The best of both worlds? A review of delayed selfing in flowering plants.

PREMISE OF STUDY: In a seminal body of theory, Lloyd showed that the fitness consequences of selfing will depend on its timing in anthesis. Selfing that occurs after opportunities for outcrossing or pollen dispersal can provide reproductive assurance when pollinators are limited and is expected to incur little cost, even when inbreeding depression is high. As a result, delayed selfing is often interpreted as a "best-of-both-worlds" mating system that combines the advantages of selfing and outcrossing. METHODS: We surveyed 65 empirical studies of delayed selfing, recording floral mechanisms and examining information on inbreeding depression, autofertility, and other parameters to test the support for delayed selfing as a best-of-both-worlds strategy. KEY RESULTS: Phylogenetic distribution of the diverse floral mechanisms suggests that some basic floral structures may predispose plant taxa to evolve delayed selfing. Delayed selfing appears to serve as a best-of-both-worlds strategy in some but not all species. While the capacity for autonomous selfing is often high, it is lower, in some cases, than in related species with earlier modes of selfing. In other delayed-selfers, low inbreeding depression and reduced investment in corollas and pollen suggest limited benefits from outcrossing. CONCLUSIONS: Despite a growing literature on the subject, experimental evidence for delayed selfing is limited and major gaps in knowledge remain, particularly with respect to the stability of delayed selfing and the conditions that may favor transitions between delayed and earlier selfing. Finally, we suggest a potential role of delayed selfing in facilitating transitions from self-incompatibility to selfing.

Global biogeography of mating system variation in seed plants.

Latitudinal gradients in biotic interactions have been suggested as causes of global patterns of biodiversity and phenotypic variation. Plant biologists have long speculated that outcrossing mating systems are more common at low than high latitudes owing to a greater predictability of plant-pollinator interactions in the tropics; however, these ideas have not previously been tested. Here, we present the first global biogeographic analysis of plant mating systems based on 624 published studies from 492 taxa. We found a weak decline in outcrossing rate towards higher latitudes and among some biomes, but no biogeographic patterns in the frequency of self-incompatibility. Incorporating life history and growth form into biogeographic analyses reduced or eliminated the importance of latitude and biome in predicting outcrossing or self-incompatibility. Our results suggest that biogeographic patterns in mating system are more likely a reflection of the frequency of life forms across latitudes rather than the strength of plant-pollinator interactions.

Interactions of hybridization and mating systems: a case study in Leptosiphon (Polemoniaceae).

PREMISE OF THE STUDY: The roles of hybridization and mating systems in the evolution of angiosperms have been well studied, but less work has focused on their interactions. Self-incompatible and self-compatible species often show asymmetry in heterospecific pollen rejection. Self-fertilization can preempt ovules before opportunities for hybridization. In turn, hybridization might affect mating system evolution through selection for selfing to avoid production of low fitness hybrids. • METHODS: AFLP and morphological analyses were used to test for hybrids in a contact zone between species with contrasting breeding systems. Crossing experiments examined the relative contributions to reproductive isolation of pollen-pistil interactions, timing of self-fertilization, and F1 viability and fertility. A diallel cross of siblings tested for an association between heterospecific incompatibility and S-genotype in the self-incompatible species. • KEY RESULTS: A low frequency of hybrids was detected in the contact zone. Pollen-pistil interactions were partially consistent with the SI × SC rule; some individuals of the self-incompatible species rejected heterospecific pollen, whereas the self-compatible species was fully receptive to it. In the selfing species, individuals with early selfing produced fewer hybrid progeny than did those with delayed self-compatibility when heterospecific pollen was applied after self-pollen. Viability of F1s was high but fertility was low. Variability in heterospecific pollen rejection was not related to S-genotype. • CONCLUSIONS: Both self-fertilization and self-incompatibility are associated with limits to hybridization at this site. The strong effect of timing of selfing on production of low fitness F1s suggests that hybridization might select for early selfing in this population.

Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation.

