scholarly journals Breakdown of gametophytic self-incompatibility in subdivided populations

2018 ◽  
Author(s):  
Thomas Brom ◽  
Vincent Castric ◽  
Sylvain Billiard
Keyword(s):  
Inbreeding Depression ◽  
Natural Populations ◽  
Simulation Models ◽  
Population Subdivision ◽  
Self Incompatibility ◽  
S Locus ◽  
Isolated Populations ◽  
Data Accessibility ◽  
Local Diversity ◽  
Subdivided Populations

AbstractMany hermaphroditic flowering plants species possess a genetic self-incompatibility (SI) system that prevents self-fertilization and is typically controlled by a single multiallelic locus, the S-locus. The conditions under which SI can be stably maintained in single isolated populations are well known and depend chiefly on the level of inbreeding depression and the number of SI alleles segregating at the S-locus. However, while both the number of SI alleles and the level of inbreeding depression are potentially affected by population subdivision, the conditions for the maintenance of SI in subdivided populations remain to be studied. In this paper, we combine analytical predictions and two different individual-based simulation models to show that population subdivision can severely compromise the maintenance of SI. Under the conditions we explored, this effect is mainly driven by the decrease of the local diversity of SI alleles rather than by a change in the dynamics of inbreeding depression. We discuss the implications of our results for the interpretation of empirical data on the loss of SI in natural populations.Data accessibility statementNo data to be archived

scholarly journals Hitch-hiking to a locus under balancing selection: high sequence diversity and low population subdivision at the S-locus genomic region in Arabidopsis halleri

2008 ◽  
Vol 90 (1) ◽  
pp. 37-46 ◽  
Author(s):  
MARIA VALERIA RUGGIERO ◽  
BERTRAND JACQUEMIN ◽  
VINCENT CASTRIC ◽  
XAVIER VEKEMANS
Keyword(s):  
Balancing Selection ◽  
Genomic Region ◽  
Population Subdivision ◽  
Herbaceous Plant ◽  
Self Incompatibility ◽  
S Locus ◽  
Arabidopsis Halleri ◽  
Subdivided Populations ◽  
Incompatibility Reaction ◽  
A Site

SummaryHitch-hiking to a site under balancing selection is expected to produce a local increase in nucleotide polymorphism and a decrease in population differentiation compared with the background genomic level, but empirical evidence supporting these predictions is scarce. We surveyed molecular diversity at four genes flanking the region controlling self-incompatibility (the S-locus) in samples from six populations of the herbaceous plant Arabidopsis halleri, and compared their polymorphism with sequences from five control genes unlinked to the S-locus. As a preliminary verification, the S-locus flanking genes were shown to co-segregate with SRK, the gene involved in the self-incompatibility reaction at the pistil level. In agreement with theory, our results demonstrated a significant peak of nucleotide diversity around the S-locus as well as a significant decrease in population genetic structure in the S-locus region compared with both control genes and a set of seven unlinked microsatellite markers. This is consistent with the theoretical expectation that balancing selection is increasing the effective migration rate in subdivided populations. Although only four S-locus flanking genes were investigated, our results suggest that these two signatures of the hitch-hiking effect are localized in a very narrow genomic region.

scholarly journals Balancing selection and the crossing of fitness valleys in structured populations: diversification in the gametophytic self-incompatibility system

2021 ◽  
Author(s):  
Roman Stetsenko ◽  
Thomas Brom ◽  
Vincent Castric ◽  
Sylvain Billiard
Keyword(s):  
Population Structure ◽  
Allelic Diversity ◽  
Structured Populations ◽  
The Self ◽  
Population Subdivision ◽  
Island Population ◽  
Single Mutation ◽  
Self Incompatibility ◽  
S Locus ◽  
Incompatibility Locus

The self-incompatibility locus (S-locus) of flowering plants displays a striking allelic diversity. How such a diversity has emerged remains unclear. In this paper, we performed numerical simulations in a finite island population genetics model to investigate how population subdivision affects the diversification process at a S-locus, given that the two-genes architecture typical of S-loci involves the crossing of a fitness valley. We show that population structure increases the number of self-incompatibility haplotypes (S-haplotypes) maintained in the whole metapopulation, but at the same time also slightly reduces the parameter range allowing for their diversification. This increase is partly due to a reinforcement of the diversification and replacement dynamics of S-haplotypes within and among demes. We also show that the two-genes architecture leads to a higher diversity compared with a simpler genetic architecture where new S-haplotypes appear in a single mutation step. We conclude that population structure helps explain the large allelic diversity at the self-incompatibility locus. Overall, our results suggest that population subdivision can act in two opposite directions: it makes easier S-haplotypes diversification but increases the risk that the SI system is lost.

