Evidence for widespread selection in shaping the genomic landscape during speciation of Populus

AbstractIncreasing our understanding of how various evolutionary processes drive the genomic landscape of variation is fundamental to a better understanding of the genomic consequences of speciation. However, the genome-wide patterns of within- and between-species variation have not been fully investigated in most forest tree species despite their global ecological and economic importance. Here, we use whole-genome resequencing data from four Populus species spanning the speciation continuum to reconstruct their demographic histories, investigate patterns of diversity and divergence, infer their genealogical relationships and estimate the extent of ancient introgression across the genome. Our results show substantial variation in these patterns along the genomes although this variation is not randomly distributed but is strongly predicted by the local recombination rates and the density of functional elements. This implies that the interaction between recurrent selection and intrinsic genomic features has dramatically sculpted the genomic landscape over long periods of time. In addition, our findings provide evidence that, apart from background selection, recent positive selection and long-term balancing selection are also crucial components in shaping patterns of genome-wide variation during the speciation process.

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Population genetics of the coral Acropora millepora: Towards a genomic predictor of bleaching

10.1101/867754 ◽

2019 ◽

Cited By ~ 7

Author(s):

Zachary L. Fuller ◽

Veronique J.L. Mocellin ◽

Luke Morris ◽

Neal Cantin ◽

Jihanne Shepherd ◽

...

Keyword(s):

Genome Wide Association Study ◽

Balancing Selection ◽

Genome Wide Association ◽

Conservation Strategies ◽

Genome Sequences ◽

Acropora Millepora ◽

Genome Wide ◽

A Genome ◽

In The Wild

AbstractAlthough reef-building corals are rapidly declining worldwide, responses to bleaching vary both within and among species. Because these inter-individual differences are partly heritable, they should in principle be predictable from genomic data. Towards that goal, we generated a chromosome-scale genome assembly for the coral Acropora millepora. We then obtained whole genome sequences for 237 phenotyped samples collected at 12 reefs distributed along the Great Barrier Reef, among which we inferred very little population structure. Scanning the genome for evidence of local adaptation, we detected signatures of long-term balancing selection in the heat-shock co-chaperone sacsin. We further used 213 of the samples to conduct a genome-wide association study of visual bleaching score, incorporating the polygenic score derived from it into a predictive model for bleaching in the wild. These results set the stage for the use of genomics-based approaches in conservation strategies.

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Transition from background selection to associative overdominance promotes diversity in regions of low recombination

10.1101/748004 ◽

2019 ◽

Cited By ~ 5

Author(s):

Kimberly J. Gilbert ◽

Fanny Pouyet ◽

Laurent Excoffier ◽

Stephan Peischl

Keyword(s):

Genetic Diversity ◽

Balancing Selection ◽

Purifying Selection ◽

Heterozygote Advantage ◽

Background Selection ◽

Deleterious Mutations ◽

Recombination Rates ◽

Locus Model ◽

Genome Wide ◽

Linked Selection

SummaryLinked selection is a major driver of genetic diversity. Selection against deleterious mutations removes linked neutral diversity (background selection, BGS, Charlesworth et al. 1993), creating a positive correlation between recombination rates and genetic diversity. Purifying selection against recessive variants, however, can also lead to associative overdominance (AOD, Ohta 1971, Zhao & Charlesworth, 2016), due to an apparent heterozygote advantage at linked neutral loci that opposes the loss of neutral diversity by BGS. Zhao & Charlesworth (2016) identified the conditions when AOD should dominate over BGS in a single-locus model and suggested that the effect of AOD could become stronger if multiple linked deleterious variants co-segregate. We present a model describing how and under which conditions multi-locus dynamics can amplify the effects of AOD. We derive the conditions for a transition from BGS to AOD due to pseudo-overdominance (Ohta & Kimura 1970), i.e. a form of balancing selection that maintains complementary deleterious haplotypes that mask the effect of recessive deleterious mutations. Simulations confirm these findings and show that multi-locus AOD can increase diversity in low recombination regions much more strongly than previously appreciated. While BGS is known to drive genome-wide diversity in humans (Pouyet et al. 2018), the observation of a resurgence of genetic diversity in regions of very low recombination is indicative of AOD. We identify 21 such regions in the human genome showing clear signals of multi-locus AOD. Our results demonstrate that AOD may play an important role in the evolution of low recombination regions of many species.

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Heterogeneity in effective size across the genome: effects on the Inverse Instantaneous Coalescence Rate (IICR) and implications for demographic inference under linked selection.