Reduced allocation to structures for pollinator attraction is predicted in selfing species. We explored the association between outcrossing and floral display in a broad sample of angiosperms. We used the demonstrated relationship to test for bias against selfing species in the outcrossing rate distribution, the shape of which has relevance for the stability of mixed mating. Relationships between outcrossing rate, flower size, flower number and floral display, measured as the product of flower size and number, were examined using phylogenetically independent contrasts. The distribution of floral displays among species in the outcrossing rate database was compared with that of a random sample of the same flora. The outcrossing rate was positively associated with the product of flower size and number; individually, components of display were less strongly related to outcrossing. Compared with a random sample, species in the outcrossing rate database showed a deficit of small floral display sizes. We found broad support for reduced allocation to attraction in selfing species. We suggest that covariation between mating systems and total allocation to attraction can explain the deviation from expected trade-offs between flower size and number. Our results suggest a bias against estimating outcrossing rates in the lower half of the distribution, but not specifically against highly selfing species.

Long-Term Nutrient Enrichment of an Oligotroph-Dominated Wetland Increases Bacterial Diversity in Bulk Soils and Plant Rhizospheres.

In nutrient-limited conditions, plants rely on rhizosphere microbial members to facilitate nutrient acquisition, and in return, plants provide carbon resources to these root-associated microorganisms. However, atmospheric nutrient deposition can affect plant-microbe relationships by changing soil bacterial composition and by reducing cooperation between microbial taxa and plants. To examine how long-term nutrient addition shapes rhizosphere community composition, we compared traits associated with bacterial (fast-growing copiotrophs, slow-growing oligotrophs) and plant (C3 forb, C4 grass) communities residing in a nutrient-poor wetland ecosystem. Results revealed that oligotrophic taxa dominated soil bacterial communities and that fertilization increased the presence of oligotrophs in bulk and rhizosphere communities. Additionally, bacterial species diversity was greatest in fertilized soils, particularly in bulk soils. Nutrient enrichment (fertilized versus unfertilized) and plant association (bulk versus rhizosphere) determined bacterial community composition; bacterial community structure associated with plant functional group (grass versus forb) was similar within treatments but differed between fertilization treatments. The core forb microbiome consisted of 602 unique taxa, and the core grass microbiome consisted of 372 unique taxa. Forb rhizospheres were enriched in potentially disease-suppressive bacterial taxa, and grass rhizospheres were enriched in bacterial taxa associated with complex carbon decomposition. Results from this study demonstrate that fertilization serves as a strong environmental filter on the soil microbiome, which leads to distinct rhizosphere communities and can shift plant effects on the rhizosphere microbiome. These taxonomic shifts within plant rhizospheres could have implications for plant health and ecosystem functions associated with carbon and nitrogen cycling.IMPORTANCE Over the last century, humans have substantially altered nitrogen and phosphorus cycling. Use of synthetic fertilizer and burning of fossil fuels and biomass have increased nitrogen and phosphorus deposition, which results in unintended fertilization of historically low-nutrient ecosystems. With increased nutrient availability, plant biodiversity is expected to decline, and the abundance of copiotrophic taxa is anticipated to increase in bacterial communities. Here, we address how bacterial communities associated with different plant functional types (forb, grass) shift due to long-term nutrient enrichment. Unlike other studies, results revealed an increase in bacterial diversity, particularly of oligotrophic bacteria in fertilized plots. We observed that nutrient addition strongly determines forb and grass rhizosphere composition, which could indicate different metabolic preferences in the bacterial communities. This study highlights how long-term fertilization of oligotroph-dominated wetlands could alter diversity and metabolism of rhizosphere bacterial communities in unexpected ways.

Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses?

BACKGROUND: How photosynthetic organelles, or plastids, were acquired by diverse eukaryotes is among the most hotly debated topics in broad scale eukaryotic evolution. The history of plastid endosymbioses commonly is interpreted under the "chromalveolate" hypothesis, which requires numerous plastid losses from certain heterotrophic groups that now are entirely aplastidic. In this context, discoveries of putatively algal genes in plastid-lacking protists have been cited as evidence of gene transfer from a photosynthetic endosymbiont that subsequently was lost completely. Here we examine this evidence, as it pertains to the chromalveolate hypothesis, through genome-level statistical analyses of similarity scores from queries with two diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana, and two aplastidic sister taxa, Phytophthora ramorum and P. sojae. RESULTS: Contingency tests of specific predictions of the chromalveolate model find no evidence for an unusual red algal contribution to Phytophthora genomes, nor that putative cyanobacterial sequences that are present entered these genomes through a red algal endosymbiosis. Examination of genes unrelated to plastid function provide extraordinarily significant support for both of these predictions in diatoms, the control group where a red endosymbiosis is known to have occurred, but none of that support is present in genes specifically conserved between diatoms and oomycetes. In addition, we uncovered a strong association between overall sequence similarities among taxa and relative sizes of genomic data sets in numbers of genes. CONCLUSION: Signal from "algal" genes in oomycete genomes is inconsistent with the chromalveolate hypothesis, and better explained by alternative models of sequence and genome evolution. Combined with the numerous sources of intragenomic phylogenetic conflict characterized previously, our results underscore the potential to be mislead by a posteriori interpretations of variable phylogenetic signals contained in complex genome-level data. They argue strongly for explicit testing of the different a priori assumptions inherent in competing evolutionary hypotheses.

