Extensive gene flow in secondary sympatry after allopatric speciation

Abstract

Abstract In the conventional view, species are separate gene pools delineated by reproductive isolation (RI). In an alternative view, species may also be delineated by a small set of ‘speciation genes’ without full RI, a view that has gained broad acceptance. A recent survey, however, suggested that the extensive literature on ‘speciation with gene flow’ is mostly (if not all) about exchanges in the early stages of speciation. There is no definitive evidence that the observed gene flow actually happened after speciation is completed. Here, we wish to know whether ‘good species’ (defined by the ‘secondary sympatry’ test) do continue to exchange genes and, importantly, under what conditions such exchanges can be observed. De novo whole-genome assembly and re-sequencing of individuals across the range of two closely related mangrove species (Rhizophora mucronata and R. stylosa) reveal the genomes to be well delineated in allopatry. They became sympatric in northeastern Australia but remain distinct species. Nevertheless, their genomes harbor ∼4000–10 000 introgression blocks averaging only about 3–4 Kb. These fine-grained introgressions indicate continual gene flow long after speciation as non-introgressable ‘genomic islets,’ ∼1.4 Kb in size, often harbor diverging genes of flower or gamete development. The fine-grained introgression in secondary sympatry may help settle the debate about sympatric vs. micro-allopatric speciation. In conclusion, true ‘good species’ may often continue to exchange genes but the opportunity for detection is highly constrained.