Toward understanding the genetic mechanisms of speciation: Fine-grained introgressions between species

Abstract The biological species concept (BSC) is the prevailing definition of species whereby genes cannot be exchanged during or after speciation. In contrast, since only genes that contribute to the adaptive divergence between species should be non-exchangeable, BSC appears to bear little relationship to the genetic process of speciation. The rejection of BSC demands evidence of continual gene flow until the completion of speciation. Here, we carry out the sequencing and de novo high-quality assembly of the genomes of two closely related mangrove species (Rhizophora mucronata and R. stylosa). Whole-genome re-sequencing of individuals from their distributions on the tropical coasts shows their genomes to be well delineated in allopatry. They became sympatric in northeastern Australia where their genomes harbor 9,963 and 3,874 introgression blocks, respectively, with each block averaging only about 3-4 Kb. These fine-grained introgressions indicate that gene flow continues even after numerous loci have evolved to become non-introgressable “genomic islets”. Many of these islets, only 1.4 Kb on average, harbor “speciation loci” which contribute to the divergence in flower development or gamete production and thus result in fitness reduction upon introgression. Our fine-grained analysis may thus be the first one to show that gene flow not only happens during speciation, but often continues until the completion of speciation. Under the weight of the extensive literature, BSC may deserve to be retired.