10.1101/2021.06.11.448122 ◽

2021 ◽

Author(s):

Simon Boitard ◽

Armando Arredondo ◽

Camille Noûs ◽

Lounes Chikhi ◽

Olivier Mazet

Keyword(s):

Genetic Diversity ◽

Balancing Selection ◽

Effective Population ◽

Recombination Rates ◽

Genome Wide ◽

Coalescence Rate ◽

Demographic Inference ◽

The Impact ◽

Linked Selection ◽

Coalescence Times

The relative contribution of selection and neutrality in shaping species genetic diversity is one of the most central and controversial questions in evolutionary theory. Genomic data provide growing evidence that linked selection, i.e. the modification of genetic diversity at neutral sites through linkage with selected sites, might be pervasive over the genome. Several studies proposed that linked selection could be modelled as first approximation by a local reduction (e.g. purifying selection, selective sweeps) or increase (e.g. balancing selection) of effective population size (Ne). At the genome-wide scale, this leads to a large variance of Ne from one region to another, reflecting the heterogeneity of selective constraints and recombination rates between regions. We investigate here the consequences of this variation of Ne on the genome-wide distribution of coalescence times. The underlying motivation concerns the impact of linked selection on demographic inference, because the distribution of coalescence times is at the heart of several important demographic inference approaches. Using the concept of Inverse Instantaneous Coalescence Rate, we demonstrate that in a panmictic population, linked selection always results in a spurious apparent decrease of Ne along time. Balancing selection has a particularly large effect, even when it concerns a very small part of the genome. We quantify the expected magnitude of the spurious decrease of Ne in humans and Drosophila melanogaster, based on Ne distributions inferred from real data in these species. We also find that the effect of linked selection can be significantly reduced by that of population structure.

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The Genomic Landscape of Divergence Across the Speciation Continuum in Island-Colonising Silvereyes (Zosterops lateralis)

G3 Genes|Genome|Genetics ◽

10.1534/g3.120.401352 ◽

2020 ◽

Vol 10 (9) ◽

pp. 3147-3163

Author(s):

Ashley T Sendell-Price ◽

Kristen C Ruegg ◽

Eric C Anderson ◽

Claudio S Quilodrán ◽

Benjamin M Van Doren ◽

...

Keyword(s):

Gene Flow ◽

Evolutionary Dynamics ◽

Population Genomics ◽

A Priori ◽

Genomic Islands ◽

Zosterops Lateralis ◽

Genome Wide ◽

Genomic Landscape ◽

Speciation Continuum ◽

Genomic Patterns

Abstract Inferring the evolutionary dynamics at play during the process of speciation by analyzing the genomic landscape of divergence is a major pursuit in population genomics. However, empirical assessments of genomic landscapes under varying evolutionary scenarios that are known a priori are few, thereby limiting our ability to achieve this goal. Here we combine RAD-sequencing and individual-based simulations to evaluate the genomic landscape of divergence in the silvereye (Zosterops lateralis). Using pairwise comparisons that differ in divergence timeframe and the presence or absence of gene flow, we document how genomic patterns accumulate along the speciation continuum. In contrast to previous predictions, our results provide limited support for the idea that divergence accumulates around loci under divergent selection or that genomic islands widen with time. While a small number of genomic islands were found in populations diverging with and without gene flow, in few cases were SNPs putatively under selection tightly associated with genomic islands. The transition from localized to genome-wide levels of divergence was captured using individual-based simulations that considered only neutral processes. Our results challenge the ubiquity of existing verbal models that explain the accumulation of genomic differences across the speciation continuum and instead support the idea that divergence both within and outside of genomic islands is important during the speciation process.

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Population genetics of the coral Acropora millepora: Toward genomic prediction of bleaching

Science ◽

10.1126/science.aba4674 ◽

2020 ◽

Vol 369 (6501) ◽

pp. eaba4674 ◽

Cited By ~ 14

Author(s):

Zachary L. Fuller ◽

Veronique J. L. Mocellin ◽

Luke A. Morris ◽

Neal Cantin ◽

Jihanne Shepherd ◽

...