Transient SI and the dynamics of self-incompatibility alleles: a simulation model and empirical test.

A stochastic computer simulation model was created to compare the combined effects of selection and genetic drift on the dynamics of S-alleles under full sporophytic self-incompatibility (SI) versus transient SI, a form of partial SI in which flowers become self-compatible as they age. S-alleles were lost more rapidly with transient than with full SI, as is expected with weakened frequency-dependent selection. Based on these results, equilibrium S-allele diversity is expected to be lower with partial SI for populations of comparable size and migration rates. Consistent with model results, a comparison of the proportion of incompatible crosses in full diallel experiments for a fully SI and a transiently SI species in the annual genus Leptosiphon suggests that S-allele diversity is lower in the partially SI species. Results of the simulation model indicate that the transmission advantage of self-fertilization can have complex effects on S-allele dynamics in partial SI systems.

The genetic basis of floral traits associated with mating system evolution in Leptosiphon (Polemoniaceae): an analysis of quantitative trait loci.

Mapping of quantitative trait loci (QTL) was used to investigate the genetic architecture of divergence in floral characters associated with the mating system, an important adaptive trait in angiosperms. Two species of Leptosiphon (Polemoniaceae), one strongly self-fertilizing (L. bicolor) and the other partially outcrossing (L. jepsonii), were crossed to produce F2 and both backcross progenies. For each crossing population, a linkage map was created using amplified fragment length polymorphism markers, and QTL were identified for several dimensions of floral size. For each of the five traits examined, three to seven QTL were detected, with independent datasets yielding congruent results in some but not all cases. The phenotypic effect of individual QTL was generally moderate. We estimated that many of the QTL were additive or showed dominance toward L. bicolor, whereas comparison of mean trait values for parental and cross progenies showed apparent overall dominance of L. jepsonii traits. Colocalization of QTL for different dimensions of floral size was consistent with high phenotypic correlations between floral traits. Substantial segregation distortion was observed in marker loci, the majority favoring alleles from the large-flowered parent. A low frequency of male sterility in the F2 population is consistent with the Dobzhansky-Muller model for the evolution of reproductive isolation.

Pollen competition as a unilateral reproductive barrier between sympatric diploid and tetraploid Chamerion angustifolium.

Speciation requires the evolution of barriers to gene exchange between descendant and progenitor populations. Cryptic reproductive barriers in plants arise after pollination but before fertilization as a result of pollen competition and interactions between male gametophytes and female reproductive tissues. We tested for such gametic isolation between the polyploid Chamerion angustifolium and its diploid progenitor by conducting single (diploid or tetraploid) and mixed ploidy (1 : 1 diploid and tetraploid) pollinations on both cytotypes and inferring siring success from paternity analysis and pollen-tube counts. In mixed pollinations, polyploids sired most (79%) of their own seeds as well as those of diploids (61%) (correcting for triploid block, siring success was 70% and 83%, respectively). In single donor pollinations, pollen tubes from tetraploids were more numerous than those from diploids at four different positions in each style and for both diploid and tetraploid pollen recipients. The lack of a pollen donor x recipient interaction indicates that the tetraploid siring advantage is a result of pollen competition rather than pollen-pistil interactions. Such unilateral pollen precedence results in an asymmetrical pattern of isolation, with tetraploids experiencing less gene flow than diploids. It also enhances tetraploid establishment in sympatric populations, by maximizing tetraploid success and simultaneously diminishing that of diploids through the production of inviable triploid offspring.

Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating.

