Genomic evidence for rapid speciation and gene flow between sympatric carnivorous Nepenthes pitcher plants

Speciation can result from both neutral and adaptive processes, but their relative importance and the factors exerting selective pressures are incompletely understood. In theory, interspecific gene flow could suffice to reverse speciation, or else erode neutral divergence and expose traits and underlying genes whose divergence is due to selection. Hence, introgression can shed light on selection during the speciation process. Here we study mixed assemblages of carnivorous Nepenthes pitcher plants, which frequently produce natural hybrids yet maintain distinct phenotypes. Using ddRAD-seq markers, we characterize divergence and introgression for eight Nepenthes species that grow sympatrically in communities of three to seven species at four locations in Southeast Asia, totalling 22 populations. The sympatric species fell into two discrete classes of high and low divergence. Five lineages with high divergence displayed little recent introgression in tests of location-dependent allele sharing (ABBA-BABA) despite the presence of some natural hybrids. However, all five lineages appear to have introgressed in the more distant past, as revealed by coalescent models with Approximate Bayesian Computation. In the same locations occur three further sympatric species with low genetic divergence. These incipient species also showed some natural hybrids, but in addition both ABBA-BABA tests and ABC suggested very recent or ongoing introgression, raising the question how divergence is maintained in these hybrid zones. One trait possibly involved in maintenance of divergence against gene flow might be the carnivorous pitcher traps, whose morphology showed greater divergence than expected under neutral evolution (Pst-Fst) in the introgressing species pair N. hemsleyana and N. rafflesiana t.f..