Single Gene Control of Postzygotic Self-Incompatibility in Poke Milkweed, Asclepias exaltata L.

Genetics ◽  
2000 ◽  
Vol 154 (2) ◽  
pp. 893-907
Author(s):  
Sara R Lipow ◽  
Robert Wyatt
Keyword(s):  
Inbreeding Depression ◽  
Single Gene ◽  
Diallel Cross ◽  
Gene Control ◽  
Self Incompatibility ◽  
S Locus ◽  
Fertile Plant ◽  
Diallel Crosses ◽  
Prezygotic Barriers ◽  
Self Fertilization

Abstract Most individuals of Asclepias exaltata are self-sterile, but all plants lack prezygotic barriers to self-fertilization. To determine whether postzygotic rejection of self-fertilized ovules is due to late-acting self-incompatibility or to extreme, early acting inbreeding depression, we performed three diallel crosses among self-sterile plants related as full-sibs. The full-sibs segregated into four compatibility classes, suggesting that late acting self-incompatibility is controlled by a single gene (S-locus). Crosses between plants sharing one or both alleles at the S-locus are incompatible. An additional diallel cross was done among full-sib progeny from a cross of a self-sterile and a self-fertile plant. These progeny grouped into two compatibility classes, and plants within classes displayed varying levels of self-fertility. This suggests that the occasional self-fertility documented in natural pollinations is caused by pseudo-self-fertility alleles that alter the functioning of the S-locus.

scholarly journals Patterns of Inbreeding Depression and Architecture of the Load in Subdivided Populations

Genetics ◽  
2003 ◽  
Vol 165 (4) ◽  
pp. 2193-2212 ◽  
Author(s):  
Sylvain Glémin ◽  
Joëlle Ronfort ◽  
Thomas Bataillon
Keyword(s):  
Population Size ◽  
Effective Population Size ◽  
Inbreeding Depression ◽  
Local Population ◽  
Population Subdivision ◽  
Deleterious Mutations ◽  
Effective Population ◽  
Subdivided Populations ◽  
And Migration ◽  
Insight Into

AbstractInbreeding depression is a general phenomenon that is due mainly to recessive deleterious mutations, the so-called mutation load. It has been much studied theoretically. However, until very recently, population structure has not been taken into account, even though it can be an important factor in the evolution of populations. Population subdivision modifies the dynamics of deleterious mutations because the outcome of selection depends on processes both within populations (selection and drift) and between populations (migration). Here, we present a general model that permits us to gain insight into patterns of inbreeding depression, heterosis, and the load in subdivided populations. We show that they can be interpreted with reference to single-population theory, using an appropriate local effective population size that integrates the effects of drift, selection, and migration. We term this the “effective population size of selection” (NeS). For the infinite island model, for example, it is equal to NeS=N(1+m∕hs), where N is the local population size, m the migration rate, and h and s the dominance and selection coefficients of deleterious mutation. Our results have implications for the estimation and interpretation of inbreeding depression in subdivided populations, especially regarding conservation issues. We also discuss the possible effects of migration and subdivision on the evolution of mating systems.

scholarly journals Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction

2018 ◽  
Author(s):  
Jacqueline A. Robinson ◽  
Jannikke Räikkönen ◽  
Leah M. Vucetich ◽  
John A. Vucetich ◽  
Rolf O. Peterson ◽  
...  
Keyword(s):  
Inbreeding Depression ◽  
Natural Populations ◽  
Theory And Practice ◽  
Modern World ◽  
Fragmented Landscape ◽  
Isle Royale ◽  
Isolated Populations ◽  
Gray Wolves ◽  
Recessive Mutations ◽  
Genome Wide

AbstractThe observation that small, isolated populations often suffer reduced fitness as a result of inbreeding depression has guided conservation theory and practice for decades. However, investigating the genome-wide dynamics associated with inbreeding depression in natural populations is only now feasible with relatively inexpensive sequencing technology and annotated reference genomes. To characterize the genome-wide effects of intense inbreeding and isolation, we sequenced complete genomes from an iconic inbred population, the gray wolves (Canis lupus) of Isle Royale. Through comparison with other wolf genomes from a variety of demographic histories, we found that Isle Royale wolf genomes contain extensive runs of homozygosity, but neither the overall level of heterozygosity nor the number of deleterious variants per genome were reliable predictors of inbreeding depression. These findings are consistent with the hypothesis that severe inbreeding depression results from increased homozygosity of strongly deleterious recessive mutations, which are more prevalent in historically large source populations. Our results have particular relevance in light of the recently proposed reintroduction of wolves to Isle Royale, as well as broader implications for management of genetic variation in the fragmented landscape of the modern world.

