Master’s Project proposal: Using patterns of genomic base composition to infer past transitions in mating systems

Contact: Sylvain Glemin sylvain.glemin@ebc.uu.se

Based on the distribution of selfing species on phylogenies, selfing is often considered to be of recent origin. However, except for well-documented and specific cases (such as Capsella rubella [1,2,3]) it is difficult to date precisely the origin of selfing. Indeed the shift from outcrossing to selfing does not necessarily coincide with the formation of a new species.

Selfing strongly affects population genetic parameters such as homozygosity, effective size and effective recombination rate, which, in turn, affect patterns of polymorphism and genome evolution [reviewed in 4,5]. Contemporary or very recent selfing rates can be estimated using genetic markers, but it is not clear if more ancient selfing rate, and especially the shift in selfing rates, could also be inferred from population genetic data. An alternative approach would be to use the signature of the effect of selfing that can last on a genome for longer time periods and that could be recorded in patterns of divergence among species.

A strong candidate is GC content that is affected by GC-biased gene conversion (gBGC) in many species [6,7]. gBGC is a recombination-associated process mimicking selection in favour of G and C bases [8]. During recombination mismatches induced by pairing heterozygotes during heteroduplex formation are preferentially corrected towards G or C instead of A or T. gBGC is supposed to be the main driver of the frequently-observed correlation between recombination and GC content and one of the main driver of variation of base composition within and among genomes [6,9]. Because gBGC occurs on heterozygote sites it is thus expected to be absent or nearly absent in highly selfing species [10] and a decline in GC content in selfing species has been observed both at the divergence and polymorphism levels [11,12,13,14]. GC-content and gBGC also vary along genes, likely as a function of recombination gradients, first exons and introns being GC-richer than others [15,16,17,18].

The aim of the project is to use the dynamics of GC-content evolution among closely related species with different mating systems to date the shift from outcrossing to selfing by combining information from genomic regions with contrasted GC content (for example first exons versus last ones). The principle of the method is already developed but remains to be tested and applied. The project will include two parts:
(i) a simulation part to assess the power and the robustness of the method and (ii) a data-analysis part where the method will be applied to empirical datasets for which genome-wide data are already available. Possible datasets are:
Arabidopsis thaliana: the age of selfing in this model species is likely much more recent that the divergence with its outcrossing relative A. lyrata but is it still debated [e.g.19].
Capsella orientalis: the Capsella genus, on which we work in the lab, is interesting to study the evolution of mating systems. C. rubella is a very recent species (20,000/50,000 yrs) and the transition to selfing is concomitant to speciation [1,2,3]. C. orientalis is much older (~1 Myrs) but we don’t know if the transition occurred at the speciation time as in C. rubella or much later as in A. thaliana.
Oryza genus (AA clade): among the rice species close to the domesticated ones, there is variation in mating systems from outcrossing to different level of selfing and the age and number of transition are unclear. All species of the group are fully sequenced [20].
Caenorhabiditis nematodes: selfing evolved three times independently in this genus and, as for C. orientalis, the age of transition is still unknown and could differ among the three species [21,22]

References

1. Foxe JP, Slotte T, Stahl EA, Neuffer B, Hurka H, et al. (2009) Recent speciation associated with the evolution of selfing in Capsella. Proceedings of the National Academy of Sciences of the United States of America 106: 5241-5245.

2. Guo YL, Bechsgaard JS, Slotte T, Neuffer B, Lascoux M, et al. (2009) Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck. Proceedings of the National Academy of Sciences of the United States of America 106: 5246-5251.

3. Brandvain Y, Slotte T, Hazzouri KM, Wright SI, Coop G (2013) Genomic identification of founding haplotypes reveal the history of the selfing species Capsella rubella. PLoS Genetics 9.

4. Burgarella C, Glémin S (2017) Population Genetics and Genome Evolution of Selfing Species. Encyclopedia of Life Sciences: John Wiley and Sons.

