Three-phase transitions to reproductive isolation: The roles of utilization mismatch and residual selection

The adaptive emergence of reproductive isolation is increasingly recognized as a key mechanism of sympatric speciation. Here we aim at establishing a deeper understanding of the complex multilocus dynamics underlying such speciation transitions under resource competition. In reality, a single populations resource utilization can never exactly match a resource distribution, making residual selection pressures inevitable. We find that this commonly leads to three-phase transitions to reproductive isolation. First, partial assortativity emerges, quickly adjusting a populations variance to the resource distributions variance. Second, allelic variance slowly erodes across loci, allowing an increasingly bimodal phenotype distribution to emerge. Third, a fast transition occurs toward full bimodality in conjunction with practically complete reproductive isolation of the emerging two species. The first phase is driven by frequency-dependent divergent ecological selection. The second phase is driven by self-accelerating residual ecological selection: the more loci code for the selected phenotype, the slower is this intermediate phase. The third phase is driven by self-accelerating sexual selection. We study three types of mismatch-driven speciation, resulting from (i) incongruences between the shapes of resource distributions and competition kernels, (ii) low numbers of loci, and (iii) premature cessations of the first phases variance expansion. Our results suggest that the incomplete separation of incipient species, a characteristic of the second phase, is common in nature, which is likely resulting in detectable genetic footprints of three-phase transitions to reproductive isolation occurring in nature.