Evolution Of Self-fertilization Research Articles

Fisher's automatic advantage of self-fertilization does not apply in cleistogamous species.

In hermaphroditic plants, the evolution of self-fertilization is driven by two major forces; the cost of outcrossing or Fisher's automatic advantage of selfing and inbreeding depression. Seminal theoretical works have established that an inbreeding depression threshold of 0.5 governs the evolution. Below that threshold, selfing evolves, above that, outcrossing evolves. Does this threshold apply to cleistogamous plants? I developed a model using a Lloydian approach to analyze the evolution of cleistogamy. I showed that the inbreeding depression threshold does not apply in cleistogamous species, and that because cleistogamous (closed) flowers do not export pollen, Fisher's advantage of selfing is totally cancelled. In line with model predictions, I discuss the fact that cleistogamous species often exhibit low inbreeding depression in empirical studies.

Rewiring the Sex-Determination Pathway During the Evolution of Self-Fertility.

Although evolution is driven by changes in how regulatory pathways control development, we know little about the molecular details underlying these transitions. The TRA-2 domain that mediates contact with TRA-1 is conserved in Caenorhabditis. By comparing the interaction of these proteins in two species, we identified a striking change in how sexual development is controlled. Identical mutations in this domain promote oogenesis in Caenorhabditis elegans but promote spermatogenesis in Caenorhabditis briggsae. Furthermore, the effects of these mutations involve the male-promoting gene fem-3 in C. elegans but are independent of fem-3 in C. briggsae. Finally, reciprocal mutations in these genes show that C. briggsae TRA-2 binds TRA-1 to prevent expression of spermatogenesis regulators. By contrast, in C. elegans TRA-1 sequesters TRA-2 in the germ line, allowing FEM-3 to initiate spermatogenesis. Thus, we propose that the flow of information within the sex determination pathway has switched directions during evolution. This result has important implications for how evolutionary change can occur.

Evolution of seed mass associated with mating systems in multiple plant families.

In flowering plants, the evolution of self‐fertilization (selfing) from obligate outcrossing is regarded as one of the most prevalent evolutionary transitions. The evolution of selfing is often accompanied by various changes in genomic, physiological and morphological properties. In particular, a set of reproductive traits observed typically in selfing species is called the “selfing syndrome”. A mathematical model based on the kinship theory of genetic imprinting predicted that seed mass should become smaller in selfing species compared with outcrossing congeners, as a consequence of the reduced conflict between maternally and paternally derived alleles in selfing plants. Here, we test this prediction by examining the association between mating system and seed mass across a wide range of taxa (642 species), considering potential confounding factors: phylogenetic relationships and growth form. We focused on three plant families—Solanaceae, Brassicaceae and Asteraceae—where information on mating systems is abundant, and the analysis was performed for each family separately. When phylogenetic relationships were controlled, we consistently observed that selfers (represented by self‐compatible species) tended to have a smaller seed mass compared with outcrossers (represented by self‐incompatible species) in these families. In summary, our analysis suggests that small seeds should also be considered a hallmark of the selfing syndrome, although we note that mating systems have relatively small effects on seed mass variation.

Ecological correlates and genetic consequences of evolutionary transitions from distyly to homostyly.

The outbreeding floral polymorphism heterostyly frequently breaks down, resulting in the evolution of self-fertilization as a result of homostyle formation. Here, the loss of floral polymorphism in distylous Primula oreodoxa, a sub-alpine species restricted to western Sichuan, China, was examined by investigating the ecological correlates and genetic consequences of mating system transitions. Several key questions were addressed. (1) What are the frequencies, geographical distribution and reproductive characteristics of floral morphs in distylous and homostylous populations? (2) Does increased elevation influence pollinator service and the likelihood of inbreeding in populations? (3) How often has homostyly originated and what are the consequences of the breakdown of distyly for the amounts and distribution of genetic diversity in populations? Fourteen populations throughout the range of P. oreodoxa were sampled, and morph frequencies and floral characteristics were recorded. Polymorphism at microsatellite loci and chloroplast DNA (cpDNA) variation were used to quantify population genetic structure and genetic relationships among populations. Controlled pollinations and studies of pollen tube growth and fertility were conducted to determine the compatibility status of populations and their facility for autonomous self-pollination. Finally, visitation rates of long- and short-tongued pollinators to distylous and homostylous populations at different elevations were compared to determine if increased elevation was associated with deterioration in pollinator service. In contrast to most heterostylous species, both distylous and homostylous morphs of P. oreodoxa are highly self-compatible, but only homostyles have the facility for autonomous self-pollination. Homostyles set significantly more fruit and seeds following open pollination than the distylous morphs. Visitation by long-tongued pollinators was significantly lower in homostylous populations, and overall rates of insect visitation decreased with elevation. Genetic diversity was significantly lower in homostylous populations, with evidence of increased inbreeding at higher elevation. Patterns of cpDNA variation were consistent with multiple transitions from distyly to homostyly and limited gene flow among populations. The results of this study support the hypothesis that the multiple loss of floral polymorphism in distylous P. oreodoxa is associated with unsatisfactory pollinator service, with homostyles benefiting from reproductive assurance as a result of autonomous self-pollination.

