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Multispecies pangenomes reveal a pervasive influence of population size on structural variation.

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Title: Multispecies pangenomes reveal a pervasive influence of population size on structural variation.
Authors: Edwards, Scott V. (AUTHOR), Fang, Bohao (AUTHOR), Khost, Danielle (AUTHOR), Kolyfetis, George E. (AUTHOR), Cheek, Rebecca G. (AUTHOR), DeRaad, Devon A. (AUTHOR), Chen, Nancy (AUTHOR), Fitzpatrick, John W. (AUTHOR), McCormack, John E. (AUTHOR), Funk, W. Chris (AUTHOR), Ghalambor, Cameron K. (AUTHOR), Garrison, Erik (AUTHOR), Guarracino, Andrea (AUTHOR), Li, Heng (AUTHOR), Sackton, Timothy B. (AUTHOR)
Source: Science. 12/11/2025, Vol. 390 Issue 6778, p1-18. 18p.
Subjects: Pan-genome, DNA copy number variations, Evolutionary models, Species diversity, Chromosome structure, Gene rearrangement, Animal population density
Abstract: Structural variants (SVs) are widespread in vertebrate genomes, yet their evolutionary dynamics remain poorly understood. Using 45 long-read de novo genome assemblies and pangenome tools, we analyze SVs among three closely related species of North American jays (Aphelocoma, scrub-jays) displaying a 55-fold range in effective population size. We find rapid evolution of genome architecture, including ~100-megabase decreases in genome size driven by shifts in complex satellite landscapes. SVs exhibit slightly deleterious dynamics modulated by variant length and population size, with consistent evidence of adaptive fixation only in the largest population. Gene copy number variants exhibit an inverse relationship with population size, indicating strongly deleterious dynamics, with consequences for gene expression. Our long-read dataset and pangenome analysis demonstrate how population size shapes genome complexity. Editor's summary: Structural variants such as genomic deletions, insertions, and inversions have often received focus for their adaptive potential but are difficult to identify and study systematically without long-read sequencing. Edwards et al. assembled a pangenome for three species of North American jays with very different population histories. Contrary to other systems, they found that the species with the smallest population size also had the smallest genome and the fewest repeats. The researchers posit that this difference is due to stochastic loss of repeats after a large expansion in the ancestor of these three species. These data represent one of the first pangenomes for nonmodel organisms and give a better understanding of the dynamics influencing structural variants. —Corinne Simonti INTRODUCTION: Structural variants are a diverse class of mutations, including insertions, deletions, translocations, inversions, and other multinucleotide mutations. The number, chromosomal distribution, and fitness effects of structural variants as well as the effect of demographic events on their diversity and evolution make up a major frontier in evolutionary genomics. Yet what little we know about these issues is based on DNA sequencing and computational methods that cannot capture the full diversity of structural variants. Several recent studies have demonstrated that structural variants are often deleterious, but most of these studies have used DNA sequencing methods involving short reads and bioinformatics pipelines involving mapping variants to a single reference genome. Population-scale long-read datasets, involving sequencing and de novo assembly of multiple individuals within a species, are better at capturing the full spectrum of structural variants, but such datasets are rare outside of humans. Pangenome methods using all-versus-all approaches to genome alignment without designating a reference genome are also rarely applied in nonmodel species, but they allow better characterization of the full landscape of structural variants. Together, pangenomes based on population-scale long-read datasets provide opportunities for understanding the full diversity of structural variants and their evolutionary properties. RATIONALE: We used population-scale long-read sequencing and pangenome methods to characterize diversity and evolution of structural variants in three species of North American scrub-jays (Aphelocoma) that exhibit a strong gradient in effective population sizes. Whereas the widespread Woodhouse's scrub-jay (Aphelocoma woodhouseii) has six times the variation found in humans, the island scrub-jay (Aphelocoma insularis) underwent a strong bottleneck and has one-tenth the variation of humans, resulting in an ~55-fold range in effective population size among the species. We sequenced 45 long-read genomes across three scrub-jay species, reasoning that these birds would provide a powerful setting for applying comparative population genomics to understand the evolutionary forces acting on structural variants in natural populations. RESULTS: Our pangenome survey revealed unexpected