On the evolution of genetic incompatibility systems. VI. A three-locus modifier model for the origin of gametophytic self-incompatibility.

Genetics ◽  
1991 ◽  
Vol 128 (2) ◽  
pp. 453-469
Author(s):  
M K Uyenoyama
Keyword(s):  
Inbreeding Depression ◽  
Genetic System ◽  
Rare Allele ◽  
Self Incompatibility ◽  
S Locus ◽  
Genetic Incompatibility ◽  
Genetic Determination ◽  
Modifier Locus ◽  
Coordinated Expression ◽  
Conventional Models

Abstract Recent genetic analyses have demonstrated that self-incompatibility in flowering plants derives from the coordinated expression of a system of loci. To address the selective mechanisms through which a genetic system of this kind evolves, I present a three-locus model for the origin of gametophytic self-incompatibility. Conventional models assume that a single locus encodes all physiological effects associated with self-incompatibility and that the viability of offspring depends only on whether they were derived by selfing or outcrossing. My model explicitly represents the genetic determination of offspring viability by a locus subject to symmetrically overdominant selection. Initially, the level of expression of the proto-S locus is insufficient to induce self-incompatibility. Weak gametophytic self-incompatibility arises upon the introduction of a rare allele at an unlinked modifier locus which enhances the expression of the proto-S locus. While conventional models predict that the origin of self-incompatibility requires at least two- to threefold levels of inbreeding depression, I find that the comparatively low levels of inbreeding depression generated by a single overdominant locus can ensure the invasion of an enhancer of self-incompatibility under sufficiently high rates of receipt of self-pollen. Associations among components of the incompatibility system promote the origin of self-incompatibility. Enhancement of heterozygosity at the initially neutral proto-S locus improves offspring viability through associative overdominance. Further, the modifier that enhances the expression of self-incompatibility develops a direct association with heterozygosity at the overdominant viability locus. These results suggest that the evolutionary processes by which incompatibility systems originate may differ significantly from those associated with their breakdown. The genetic mechanism explored here may apply to the evolution of other systems that restrict reproduction, including maternal-fetal incompatibility in mammals.

scholarly journals When gametophytic self-incompatibility meets gynodioecy

2008 ◽  
Vol 90 (1) ◽  
pp. 27-35 ◽  
Author(s):  
BODIL K. EHLERS ◽  
MIKKEL H. SCHIERUP
Keyword(s):  
Inbreeding Depression ◽  
Self Incompatibility ◽  
S Locus ◽  
Selfing Rate ◽  
Female Function ◽  
Fecundity Selection ◽  
Incompatibility System ◽  
S Alleles ◽  
Self Compatibility

SummaryThe occurrence of gynodioecy among angiosperms appears to be associated with self-compatibility. We use individual-based simulations to investigate the conditions for breakdown of a gametophytic self-incompatibility system in gynodioecious populations and make a comparison with hermaphroditic populations where the conditions are well known. We study three types of mutations causing self-compatibility. We track the fate of these mutations in both gynodioecious and hermaphroditic populations, where we vary the number of S-alleles, inbreeding depression and selfing rate. We find that the conditions for breakdown are less stringent if the population is gynodioecious and that the breakdown of self-incompatibility tends to promote stability of gynodioecious populations since it results in a higher frequency of females. We also find that fecundity selection has a large effect on the probability of breakdown of self-incompatibility, in particular if caused by a mutation destroying the female function of the S-locus.

scholarly journals Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction

2019 ◽  
Vol 5 (5) ◽  
pp. eaau0757 ◽  
Author(s):  
Jacqueline A. Robinson ◽  
Jannikke Räikkönen ◽  
Leah M. Vucetich ◽  
John A. Vucetich ◽  
Rolf O. Peterson ◽  
...  
Keyword(s):  
Inbreeding Depression ◽  
Natural Populations ◽  
Theory And Practice ◽  
Modern World ◽  
Fragmented Landscape ◽  
Isle Royale ◽  
Isolated Populations ◽  
Gray Wolves ◽  
Recessive Mutations ◽  
Genome Wide

