Genome polarisation for detecting barriers to geneflow

Baird, Stuart J. E.; Petružela, Jan; Jaroň, Izar; Škrabánek, Pavel; Martínková, Natália

doi:10.1101/2022.03.24.485605

Cited by 3 publications

(3 citation statements)

References 14 publications

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“…Considering our results, it may originate from standing variation present in allopatric populations or differential introgression of Mus musculus domesticus alleles across the hybrid zone. The large genomic clusters identified as outlier regions could fit the second scenario, which echoes the recent evidence of adaptive introgression of OR and VR gene clusters across species boundaries in the Mus genus (Baird et al unpublished data; Ullrich et al unpublished data; Banker et al 2022). This scenario would be compatible with the role of these genomic regions in reproductive isolation with the nearby subspecies M. m. domesticus: the selective pressure of reinforcement could have favoured the adaptive introgression of alleles conferring choosiness on either side of the hybrid zone, the direction of the choice being expressed according to the genomic background, including at the mating signal loci, of the individuals.…”

Section: Discussionsupporting

confidence: 72%

Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice

Smadja

Loire

Caminade

et al. 2022

Preprint

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Deciphering the genetic bases of behavioural traits is essential to understanding how they evolve and contribute to adaptation and biological diversification, but it remains a great challenge, especially for complex behavioural traits with polygenic architectures. In this study, we developed a population genomics approach coupled with functional predictions to address the evolution and genetic basis of a complex behavioural trait: olfactory-based assortative mate preferences in the house mouse, suspected to have evolved as a response to selection against hybridisation. We used whole genome resequencing data and the C2 statistic of the program BAYPASS, which contrasts allele frequencies corrected for population structure, to characterize genetic differentiation between sets of populations with strong contrast in behaviour (expressing or not assortative mate preferences) and we identified some regions of the genome showing the expected significant and consistent association with behavioural divergence. A series of Olfactory and Vomeronasal Receptor genes, among the most differentiated genomic regions and in line with functional predictions, stand out as the prime candidates underlying this olfactory-based behavioural divergence. These genes form large gene clusters in the genome, with two main candidate clusters extending up to 1.8 Mb. Variant analyses indicate a potential dual role of regulatory and protein-coding changes in the evolution of choosiness. This study shows that combining expectations on the genomic patterns of divergence with functional expectations is a promising route to unravelling the genetic architecture of complex trait variation and provides new insights into the role of olfactory and vomeronasal receptors in mammal adaptation and speciation.

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Section: Discussionsupporting

confidence: 72%

Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice

Smadja

Loire

Caminade

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…Considering our results, it may originate from standing variation present in allopatric populations or differential introgression of Mus musculus domesticus alleles across the hybrid zone. The large genomic clusters identified as outlier regions could fit the second scenario, which echoes the recent evidence of adaptive introgression of OR and VR gene clusters across species boundaries in the Mus genus (Ullrich et al 2017;Baird et al 2022;Banker et al 2022). This scenario would be compatible with the role of these genomic regions in reproductive isolation with the nearby subspecies M. m. domesticus: the selective pressure of reinforcement could have favoured the adaptive introgression of alleles conferring choosiness on either side of the hybrid zone (a case of one-allele mechanism), the direction of the choice being possibly expressed via a matching rule, i.e.…”

Section: Genetic Architecture Of Candidate Regions and Selective Regimessupporting

confidence: 69%

Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice

Smadja¹,

Loire²,

Caminade³

et al. 2022

Peer Community Journal

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Deciphering the genetic bases of behavioural traits is essential to understanding how they evolve and contribute to adaptation and biological diversification, but it remains a substantial challenge, especially for behavioural traits with polygenic architectures. In this study, we developed a population genomics approach coupled with functional predictions to address the evolution and genetic basis of olfactory-based assortative mate preferences in the house mouse, suspected to have evolved as a response to selection against hybridisation. We used whole genome resequencing data and the C2 statistic of the program BAYPASS, which contrasts allele frequencies corrected for population structure, to characterize genetic differentiation between sets of populations with strong contrast in behaviour (expressing or not assortative mate preferences) and we identified some regions of the genome showing the expected significant and consistent association with behavioural divergence. A series of Olfactory and Vomeronasal Receptor genes, among the most differentiated genomic regions and in line with functional predictions, stand out as the prime candidates underlying this olfactory-based behavioural divergence. These genes form large gene clusters in the genome, with two main candidate clusters extending up to 1.8 Mb. Variant analyses indicate a potential dual role of regulatory and protein-coding changes in the evolution of choosiness. This study shows that combining expectations on the genomic patterns of divergence with functional expectations represents a promising route to unravelling the genetic architecture of complex trait variation and provides novel insights into the role of olfactory and vomeronasal receptors in mammal adaptation and speciation.

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“…The diem method is implemented in Mathematica, Python and R. The Mathematica and Python codes are available at github through https://github.com/StuartJEBaird as diemmca and diempy, respectively (Baird & Martínková, 2022), and the R package diemr is available at CRAN through https://cran.r-project.org/package=diemr.…”

Section: Peer Reviewmentioning

confidence: 99%

Genome polarisation for detecting barriers to geneflow

et al. 2022

Self Cite

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Semi‐permeable barriers to geneflow in principle allow distantly related organisms to capture and exchange pre‐adapted genes potentially speeding adaptation. However, describing barriers to geneflow on a genomic scale is non‐trivial. We extend classic diagnostic allele counting measures of geneflow across a barrier to the case of genome‐scale data. Diagnostic index expectation maximisation (diem) polarises the labelling of bistate markers with respect to the sides of a barrier. An initial state of ignorance is enforced by starting with randomly generated marker polarisations. This means there is no prior on population or taxon membership of the genomes concerned. Using a deterministic data labelling, small numbers of classic diagnostic markers can be replaced by large numbers of markers, each with a diagnostic index. Individuals' hybrid indices (genome admixture proportions) are then calculated genome wide conditioned on marker diagnosticity; within diploid, haplodiploid and/or haploid genome compartments; or indeed over any subset of markers, allowing classical cline width/barrier strength comparisons along genomes. Along‐genome barrier strength heterogeneity allows for barrier regions to be identified. Furthermore, blocks of genetic material that have introgressed across a barrier are easily identified with high power. diem indicates panmixis among Myotis myotis bat genomes, with a barrier separating low data quality outliers. In a Mus musculus domesticus/Mus spretus system, diem adds multiple introgressions of olfactory (and vomeronasal) gene clusters in one direction to previous demonstrations of a pesticide resistance gene introgressing in the opposite direction across a strong species barrier. diem is a genome analysis solution, which scales over reduced representation genomics of thousands of markers to treatment of all variant sites in large genomes. While the method lends itself to visualisation, its output of markers with barrier‐informative annotation will fuel research in population genetics, phylogenetics and association studies. diem can equip such downstream applications with millions of informative markers.

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Genome polarisation for detecting barriers to geneflow

Cited by 3 publications

References 14 publications

Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice

Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice

Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice

Genome polarisation for detecting barriers to geneflow

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