Rapid speciation in small populations challenges the dominance of ecological speciation

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Abstract
Speciation – the process by which two lineages become reproductively isolated – plays a key role in the emergence and maintenance of biodiversity. Yet, our understanding of the time it takes for speciation to occur, and of the microevolutionary processes that influence this tempo, remains limited. Here, we thoroughly characterize how population size, mutation rate, local adaptation and migration are expected to influence the duration of speciation, as well as the shape of the “grey zone” of speciation. We show that the relationship between population size and speciation time is indicative of the speciation mode, as faster speciation in smaller populations only occurs in the case of non-ecological speciation. Leveraging genomic estimates of population size and speciation duration across 196 pairs of plant species, we uncover a positive association between population size and speciation duration. Taken together, these results challenge the view that ecological speciation is the source of much of species diversity. Significance statement: How new species arise, and how quickly they do so, plays a key role in shaping Earth’s biodiversity. Yet, the links between how speciation occurs, how fast it proceeds, and basic properties of species such as population size, remain debated. We clarify these relationships using an integrative model of speciation. We show, in particular, that faster speciation in smaller populations is a signature of non-ecological speciation. Analyses of genomic data from plants reveal precisely this pattern, challenging the prevailing view that speciation in nature is predominantly ecological.
Funding Information
  • Institut des mathématiques pour la Planète Terre, Lyon, FR

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