differences in genome size between these closely related species; identified more than 3 million insertion-deletion polymorphisms and nearly 450,000 structural variants; facilitated visualizing the pangenomic signatures of these variants; and helped quantify their interaction with prominent repetitive features of avian genomes, such as the highly dynamic satellite landscape. Structural variants, including more than 300 inversions ranging in length up to ~3 megabases, were most abundant in A. woodhouseii, followed by Aphelocoma coerulescens and A. insularis. These variants were estimated to be, on average, more deleterious than single-nucleotide variants and potentially adaptive only in the species with large population size. Gene copy number variants, such as gene deletions, were widespread, yet occurred most frequently in A. insularis—the species with the smallest population size—suggesting even greater deleteriousness. Through transcriptomes, we show that gene copy number variation influences gene expression and therefore likely has detectable effects on organismal function. CONCLUSION: Population-scale long-read sequencing and pangenome tools provided a high-resolution lens on the rapid evolution of genome architecture, repeat landscapes, and structural variant and gene copy number diversity in this trio of closely related species. The use of pangenome tools in natural populations will facilitate our understanding of the evolutionary drivers of structural variation. Pangenomes across a gradient of effective population sizes.: Long-read sequencing and pangenome analysis of 45 scrub-jays (Aphelocoma) and outgroups reveal a dynamic repeat landscape. The abundance of most structural variants scales with effective population size. Gene copy number deletions show an inverse relationship with population size and drive variation in gene expression. Statistical analysis reveals that structural variants are, on average, more deleterious than single-nucleotide polymorphisms and only rarely are adaptive. [ABSTRACT FROM AUTHOR]
Copyright of Science is the property of American Association for the Advancement of Science and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract. (Copyright applies to all Abstracts.)
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  Data: Multispecies pangenomes reveal a pervasive influence of population size on structural variation.
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  Data: <searchLink fieldCode="JN" term="%22Science%22">Science</searchLink>. 12/11/2025, Vol. 390 Issue 6778, p1-18. 18p.
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  Data: <searchLink fieldCode="DE" term="%22Pan-genome%22">Pan-genome</searchLink><br /><searchLink fieldCode="DE" term="%22DNA+copy+number+variations%22">DNA copy number variations</searchLink><br /><searchLink fieldCode="DE" term="%22Evolutionary+models%22">Evolutionary models</searchLink><br /><searchLink fieldCode="DE" term="%22Species+diversity%22">Species diversity</searchLink><br /><searchLink fieldCode="DE" term="%22Chromosome+structure%22">Chromosome structure</searchLink><br /><searchLink fieldCode="DE" term="%22Gene+rearrangement%22">Gene rearrangement</searchLink><br /><searchLink fieldCode="DE" term="%22Animal+population+density%22">Animal population density</searchLink>
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  Data: Structural variants (SVs) are widespread in vertebrate genomes, yet their evolutionary dynamics remain poorly understood. Using 45 long-read de novo genome assemblies and pangenome tools, we analyze SVs among three closely related species of North American jays (Aphelocoma, scrub-jays) displaying a 55-fold range in effective population size. We find rapid evolution of genome architecture, including ~100-megabase decreases in genome size driven by shifts in complex satellite landscapes. SVs exhibit slightly deleterious dynamics modulated by variant length and population size, with consistent evidence of adaptive fixation only in the largest population. Gene copy number variants exhibit an inverse relationship with population size, indicating strongly deleterious dynamics, with consequences for gene expression. Our long-read dataset and pangenome analysis demonstrate how population size shapes genome complexity. Editor's summary: Structural variants such as genomic deletions, insertions, and inversions have often received focus for their adaptive potential but are difficult to identify and study systematically without long-read sequencing. Edwards et al. assembled a pangenome for three species of North American jays with very different population histories. Contrary to other systems, they found that the species with the smallest population size also had the smallest genome and the fewest repeats. The researchers posit that this difference is due to stochastic loss of repeats after a large expansion in the ancestor of these three species. These data represent one of the first pangenomes for