Hermaphroditic individuals can produce both selfed and outcrossed progeny, termed mixed mating. General theory predicts that mixed-mating populations should evolve quickly toward high rates of selfing, driven by rapid purging of genetic load and loss of inbreeding depression (ID), but the substantial number of mixed-mating species observed in nature calls this prediction into question. Lower average ID reported for selfing than for outcrossing populations is consistent with purging and suggests that mixed-mating taxa in evolutionary transition will have intermediate ID. We compared the magnitude of ID from published estimates for highly selfing (r > 0.8), mixed-mating (0.2 ≤ r ≥ 0.8), and highly outcrossing (r < 0.2) plant populations across 58 species. We found that mixed-mating and outcrossing taxa have equally high average lifetime ID (δ= 0.58 and 0.54, respectively) and similar ID at each of four life-cycle stages. These results are not consistent with evolution toward selfing in most mixed-mating taxa. We suggest that prevention of purging by selective interference could explain stable mixed mating in many natural populations. We identify critical gaps in the empirical data on ID and outline key approaches to filling them.

A role for nonadaptive processes in plant genome size evolution?

Genome sizes vary widely among species, but comprehensive explanations for the emergence of this variation have not been validated. Lynch and Conery (2003) hypothesized that genome expansion is maladaptive, and that lineages with small effective population size (N(e)) evolve larger genomes than those with large N(e) as a consequence of the lowered efficacy of natural selection in small populations. In addition, mating systems likely affect genome size evolution via effects on both N(e) and the spread of transposable elements (TEs). We present a comparative analysis of the effects of N(e) and mating system on genome size evolution in seed plants. The dataset includes 205 species with monoploid genome size estimates (corrected for recent polyploidy) ranging from 2Cx = 0.3 to 65.9 pg. The raw data exhibited a strong positive relationship between outcrossing and genome size, a negative relationship between N(e) and genome size, but no detectable N(e)x outcrossing interaction. In contrast, phylogenetically independent contrast analyses found only a weak relationship between outcrossing and genome size and no relationship between N(e) and genome size. Thus, seed plants do not support the Lynch and Conery mechanism of genome size evolution. Further work is needed to disentangle contrasting effects of mating systems on the efficacy of selection and TE transmission.

Plant mating systems in a changing world.

There is increasing evidence that human disturbance can negatively impact plant-pollinator interactions such as outcross pollination. We present a meta-analysis of 22 studies involving 27 plant species showing a significant reduction in the proportion of seeds outcrossed in response to anthropogenic habitat modifications. We discuss the evolutionary consequences of disturbance on plant mating systems, and in particular whether reproductive assurance through selfing effectively compensates for reduced outcrossing. The extent to which disturbance reduces pollinator versus mate availability could generate diverse selective forces on reproductive traits. Investigating how anthropogenic change influences plant mating will lead to new opportunities for better understanding of how mating systems evolve, as well as of the ecological and evolutionary consequences of human activities and how to mitigate them.

Timing of self-compatibility, flower longevity, and potential for male outcross success in Leptosiphon jepsonii (Polemoniaceae).

When fertilization triggers flower senescence, early autonomous selfing may cause flowers to senesce before pollen has dispersed, discounting unused pollen. Selfing-induced flower senescence was examined in Leptosiphon jepsonii, a species that varies in the timing of self-compatibility. In field and greenhouse experiments, fertilization had a large effect on flower senescence; most outcrossed flowers senesced after 1 d whereas emasculated flowers lasted 2-5 d. In a comparison of inbred lines from three populations, longevity of autonomously selfed flowers of early self-compatible individuals was significantly less than that of late self-compatible individuals. In field experiments, autonomously selfed flowers were shorter-lived in a predominantly early-selfing population than in a predominantly late-selfing population. Pollen was available and viable beyond the first day of anthesis, suggesting that reductions in flower longevity caused by autonomous selfing could incur a cost to male outcross fitness. We argue that this effect is likely to be most pronounced under intermediate rates of pollinator visitation. Observed pollinator visitation rates ranged from 0.035-0.775 visits per flower per day, indicating a potential for selfing-induced flower senescence to incur pollen discounting in Leptosiphon jepsonii.

Phylogenetic evidence for a flower size and number trade-off.