The demography and population genomics of evolutionary transitions to self-fertilization in plants.

The evolution of self-fertilization from outcrossing has occurred on numerous occasions in flowering plants. This shift in mating system profoundly influences the morphology, ecology, genetics and evolution of selfing lineages. As a result, there has been sustained interest in understanding the mechanisms driving the evolution of selfing and its environmental context. Recently, patterns of molecular variation have been used to make inferences about the selective mechanisms associated with mating system transitions. However, these inferences can be complicated by the action of linked selection following the transition. Here, using multilocus simulations and comparative molecular data from related selfers and outcrossers, we demonstrate that there is little evidence for strong bottlenecks associated with initial transitions to selfing, and our simulation results cast doubt on whether it is possible to infer the role of bottlenecks associated with reproductive assurance in the evolution of selfing. They indicate that the effects of background selection on the loss of diversity and efficacy of selection occur rapidly following the shift to high selfing. Future comparative studies that integrate explicit ecological and genomic details are necessary for quantifying the independent and joint effects of selection and demography on transitions to selfing and the loss of genetic diversity.

TRANSMISSION ADVANTAGE FAVORS SELFING ALLELE IN EXPERIMENTAL POPULATIONS OF SELF-INCOMPATIBLEWITHERINGIA SOLANACEA(SOLANACEAE)

The evolution of self-fertilization is one of the most commonly traversed transitions in flowering plants, with profound implications for population genetic structure and evolutionary potential. We investigated factors influencing this transition using Witheringia solanacea, a predominantly self-incompatible (SI) species within which self-compatible (SC) genotypes have been identified. We showed that self-compatibility in this species segregates with variation at the S-locus as inherited by plants in F1 and F2 generations. To examine reproductive assurance and the transmission advantage of selfing, we placed SC and SI genotypes in genetically replicated gardens and monitored male and female reproductive success, as well as selfing rates of SC plants. Self-compatibility did not lead to increased fruit or seed set, even under conditions of pollinator scarcity, and the realized selfing rate of SC plants was less than 10%. SC plants had higher fruit abortion rates, consistent with previous evidence showing strong inbreeding depression at the embryonic stage. Although the selfing allele did not provide reproductive assurance under observed conditions, it also did not cause pollen discounting, so the transmission advantage of selfing should promote its spread. Given observed numbers of S-alleles and selfing rates, self-compatibility should spread even under conditions of exceedingly high initial inbreeding depression.

The Capsella rubella genome and the genomic consequences of rapid mating system evolution

The shift from outcrossing to selfing is common in flowering plants, but the genomic consequences and the speed at which they emerge remain poorly understood. An excellent model for understanding the evolution of self fertilization is provided by Capsella rubella, which became self compatible <200,000 years ago. We report a C. rubella reference genome sequence and compare RNA expression and polymorphism patterns between C. rubella and its outcrossing progenitor Capsella grandiflora. We found a clear shift in the expression of genes associated with flowering phenotypes, similar to that seen in Arabidopsis, in which self fertilization evolved about 1 million years ago. Comparisons of the two Capsella species showed evidence of rapid genome-wide relaxation of purifying selection in C. rubella without a concomitant change in transposable element abundance. Overall we document that the transition to selfing may be typified by parallel shifts in gene expression, along with a measurable reduction of purifying selection.

Reduced Petal Size and Color Associated with Transitions from Outcrossing to Selfing inCamissoniopsis Cheiranthifolia(Onagraceae)

Floral traits used to attract and reward pollinators should become vestigial during the evolution of self-fertilization from outcrossing due to the reduced fitness benefits of investing in pollinator attraction. However, few traits have been studied, and covariation with outcrossing is rarely evaluated using genetic estimates of the mating system. We examined covariation between petal size and color and genetic estimates of outcrossing among populations of the yellow-flowered, bee-pollinated Camissoniopsis cheiranthifolia that exhibit striking variation in the mating system. We measured brightness, chroma, and hue, using a spectrophotometer, and petal size, using image analysis for flowers sampled in the field from 25 populations across the species’ geographic range. Petals were brighter with higher chroma and lower hue (less red) in large-flowered populations than in small-flowered populations. Petal size, brightness, and chroma also correlated positively with the proportion of seeds outcrossed estimated...

