Mitonuclear divergence predicts gradual speciation in animal hybrid zones

Derek Daniel Eddo, Bailey Rouse, Silu Wang

The core of speciation is the genetic incompatibilities underlying the evolution of reproductive isolation. Hybrid zones provide unique opportunities to unravel the evolutionary rate of reproductive isolation in the origin of species. The selection against hybrids accrues with increased genetic incompatibilities and drives the evolution of reproductive isolation in the face of gene flow. There have been decades of debates over the relationship between the selection against hybrids and the genetic divergence between parental lineages. The debates occur primarily among three models: (1) the Additive Effect Model predicts a linear growth of selection against hybrids with the divergence of parental lineages; (2) the Snowball Effect Model predicts exponential growth of selection; whereas (3) the Slowdown Effect Model predicts a logarithmic growth of selection. Here, we tested the three models with animal hybrid zones worldwide. The Slowdown Effect Model (3) is best supported with the full dataset. We refined the three models to consider independent and interactive effects of mitochondrial (mtDNA) and nuclear genetic (nDNA) divergence on the selection against hybrids. The refined Snowball Model (2) was best supported by the data, revealing a significant effect of nuclear genetic distance and its interaction with mtDNA distance on the selection against hybrid DNA in the hybrid zones. Collectively, this data synthesis in the early stage of animal speciation reveals a gradual development of reproductive isolation with mitonuclear genetic divergence.