Evolution Of Self-compatibility Research Articles

Strong habitat and seasonal phenology effects on the evolution of self-compatibility, clonality and pollinator shifts in Lachenalia (Asparagaceae: Scilloideae).

Plants employ a diversity of reproductive safeguarding strategies to circumvent the challenge of pollen limitation. Focusing on southern African Lachenalia (Asparagaceae: Scilloideae), we test the hypothesis that the evolution of reproductive safeguarding traits (self-compatibility, autonomous selfing, bird pollination and clonal propagation) is favoured in species occupying conditions of low insect abundance imposed by critically infertile fynbos heathland vegetation and by flowering outside the austral spring insect abundance peak. We trace the evolution of these traits and selective regimes on a dated, multi-locus phylogeny of Lachenalia and assess their evolutionary associations using ordinary and phylogenetic regression. Ancestral state reconstructions identify an association with non-fynbos vegetation and spring flowering as ancestral in Lachenalia, the transition to fynbos vegetation and non-spring flowering taking place multiple times. They also show that self-compatibility, autofertility, bird pollination and production of multiple clonal offsets have evolved repeatedly. Regression models suggest that bird pollination and self-compatibility are selected for in fynbos and in non-spring flowering lineages, with autofertility being positively associated with non-spring flowering. These patterns support the interpretation of these traits as reproductive safeguarding adaptations under reduced insect pollinator abundance. We find no evidence to support the interpretation of clonal propagation as a reproductive safeguarding strategy.

Self-compatibility in yeast is selected for reproductive assurance not population-level compatibility.

In haploid species, sexual reproduction by selfing lacks the common benefits from recombination and is indistinguishable from asexual reproduction at the genetic level. Nevertheless, the evolution of self-compatibility, known as homothallism in organisms with mating types, has occurred hundreds of times in fungi. Two main hypotheses have been proposed for the evolution of homothallism. First, that homothallism offers reproductive assurance, which is especially important when species have an obligatory sexual phase in their lifecycle. Second, that homothallism is associated with population-level compatibility, increasing the chance of outbreeding. Here, we test these hypotheses using the fission yeast Schizosaccharomyces pombe, which is homothallic by mating-type switching, leveraging natural variation for switching efficiency in this species. Combining empirical tests with cellular automaton simulations, we show that homothallism by switching increases mating success of switching genotypes, but does not affect population-level compatibility. Experiments show that outcrossing is actually reduced under homothallism. This reduction in outcrossing is explained by our simulations, which show that due to local mating, gametes that mated through intraclonal selfing are no longer available for outcrossing. Our results suggest that the recurrent evolution of haploid self-compatibility is likely driven by selection for mating assurance, not to increase the potential for outcrossing.

Evolution of self-compatibility by a mutant Sm-RNase in citrus.

Self-incompatibility (SI) is an important mechanism that prevents self-fertilization and avoids inbreeding in flowering plants. The most widespread SI system utilizes S-ribonucleases (S-RNases) and S-locus F-boxes (SLFs) as S-determinants. In citrus, SI is ancestral; Citrus maxima (pummelo) is self-incompatible, while Citrus reticulata (mandarin) and its hybrids are self-compatible (SC). Here we identified nine highly polymorphic pistil-specific, developmentally expressed S-RNases from pummelo that segregate with S-haplotypes in a gametophytic manner and cluster with authentic S-RNases. We provide evidence that these S-RNases function as the female S-determinants in citrus. Moreover, we found that each S-RNase is linked to ~nine SLFs. Analysis of 117 citrus SLF/SLFL genes revealed clustering into 12 types and evidence that the S-RNases and intra-haplotypic SLFs/SLFLs co-evolved. Our data are consistent with citrus having an S-locus comprising a S-RNase and several SLFs that fit the non-self-recognition model. We identified a predominant single nucleotide mutation, Sm-RNase, in SC citrus, which provides a ‘natural’ loss of function. We present evidence that SI-SC transitions due to the Sm-RNase, initially arose in mandarin, spreading to its hybrids and became fixed. Identification of an evolutionarily distant new genus utilizing the S-RNase-based SI system, >100 million years separated from the nearest S-RNase family, is a milestone for evolutionary comparative studies.

