Unexpectedly low recombination rates and presence of hotspots in termite genomes

Abstract

Meiotic recombination is a fundamental evolutionary process that facilitates adaptation and the removal of deleterious genetic variation. Social Hymenoptera exhibit some of the highest recombination rates among metazoans, whereas high recombination rates have not been found among non-social species from this insect order. It is unknown whether elevated recombination rates are a ubiquitous feature of all social insects. In many metazoan taxa, recombination is mainly restricted to hotspots a few kilobases in length. However, little is known about the prevalence of recombination hotspots in insect genomes. Here we infer recombination rate and its fine-scale variation across the genomes of two social species from the insect order Blattodea: the termitesCryptotermes secundusandMacrotermes bellicosus. We used linkage-disequilibrium-based methods to infer recombination rate. We infer that recombination rates are less than 1 cM/Mb in both species, which is lower than the average metazoan rate. We also observed a highly punctate distribution of recombination in both termite genomes, indicative of the presence of recombination hotspots. We infer the presence of full-length PRDM9 genes in the genomes of both species. We also find that recombination rates in genes are correlated with inferred levels of germline DNA methylation. The finding of low recombination rates in termites indicates that eusociality is not universally connected to elevated recombination rate. We speculate that intense selection among haploid males promotes high recombination rates in social Hymenoptera. This study is one of the first to indicate the presence of PRDM9-based recombination hotspots in an insect genome.

Understanding the Genetic Basis of Variation in Meiotic Recombination: Past, Present, and Future

“…At the time of writing, insights into the ubiquity and relative importance of PRDM9-mediated hotspots are still emerging. PRDM9 was first shown to be the major driver of hotspot positioning in humans and mice ( Baudat et al 2010 ), and there is now evidence that it is associated with hotspots in nearly all mammals, some teleost fish, turtles, snakes, and lizards ( Baker et al 2017 ; Schield et al 2020 ; Hoge et al 2024 ; Raynaud et al 2024 ); there is also emerging evidence that PRDM9 may direct hotspot positioning in some insects ( Everitt et al 2024 ). However, PRDM9 function has been lost in some groups, such as canids, birds, crocodiles, and amphibians ( Baker et al 2017 ), which have reverted back to the stable, ancestral hotspots enriched at functional elements ( Singhal et al 2015 ).…”