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Antagonism between local dispersal and self-incompatibility systems in a continuous plant population.

ABSTRACT: Many self-incompatible plant species exist in continuous populations in which individuals disperse locally. Local dispersal of pollen and seeds facilitates inbreeding because pollen pools are likely to contain relatives. Self-incompatibility promotes outbreeding because relatives are likely to carry incompatible alleles. Therefore, populations can experience an antagonism between these forces. In this study, a novel computational model is used to explore the effects of this antagonism on gene flow, allelic diversity, neighbourhood sizes, and identity by descent. I confirm that this antagonism is sensitive to dispersal levels and linkage. However, the results suggest that there is little to no difference between the effects of gametophytic and sporophytic self-incompatibility systems (GSI and SSI) on unlinked loci. More importantly, both GSI and SSI affect unlinked loci in a manner similar to obligate outcrossing without mating types. This suggests that the primary evolutionary impact of self-incompatibility systems may be to prevent selfing, and prevention of biparental inbreeding might be a beneficial side-effect.

SUBMITTER: Cartwright RA

PROVIDER: S-EPMC2743200 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Antagonism between local dispersal and self-incompatibility systems in a continuous plant population.

Cartwright Reed A RA

Molecular ecology 20090423 11

Many self-incompatible plant species exist in continuous populations in which individuals disperse locally. Local dispersal of pollen and seeds facilitates inbreeding because pollen pools are likely to contain relatives. Self-incompatibility promotes outbreeding because relatives are likely to carry incompatible alleles. Therefore, populations can experience an antagonism between these forces. In this study, a novel computational model is used to explore the effects of this antagonism on gene fl ...[more]

PMID: 19389171

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Project description:Frugivorous birds play an important role in seed dispersal. Alien plant species' seeds are dispersed by local birds in order to establish populations in new habitats. Alien plant species that produce fruits similar to that of native species have the potential to attract local birds, creating new mutualistic systems that are similar to the local ones. In autumn 2018 and 2019, we studied the seed dispersal systems of an alien plant species, Phytolacca americana, and a native species, Cayratia japonica, in a coastal seawall forest. Both plant species' fruit, frugivorous bird foraging behaviors, seed germination rates, and seedling microhabitats were examined to determine whether the alien species had a similar seed dispersal system to that of the native species. Our results showed that P. americana and C. japonica had similar fruit type, color, and ripening period. There was a positive correlation between the percentage rate of fruit ripening and the percentage rate of fruit missing for both plant species, indicating that local frugivorous birds have the potential to sufficiently disperse the alien seeds to enable its spread in the coastal seawall forest (simple linear regression, P. americana: β = 0.863 ± 0.017, R2 adj = 0.978, P < 0.01; C. japonica: β = 0.787 ± 0.034, R2 adj = 0.898, P < 0.01). Eleven bird species consumed the fruits of the alien species or native species during the study period. Similar results were shown across alien and native species in bird foraging behavior (feeding frequency, feeding duration and first stop distance) indicating that a similar seed dispersal relationship had been established between local frugivorous and both plant species. The alien plant had a higher number of fruits carried by birds, suggesting that P. americana had a slightly higher fruit consumption than that of C. japonica (t-test, P < 0.01). Alien plant seedlings grow more abundant in forest gap microhabitat (t-test, P < 0.01). Our results confirmed that bird digestion promotes seed germination success in both plant species. Our study suggests that in a narrow coastal seawall forest, alien plant species can successfully establish their populations by relying on similar seed dispersal systems as the local species.

Project description:Inbreeding in hermaphroditic plants can occur through two different mechanisms: biparental inbreeding, when a plant mates with a related individual, or self-fertilization, when a plant mates with itself. To avoid inbreeding, many hermaphroditic plants have evolved self-incompatibility (SI) systems which prevent or limit self-fertilization. One particular SI system-homomorphic SI-can also reduce biparental inbreeding. Homomorphic SI is found in many angiosperm species, and it is often assumed that the additional benefit of reduced biparental inbreeding may be a factor in the success of this SI system. To test this assumption, we developed a spatially-explicit, individual-based simulation of plant populations that displayed three different types of homomorphic SI. We measured the total level of inbreeding avoidance by comparing each population to a self-compatible population (NSI), and we measured biparental inbreeding avoidance by comparing to a population of self-incompatible plants that were free to mate with any other individual (PSI). Because biparental inbreeding is more common when offspring dispersal is limited, we examined the levels of biparental inbreeding over a range of dispersal distances. We also tested whether the introduction of inbreeding depression affected the level of biparental inbreeding avoidance. We found that there was a statistically significant decrease in autozygosity in each of the homomorphic SI populations compared to the PSI population and, as expected, this was more pronounced when seed and pollen dispersal was limited. However, levels of homozygosity and inbreeding depression were not reduced. At low dispersal, homomorphic SI populations also suffered reduced female fecundity and had smaller census population sizes. Overall, our simulations showed that the homomorphic SI systems had little impact on the amount of biparental inbreeding in the population especially when compared to the overall reduction in inbreeding compared to the NSI population. With further study, this observation may have important consequences for research into the origin and evolution of homomorphic self-incompatibility systems.

Dataset Information

Antagonism between local dispersal and self-incompatibility systems in a continuous plant population.

Publications

Antagonism between local dispersal and self-incompatibility systems in a continuous plant population.

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