Physiological performance and mating system in Clarkia (Onagraceae): Does phenotypic selection predict divergence between sister species?

The evolution of self-fertilization often occurs in association with other floral, life history, and fitness-related traits. A previous study found that field populations of Clarkia exilis (a predominantly autogamous selfer) and its sister species, Clarkia unguiculata (a facultative outcrosser) differ in mean photosynthetic rates and instantaneous water use efficiency (WUE(i)). Here, we investigate the strength and direction of selection on these traits in multiple populations of each taxon to determine whether natural selection may contribute to the phenotypic differences between them. In spring 2008, we measured instantaneous gas exchange rates in nine populations during vegetative growth (Early) and/or during flowering (Late). We conducted selection gradient analyses and estimated selection differentials within populations and across pooled conspecific populations to evaluate the strength, direction, and consistency of selection on each trait early and late in the season. The direction and relative strength of selection on photosynthetic rates in these taxa corresponds to the phenotypic difference between them; C. exilis has higher photosynthetic rates than C. unguiculata, as well as stronger, more consistent selection favoring rapid photosynthesis throughout the growing season. Patterns of selection on transpiration, WUE(i), and the timing of flowering progression are less consistent with phenotypic differences (or lack thereof) between taxa. We detected several examples where selection was consistent with the phenotypic divergence between sister taxa, but there were also numerous instances that were equivocal or in which selection did not predict the realized phenotypic difference between taxa.

INCREASED FLORAL DIVERGENCE IN SYMPATRIC MONKEYFLOWERS

Sympatric sister species are predicted to have greater divergence in reproductive traits than allopatric sister species, especially if mating system shifts, such as the evolution of self-fertilization, are more likely to originate within the geographic range of the outcrossing ancestor. We present evidence that supports this expectation-sympatric sister species in the monkeyflower genus, Mimulus, exhibit greater divergence in flower size than allopatric sister species. Additionally, we find that sympatric sister species are more likely to have one species with anthers that overtop their stigmas than allopatric sister species, suggesting that the evolution of automatic self-pollination may contribute to this pattern. Potential mechanisms underlying this pattern include reinforcement and a stepping stone model of parapatric speciation.

Flower Development and the Evolution of Self-fertilization in Amsinckia: The Role of Heterochrony

We studied the development of 26 flower traits under natural conditions in three clades of the genus Amsinckia (Boraginaceae). Each clade contained both a derived highly self-fertilizing taxon and an ancestral more highly outcrossing taxon. The more outcrossing taxa contained two flower morphs—pins and thrums—with opposite positioning of the sex organs (heterostyly). The highly selfing taxa had smaller flowers with sex organs in close proximity (homostyly). Growth trajectories were quantified over the entire or nearly the entire period from primordium initiation to flower opening. These trajectories were compared in the heterochronic framework and, in contrast with previous studies, character size was tracked over time rather than relative to another character. We focused on three hypotheses: (1) The distinct developmental trajectories leading to pins and thrums should be similar in all clades, while the trajectories leading to homostylous flowers might differ among clades. This was supported. Specifically, contrasting growth rates of stamen and pistil heights in heterostylous flowers caused pin and thrum flowers to have the reciprocal arrangement of anther and stigma heights. From the viewpoint of heterochrony, the decreased size (paedomorphosis) of the homostylous morph, compared to pins and thrums, resulted from decreased growth rate (neoteny) and earlier offset (progenesis) in all clades. Nevertheless, multiple heterochronic processes were involved in the mosaic development and evolution of homostylous flowers. (2) We tested the hypothesis that small, self-fertilizing flowers have reduced development times, one of the proposed selective advantages of increased self-fertilization rates. We found in contrast that developmental duration of homostylous flowers was either the same (two clades) or longer (one clade) compared to duration of pins and thrums. (3) Finally, we tested von Baer’s Law, which proposes that developmental differences among closely related taxa should arise later in development than differences among more distantly related taxa. Von Baer’s Law was supported strongly among homostyles, moderately among thrums and weakly among pins.

