On the Accumulation of Genomic Barriers to Gene Flow in the Origin of Animal Species

Derek Daniel Eddo, Bailey Rouse, Silu Wang

The accumulation of genomic barriers to gene flow underpins speciation. We synthesized decades of micro- and macroevolutionary investigations on speciation and formulated a statistical foundation to test alternative speciation genetic hypotheses: (1) the Beanbag Effect Model predicts a linear establishment of barriers to gene flow with the genetic divergence between the parental lineages; (2) the Snowball Effect Model predicts exponential spread of barriers, whereas (3) the Slowdown Effect Model predicts a logarithmic buildup of barriers. Testing the three models requires quantifying the progression of reproductive isolation as speciation unfolds in the face of gene flow. Here, we established a global hybrid zone database, Hybrid Zone Explorer, with all the animal hybrid zones reported to date. This database empowered a rare opportunity to directly infer in situ speciation with gene flow and test the three speciation rate models. We used cline width over dispersal rate, or the selection against hybrids in the tension zone model, to reflect the establishment of barriers to gene flow. The Snowball Effect Model (2) is best supported with the full dataset, implying predominant epistasis among barriers to gene flow. We further refined the three models to consider independent and interactive effects of mitochondrial (mtDNA) and nuclear genetic (nDNA) divergence on the selection against hybrids. The Snowball Effect Model (2) was again best supported by the data, revealing positive roles of independent mitonuclear genetic divergence. However, the interaction between mtDNA and nDNA divergence negatively contributed to barriers to gene flow, indicating introgressive mitonuclear discordance. Collectively, this data synthesis across animal speciation continuum is consistent with an accelerated growth of barriers to gene flow with mitonuclear genetic divergence. This speciation momentum profoundly illuminates the genomic principle shaping speciation rate heterogeneity underlying animal biodiversity on our planet.