing replicated systems to study Y chromosome evolution. This project aims to understand the evolutionary forces and dynamics of mammalian Y chromosomes by studying several species groups with similar divergence as humans and apes (2-20 mya) in parallel. In the first phase of the project, the student will build Y-chromosomal assemblies within domestic bovids, equids, camelids and canids and annotate the orthologous Y chromosomal genes. Based on these assemblies, gene composition and turnover will be determined and purifying selection will be estimated from the ratio of synonymous to non-synonymous substitutions. In the second phase, the student will measure selection on the population level by using NGS data. In the context of this project we will focus on lineage-specific as well as shared evolutionary constraints of the Y chromosomal genes and will study the extent to which different types of selection act to maintain genes within this unique genomic environment. Apart from the insights into the evolutionary dynamics of the Y chromosome within and between species, the Y chromosome assemblies generated will provide the basis for future fine grained male demographies of domestic mammals.

Related literature:

  • Mahajan S and Bachtrog D. Convergent evolution of Y chromosome gene content in flies. Nat. Commun. 8(1). (2017) doi: 10.1038/s41467-017-00653-x
  • Tobler R, Nolte V and Schlötterer C. High rate of translocation-based gene birth on the Drosophila Y chromosome. Proc. Natl. Acad. Sci. 114(44), 11721–11726. (2017) doi: 10.1073/pnas.1706502114
  • Wallner B, Palmieri N, Vogl C, Rigler D, Bozlak E, Druml T, Jagannathan V, Leeb T, Fries R, Tetens J, Thaller G, Metzger J, Distl O, Lindgren G, Rubin CJ, Andersson L, Schaefer R, … Brem G. Y chromosome uncovers the recent oriental origin of modern stallions. Curr. Biol. 27(13), 2029–2035.e5. (2017) doi: 10.1016/j.cub.2017.05.086


The genetics of local adaptation in Arabidopsis thaliana

Principal advisor: Magnus Nordborg

We have been carrying out a number of long-term field experiments in Sweden, using native Swedish lines of A. thaliana (Long et al., 2013). Rather than just growing plants in plots and measuring seed set as a proxy for fitness, we established “natural” sites where the plants can compete over multiple generations, and sampled individuals throughout the experiment. Over 10,000 plants have been sampled, and we are currently in the process of sequencing them in order to map genes responsible for fitness differences using genome-wide association. The results will be compared with phenotypes (including transcriptome and epigenome) data taken from common-garden experiments carried out at the same sites. This will make it possible to investigate whether loci that show signs of selection are also associated with particular phenotypes.

Related literature:

  • Long Q, Rabanal FA, Meng D, Huber CD, Farlow A, Platzer A, Zhang Q, Vilhjálmsson BJ, Korte A, Nizhynska V, Voronin V, Korte P, Sedman L, Mandáková T, Lysak MA, Seren Ü, Hellmann I and Nordborg M. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat. Genet. 45(8), 884–890. (2013) doi: Doi 10.1038/Ng.2678


The molecular basis of recurring, multi-trait plant adaptation to substrate

Principal advisor: Ovidiu Paun

The radiation of ca 25 species of persimmons (Diospyros, Ebenaceae) on New Caledonia, one of the areas with the highest plant endemism in the world, has largely been driven by divergent adaptation to distinct substrates (i.e., ultramafic, volcanic, schist, limestone and serpentine), that happened iteratively within this clade (Paun et al., 2016). Serpentine and ultramafic soils are characterized by dramatically skewed elemental contents and we will focus here on two pairs of sister species within this radiation that show divergent adaptation to these types of soils (ie, volcanic vs. ultramafic). In this project we will test the roles and the inter-relationships between pre- and post-transcriptional mechanisms in recurrent adaptation to stressful substrates. With RNA-Seq and smRNA-Seq we will investigate differential expression, alternative splicing and adaptive sequence evolution for the two species pairs. The molecular data will be complemented by profiling soil chemistry and quantifying mineral nutrient uptake, in particular in reciprocal transplants. Altogether, we will test if the responses to challenging mineral compositions involve exclusion or accumulation of different elements, aiming for understanding the molecular pathways that are affected.

