Morning glory species co-occurrence is associated with asymmetrically decreased and cascading reproductive isolation

Abstract

Hybridization between species can affect the strength of the reproductive barriers that separate those species. Two extensions of this effect are (1) the expectation that asymmetric hybridization or gene flow will have asymmetric effects on reproductive barrier strength and (2) the expectation that local hybridization will affect only local reproductive barrier strength and could therefore alter within‐species compatibility. We tested these hypotheses in a pair of morning glory species that exhibit asymmetric gene flow from highly selfing Ipomoea lacunosa into mixed‐mating Ipomoea cordatotriloba in regions where they co‐occur. Because of the direction of this gene flow, we predicted that reproductive barrier strength would be more strongly affected in I. cordatotriloba than I. lacunosa. We also predicted that changes to reproductive barriers in sympatric I. cordatotriloba populations would affect compatibility with allopatric populations of that species. We tested these predictions by measuring the strength of a reproductive barrier to seed set across the species’ ranges. Consistent with our first prediction, we found that sympatric and allopatric I. lacunosa produce the same number of seeds in crosses with I. cordatotriloba, whereas crosses between sympatric I. cordatotriloba and I. lacunosa are more successful than crosses between allopatric I. cordatotriloba and I. lacunosa. This difference in compatibility appears to reflect an asymmetric decrease in the strength of the barrier to seed set in sympatric I. cordatotriloba, which could be caused by I. lacunosa alleles that have introgressed into I. cordatotriloba. We further demonstrated that changes to sympatric I. cordatotriloba have decreased its ability to produce seeds with allopatric populations of the same species, in line with our second prediction. Thus, in a manner analogous to cascade reinforcement, we suggest that introgression associated with hybridization not only influences between‐species isolation but can also contribute to isolation within a species.

Rapid evolution of post-zygotic reproductive isolation is widespread in Arctic plant lineages

“…In Capsella , different effective ploidy resulted in endosperm-based reproductive barriers ( Lafon-Placette et al , 2018 ). Rapid evolution of HSF has also been revealed among closely related species of Ipomoea ( Ostevik et al , 2020 ) and Clarkia ( Briscoe Runquist et al , 2014 ).…”

Against the Odds: Hybrid Zones between Mangrove Killifish Species with Different Mating Systems

“…While hard to disentangle from other reproductive barriers, the asymmetry in hybridization and backcrossing found here suggest that fertilization opportunities may have had a strong role in shaping the direction of gene flow between the mangrove killifish species. In addition to influencing the degree of reproductive isolation between sympatric species, asymmetrical introgression can also affect the reproductive compatibility within species between allopatric and sympatric populations, if the latter are experiencing asymmetrical introgression [71]. Further studies are needed to investigate whether the asymmetric gene flow of K. hermaphroditus genome into K. ocellatus in the hybrid zones has impacted the reproductive isolation between allopatric vs sympatric K. ocellatus populations.…”

The role of ecology and geography in the evolution of habitat isolation and sexual isolation among sister species of host-plant-specific insects

“…Another important aspect of the dynamics of population divergence and speciation, often underappreciated in theoretical studies but increasingly reported by empirical research, is that migration of individuals is commonly found to be asymmetrical between populations and species. This pattern is observed across multiple spatial scales and across taxa including plants [7,[22][23][24], fish [25][26][27], birds [28], and insects [29]. As well, meta-populations studies within species document general asymmetric migration patterns where the net movement of individuals between any two subpopulations is typically non-zero and where subpopulations vary in size in tandem with rates of immigrants/emigration.…”

“…Both Nosil and Yukilevich [10] and Kyogoku and Kokko [21] predict habitat isolation and sexual isolation could evolve within a single study system under reinforcing selection; however, neither model examined the effect of asymmetric migration on the evolvability of multiple prezygotic reproductive isolating mechanisms. Asymmetric migration within and between species is a common phenomenon across different taxa [22][23][24][25][26][27][28][29]. Therefore, we stress the need for both theoretical and empirical studies to test the generality of asymmetric reinforcement in driving the asymmetry in the direction of habitat isolation and sexual isolation.…”