Understanding the relative roles of intrinsic and extrinsic reproductive barriers, and their interplay within the geographic context of diverging taxa, remains an outstanding challenge in the study of speciation. We conducted a comparative analysis of reproductive isolation in California Jewelflowers (Streptanthus, s.l., Brassicaceae) by quantifying potential barriers to gene flow at multiple life history stages in 39 species pairs spanning five million years of evolutionary divergence. We quantified nine potential pre- and postzygotic barriers and explored patterns of reproductive isolation in relation to genetic distance. Intrinsic postzygotic isolation was initially weak, increased at intermediate genetic distances, and reached a threshold characterized by complete genetic incompatibility. Climatic niche differences were strong at shallow genetic distances, and species pairs with overlapping ranges showed slight but appreciable phenological isolation, highlighting the potential for ecological barriers to contribute to speciation. Geographic analyses suggest that speciation is not regionally allopatric in the California Jewelflowers, as recently diverged taxa occur in relatively close proximity and display substantial range overlap. Young pairs are characterized by incomplete intrinsic postzygotic isolation, suggesting that extrinsic barriers or fine-scale spatial segregation are more important early in the divergence process than genetic incompatibilities.

Speciation is driven by the evolution of reproductive isolating barriers that reduce, and ultimately prevent, substantial gene flow between lineages. Despite its central role in evolutionary biology, the process can be difficult to study because it proceeds differently among groups and may occur over long timescales. Due to this complexity, we typically rely on generalizations of empirical data to describe and understand the process. Previous reviews of reproductive isolation (RI) in flowering plants have suggested that prezygotic or extrinsic barriers generally have a stronger effect on reducing gene flow compared to postzygotic or intrinsic barriers. Past conclusions have rested on relatively few empirical estimates of RI; however, RI data have become increasingly abundant over the past 15 years. We analyzed data from recent studies quantifying multiple pre‐ and postmating barriers in plants and compared the strengths of isolating barriers across 89 taxa pairs using standardized RI metrics. Individual prezygotic barriers were on average stronger than individual postzygotic barriers, and the total strength of prezygotic RI was approximately twice that of postzygotic RI. These findings corroborate that ecological divergence and extrinsic factors, as opposed to solely the accumulation of genetic incompatibilities, are important to speciation and the maintenance of species boundaries in plants. Despite an emphasis in the literature on asymmetric postmating and postzygotic RI, we found that prezygotic barriers acted equally asymmetrically. Overall, substantial variability in the strengths of 12 isolating barriers highlights the great diversity of mechanisms that contribute to plant diversification.

Speciation occurs when reproductive barriers substantially reduce gene flow between lineages. Understanding how specific barriers contribute to reproductive isolation offers insight into the initial forces driving divergence and the evolutionary and ecological processes responsible for maintaining diversity. Here, we quantified multiple pre‐ and post‐pollination isolating barriers in a pair of closely related California Jewelflowers (Streptanthus, Brassicaceae) living in an area of sympatry. S. breweri and S. hesperidis are restricted to similar serpentine habitats; however, populations are spatially isolated at fine‐scales and rarely co‐occur in intermixed stands. Several intrinsic postzygotic barriers were among the strongest we quantified, yet, postzygotic barriers currently contribute little to overall reproductive isolation due to the cumulative strength of earlier‐acting extrinsic barriers, including spatial isolation, and flowering time and pollinator differences. Data from multiple years suggest that pre‐pollination barriers may have different strengths depending on annual environmental conditions. Similarly, crossing data suggest that the strength of intrinsic isolation may vary among different population pairs. Estimates of total reproductive isolation in S. breweri and S. hesperidis are robust to uncertainty and variability in individual barrier strength estimates, demonstrating how multiple barriers can act redundantly to prevent gene flow between close relatives living in sympatry.

Coexistence results from a complex suite of past and contemporary processes including biogeographic history, adaptation, ecological interactions and reproductive dynamics. Here we explore drivers of local micro-parapatry in which two closely related and reproductively isolated Streptanthus species (jewelflower, Brassicaceae) inhabit continuous or adjacent habitat patches and occur within seed dispersal range, yet rarely overlap in fine-scale distribution. We find some evidence for abiotic niche partitioning and local adaptation, however differential survival across habitats cannot fully explain the scarcity of coexistence. Competition may also reduce the fitness of individuals migrating into occupied habitats, yet its effects are insufficient to drive competitive exclusion. Experimental migrants suffered reduced seed production and seed viability at sites occupied by heterospecifics, and we infer that heterospecific pollen transfer by shared pollinators contributes to wasted gametes when the two congeners come into contact. A minority disadvantage may reduce effective colonization of patches already occupied by heterospecifics, even when habitat patches are environmentally suitable. Differential adaptation and resource competition have often been evoked as primary drivers of habitat segregation in plants, yet negative reproductive interactions—including reproductive interference and decreased fecundity among low-frequency migrants—may also contribute to non-overlapping distributions of related species along local tension zones.