Recent selection for self-compatibility in a population of Leavenworthia alabamica.

The evolution of self-compatibility (SC) is the first step in the evolutionary transition in plants from outcrossing enforced by self-incompatibility (SI) to self-fertilization. In the Brassicaceae, SI is controlled by alleles of two tightly linked genes at the S-locus. Despite permitting inbreeding, mutations at the S-locus leading to SC may be selected if they provide reproductive assurance and/or gain a transmission advantage in a population when SC plants self- and outcross. Positive selection can leave a genomic signature in the regions physically linked to the focus of selection when selection has occurred recently. From an SC population of Leavenworthia alabamica with a known nonfunctional mutation at the S-locus, we collected sequence data from a ∼690 Kb region surrounding the S-locus, as well as from regions not linked to the S-locus. To test for recent positive selection acting at the S-locus, we examined polymorphism and the site-frequency spectra. Using forward simulations, we demonstrate that recent selection of the strength expected for SC at a locus formerly under balancing selection can generate patterns similar to those seen in our empirical data.

Effects of pollen availability and the mutation bias on the fixation of mutations disabling the male specificity of self‐incompatibility

The evolution of self-compatibility (SC) by the loss of self-incompatibility (SI) is regarded as one of the most frequent transitions in flowering plants. SI systems are generally characterized by specific interactions between the male and female specificity genes encoded at the S-locus. Recent empirical studies have revealed that the evolution of SC is often driven by male SC-conferring mutations at the S-locus rather than by female mutations. In this study, using a forward simulation model, we compared the fixation probabilities of male vs. female SC-conferring mutations at the S-locus. We explicitly considered the effects of pollen availability in the population and bias in the occurrence of SC-conferring mutations on the male and female specificity genes. We found that male SC-conferring mutations were indeed more likely to be fixed than were female SC-conferring mutations in a wide range of parameters. This pattern was particularly strong when pollen availability was relatively high. Under such a condition, even if the occurrence of mutations was biased strongly towards the female specificity gene, male SC-conferring mutations were much more often fixed. Our study demonstrates that fixation probabilities of those two types of mutation vary strongly depending on ecological and genetic conditions, although both types result in the same evolutionary consequence-the loss of SI.

The Genetics of Self-Compatibility and Associated Floral Characters inTolpis(Asteraceae) in the Canary Islands

Members of the genus Tolpis (Asteraceae) endemic to the Canary Islands comprise a monophyletic group with the dispersal of one species to the Cape Verde Islands. Most species are self-incompatible or pseudo-self-compatible perennials. However, one species, Tolpis coronopifolia, consists of self-compatible annual plants with several floral features typical of the selfing syndrome. The evolution of self-compatibility and the selfing syndrome was studied by producing synthetic hybrids between self-incompatible/pseudo-self-compatible and self-compatible plants to determine the genetic architecture of breeding system and floral trait differences. There was a correlation between self-compatibility and selfing floral traits in the F2 generation. Self-incompatibility in Tolpis appears to be controlled by a locus of major effect but with modifier loci affecting seed set. Segregation of floral traits indicates that they are controlled by multiple loci. The high molecular similarity between plants with the two breeding systems suggests that divergence of the self-compatible T. coronopifolia from self-incompatible/pseudo-self-compatible ancestors has been recent. The association between breeding system and floral features likely results from pleiotropy or close linkage and may have facilitated the rapid evolution of the morphologically distinct self-compatible T. coronopifolia.

Plant sexual reproduction during climate change: gene function in natura studied by ecological and evolutionary systems biology