Keyword(s):

Genome Wide Association Study ◽

Balancing Selection ◽

Conservation Strategies ◽

Genome Sequences ◽

Acropora Millepora ◽

Genome Wide ◽

A Genome ◽

Bleaching Response ◽

In The Wild

Although reef-building corals are declining worldwide, responses to bleaching vary within and across species and are partly heritable. Toward predicting bleaching response from genomic data, we generated a chromosome-scale genome assembly for the coral Acropora millepora. We obtained whole-genome sequences for 237 phenotyped samples collected at 12 reefs along the Great Barrier Reef, among which we inferred little population structure. Scanning the genome for evidence of local adaptation, we detected signatures of long-term balancing selection in the heat-shock co-chaperone sacsin. We conducted a genome-wide association study of visual bleaching score for 213 samples, incorporating the polygenic score derived from it into a predictive model for bleaching in the wild. These results set the stage for genomics-based approaches in conservation strategies.

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Recombining without hotspots: A comprehensive evolutionary portrait of recombination in two closely related species of Drosophila

10.1101/016972 ◽

2015 ◽

Author(s):

Caiti Smukowski Heil ◽

Chris Ellison ◽

Matthew Dubin ◽

Mohamed Noor

Keyword(s):

Recombination Rate ◽

Multiple Scales ◽

Sequence Data ◽

Scale Effects ◽

Recombination Rates ◽

Recombination Hotspots ◽

Genome Wide ◽

Genomic Landscape ◽

Species Specific

Meiotic recombination rate varies across the genome within and between individuals, populations, and species in virtually all taxa studied. In almost every species, this variation takes the form of discrete recombination hotspots, determined in Metazoans by a protein called PRDM9. Hotspots and their determinants have a profound effect on the genomic landscape, and share certain features that extend across the tree of life. Drosophila, in contrast, are anomalous in their absence of hotspots, PRDM9, and other species-specific differences in the determination of recombination. To better understand the evolution of meiosis and general patterns of recombination across diverse taxa, we present what may be the most comprehensive portrait of recombination to date, combining contemporary recombination estimates from each of two sister species along with historic estimates of recombination using linkage-disequilibrium-based approaches derived from sequence data from both species. Using Drosophila pseudoobscura and Drosophila miranda as a model system, we compare recombination rate between species at multiple scales, and we replicate the pattern seen in human-chimpanzee that recombination rate is conserved at broad scales and more divergent at finer scales. We also find evidence of a species-wide recombination modifier, resulting in both a present and historic genome wide elevation of recombination rates in D. miranda, and identify broad scale effects on recombination from the presence of an inter-species inversion. Finally, we reveal an unprecedented view of the distribution of recombination in D. pseudoobscura, illustrating patterns of linked selection and where recombination is taking place. Overall, by combining these estimation approaches, we highlight key similarities and differences in recombination between Drosophila and other organisms.

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Signatures of long-term balancing selection in human genomes

10.1101/119529 ◽

2017 ◽

Cited By ~ 2

Author(s):

Bárbara Domingues Bitarello ◽

Cesare de Filippo ◽

João Carlos Teixeira ◽

Joshua M. Schmidt ◽

Philip Kleinert ◽

...

Keyword(s):

Balancing Selection ◽

Theoretical Perspective ◽

Human Populations ◽

Protein Coding ◽

Human Genomes ◽

Genome Wide ◽

Higher Power ◽

Genome Wide Data ◽

Immune Related Genes

AbstractBalancing selection maintains advantageous diversity in populations through various mechanisms. While extensively explored from a theoretical perspective, an empirical understanding of its prevalence and targets lags behind our knowledge of positive selection. Here we describe the Non-Central Deviation (NCD), a simple yet powerful statistic to detect long-term balancing selection (LTBS) that quantifies how close frequencies are to expectations under LTBS, and provides the basis for a neutrality test. NCD can be applied to a single locus or genomic data, and can be implemented considering only polymorphisms (NCD1) or also considering fixed differences with respect to an outgroup (NCD2) species. Incorporating fixed differences improves power, and NCD2 has higher power to detect LTBS in humans under different frequencies of the balanced allele(s) than other available methods. Applied to genome-wide data from African and European human populations, in both cases using chimpanzee as an outgroup, NCD2 shows that, albeit not prevalent, LTBS affects a sizable portion of the genome: about 0.6% of analyzed genomic windows and 0.8% of analyzed positions. Significant windows (p < 0.0001) contain 1.6% of SNPs in the genome, which disproportionally fall within exons and change protein sequence, but are not enriched in putatively regulatory sites. These windows overlap about 8% of the protein-coding genes, and these have larger number of transcripts than expected by chance even after controlling for gene length. Our catalog includes known targets of LTBS but a majority of them (90%) are novel. As expected, immune-related genes are among those with the strongest signatures, although most candidates are involved in other biological functions, suggesting that LTBS potentially influences diverse human phenotypes.