The observation that small isolated populations often suffer reduced fitness from inbreeding depression has guided conservation theory and practice for decades. However, investigating the genome-wide dynamics associated with inbreeding depression in natural populations is only now feasible with relatively inexpensive sequencing technology and annotated reference genomes. To characterize the genome-wide effects of intense inbreeding and isolation, we performed whole-genome sequencing and morphological analysis of an iconic inbred population, the gray wolves (Canis lupus) of Isle Royale. Through population genetic simulations and comparison with wolf genomes from a variety of demographic histories, we find evidence that severe inbreeding depression in this population is due to increased homozygosity of strongly deleterious recessive mutations. Our results have particular relevance in light of the recent translocation of wolves from the mainland to Isle Royale, as well as broader implications for management of genetic variation in the fragmented landscape of the modern world.

scholarly journals Consistent scaling of inbreeding depression in space and time in a house sparrow metapopulation

2020 ◽  
pp. 201909599
Author(s):  
Alina K. Niskanen ◽  
Anna M. Billing ◽  
Håkon Holand ◽  
Ingerid J. Hagen ◽  
Yimen G. Araya-Ajoy ◽  
...  
Keyword(s):  
Inbreeding Depression ◽  
House Sparrow ◽  
Extinction Risk ◽  
Demographic History ◽  
Natural Populations ◽  
Ecological Factors ◽  
Genomic Tools ◽  
Subdivided Populations ◽  
Modern Genomic

Inbreeding may increase the extinction risk of small populations. Yet, studies using modern genomic tools to investigate inbreeding depression in nature have been limited to single populations, and little is known about the dynamics of inbreeding depression in subdivided populations over time. Natural populations often experience different environmental conditions and differ in demographic history and genetic composition, characteristics that can affect the severity of inbreeding depression. We utilized extensive long-term data on more than 3,100 individuals from eight islands in an insular house sparrow metapopulation to examine the generality of inbreeding effects. Using genomic estimates of realized inbreeding, we discovered that inbred individuals had lower survival probabilities and produced fewer recruiting offspring than noninbred individuals. Inbreeding depression, measured as the decline in fitness-related traits per unit inbreeding, did not vary appreciably among populations or with time. As a consequence, populations with more resident inbreeding (due to their demographic history) paid a higher total fitness cost, evidenced by a larger variance in fitness explained by inbreeding within these populations. Our results are in contrast to the idea that effects of inbreeding generally depend on ecological factors and genetic differences among populations, and expand the understanding of inbreeding depression in natural subdivided populations.

scholarly journals S-RNase Alleles Associated With Self-Compatibility in the Tomato Clade: Structure, Origins, and Expression Plasticity

2021 ◽  
Vol 12 ◽  
Author(s):  
Amanda K. Broz ◽  
Christopher M. Miller ◽  
You Soon Baek ◽  
Alejandro Tovar-Méndez ◽  
Pablo Geovanny Acosta-Quezada ◽  
...  
Keyword(s):  
Natural Populations ◽  
Reproductive Barriers ◽  
Self Incompatibility ◽  
S Locus ◽  
Loss Of Function ◽  
Resistance Factors ◽  
Tomato Species ◽  
Genes Encoding ◽  
Self Compatibility ◽  
Barrier Resistance

The self-incompatibility (SI) system in the Solanaceae is comprised of cytotoxic pistil S-RNases which are countered by S-locus F-box (SLF) resistance factors found in pollen. Under this barrier-resistance architecture, mating system transitions from SI to self-compatibility (SC) typically result from loss-of-function mutations in genes encoding pistil SI factors such as S-RNase. However, the nature of these mutations is often not well characterized. Here we use a combination of S-RNase sequence analysis, transcript profiling, protein expression and reproductive phenotyping to better understand different mechanisms that result in loss of S-RNase function. Our analysis focuses on 12 S-RNase alleles identified in SC species and populations across the tomato clade. In six cases, the reason for gene dysfunction due to mutations is evident. The six other alleles potentially encode functional S-RNase proteins but are typically transcriptionally silenced. We identified three S-RNase alleles which are transcriptionally silenced under some conditions but actively expressed in others. In one case, expression of the S-RNase is associated with SI. In another case, S-RNase expression does not lead to SI, but instead confers a reproductive barrier against pollen tubes from other tomato species. In the third case, expression of S-RNase does not affect self, interspecific or inter-population reproductive barriers. Our results indicate that S-RNase expression is more dynamic than previously thought, and that changes in expression can impact different reproductive barriers within or between natural populations.

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