Reconciling Santa Rosalia: Both Reproductive Isolation and Coexistence Constrain Diversification

Understanding patterns of diversification necessarily requires accounting for both the generation and the persistence of species. Formal models of speciation genetics, however, focus on the generation of new species without explicitly considering the maintenance of biodiversity (e.g., coexistence, the focus of ecological studies of diversity). Consequently, it remains unclear whether and how new species will coexist following a speciation event, a gap limiting our ability to understand the rate-limiting controls of diversification over macroevolutionary timescales. To connect coexistence and speciation theory and assess the relative importance of ecological versus genetic constraints in diversification events, we develop a deterministic, three-locus, population-genetic model that includes a skewed distribution of available resources (to generate variation in fitness differences), frequency-dependent competition, and assortative mating. Both ecology and genetics play vital and interacting roles in shaping initial speciation events and long-term eco-evolutionary outcomes. Ecological constraints are especially important when fitness differences are large and competition remains strong among dissimilar phenotypes. Ephemeral species can occur in our model and are typically lost because of competitive exclusion, a result demonstrating that species persistence may serve as the rate-limiting control of long-term diversification rates. More broadly, our model adds evidence that the unification of ecological and evolutionary (including genetic) perspectives on biodiversity is needed to predict large-scale patterns.