BackgroundIt is essential to understand and predict the effects of changing environments on plants. This review focuses on the sexual reproduction of plants, as previous studies have suggested that this trait is particularly vulnerable to climate change, and because a number of ecologically and evolutionarily relevant genes have been identified.ScopeIt is proposed that studying gene functions in naturally fluctuating conditions, or gene functions in natura, is important to predict responses to changing environments. First, we discuss flowering time, an extensively studied example of phenotypic plasticity. The quantitative approaches of ecological and evolutionary systems biology have been used to analyse the expression of a key flowering gene, FLC, of Arabidopsis halleri in naturally fluctuating environments. Modelling showed that FLC acts as a quantitative tracer of the temperature over the preceding 6 weeks. The predictions of this model were verified experimentally, confirming its applicability to future climate changes. Second, the evolution of self-compatibility as exemplifying an evolutionary response is discussed. Evolutionary genomic and functional analyses have indicated that A. thaliana became self-compatible via a loss-of-function mutation in the male specificity gene, SCR/SP11. Self-compatibility evolved during glacial–interglacial cycles, suggesting its association with mate limitation during migration. Although the evolution of self-compatibility may confer short-term advantages, it is predicted to increase the risk of extinction in the long term because loss-of-function mutations are virtually irreversible.ConclusionsRecent studies of FLC and SCR have identified gene functions in natura that are unlikely to be found in laboratory experiments. The significance of epigenetic changes and the study of non-model species with next-generation DNA sequencers is also discussed.

Extreme environments select for reproductive assurance: evidence from evening primroses (Oenothera)

Competing evolutionary forces shape plant breeding systems (e.g. inbreeding depression, reproductive assurance). Which of these forces prevails in a given population or species is predicted to depend upon such factors as life history, ecological conditions, and geographical context. Here, we examined two such predictions: that self-compatibility should be associated with the annual life history or extreme climatic conditions. We analyzed data from a clade of plants remarkable for variation in breeding system, life history and climatic conditions (Oenothera, sections Anogra and Kleinia, Onagraceae). We used a phylogenetic comparative approach and Bayesian or hybrid Bayesian tests to account for phylogenetic uncertainty. Geographic information system (GIS)-based climate data and ecological niche modeling allowed us to quantify climatic conditions. Breeding system and reproductive life span are not correlated in Anogra and Kleinia. Instead, self-compatibility is associated with the extremes of temperature in the coldest part of the year and precipitation in the driest part of the year. In the 60 yr since this pattern was anticipated, this is the first demonstration of a relationship between the evolution of self-compatibility and climatic extremes. We discuss possible explanations for this pattern and possible implications with respect to anthropogenic climate change.

Insights Gained From 50 Years of Studying the Evolution of Self-Compatibility in Leavenworthia (Brassicaceae)

The shift from outcrossing to selfing is one of the most common evolutionary trends in plants, and there is intense interest in why this is so. The genus Leavenworthia has been the focus of research on this question for half of a century, with particular attention paid to the evolution of self-compatibility from self-incompatibility. In this review, we discuss the last 50 years of research concerning this evolutionary transition in Leavenworthia. Selfing appears to have evolved independently at minimum three times within this genus of eight species. Work on the ecological basis of mating system evolution in Leavenworthia has clarified that selection among individuals is likely a major force behind the recurrent evolution of selfing. Although inadequate pollination is appreciated as a factor favoring selfing, definitive ecological mechanisms that act to favor selfing are still not known and future work on the efficacy of pollinating bees and the effects of climate change is needed. Recent research has likely identified the SRK ortholog at the S-locus controlling self-incompatibility in Leavenworthia alabamica. Analyses of S-locus variation have revealed substantial S-allele diversity in outcrossing populations, with the recurrent fixation of mutations at the S-locus permitting the parallel evolution of selfing in this species. Although we appreciate some of the factors that may explain the evolution of selfing in this group, there is less known about the mechanisms underlying the widespread maintenance of outcrossing at the population and species levels. Studies in Leavenworthia have revealed that genetic diversity is lost over the long-term within selfing populations and leads to elevated population subdivision, but work is needed to determine why these genetic consequences of selfing cause lineages to become evolutionary dead ends.

