Genetic differentiation and intrinsic genomic features explain variation in recombination hotspots among cocoa tree populations

Abstract

Background Recombination plays an important evolutionary role by breaking up haplotypes and shuffling genetic variation. This process impacts the ability of selection to eliminate deleterious mutations or increase the frequency of beneficial mutations in a population. To understand the role of recombination generating and maintaining haplotypic variation in a population, we can construct fine-scale recombination maps. Such maps have been used to study a variety of model organisms and proven to be informative of how selection and demographics shape species-wide variation. Here we present a fine-scale recombination map for ten populations of Theobroma cacao – a non-model, long-lived, woody crop. We use this map to elucidate the dynamics of recombination rates in distinct populations of the same species, one of which is domesticated. Results Mean recombination rates in range between 2.5 and 8.6 cM/Mb for most populations of T. cacao with the exception of the domesticated Criollo (525 cM/Mb) and Guianna, a more recently established population (46.5 cM/Mb). We found little overlap in the location of hotspots of recombination across populations. We also found that hotspot regions contained fewer known retroelement sequences than expected and were overrepresented near transcription start and termination sites. We find mutations in FIGL-1, a protein shown to downregulate cross-over frequency in Arabidopsis, statistically associated to higher recombination rates in domesticated Criollo. Conclusions We generated fine-scale recombination maps for ten populations of Theobroma cacao and used them to understand what processes are associated with population-level variation in this species. Our results provide support to the hypothesis of increased recombination rates in domesticated plants (Criollo population). We propose a testable mechanistic hypothesis for the change in recombination rate in domesticated populations in the form of mutations to a previously identified recombination-suppressing protein. Finally, we establish a number of possible correlates of recombination hotspots that help explain general patterns of recombination in this species.

Evolutionary implications of recombination differences across diverging populations ofAnopheles

“…However, when calculating the per site recombination rate to account for effective population size, KES had an average recombination rate that was an order of magnitude larger than the other populations. As demonstrated within previous studies, populations with a small effective population size may exhibit higher recombination rates associated to an increase accumulation of deleterious mutations in homogenized genomes (Keightley and Otto 2006; Kumar et al 2019; Schwarzkopf et al 2020). Because KES has had a small historical Ne (~10,000), we hypothesize that the deleterious effects of a low Ne have contributed to a increased overall recombination rates within KES; however, this hypothesis needs to be tested.…”

“…Both fine-scale recombination rates and hotspots are poorly conserved across mammals and plants with significant differences even among closely related species (Spencer et al 2006; Choi et al 2016; Beeson et al 2019; Dreissig et al 2019). However, less is known about the onset of variation in recombination rates across diverging populations of the same species (Schwarzkopf et al 2020) and how it impacts patterns of genetic variation. Comparing recombination maps across multiple populations of humans has recently been investigated; however, this question has not been applied to other model systems and was aimed at identifying the impact of demographic changes on the recombination landscape and not how elevated recombination impacts patterns of diversity and divergence (Spencer et al 2006).…”

Evolution of recombination landscapes in diverging populations of bread wheat

“…indica (Marand et al 2019) although they diverged relatively recently (440,000-86,000 years ago (YA); Ma and Bennetzen 2004;Vitte et al 2004;Zhu and Ge 2005;Tang et al 2006). Similarly, analysis of the recombination landscapes in the cocoa-tree (Theobroma cacao) showed only little overlap of recombination hotspots across ten diverging populations with less divergent populations showing higher level of overlap (Schwarzkopf et al 2020). An analysis of the recombination landscapes in wild barley (Hordeum vulgare ssp.…”

Natural variation in meiotic recombination rate shapes introgression patterns in intraspecific hybrids between wild and domesticated barley

“…Additionally, genetic divergence and structural variations are also influencing recombination rates (Ziolkowski et al ., 2015, 2017; Crown et al ., 2018; Rowan et al ., 2019). At the population level, recombination rates were shown to vary drastically depending on variations in meiotic genes or environmental conditions (Brand et al ., 2018; Dreissig et al ., 2019; Martin et al ., 2019; Samuk et al ., 2019; Schwarzkopf et al ., 2020).…”