Résumé
Understanding reproductive isolation (RI) between lineages is a central goal of speciation research. While the strength of RI has been estimated across a broad range of taxa, synthesising these data remains challenging, partially because we lack a common language for classifying and reporting RI estimates. Here, we present the Reproductive Isolation Ontology (RIO), a structured framework designed to standardise the classification of RI estimates across the Tree of Life. The RIO comprises three interrelated domains, each organised into a nested hierarchy of classification terms. We demonstrate the utility of this approach and call for researchers to adopt the RIO to facilitate the integration of speciation research.
Why we need a standard language for reproductive isolation When two lineages meet -whether naturally or via human manipulation -their futures will be shaped by reproductive barriers between them. These barriers come in a diversity of forms, including differences in habitat preference and reduced fitness of hybrids, all of which reduce the production of fertile offspring between lineages. The total of these barriers comprises reproductive isolation (RI) (Westram et al., 2022). As the strength of RI between lineages increases, gene flow is expected to decrease, thus further promoting lineage divergence. Because RI both reflects the extent of divergence between lineages and the likelihood of further divergence, quantifying RI has become central to studying speciation (Dobzhansky, 1937a).
Most studies have explored the role of RI in speciation by pursuing focused analyses in a single clade. These studies often result in numerical estimates of RI strength between specific pairs of lineages, along with metadata on the lineages (e.g., degree of ecological or genetic divergence) and a classification of RI components (e.g., habitat preference, hybrid sterility). Comparative work has synthesized estimates of RI from these studies, attempting to uncover more general patterns about the tempo and mode of RI evolution and its role in species diversification. For example, studies have shown that intrinsic postzygotic barriers can be particularly effective in limiting gene flow early in speciation (Coughlan & Matute, 2020), that ecological divergence predicts the extent of reproductive isolation (Funk et al., 2006), and that the rate of RI evolution does not predict macroevolutionary speciation rate variation in fruit flies or birds (Rabosky & Matute, 2013).
Comparative studies are still few in number and limited in scope, partially because comparative datasets on RI are scarce. Thus, it is unclear whether these findings will hold across more diverse sets of taxa, and many further questions about the role of RI in speciation remain unanswered. Filling these gaps requires datasets that compile standardised estimates of RI across a large and diverse set of taxa, but empirical estimates of RI are collected using multiple methods and approaches, at different levels of resolution, with terminology that varies across study systems. Synthesising across this heterogeneity is non-trivial because it requires 1) a standardised approach to estimating the strength of RI components that is comparable across different study designs and taxonomic groups; and 2) a standardised language for classifying these RI components to ensure equivalent barriers are compared. Sobel and Chen (2014) proposed a set of equations that allow RI component strength to be calculated and compared across diverse taxa (i.e., the RI4 index); these measures of RI have since been widely adopted. However, while various authors have developed their own schema to classify RI components across studies (e.g. (Lowry et al.,