5. Glémin S, Galtier N (2012) Genome evolution in outcrossing versus selfing versus asexual species. Methods in Molecular Biology 855: 311-335.

6. Duret L, Galtier N (2009) Biased gene conversion and the evolution of mammalian genomic landscapes. Annual Review of Genomics and Human Genetics 10: 285-311.

7. Pessia E, Popa A, Mousset S, Rezvoy C, Duret L, et al. (2012) Evidence for widespread GC-biased gene conversion in eukaryotes. Genome Biology and Evolution 4: 675-682.

8. Marais G (2003) Biased gene conversion: implications for genome and sex evolution. Trends in Genetics 19: 330-338.

9. Mugal CF, Weber CC, Ellegren H (2015) GC-biased gene conversion links the recombination landscape and demography to genomic base composition: GC-biased gene conversion drives genomic base composition across a wide range of species. Bioessays 37: 1317-1326.

10. Marais G, Charlesworth B, Wright SI (2004) Recombination and base composition: the case of the highly self-fertilizing plant Arabidopsis thaliana. Genome Biology 5: R45.

11. Muyle A, Serres-Giardi L, Ressayre A, Escobar J, Glémin S (2011) GC-biased gene conversion and selection affect GC content in the Oryza genus (rice). Molecular Biology and Evolution 28: 2695-2706.

12. Haudry A, Cenci A, Guilhaumon C, Paux E, Poirier S, et al. (2008) Mating system and recombination affect molecular evolution in four Triticeae species. Genetical Research 90: 97-109.

13. Burgarella C, Gayral P, Ballenghien M, Bernard A, David P, et al. (2015) Molecular Evolution of Freshwater Snails with Contrasting Mating Systems. Molecular Biology & Evolution 32: 2403-2416.

14. Clement Y, Sarah G, Holtz Y, Homa F, Pointet S, et al. (2017) Evolutionary forces affecting synonymous variations in plant genomes. PLoS Genet 13: e1006799.

15. Ressayre A, Glémin S, Montalent P, Serre-Giardi L, Dillmann C, et al. (2015) Introns Structure Patterns of Variation in Nucleotide Composition in Arabidopsis thaliana and Rice Protein-Coding Genes. Genome Biol Evol 7: 2913-2928.

16. Glémin S, Clement Y, David J, Ressayre A (2014) GC content evolution in coding regions of angiosperm genomes: a unifying hypothesis. Trends in Genetics 30: 263-270.

17. Stoletzki N (2011) The surprising negative correlation of gene length and optimal codon use–disentangling translational selection from GC-biased gene conversion in yeast. BMC Evolutionary Biology 11: 93.

18. Clement Y, Fustier MA, Nabholz B, Glémin S (2015) The bimodal distribution of genic GC content is ancestral to monocot species. Genome Biology and Evolution 7: 336-348.

19. Castric V, Billiard S, Vekemans X (2014) Trait transitions in explicit ecological and genomic contexts: plant mating systems as case studies. Adv Exp Med Biol 781: 7-36.

20. Jacquemin J, Bhatia D, Singh K, Wing RA (2013) The International Oryza Map Alignment Project: development of a genus-wide comparative genomics platform to help solve the 9 billion-people question. Curr Opin Plant Biol 16: 147-156.

21. Thomas CG, Woodruff GC, Haag ES (2012) Causes and consequences of the evolution of reproductive mode in Caenorhabditis nematodes. Trends in Genetics 28: 213-220.

22. Fierst JL, Willis JH, Thomas CG, Wang W, Reynolds RM, et al. (2015) Reproductive Mode and the Evolution of Genome Size and Structure in Caenorhabditis Nematodes. PLoS Genet 11: e1005323.

