Genomics of speciation and introgression in Princess cichlid fishes from Lake Tanganyika

How variation in the genome translates into biological diversity and new species originate has endured as the mystery of mysteries in evolutionary biology. African cichlids fishes are prime model systems to address speciation-related questions for their remarkable taxonomic and phenotypic diversity, and the possible role of gene flow in this process. Here, we capitalize on genome sequencing and phylogenomic analyses to address the relative impacts of incomplete lineage sorting, introgression, and hybrid speciation in the Neolamprologus savoryi-complex (the ‘Princess cichlids’) from Lake Tanganyika. We present a time-calibrated species tree based upon whole genome sequences, and provide strong evidence for incomplete lineage sorting in the early phases of diversification and multiple introgression events affecting different stages. Importantly, we find that the Neolamprologus chromosomes show center-to-periphery biases in nucleotide diversity, sequence divergence, GC content, incomplete lineage sorting, and rates of introgression, all being modulated by recombination density and linked selection. The detection of heterogeneous genomic landscapes has strong implications related to the genomic mechanisms involved in speciation. Collinear chromosomal regions can be protected from gene flow and harbor incompatibility genes if they reside in lowly recombining regions, and coupling can evolve between non-physically linked genomic regions (chromosome centers in particular). Simultaneously, chromosome peripheries appear as more dynamic, evolvable regions where adaptation polymorphisms have a fertile ground. We propose four verbal scenarios that relate the relative contribution of chromosome centers versus peripheries to the generation of phenotypic and taxonomic diversity. Hence, genome heterogeneity might have contributed to the spectacular cichlid diversity observed today.