Background reading:

  • Balao F, Trucchi E, Wolfe TM, Hao BH, Lorenzo MT, Baar J, Sedman L, Kosiol C, Amman F, Chase MW, Hedrén M and Paun O. Adaptive sequence evolution is driven by biotic stress in a pair of orchid species (Dactylorhiza) with distinct ecological optima. Mol. Ecol. 26(14), 3649–3662. (2017) doi: 10.1111/mec.14123
  • Paun O, Turner B, Trucchi E, Munzinger J, Chase MW and Samuel R. Processes driving the adaptive radiation of a tropical tree (Diospyros, Ebenaceae) in New Caledonia, a biodiversity hotspot. Syst. Biol. 65(2), 212–227. (2016) doi: 10.1093/sysbio/syv076


The role of a nascent sex chromosome on interspecific patterns of allele sharing

Principal advisor: Christian Lexer

The role of sex chromosomes in species isolation is a topic of great current interest in evolutionary and population genetics (Charlesworth 2016 Annu Rev Plant Biol 67). While many well studied examples exist for fully evolved sex chromosomes, incipient sex chromosomes as in Populus provide a rare opportunity for study. In this PhD project, you will address patterns and determinants of genomic diversity and interspecific variant sharing in the nascent poplar sex chromosome for two different poplar species pairs at different stages of divergence, including hybrid zones for each pair. This will include a North American species pair with similar sex determination systems (both XY) and a Eurasian species pair with contrasting sex determination systems, Populus alba (ZW) and P. tremula (XY). You will use extensive whole genome and reduced representation library sequencing data for populations and hybrid zones in both species pairs to address (1) the interplay of selection and recombination in the nascent sex determination region in modifying interspecific gene flow, (2) the impact of a well characterized, extensive disease resistance (NBS-LRR) gene cluster in the nascent sex chromosome on interspecific variant sharing and genomic clines, and (3) the mechanisms that have constrained the evolution and full maturation of this enigmatic sex determination system.


The sources of variation fueling adaptive radiation after long-distance dispersal

Principal advisor: Ovidiu Paun

Adaptive radiations are dynamic interplays between speciation, expansion and extinction, often starting from long-distance dispersal events, when an alien lineage invades an array of previously unfilled niches. In such cases, habitat heterogeneity and ecological opportunity, although essential, appear by no means sufficient to explain adaptive diversifications. Springboards to explosive ecological radiation may be particular genomic configurations and the amount of phenotypic variation available to selection, together with the speed at which new variation originates, accelerating diversification rates (Schluter, 2000). Nevertheless, in the case of isolated areas like remote oceanic islands, the initial founder population is likely to have an extreme Ne, with little starting variation that can be selected to result in novel and divergent adaptations. Hence, the evolution of island biotas is intuitively expected to be shaped by neutral processes rather than natural selection. Still, species-rich adaptive diversifications are not uncommon on islands, unveiling adaptive radiation as a common process in such areas. The radiation of ca 25 species of persimmons (Diospyros, Ebenaceae) on New Caledonia, a biodiversity hotspot, is largely driven by divergent adaptation to distinct substrates (i.e., ultramafic, volcanic, schist, limestone and serpentine), that happened iteratively within this clade (Paun et al., 2016). The most puzzling aspect of this radiation is what differentiates the radiating group from three congeneric, but evolutionary lethargic lineages present on the archipelago? Due to a significant difference in genome size, that is not associated to ploidy increase, the answer may relate to a difference in the speed of accumulation of phenotypic variation, specific for each of the founders of the four long distance dispersal events. In this project, we will use whole genome resequencing to disentangle potential sources of adaptive variation, such as i) lineage-specific de novo evolution of alleles, ii) TE-induced structural variation with potential regulatory effects, together with iii) environment-specific sorting of ancestral genetic variation and/or iv) introgression of adaptive alleles (ie, gene reuse, Martin & Orgogozo, 2013) from related species, from within or outside the radiation, that share similar environments.