Master’s Project proposal: Effect of partial selfing on local adaptation

Contact: Sylvain Glemin sylvain.glemin@ebc.uu.se

Local adaptation reflects the fact that local populations tend to have a higher mean fitness in their native environment than in other environments and than other populations introduced in their home site. Local adaptation is widespread, especially in plant species, and the conditions and mechanisms promoting local adaptation have been studied for a long time, both theoretically and empirically [1,2]. A key ingredient is the existence of spatially heterogeneous selective pressure favouring locally specialised genotypes, balanced by other evolutionary forces such as migration and random genetic drift, which have been integrated in many population genetics models. However, most models of local adaptation assume local random mating [but see 3]. The effect of partial selfing thus remains unclear because of its antagonistic effects on key evolutionary forces mentioned above, and a meta-analysis of empirical studies lead to inconclusive results [4].

Selfing strongly affects population genetic parameters such as homozygosity, effective size and effective recombination rate, which should globally reduce the efficacy of selection [reviewed in 5]. This should limit the possibility for local adaptation. However, selfing also reduces pollen gene flow, which should promote local adaptation. In addition, selfing maintains linkage disequilibrium and should avoid the breakdown of locally co-adapted combinations.

The aim of the project is to develop theoretical predictions on the effect of partial selfing on local adaptation. First, we propose to study a simple single-locus model in two biological contexts:
(i) An island/mainland model, corresponding to the colonization of a new peripheral environment; the allele adapted to the new environment will be considered as deleterious in the old environment. We will determine the frequency of the beneficial allele in the new environment and the migration load. This could be done by the extension of [6].
(ii) A two-patch model where an allele is favoured is one environment and the other in the other environment. This corresponds to the classical Bulmer´s model [7], extended by Yeaman and Otto to take genetic drift into account [8]. This model will be extended by adding partial selfing. It will help determining the conditions under which polymorphism, hence local adaptation, can be maintained and whether selfing reduces or increases the range of conditions for local adaptation.

Second, two-locus models could be studied to take into account the effect of selfing on genetic linkage. The approach will rely on the development of analytical models using classical population genetics modeling tools such as diffusion methods that will be compared to stochastic simulations.

References

1. Savolainen O, Lascoux M, Merila J (2013) Ecological genomics of local adaptation. Nat Rev Genet 14: 807-820.

2. Lascoux M, Glémin S, Savolainen O (2016) Local adaptation in plants. Encyclopedia of Life Sciences: John Wiley and Sons.

3. Epinat G, Lenormand T (2009) The evolution of assortative mating and selfing with in- and outbreeding depression. Evolution 63: 2047-2060.

4. Hereford J (2010) Does selfing or outcrossing promote local adaptation? American Journal of Botany 97: 298-302.

5. Burgarella C, Glémin S (2017) Population Genetics and Genome Evolution of Selfing Species. Encyclopedia of Life Sciences: John Wiley and Sons.

6. Glémin S, Ronfort J (2013) Adaptation and maladaptation in selfing and outcrossing species: new mutations versus standing variation. Evolution 67: 225-240.

7. Bulmer M (1972) Multiple niche polymorphism. The American Naturalist 106: 254-257.

8. Yeaman S, Otto SP (2011) Establishment and maintenance of adaptive genetic divergence under migration, selection, and drift. Evolution 65: 2123-2129.

Master’s Project proposal

We are looking for a motivated student with a good background in programming to carry out a master project on the genetic basis of trade-offs during local adaptation. Local adaptation is widely observed and plays a major role in the evolution of species. Local adaptation often translates into phenotypic trade-offs: individuals that perform well in a given environment perform poorly in another. Numerous studies have tested whether trade-offs observed at the phenotypic level also translate into trade-offs at the level of individual loci controlling the trait of interest. Results have been mixed: in some cases, trade-offs, also called antagonistic pleiotropy, were not observed, , while in others they were frequent. The genetic basis is still poorly understood and there is no clear expectation on what to expect under different demographic and selection scenarios. The project will investigate  how trade-offs develop under different assumptions. It will be based on modifying the newly developed population genetics forward simulation progam SLiM (https://messerlab.org/slim/).

Learn more on the project by writing to Martin Lascoux (Martin.Lascoux@ebc.uu.se)