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The genomic landscape of divergence across the speciation continuum in island-colonising silvereyes (Zosterops lateralis)

10.1101/2020.02.18.953893 ◽

2020 ◽

Author(s):

Ashley T. Sendell-Price ◽

Kristen C. Ruegg ◽

Eric C. Anderson ◽

Claudio S. Quilodrán ◽

Benjamin M. Van Doren ◽

...

Keyword(s):

Gene Flow ◽

Evolutionary Dynamics ◽

Genomic Islands ◽

Rad Sequencing ◽

Zosterops Lateralis ◽

Genome Wide ◽

Genomic Landscape ◽

Limited Support ◽

Speciation Continuum ◽

Genomic Patterns

ABSTRACTA goal of the genomic era is to infer the evolutionary dynamics at play during the process of speciation by analysing the genomic landscape of divergence. However, empirical assessments of genomic landscapes under varying evolutionary scenarios are few, limiting the ability to achieve this goal. Here we combine RAD-sequencing and individual-based simulations to evaluate the genomic landscape in the silvereye (Zosterops lateralis). Using comparisons matched for divergence timeframe and gene flow context, we document how genomic patterns accumulate along the speciation continuum. In contrast to previous predictions, our results provide limited support for the idea that divergence accumulates around loci under divergent selection or that genomic islands widen with time. While a small number of genomic islands were found in populations diverging with and without gene flow, in few cases were SNPs putatively under selection tightly associated with genomic islands. Furthermore, we modelled the transition from localised to genome-wide levels of divergence using individual-based simulations that considered only neutral processes. Our results challenge the ubiquity of existing verbal models that explain the accumulation of genomic differences across the speciation continuum and instead support the idea that divergence both within and outside of genomic islands is important during the speciation process.DATA ACCESSION NUMBERSResequencing data from this study have been submitted to the National Center for Biotechnology Information (NCBI; https://www.ncbi.nlm.nih.gov) under accession number PRJNA489169.

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Viability, behaviour, and colour expression in the offspring of matings between common wall lizard Podarcis muralis colour morphs

Current Zoology ◽

10.1093/cz/zoab039 ◽

2021 ◽

Author(s):

Javier Abalos ◽

Guillem Pérez i de Lanuza ◽

Alicia Bartolomé ◽

Fabien Aubret ◽

Tobias Uller ◽

...

Keyword(s):

Reproductive Output ◽

Balancing Selection ◽

Phenotypic Variability ◽

Investment Strategies ◽

Podarcis Muralis ◽

Common Wall ◽

Genome Wide ◽

Colour Morphs ◽

Embryonic Viability

Abstract Colour polymorphisms are widely studied to identify the mechanisms responsible for the origin and maintenance of phenotypic variability in nature. Two of the mechanisms of balancing selection currently thought to explain the long-term persistence of polymorphisms are the evolution of alternative phenotypic optima through correlational selection on suites of traits including colour, and heterosis. Both of these mechanisms can generate differences in offspring viability and fitness arising from different morph combinations. Here, we examined the effect of parental morph combination on fertilisation success, embryonic viability, newborn quality, antipredator and foraging behaviour, as well as inter-annual survival by conducting controlled matings in a polymorphic lacertid Podarcis muralis, where colour morphs are frequently assumed to reflect alternative phenotypic optima (e.g. alternative reproductive strategies). Juveniles were kept in outdoor tubs for a year in order to study inter-annual growth, survival, and morph inheritance. In agreement with a previous genome-wide association analysis, morph frequencies in the year-old juveniles matched the frequencies expected if orange and yellow expression depended on recessive homozygosity at two separate loci. Our findings also agree with previous literature reporting higher reproductive output of heavy females and the higher overall viability of heavy newborn lizards, but we found no evidence for the existence of alternative breeding investment strategies in female morphs, or morph-combination effects on offspring viability and behaviour. We conclude that inter-morph breeding remains entirely viable and genetic incompatibilities are of little significance for the maintenance of discrete colour morphs in P. muralis from the Pyrenees.

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Correction to: Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta

Genome Biology ◽

10.1186/s13059-019-1781-5 ◽

2019 ◽

Vol 20 (1) ◽

Author(s):

Baosheng Wang ◽

Julius P. Mojica ◽

Nadeesha Perera ◽

Cheng-Ruei Lee ◽

John T. Lovell ◽

...

Keyword(s):

Balancing Selection ◽

Genome Wide ◽

Boechera Stricta

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