Testing coherent selective pathways and evaluating the loss of evolutionary information while delimiting species of Brazilian wandering spiders

Abstract

Biodiversity is structured in nested Retrospective Reproductive Communities (RRC) that reflect different levels of information about evolutionary processes. Ranking of species involves deciding which level is to be emphasized, based on a trade-off in information gain and loss. Modeling the selective processes that maintain RRCs along distinct evolutionary trajectories can inform these trade-offs in species delimitation. We illustrate this approach using the Brazilian wandering spiders (Phoneutria). By integrating genetic markers, geometric morphometrics, color patterns and environmental data, we used 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 color contributed to the formation of four distinct RRCs. Two of these RRCs also showed evidence of a lock-and-key mechanism affecting the development of genital morphology. Despite the distinct connecting 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 four RRCs as distinct species would better preserve evolutionary information and minimize downstream impact on other research fields such as pharmacology, public health, and conservation. Our approach provides a quantitative basis for pondering the implications of choosing between different species hypotheses.