Genomic structural variants constrain and facilitate adaptation in natural populations of Theobroma cacao , the chocolate tree

Abstract

Genomic structural variants (SVs) can play important roles in adaptation and speciation. Yet the overall fitness effects of SVs are poorly understood, partly because accurate population-level identification of SVs requires multiple high-quality genome assemblies. Here, we use 31 chromosome-scale, haplotype-resolved genome assemblies of Theobroma cacao—an outcrossing, long-lived tree species that is the source of chocolate—to investigate the fitness consequences of SVs in natural populations. Among the 31 accessions, we find over 160,000 SVs, which together cover eight times more of the genome than single-nucleotide polymorphisms and short indels (125 versus 15 Mb). Our results indicate that a vast majority of these SVs are deleterious: they segregate at low frequencies and are depleted from functional regions of the genome. We show that SVs influence gene expression, which likely impairs gene function and contributes to the detrimental effects of SVs. We also provide empirical support for a theoretical prediction that SVs, particularly inversions, increase genetic load through the accumulation of deleterious nucleotide variants as a result of suppressed recombination. Despite the overall detrimental effects, we identify individual SVs bearing signatures of local adaptation, several of which are associated with genes differentially expressed between populations. Genes involved in pathogen resistance are strongly enriched among these candidates, highlighting the contribution of SVs to this important local adaptation trait. Beyond revealing empirical evidence for the evolutionary importance of SVs, these 31 de novo assemblies provide a valuable resource for genetic and breeding studies in T. cacao.

Sheltering of deleterious mutations explains the stepwise extension of recombination suppression on sex chromosomes and other supergenes

“…Given the lack of knowledge about inversion rates in natural conditions and the computation challenge represented by the simulation of complex patterns of recombination, we used reasonably high inversion rates in our sex-chromosome evolution simulations, making it possible to observe the stepwise extension of a nonrecombining region within 100,000 generations. Recent studies suggested that inversions may not be too rare and that inversion breakpoints may be widely distributed throughout the genome [ 51 , 69 – 71 ]. The use of different inversion rates might result in much shorter or much longer times for the stepwise extension of the nonrecombining region, but should not change the final outcome.…”

Genome assembly, structural variants, and genetic differentiation between Lake Whitefish young species pairs (Coregonus sp.) with long and short reads

“…To achieve this, genome-graph based approaches were particularly relevant, allowing us to build a variation-aware reference graph (Garrison et al, 2018), and then perform unbiased mapping of reads to this graph (Sirén et al, 2020). Such two-step approaches have also be used in a handful of studies looking at SVs in chocolate trees Theobroma cacao (Hämälä et al, 2021), soybeans Glycine max (Lemay et al, 2021), and potato beetle Leptinotarsa decemlineata (Cohen, Hawthorne, & Schoville, 2021). Based on this, we believe that the combination of 2 nd and 3 rd generation sequencing is promising to study structural polymorphism within a population genomics framework and will allow the inclusion of SVs in studies of speciation and adaptation genomics.…”

Select and Sequence of a Segregating Sugar Beet Population Provides Genomic Perspective of Host Resistance to Seedling Rhizoctonia solani Infection

“…WGS has also been used to provide a complete picture of genetic variation within a population including structural variants (SV) and presence-absence variation (PAV) ( Pinosio et al, 2016 ; Wang et al, 2018 ). Recent research has demonstrated the impact of SV and PAV on important phenotypic variation observed between cultivars and adaptative trait variation including disease resistance ( Zhou et al, 2019 ; Hämälä et al, 2021 ). SnS experiments show potential to detect genetic variation linked to selection and adaptation in experimentally generated populations ( Schlötterer et al, 2015 ).…”