Department of Ecology and Genetics
A genomic approach to the plumage colour differences in the Willow grouse (Lagopus lagopus)
Author(s): Kozma, R
My work aims to combine the field of genetics with the application of population structure modeling as well as a more individual based genome modeling. The species of my study is the willow grouse (Lagopus lagopus), which has an interesting phenotypic diversity across its range. In Scandinavia, individuals adopt a white plumage during winter, while individuals in the northern UK forgo moulting and remain brown. Interestingly, snow free islands off the coast of Norway harbor the Scandinavian populations in fluctuating densities, which are seemingly maladapted seeing as their white plumage stands out. With the help of population modeling, one of the aims is to model the dynamics of movement to identify conditions required for local adaptation (i.e. what would it take for the island populations to stop their winter moulting). Furthermore, the genome of the willow grouse will be sequenced with the aim of finding potential genes responsible for this variation in moulting behaviour. In turn, models of the genomic data will be constructed to find out which parts of the genome are likely to respond to local selection pressures and random forces such as drift. Is it the case that local populations become divergent throughout the genome (as predicted by drift) or at key loci (as predicted by selection)? As such, the project aims to tackle these questions from an empirical as well as a theoretical perspective.
A novel genomic signature of adaptation from standing variation revealed in threespine stickleback
Author(s): Roesti, M, Gavrilets, S, Hendry, AP, Salzburger, W, Berner, D
Understanding how natural selection shapes the genome is becoming a major endeavor in evolutionary biology. Selection will often target pre-existing (standing) genetic variation. Nevertheless, theory has generally been developed for selection on novel variants. We here use extensive modeling tailored to adaptive divergence in threespine stickleback to characterize the genomic footprints of adaption from shared standing variation. The emerging predictions are then examined using genome-wide markers and targeted sequencing across many natural populations. Combined, our findings offer a novel explanation for heterogeneous genomic differentiation between diverging populations, challenge the widely held view that genomic regions of high and low population differentiation reliably point to loci under divergent and balancing selection, and allow us to propose a novel methodological framework for searching adaptation genes in natural populations.
Department for Biomedical Sciences
A population genetic model of allopolyploid speciation
Author(s): Vogl, C, Guo, Y
Allotetraploid speciation, i.e. the generation of a hybrid tetraploid species from two diploid species, and the long-term evolution of tetraploid populations and species are important in plants. A population genetic model to infer population genetic parameters of tetraploid populations from data of the progenitor and descendent species is presented. The model links different time-scales: allopolyploid hybrid speciation is presumably rare and probably results in a population bottleneck, i.e., a founder event. Immediately after allopolyploid speciation, selection must be intense, as hybrids of early generations are usually relatively unfit but often evolve to out-compete their parental species and spread to occupy new ecological niches. Later, the accumulation of mutations may render one or the other homeologous copy of a gene dysfunctional and recombination or gene conversion may lead to mixing of two homeologous gene copies. These latter processes are relatively slow. In a first attempt, we develop a population genetic model to capture key parameters and apply this model to a data set of nuclear genes of two yarrow species, Achillea alpina-4x and A. wilsoniana-4x, that arose by allotetraploidization from the diploid progenitors, Achillea acuminata-2x and A. asiatica-2x.
Ecological Genetics Laboratory
A young neo-sex chromosome is the site of divergence between incipient stickleback species
Author(s): Kitano, J, Yoshida, K
Sex chromosomes turn over rapidly in some taxonomic groups, where closely related species have different sex chromosomes. However, little is known about the functional roles of sex chromosome turnover in phenotypic diversification and speciation. We use a sympatric pair of threespine sticklebacks to understand the roles of sex chromosome turnover in phenotypic divergence and speciation. Previously, we found that the Japan Sea sticklebacks have a neo-sex chromosome system resulting from a fusion between an ancestral Y chromosome and an autosome, while sympatric Pacific Ocean sticklebacks have a XY sex chromosome system. Furthermore, we demonstrated that the Japan Sea neo-X chromosome plays an important role in phenotypic divergence and reproductive isolation between these sympatric species. Here, we conducted additional QTL mapping of other morphological and behavioral traits to confirm that both old-X and neo-X chromosomes have significant QTL important for morphological divergence, while the old-X, but not the neo-X chromosome, contributed to hybrid courtship abnormality. Next, we conducted whole genome sequencing of these two sticklebacks to find that the Japan Sea neo-Y chromosome has no large-scale deletion, but some regions on the neo-Y have started to accumulate deleterious mutations. Importantly, significant QTL on the neo-X chromosome were located at regions even outside the regions where deleterious mutations accumulate. Furthermore, comparison of genome sequences between these two species revealed that the neo-X chromosome showed faster protein evolution than autosomal genes. Thus, a young neo-sex chromosome is the site of divergence between incipient species.
