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, thus its trajectory fundamentally reflects speciation rate. Three trajectory models are: (1) the Beanbag Effect Model predicts linear; (2) the Snowball Effect Model predicts exponential, whereas (3) the Slowdown Effect Model predicts a logarithmic buildup of barriers to gene flow with the genomic divergence between the parental lineages. Testing the three models in natural populations ultimately explain speciation rate heterogeneity during the evolution of reproductive isolation. Here, we established a global hybrid zone database, Hybrid Zone Explorer, with 315 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. The Snowball Effect Model (2) is best supported with the full dataset. 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, revealing introgressive mitonuclear discordance. Collectively, this data synthesis of animal speciation in situ reveals 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.