Genomic structural variants constrain and facilitate adaptation in natural populations of Theobroma cacao, the Chocolate Tree

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 thousand SVs, which together
cover eight times more of the genome than SNPs and short indels (125 Mb
vs. 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 on this important local adaptation trait. Beyond revealing new
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.