Institut des Sciences de l'Evolution
Are Robertsonian fusions barriers to introgression in a house mouse hybrid zone?
Author(s): Britton-Davidian, J, Villafan de la Torre, E, Smadja, C, Caminade, P, Boursot, P
Genomic regions of low recombination are expected to contribute to the accumulation of incompatibilities allowing speciation with gene flow to occur. While chromosomal inversions are well documented in such processes, the role of Robertsonian (Rb) fusions (that join two acrocentric chromosomes by their centromere to form a metacentric one) is less clear. The house mouse is an emblematic model of Rb variation since one subspecies, M. m. domesticus, displays >80 Rb races. Previous cytogenetic studies demonstrated a decrease in recombination rates along the proximal 50% of Rb chromosomes in both homozygotes and heterozygotes. This study explores the role of Rb fusions in reducing gene flow by investigating their effect on genome admixture between two subspecies of the house mouse. In Denmark where the two taxa form a tension zone, M. m. domesticus carries 3 Rb fusions while M. m. musculus has an all-acrocentric karyotype. Genome admixture was assessed using 127 SNPs diagnostic of the two subspecies and covering the proximal 25% of 3 chromosomal arms involved in Rb fusions and 2 acrocentrics. We compared patterns of genomic admixture in the proximal regions to those at 86 diagnostic loci randomly distributed in the genome by fitting a genomic cline model with 3 parameters (centre and slope in each subspecific context). In the domesticus genomic context, Rb clines were much steeper than that of the average reference loci. Their centre was displaced in favour of musculus, however, due to introgression of large chromosomal blocks, and both of these patterns were stronger for the most proximal loci. This is compatible with the predicted effects of reduced recombination in Rb fusions coupled with incompatibilities in these genomic regions. In addition, clines for acrocentrics were smoother than average in the musculus genomic context, suggesting that other undescribed effects are acting, such as a possible advantage of domesticus acrocentric centromeres.
Assessing patterns of hybridization between North Atlantic eels using Genome-Wide Single Nucleotide Polymorphisms generated by RAD-Sequencing
Author(s): Pujolar, J, Jacobsen, MW, Hansen, MM
Hybridization is an important issue in evolutionary biology and conservation. We investigate the dynamics of introgressive hybridization in North Atlantic eels, the European eel (Anguilla anguilla) and its sister species the American eel (Anguilla rostrata). The two North Atlantic eels occupy a broad range of habitats from Morocco to Iceland in the eastern Atlantic and from the Caribbean to Greenland in the western Atlantic, respectively. Despite such a wide non-overlapping geographic distribution, both species spawn in partial sympatry in the remote Sargasso Sea, in a migration of over 5,000 km for the European eel and 2,000 km for the American eel, which still represent to this day one of the enigmas of the animal kingdom. Spawning grounds of both species overlap in space and time, setting the stage for interbreeding. Previous studies have pointed to the existence of hybrids limited to one particular location, Iceland, although markers used did not allow clarification of their hybrid status. In our study, diagnostic species-specific single nucleotide polymorphisms (SNPs) are developed using a RAD-sequencing approach, which is a reduced representation genome sequencing method. After generating and aligning over 8000 sequence read per individual, a total of 3,348 diagnostic SNP (FST> 0.95) were identified. 96 of of those loci were selected to design a low-density array, at which we genotyped 159 eels from Iceland and 29 eels from Faroe Islands. The study was supplemented with the analysis of 94 larvae (49 European and 45 American eel) collected in the Sargasso Sea. Our study reveals high levels of hybridization in Iceland mostly consisting of F1 hybrids but backcrosses (A. anguilla x hybrid) are also observed. In comparison, no hybrids are observed in the closely-located Faroe Islands.
Department of Biology
CONSTANS is highly prone to natural selection in Arabidopsis lyrata
Author(s): Toivainen, T, Aalto, E, Mattila, T, Niittyvuopio, A, Savolainen, O
We examined the evolution and diversity of genes related to flowering time, an important adaptive trait in plants, and a set of unrelated reference genes in the perennial Arabidopsis lyrata in several populations in Europe and North America. Among the 38 loci, CONSTANS, one of the central flowering time genes, was the only which had experienced species-wide adaptive evolution when compared to A. thaliana, as shown by multilocus MK analysis. This was consistent with earlier result of selection on this gene in A. thaliana (Bustamante et al. 2002), and of the rapid evolution of this gene in Brassicaceae (Lagercranz & Axelsson 2000). The CONSTANS gene also was highly differentiated between the widespread A. lyrata populations (Fst=0.78). Further, an association analysis suggested a role in governing fitness in an experimental field site at the University of Oulu. Thus, we found CONSTANS gene to be adaptively important in all studied time levels of natural selection. Likely selection on flowering time, may often target the CONSTANS gene.