Mixed mating in a recently derived self‐compatible population of Leavenworthia alabamica (Brassicaceae)

A mixture of outcrossing and selfing is often observed in plant populations. Although mixed mating is ubiquitous, it has several potential evolutionary explanations. Mixed mating may be actively maintained by selection, passively determined by the pollination environment, or a transitional stage during the evolution of self-fertilization. • We studied patterns of self-compatibility and selfing rates in a population of Leavenworthia alabamica that recently lost self-incompatibility. We also experimentally tested whether natural selection against selfing at the pre- or postzygotic stage is sufficient to explain mixed mating in this population. • Visualizing pollen tube growth following self-pollination, we found that nearly all plants were fully self-compatible. Progeny array analysis revealed that the average selfing rate of the population was s = 0.523. The inbreeding coefficient in the parents (F = 0.539) exceeded the amount expected if the selfing rate (s) were constant [F(eq) = s/(2 - s)], indicating either population subdivision or higher selfing rates in the past. Inference of family-level selfing rates revealed substantial variation. Experiments found that self and outcross pollen fertilized nearly equal numbers of ovules in competition. Comparison of seed production following self- or cross-pollination failed to implicate early acting inbreeding depression as a factor maintaining mixed mating. • The results of our experiments suggest that mixed mating is not maintained by selection against self-pollen or zygotes in this population. Mixed mating is most likely a byproduct of the pollination process but may also be a transitional stage during the evolution of higher selfing rates.

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.

The evolution of self-fertility in apomictic plants.

Self-fertilization and apomixis have often been seen as alternative evolutionary strategies of flowering plants that are advantageous for colonization scenarios and in bottleneck situations. Both traits have multiple origins, but different genetic control mechanisms; possible connections between the two phenomena have long been overlooked. Most apomictic plants, however, need a fertilization of polar nuclei for normal seed development (pseudogamy). If self-pollen is used for this purpose, self-compatibility is a requirement for successful pollen tube growth. Apomictic lineages usually evolve from sexual self-incompatible outcrossing plants, but pseudogamous apomicts frequently show a breakdown of self-incompatibility. Two possible pathways may explain the evolution of SC: (1) Polyploidy not only may trigger gametophytic apomixis, but also may result in a partial breakdown of SI systems. (2) Alternatively, frequent pseudo self-compatibility (PSC) via aborted pollen may induce selfing of pseudogamous apomicts (mentor effects). Self-fertile pseudogamous genotypes will be selected for within mixed sexual-apomictic populations because of avoidance of interploidal crosses; in founder situations, SC provides reproductive assurance independent from pollinators and mating partners. SI pseudogamous genotypes will be selected against in mixed populations because of minority cytotype problems and high pollen discounting; in founder populations, SI reactions among clone mates will reduce seed set. Selection for SC genotypes will eliminate SI unless the apomict maintains a high genotypic diversity and thus a diversity of S-alleles within a population, or shifts to pollen-independent autonomous apomixis. The implications of a breakdown of SI in apomictic plants for evolutionary questions and for agricultural sciences are being discussed.

Convergent Evolution: Regulatory Lightning Strikes Twice

Nematodes of the genus Caenorhabditis have evolved self-fertile hermaphrodites several times. Like Caenorhabditis elegans, C. briggsae has also recruited an F-box protein to regulate the sex determination gene tra-2 during the evolution of self-fertilization.

Modification of flower architecture during early stages in the evolution of self-fertilization.

The evolution of selfing from outcrossing is characterized by a series of morphological changes to flowers culminating in the selfing syndrome. However, which morphological traits initiate increased self-pollination and which are accumulated after self-fertilization establishes is poorly understood. Because the expression of floral traits may depend on the conditions experienced by an individual during flower development, investigation of changes in mating system should also account for environmental and developmental factors. Here, early stages in the evolution of self-pollination are investigated by comparing floral traits among Brazilian populations of Eichhornia paniculata (Pontederiaceae), an annual aquatic that displays variation in selfing rates associated with the breakdown of tristyly to semi-homostyly. Thirty-one Brazilian populations under uniform glasshouse conditions were compared to investigate genetic and environmental influences on flower size and stigma-anther separation (herkogamy), two traits that commonly vary in association with transitions to selfing. Within-plant variation in herkogamy was also examined and plants grown under contrasting environmental conditions were compared to examine to what extent this trait exhibits phenotypic plasticity. In E. paniculata a reduction in herkogamy is the principal modification initiating the evolution of selfing. Significantly, reduced herkogamy was restricted to the mid-styled morph and occurred independently of flower size. Significant genetic variation for herkogamy was detected among populations and families, including genotypes exhibiting developmental instability of stamen position with bimodal distributions of herkogamy values. Cloned genets exposed to contrasting growth conditions demonstrated environmental control of herkogamy and genotypic differences in plasticity of this trait. The ability to modify herkogamy independently of other floral traits, genetic variation in the environmental sensitivity of herkogamy, and the production of modified and unmodified flowers within some individuals, reveal the potential for dynamic control of the mating system in a species that commonly confronts heterogeneous aquatic environments.