nonmodel organisms and give a better understanding of the dynamics influencing structural variants. —Corinne Simonti INTRODUCTION: Structural variants are a diverse class of mutations, including insertions, deletions, translocations, inversions, and other multinucleotide mutations. The number, chromosomal distribution, and fitness effects of structural variants as well as the effect of demographic events on their diversity and evolution make up a major frontier in evolutionary genomics. Yet what little we know about these issues is based on DNA sequencing and computational methods that cannot capture the full diversity of structural variants. Several recent studies have demonstrated that structural variants are often deleterious, but most of these studies have used DNA sequencing methods involving short reads and bioinformatics pipelines involving mapping variants to a single reference genome. Population-scale long-read datasets, involving sequencing and de novo assembly of multiple individuals within a species, are better at capturing the full spectrum of structural variants, but such datasets are rare outside of humans. Pangenome methods using all-versus-all approaches to genome alignment without designating a reference genome are also rarely applied in nonmodel species, but they allow better characterization of the full landscape of structural variants. Together, pangenomes based on population-scale long-read datasets provide opportunities for understanding the full diversity of structural variants and their evolutionary properties. RATIONALE: We used population-scale long-read sequencing and pangenome methods to characterize diversity and evolution of structural variants in three species of North American scrub-jays (Aphelocoma) that exhibit a strong gradient in effective population sizes. Whereas the widespread Woodhouse's scrub-jay (Aphelocoma woodhouseii) has six times the variation found in humans, the island scrub-jay (Aphelocoma insularis) underwent a strong bottleneck and has one-tenth the variation of humans, resulting in an ~55-fold range in effective population size among the species. We sequenced 45 long-read genomes across three scrub-jay species, reasoning that these birds would provide a powerful setting for applying comparative population genomics to understand the evolutionary forces acting on structural variants in natural populations. RESULTS: Our pangenome survey revealed unexpected differences in genome size between these closely related species; identified more than 3 million insertion-deletion polymorphisms and nearly 450,000 structural variants; facilitated visualizing the pangenomic signatures of these variants; and helped quantify their interaction with prominent repetitive features of avian genomes, such as the highly dynamic satellite landscape. Structural variants, including more than 300 inversions ranging in length up to ~3 megabases, were most abundant in A. woodhouseii, followed by Aphelocoma coerulescens and A. insularis. These variants were estimated to be, on average, more deleterious than single-nucleotide variants and potentially adaptive only in the species with large population size. Gene copy number variants, such as gene deletions, were widespread, yet occurred most frequently in A. insularis—the species with the smallest population size—suggesting even greater deleteriousness. Through transcriptomes, we show that gene copy number variation influences gene expression and therefore likely has detectable effects on organismal function. CONCLUSION: Population-scale long-read sequencing and pangenome tools provided a high-resolution lens on the rapid evolution of genome architecture, repeat landscapes, and structural variant and gene copy number diversity in this trio of closely related species. The use of pangenome tools in natural populations will facilitate our understanding of the evolutionary drivers of structural variation. Pangenomes across a gradient of effective population sizes.: Long-read sequencing and pangenome analysis of 45 scrub-jays (Aphelocoma) and outgroups reveal a dynamic repeat landscape. The abundance of most structural variants scales with effective population size. Gene copy number deletions show an inverse relationship with population size and drive variation in gene expression. Statistical analysis reveals that structural variants are, on average, more deleterious than single-nucleotide polymorphisms and only rarely are adaptive. [ABSTRACT FROM AUTHOR]
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  Data: <i>Copyright of Science is the property of American Association for the Advancement of Science and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract.</i> (Copyright applies to all Abstracts.)
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      – SubjectFull: Evolutionary models
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      – SubjectFull: Animal population density
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