Complete mitochondrial genomes of the Baltic clam Macoma balthica (Bivalvia: Tellinidae): variable gene arrangements between and within lineages and genetic incompatibility
Author(s): Saunier, A, Pante, E, Bouchez, O, Becquet, V, Garcia, P
Despite their large population sizes, high fecundity and dispersive potential, marine bivalves maintain adaptive polymorphism that help them cope with local environmental variations. The study of adaptive evolution can be facilitated by examining contact zones between close taxa. In these zones, maintained by endogenic genetic incompatibilities or exogenic barriers, hybrid genotypes persist despite a maladaptation state. The Baltic tellin Macoma balthica offers an opportunity to study the evolution of a hybrid zone within the context of contemporary climate change. A key species in intertidal trophic webs of northwest Europe, this bivalve seems to be affected by the warming of surface waters in the Bay of Biscay as its distribution range contracted 300 km poleward during the last thirty years. On European coasts, two lineages of M. balthica are present, and result from separate trans-arctic invasion events from the Pacific to the Atlantic Ocean, leading to strong admixture and hybridisation. How can these lineages maintain local adaptations? What are the genes implied? While screening for nuclear markers highly differentiated across populations, we found that the nuclear-encoded gamma subunit of the mitochondrial ATP synthase protein complex had high FST values, and may be undergoing adaptive selection. As proteins involved in the mitochondrial oxidative phosphorylation chain are prone to mito-nuclear genetic incompatibilities and contribute to the maintenance of genetic barriers, we have set to sequence eight mitogenomes of M. balthica, describe gene content and genome organisation. Using long-range PCR, these mitogenomes were amplified and sequenced (MiSeq, Illumina). These results will help identify the mitochondrial genes under selective pressure by analysis of non-synonymous to synonymous mutation ratios, and test the hypothesis that the mitochondrial subunits of the ATP synthase complex are under going positive selection, as their nuclear counterpart.
Département d'écologie et d'évolution
Crossing the species barrier: genomic islands of introgression between two extremely divergent Ciona intestinalis species
Author(s): Roux, C, Tsagkogeorga, G, Bierne, N, Galtier, N
Inferring a realistic demographic model from genetic data is an important challenge to gain insights into the historical events during the speciation process and to detect the molecular signature of selection along genomes. Recent advances in divergence population genetics have reported that speciation in face of gene flow occurred more frequently than theoretically expected, but the approaches used rarely account for genome wide heterogeneity (GWH) in introgression rates. However, GWH is expected as a consequence of variation in effects of natural selection on migrant alleles. We investigated the impact of GWH on the inference of divergence with gene flow between two cryptic species of the marine model Ciona intestinalis. These morphologically indistinguishable entities are highly diverged molecular-wise, but evidence of hybridisation has been reported in both laboratory and field studies. We examined polymorphism and divergence patterns across 852 genes scattered throughout the C. intestinalis genome. We compared various speciation models and statistically tested for GWH under the ABC framework. Our results demonstrate the presence of significant extents of gene flow resulting from a recent secondary contact between the two gene pools, after more than 3My of divergence in isolation. The inferred rates of introgression are relatively low, highly variable across loci and mostly unidirectional, which is consistent with the idea that numerous genetic incompatibilities have accumulated over time throughout the genomes of these highly-diverged species and that introgression could be adaptive. A genomic map of the level of gene flow identified two islands of introgression, i.e. large genome regions of unidirectional introgression. This study clarifies the history and degree of isolation of two cryptic and partially sympatric model species, and provides a methodological framework for the study of GWH in introgression rates at various stages of the speciation process.
Divergence between lake and stream populations in an East African cichlid fish
Author(s): Egger, B, Theis, A, Ronco, F, Indermaur, A, Roesti, M, Berner, D, Salzburger, W
Integrative studies of species that occur along an environmental gradient provide important insights into ecological speciation and serve as prime examples for the presence of a speciation continuum. The cichlid species Astatotilapia burtoni occurs in lacustrine environment as well as in the surrounding rivers of Lake Tanganyika (LT), offering the possibility to study a lake-stream environmental gradient in a member of a large cichlid adaptive radiation in East Africa. We have established phylogeographic relationships and assessed the population structure in A. burtoni from the southern LT drainage using neutral nuclear (microsatellite) and mtDNA markers. We detect an unexpectedly high genetic diversity in A. burtoni, exceeding – at least in mtDNA – the diversity of the entire cichlid species flock of Lake Victoria, and a relatively complex phylogeographic pattern. Next, we have examined morphological differences among these populations by analyzing body shape. Based on these results, we focused on four lake-stream systems in detail. We here find that stream fish show a more inferior mouth, a more streamlined body, and shorter gill-rakers compared to lake fish, shifts presumably associated with differential foraging styles. Current work is now evaluating this hypothesis directly, and includes high-density SNP marker data generated by RADseq for population genomic analyses.