Testing cohesive selective paths and evaluating loss of evolutionary information while delimiting species of...

Biodiversity is structured in nested Retrospective Reproductive Communities (RRCs) reflecting different levels of information about evolutionary processes. Ranking species involves deciding which level to emphasize, based on a trade-off in information gain and loss. Modeling the selective processes that maintain RRCs along distinct evolutionary paths can inform these trade-offs in species delimitation. We illustrate this approach using the Brazilian wandering spiders (Phoneutria). Integrating genetic markers, geometric morphometrics, color patterns, and environmental data, we applied both established and novel approaches to test divergence through historical natural and sexual selection. We found evidence that selection on ecological niche and ventral abdominal coloration contributed to the formation of 4 distinct RRCs. Two of these RRCs also showed evidence of a lock-and-key mechanism influencing genital morphology evolution. Despite the distinct cohesive forces, gene flow modeling revealed incomplete reproductive isolation, with potential hybrid individuals. We evaluate the implications of lumping versus splitting these lineages and argue that recognizing all 4 RRCs as distinct species would better preserve evolutionary information and minimize downstream impacts on other research fields such as pharmacology, public health, and conservation. Our approach provides a quantitative basis to ponder the implications of choosing between different species hypotheses.