Evolutionary Consequences of Unusually Large Pericentric TE-rich Regions in the Genome of a Neotropical Fig Wasp

Abstract

Transposable elements (TEs), despite generally being considered deleterious, represent a substantial portion of most eukaryotic genomes. Specific genomic regions, such as telomeres and pericentromeres, are often densely populated with TEs. In these regions, which tend to be gene-poor, reduced recombination shelters the genome from the deleterious effects of TEs. Here, we describe unusually large and continuous pericentromeric TE-rich regions in all chromosomes of the genome assembly of Pegoscapus hoffmeyeri Sp. A (511.79 Mbp), a Neotropical fig wasp that is the obligate pollinator of Ficus obtusifolia. The identified pericentromeric TE-rich regions span nearly half (46%) of the genome, and harbor over 40% of all annotated genes, including 30% of conserved BUSCO genes. We present evidence that low recombination in these TE-rich regions generates strong bimodal molecular evolution patterns genome-wide. Patterns of nucleotide diversity and protein-coding gene evolution in TE-rich regions are consistent with a reduced efficiency of selection and suggestive of strong Hill-Robertson effects. A significant reduction in third codon position GC content (GC3) in TE-rich regions emerged as the most distinctive gene feature differentiating genes in TE-rich regions from those in the rest of the genome, a pattern that likely results from the absence of GC-biased gene conversion. This remarkable binary compartmental genome organization in the genome of P. hoffmeyeri provides a unique example of how genome organization with compartmental TE distribution can lead to context-dependent gene evolution shaped by common evolutionary forces.