Variation in reproductive isolation across a species range

Abstract

Reproductive isolation is often variable within species, a phenomenon that while largely ignored by speciation studies, can be leveraged to gain insight into the potential mechanisms driving the evolution of genetic incompatibilities. We used experimental greenhouse crosses to characterize patterns of reproductive isolation among three divergent genetic lineages of Campanulastrum americanum that occur in close geographic proximity in the Appalachian Mountains. Substantial, asymmetrical reproductive isolation for survival due to cytonuclear incompatibility was found among the lineages (up to 94% reduction). Moderate reductions in pollen viability, as well as cytoplasmic male sterility, were also found between some Mountain populations. We then compared these results to previously established patterns of reproductive isolation between these Mountain lineages and a fourth, widespread Western lineage to fully characterize reproductive isolation across the complete geographic and genetic range of C. americanum. Reproductive isolation for survival and pollen viability was consistent across studies, indicating the evolution of the underlying genetic incompatibilities is primarily determined by intrinsic factors. In contrast, reproductive isolation for germination was only found when crossing Mountain populations with the Western lineage, suggesting the underlying genetic incompatibility is likely influenced by environmental or demographic differences between the two lineages. Cytoplasmic male sterility was also limited in occurrence, being restricted to a handful of Mountain populations in a narrow geographic range. These findings illustrate the complexity of speciation by demonstrating multiple, independent genetic incompatibilities that lead to a mosaic of genetic divergence and reproductive isolation across a species range.

Reproductive isolation and the maintenance of species boundaries in two serpentine endemic Jewelflowers

“…). Similarly, population specific loci may be responsible for intrinsic incompatibility (Sweigart and Flagel ; Zuellig and Sweigart ), so crossing results from specific population pairs may not accurately extend to the species level, particularly when demographic or environmental interactions drive these outcomes (Barnard‐Kubow and Galloway ). The potentially transitory nature of isolating barriers (we observed prezygotic variability between years, and postzygotic variability across space), as well as possible error in empirical data used to calculate mean estimates of RI, motivated us to further explore the ramifications of barrier strength uncertainty using a bootstrapping approach.…”

Cytonuclear Genetic Incompatibilities in Plant Speciation

“…The plastid genetic distance seemed to determine the strength of the RI: even if the populations were in a narrow geographical area, hybrid fitness decreased more when hybrids originated from more genetically divergent populations [56]. The accelerated rate of plastome evolution, influencing plastid genetic distances between populations, drove the evolution and strength of PNI [28,55,56]. Male sterility was also observed among Mountain lineages of this species, with a probable cytoplasmic contribution [56].…”

“…RI was asymmetric and dependent on the direction of the crosses and backcrosses, for all the measured traits [41]. The plastid genetic distance seemed to determine the strength of the RI: even if the populations were in a narrow geographical area, hybrid fitness decreased more when hybrids originated from more genetically divergent populations [56]. The accelerated rate of plastome evolution, influencing plastid genetic distances between populations, drove the evolution and strength of PNI [28,55,56].…”

Parallel patterns of development between independent cases of hybrid seed inviability in Mimulus

“…2007; Case & Willis 2008; Martin & Willis 2010; Sicard et al . 2015; Barnard-Kubow & Galloway 2017; Zuellig & Sweigart 2018). Total reproductive isolation in these crosses was ~52% for both species pairs, and thus may represent a significant barrier to reproduction.…”