Recent advances and current challenges in population genomics of structural variation in animals and plants

Abstract

The field of population genomics has seen a surge of studies on genomic structural variation over the past two decades. These studies witnessed that structural variation is taxonomically ubiquitous and represent a dominant form of genetic variation within species. Recent advances in technology, especially the development of long-read sequencing platforms, have enabled the discovery of structural variants (SVs) in previously inaccessible genomic regions which unlocked additional structural variation for population studies and revealed that more SVs contribute to evolution than previously perceived. An increasing number of studies suggest that SVs of all types and sizes may have a large effect on phenotype and consequently major impact on rapid adaptation, population divergence, and speciation. However, the functional effect of the vast majority of SVs is unknown and the field generally lacks evidence on the phenotypic consequences of most SVs that are suggested to have adaptive potential. Non-human genomes are heavily under-represented in population-scale studies of SVs. We argue that more research on other species is needed to objectively estimate the contribution of SVs to evolution. We discuss technical challenges associated with SV detection and outline the most recent advances towards more representative reference genomes, which opens a new era in population-scale studies of structural variation.

Exploring polymorphic interspecies structural variants in Eucalyptus: Unravelling Their Role in Reproductive Isolation and Adaptive Divergence

“…Similar to reproductive isolation, understanding how all types of genetic mutations contribute to the creation and maintenance of genetic diversity is crucial to understanding how organisms improve fitness and adapt to their changing environments (Gregory, 2009; Loewe & Hill, 2010; Pokrovac & Pezer, 2022). Inversions and translocations aid in adaptive evolution by fixing allele combinations, duplications contribute to the development of new genes, and insertions and deletions, often described as PAVs, modify gene expression and gene content (De Oliveira et al, 2020; Mérot et al, 2020; Wellenreuther et al, 2019).…”

“…Duplications, highly common and also likely to be selected against (Flagel & Wendel, 2009; Wu & Cox, 2019), could be preserved due to their ability to acquire new function (neofunctionalisation) or by retaining a subset of original function (subfunctionalisation) (Braasch et al, 2016; Freeling et al, 2015; Lien et al, 2016; Wu & Cox, 2019). Large (> 50 bp) insertions and deletions, which are often genotyped as presence/absence variants (PAVs), copy number variations (CNV), or gene duplications, are also very common within genomes (Conrad & Hurles, 2007; Pokrovac & Pezer, 2022). These SVs are known to impact genes and gene structure, and to affect phenotypes (Sun et al, 2022; Yuan et al, 2021), although many can also be neutral.…”

“…Typically termed chromosomal rearrangements or structural variations (SV), these large mutations include inversions, translocations, duplications, insertions, and deletions (Savocco & Piazza, 2021). Until recently however, technological constraints, namely sequencing read lengths, have inhibited their discovery (Sedlazeck et al, 2018), and their role in population evolutionary processes remains poorly understood (Pokrovac & Pezer, 2022). Using third-generation long-read sequencing, such as those offered by Oxford Nanopore Technologies and PacBio, evolutionary genomic studies can now affordably assemble highly contiguous genomes of several individuals across related species.…”

Deciphering male influence in gynogenetic Pengze crucian carp (Carassius auratus var. pengsenensis): insights from Nanopore sequencing of structural variations

“…Compared to single nucleotide polymorphisms (SNPs), SVs encompass larger genomic regions and offer more complex genetic information. As vital genetic markers, SVs play a crucial role in regulating gene expression, enhancing crop traits, and investigating crop adaptability ( Pokrovac and Pezer, 2022 ; Liu et al, 2023 ).…”

The prevalence of copy number increase at multiallelic copy number variants associated with cave colonization

“…Multiple factors complicate the reconciliation between studies such as the heterogeneity of CNVs in terms of type, size, genomic context, and mutation rate, as well as technical difficulties and limitations pertaining to the choice of methodology (reviewed in Pokrovac & Pezer, 2022). Moreover, experimental evolution as a tool is generally not feasible for more complex multicellular organisms.…”