The molecular basis of convergent phenotypes is often unknown. However, convergence at a genomic level is predicted when there are large population sizes, gene flow among diverging lineages or strong genetic constraints. We used whole-genome resequencing to investigate genomic convergence in fishes ( Poecilia spp.) that have repeatedly colonized hydrogen sulfide (H 2 S)-rich environments in Mexico. We identified genomic similarities in both single nucleotide polymorphisms (SNPs) and structural variants (SVs) among independently derived sulfide spring populations, with approximately 1.2% of the genome being shared among sulfidic ecotypes. We compared these convergent genomic regions to candidate genes for H 2 S adaptation identified from transcriptomic analyses and found that a significant proportion of these candidate genes (8%) were also in regions where sulfidic individuals had similar SNPs, while only 1.7% were in regions where sulfidic individuals had similar SVs. Those candidate genes included genes involved in sulfide detoxification, the electron transport chain (the main toxicity target of H 2 S) and other processes putatively important for adaptation to sulfidic environments. Regional genomic similarity across independent populations exposed to the same source of selection is consistent with selection on standing variation or introgression of adaptive alleles across divergent lineages. However, combined with previous analyses, our data also support that adaptive changes in mitochondrially encoded subunits arose independently via selection on de novo mutations. Pressing questions remain on what conditions ultimately facilitate the independent rise of adaptive alleles at the same loci in separate populations, and thus, the degree to which evolution is repeatable or predictable. This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions'.

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.

AbstractOur study investigates the possible drivers of recombination hotspots in Theobroma cacao using ten genetically differentiated populations. By comparing recombination patterns between multiple populations, we obtain a novel view of recombination at the population-divergence timescale. For each population, a fine-scale recombination map was generated using the coalescent with a standard method based on linkage disequilibrium (LD). These maps revealed higher recombination rates in a domesticated population and a population that has undergone a recent bottleneck. We inferred hotspots of recombination for each population and find that the genomic locations of hotspots correlate with genetic differentiation between populations (FST). We used randomization approaches to generate appropriate null models to understand the association between hotspots of recombination and both DNA sequence motifs and genomic features. We found that hotspot regions contained fewer known retroelement sequences than expected and were overrepresented near transcription start and termination sites. Our findings indicate that recombination hotspots are evolving in a way that is consistent with genetic differentiation but are also preferentially driven to near coding regions. We illustrate that, consistent with predictions in plant domestication, the recombination rate of the domesticated population is orders of magnitude higher than that of other populations. More importantly, we find two fixed mutations in the domesticated population’s FIGL1 protein. FIGL1 has been shown to increase recombination rates in Arabidopsis by several orders of magnitude, suggesting a possible mechanism for the observed increased recombination rate in the domesticated population.

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