Reproductive Evolution: Symptom of a Selfing Syndrome

In the nematode Caenorhabditis elegans, a single gene (plg-1) encodes the dominant protein found in mating plugs - a means of inhibiting multiple matings. Naturally occurring loss of plg-1 function results in males that fail to deposit mating plugs - a manifestation of relaxed sexual selection since the evolution of self-fertilization in this species.

MATING SYSTEM AND PLOIDY INFLUENCE LEVELS OF INBREEDING DEPRESSION IN CLARKIA (ONAGRACEAE)

Inbreeding depression is the reduction in offspring fitness associated with inbreeding and is thought to be one of the primary forces selecting against the evolution of self-fertilization. Studies suggest that most inbreeding depression is caused by the expression of recessive deleterious alleles in homozygotes whose frequency increases as a result of self-fertilization or mating among relatives. This process leads to the selective elimination of deleterious alleles such that highly selfing species may show remarkably little inbreeding depression. Genome duplication (polyploidy) has also been hypothesized to influence levels of inbreeding depression, with polyploids expected to exhibit less inbreeding depression than diploids. We studied levels of inbreeding depression in allotetraploid and diploid species of Clarkia (Onagraceae) that vary in mating system (each cytotype was represented by an outcrossing and a selfing species). The outcrossing species exhibited more inbreeding depression than the selfing species for most fitness components and for two different measures of cumulative fitness. In contrast, though inbreeding depression was generally lower for the polyploid species than for the diploid species, the difference was statistically significant only for flower number and one of the two measures of cumulative fitness. Further, we detected no significant interaction between mating system and ploidy in determining inbreeding depression. In sum, our results suggest that a taxon's current mating system is more important than ploidy in influencing levels of inbreeding depression in natural populations of these annual plants.

Natural variation in expression of self-incompatibility in Arabidopsis thaliana : Implications for the evolution of selfing

The switch from an out-crossing to a self-fertilizing mating system is one of the most prevalent evolutionary trends in plant reproduction and is thought to have occurred repeatedly in flowering plants. However, little is known about the evolution of self-fertility and the genetic architecture of selfing. Here, we establish Arabidopsis thaliana as a model for genetic analysis of the switch to self-fertility in the crucifer family, where the ancestral out-crossing mode of mating is determined by self-incompatibility (SI), a genetic system controlled by the S locus. We show that A. thaliana ecotypes exhibit S-locus polymorphisms and differ in their ability to express the SI trait upon transformation with S-locus genes derived from the obligate out-crosser Arabidopsis lyrata. Remarkably, at least one ecotype was reverted to a stable, self-incompatible phenotype identical to that of naturally self-incompatible species. These ecotype differences are heritable and reflect the fixation in different A. thaliana populations of independent mutations that caused or enforced the switch to self-fertility. Their continued analysis promises to identify the loci that were the targets of natural selection for selfing and to contribute to a mechanistic understanding of the SI response.

Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating.

The evolution of self-fertilization in hermaphrodites is opposed by costs that decrease the value of self progeny relative to that of outcross progeny. However, self-fertilization is common in plants; 20% are highly selfing and 33% are intermediate between selfing and outcrossing. Darwin proposed an adaptive benefit of self-pollination in providing reproductive assurance when outcrossing is impossible. Moreover, if outcross pollen receipt is inconsistent within or between years, these conditions likewise favour self-pollination, and this can result in a mixture of self and outcross seed production (mixed mating). Despite wide acceptance, the reproductive assurance hypothesis has lacked the support of complete empirical evidence to show that variable pollination can create both the ecological and genetic conditions favouring self-pollination. We recently showed in Collinsia verna that during periods of infrequent pollinator visits, autonomous self-pollination boosted seed output per flower, the key ecological condition. Here we show low inbreeding depression and marker-based estimates of selfing, demonstrating that when the pollination environment in wild populations necessitates reproductive assurance, selfing rates increase. We provide a complete demonstration of reproductive assurance under variable pollination environments and mechanistically link reproductive assurance to intermediate selfing rates through mixed mating.