Related literature:

  • Martin A and Orgogozo V. The loci of repeated evolution: A catalog of genetic hotspots of phenotypic variation. Evolution 67(5), 1235–1250. (2013) doi: 10.1111/evo.12081
  • Paun O, Turner B, Trucchi E, Munzinger J, Chase MW and Samuel R. Processes driving the adaptive radiation of a tropical tree (Diospyros, Ebenaceae) in New Caledonia, a biodiversity hotspot. Syst. Biol. 65(2), 212–227. (2016) doi: 10.1093/sysbio/syv076
  • Schluter D. The Ecology of Adaptive Radiation. Oxford Ser. Ecol. Evol. (2000) doi: 10.2307/3558417


Transposon polymorphism in Arabidopsis thaliana

Principal advisor: Magnus Nordborg

Because transposons are too repetitive to be sequenced using short-read sequencing methods, our understanding of transposon polymorphism is extremely limited. This has led to a literature of transposon evolution that is almost exclusively based on comparison between reference genomes — which is the wrong time-scale for highly dynamic transposons. Arabidopsis thaliana has low transposon content compared to other plants (less than 25% of the reference genome consist of annotated transposons), and it has been argued that transposons are mostly inactive in this species. However, we now know that this is not correct. Our analysis of the 1001 Genomes data suggests that roughly 50% of the annotated transposons are polymorphic, and that most of the insertions are in fact quite rare, i.e. most individuals do not carry them (they carry other insertions instead). Furthermore, we have identified lines that appear to carry twice as many transposons as the reference lines. This highlights the need for better data, and we are thus sequencing 200 genomes de novo using long-read technologies in order to get a comprehensive picture of transposon polymorphism and better understand the dynamics of transposons in populations. Analyzing these data will be perfect for a motivated PhD student with keen interest in population genetics.


Within-species consequences of genomic interactions in ecologically important species

Principal advisor: Christian Lexer

Adaptive introgression across ´porous´ species barriers has long been suspected to fuel a variety of eco-evolutionary processes, ranging from the origin of local adaptation within species to the explosive bursts of speciation seen during adaptive radiations. We have recently discovered a case of adaptive introgression between two North American members of the model forest tree genus Populus (Suarez-Gonzalez et al., 2016, 2018a, 2018b). This PhD project will test the ability of introgressed alleles to spread across the recipient species´ ranges, making use of extensive, available whole genome sequence data. Within an established international collaboration, you will address the mode and tempo of spread of introgressed alleles across species´ ranges using (1) a range of analytical tools from population genomics including HMM-based inference of local ancestry segments across genomes and populations, (2) spatially and ecologically explicit tools from niche modeling to project the spread of intogressed alleles into climate niche space. An interesting aspect will also be to evaluate the relative roles of gene flow, balancing selection, and variable sorting of ancestral alleles to genome-wide patterns of allele sharing in recently diverged species.

Background reading:

  • Suarez-Gonzalez A, Hefer CA, Christe C, Corea O, Lexer C, Cronk QCB and Douglas CJ. Genomic and functional approaches reveal a case of adaptive introgression from Populus balsamifera (balsam poplar) in P. trichocarpa (black cottonwood). Mol. Ecol. 25(11), 2427–2442. (2016) doi: 10.1111/mec.13539
  • Suarez-Gonzalez A, Hefer CA, Lexer C, Douglas CJ and Cronk QCB. Introgression from Populus balsamifera underlies adaptively significant variation and range boundaries in P. trichocarpa. New Phytol. 217(1), 416–427. (2018a) doi: 10.1111/nph.14779
  • Suarez-Gonzalez A, Hefer CA, Lexer C, Cronk QCB and Douglas CJ. Scale and direction of adaptive introgression between black cottonwood (Populus trichocarpa) and balsam poplar (P. balsamifera). Mol. Ecol. 27(7), 1667–1680. (2018b) doi: 10.1111/mec.14561
Fond zur Förderung der wissenschaftlichen Forschung
vetmed uni vienna
Gregor Mendel Institute of Molecular Plant Biology
Universität Wien