COMPARATIVE EVIDENCE FOR THE CORRELATED EVOLUTION OF POLYPLOIDY AND SELF-COMPATIBILITY IN SOLANACEAE

Breakdown of self-incompatibility occurs repeatedly in flowering plants with important evolutionary consequences. In plant families in which self-incompatibility is mediated by S-RNases, previous evidence suggests that polyploidy may often directly cause self-compatibility through the formation of diploid pollen grains. We use three approaches to examine relationships between self-incompatibility and ploidy. First, we test whether evolution of self-compatibility and polyploidy is correlated in the nightshade family (Solanaceae), and find the expected close association between polyploidy and self-compatibility. Second, we compare the rate of breakdown of self-incompatibility in the absence of polyploidy against the rate of breakdown that arises as a byproduct of polyploidization, and we find the former to be greater. Third, we apply a novel extension to these methods to show that the relative magnitudes of the macroevolutionary pathways leading to self-compatible polyploids are time dependent. Over small time intervals, the direct pathway from self-incompatible diploids is dominant, whereas the pathway through self-compatible diploids prevails over longer time scales. This pathway analysis is broadly applicable to models of character evolution in which sequential combinations of rates are compared. Finally, given the strong evidence for both irreversibility of the loss of self-incompatibility in the family and the significant association between self-compatibility and polyploidy, we argue that ancient polyploidy is highly unlikely to have occurred within the Solanaceae, contrary to previous claims based on genomic analyses.

Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene

Ever since Darwin's pioneering research, the evolution of self-fertilisation (selfing) has been regarded as one of the most prevalent evolutionary transitions in flowering plants. A major mechanism to prevent selfing is the self-incompatibility (SI) recognition system, which consists of male and female specificity genes at the S-locus and SI modifier genes. Under conditions that favour selfing, mutations disabling the male recognition component are predicted to enjoy a relative advantage over those disabling the female component, because male mutations would increase through both pollen and seeds whereas female mutations would increase only through seeds. Despite many studies on the genetic basis of loss of SI in the predominantly selfing plant Arabidopsis thaliana, it remains unknown whether selfing arose through mutations in the female specificity gene (S-receptor kinase, SRK), male specificity gene (S-locus cysteine-rich protein, SCR; also known as S-locus protein 11, SP11) or modifier genes, and whether any of them rose to high frequency across large geographic regions. Here we report that a disruptive 213-base-pair (bp) inversion in the SCR gene (or its derivative haplotypes with deletions encompassing the entire SCR-A and a large portion of SRK-A) is found in 95% of European accessions, which contrasts with the genome-wide pattern of polymorphism in European A. thaliana. Importantly, interspecific crossings using Arabidopsis halleri as a pollen donor reveal that some A. thaliana accessions, including Wei-1, retain the female SI reaction, suggesting that all female components including SRK are still functional. Moreover, when the 213-bp inversion in SCR was inverted and expressed in transgenic Wei-1 plants, the functional SCR restored the SI reaction. The inversion within SCR is the first mutation disrupting SI shown to be nearly fixed in geographically wide samples, and its prevalence is consistent with theoretical predictions regarding the evolutionary advantage of mutations in male components.

Ant Pollination of the Perennial Herb Blandfordia grandiflora (Liliaceae)

Blandfordia grandiflora plants are self-compatible, but do not self-pollinate autonomously. Worker ants of an unidentified Iridomyrmex sp. self-pollinated flowers. Seed-set was about 17%, which was significantly greater than autonomous self-pollination (< 1%), but less than experimental self-pollination (40%). Seed-set of emasculated flowers visited by ants was only 0.1%, indicating that ants do not cross-pollinate flowers. Differences in anther-stigma seperation did not affect seed-set ; seed-sets of flowers with exserted or included stigmas were 1% for autonomous self-pollination and 21% for ant-pollination treatments. Ants possessed thoracic metapleural glands, suggesting that antibiotic secretions that inhibit pollen function are produced. Although significantly fewer pollen grains germinated after thoracic contact compared to control pollen, the difference was only 6% (72.7% vs 78.7%). Seed-set of flowers that were cross-pollinated with pollen that either had been in contact with ants or had not did not differ significantly (78.3% vs 76.3%), suggesting that, if secretions are produced, they only marginally affect pollen function. Pollen loads of ants were small ; individual ants carried about 28 pollen grains, 50% of which were carried on the legs and, hence, away from potential metapleural gland secretions. Ants were observed more often on bagged flowers from which introduced honeybees were excluded than on unbagged flowers ; honeybees probably removed floral nectar from unbagged flowers before ants could recruit to them. In B. grandiflora, avian pollinators infreqeuntly visit flowers. By assuring reproduction, ant-mediated self-pollination may have been an important factor in the evolution of self-compatibility, and may have reduced selection for autonomous self-pollination.

Evolution of self-compatibility and racial differentiation in Leavenworthia (Cruciferae)

Evolution of self-compatibility and racial differentiation in Leavenworthia (Cruciferae)