The size and number of flowers displayed together on an inflorescence (floral display) influences pollinator attraction and pollen transfer and receipt, and is integral to plant reproductive success and fitness. Life history theory predicts that the evolution of floral display is constrained by trade-offs between the size and number of flowers and inflorescences. Indeed, a trade-off between flower size and flower number is a key assumption of models of inflorescence architecture and the evolution of floral display. Surprisingly, however, empirical evidence for the trade-off is limited. In particular, there is a lack of phylogenetic evidence for a trade-off between flower size and number. Analyses of phylogenetic independent contrasts (PICs) of 251 angiosperm species spanning 63 families yielded a significant negative correlation between flower size and flower number. At smaller phylogenetic scales, analyses of individual genera did not always find evidence of a trade-off, a result consistent with previous studies that have examined the trade-off for a single species or genus. Ours is the first study to support an angiosperm-wide trade-off between flower size and number and supports the theory that life history constraints have influenced the evolution of floral display.

Inbreeding depression and mixed mating in Leptosiphon jepsonii: a comparison of three populations.

BACKGROUND AND AIMS: Inbreeding depression is thought to play a central role in the evolution and maintenance of cross-fertilization. Theory indicates that inbreeding depression can be purged with self-fertilization, resulting in positive feedback for the selection of selfing. Variation among populations of Leptosiphon jepsonii in the timing and rate of self-fertilization provides an opportunity to study the evolution of inbreeding depression and mating systems. In addition, the hypothesis that differences in inbreeding depression for male and female fitness can stabilize mixed mating in L. jepsonii is tested. METHODS: In a growth room experiment, inbreeding depression was measured in three populations with mean outcrossing rates ranging from 0.06 to 0.69. The performance of selfed and outcrossed progeny is compared at five life history stages. To distinguish between self-incompatibility and early inbreeding depression, aborted seeds and unfertilized ovules were counted in selfed and outcrossed fruits. In one population, pollen and ovule production was quantified to estimate inbreeding depression for male and female fitness. KEY RESULTS: Both prezygotic barriers and inbreeding depression limited self seed set in the most outcrossing population. Cumulative inbreeding depression ranged from 0.297 to 0.501, with the lowest value found in the most selfing population. Significant inbreeding depression for early life stages was found only in the more outcrossing populations. Inbreeding depression was not significant for pollen or ovule production. CONCLUSIONS: The results provide modest support for the hypothesized relationship between inbreeding depression and mating systems. The absence of early inbreeding depression in the more selfing populations is consistent with theory on purging. Differences in male and female expression of inbreeding depression do not appear to stabilize mixed mating in L. jepsonii. The current estimates of inbreeding depression for L. jepsonii differ from those of previous studies, underscoring the effects of environmental variation on its expression.

MULTIPLE ORIGINS OF SELF-COMPATIBILITY IN LINANTHUS SECTION LEPTOSIPHON (POLEMONIACEAE): PHYLOGENETIC EVIDENCE FROM INTERNAL-TRANSCRIBED-SPACER SEQUENCE DATA.

Phylogenetic reconstruction based on sequence variation in the internal transcribed spacer (ITS) region of rDNA was used to investigate the evolutionary dynamics of homomorphic self-incompatibility in Linanthus section Leptosiphon (Polemoniaceae), a group of annual plant species. Hand-pollination experiments revealed that five species were self-incompatible and four were self-compatible. Optimization of breeding systems onto the tree resulting from maximum-likelihood analysis, with no assumptions made about the ancestral condition, indicated that self-incompatibility has been lost four times in this section. An alternative tree rearrangement conforming to the hypothesis of three losses of self-incompatibility did not have a significantly lower likelihood than the maximum-likelihood tree as determined by a paired-sites test, but all rearrangements resulting in fewer than three losses were statistically rejected. Linanthus bicolor, a selfing species, was found to be polyphyletic, with populations from different geographic regions occurring in three well-supported clades. Morphological similarity in these distinct lineages is likely to have resulted from convergent evolution of traits associated with self-fertilization. Selection for reproductive assurance is hypothesized to have played an important role in the recurrent transformations from self-incompatibility to selfing in this group of annual species.

Joining genetic linkage maps using a joint likelihood function.

We present an efficient method to join genetic maps derived from different crosses, which is especially appropriate for dominant markers. In contrast to the "JoinMap" algorithm, which estimates information about recombination in a given cross from the LOD values and then combines estimates among crosses assuming a binomial sampling distribution, we construct a joint likelihood function that combines information across all crosses, to obtain a joint estimate of recombination. Simulations indicated that the difference between these two approaches is small when codominant markers are used, but that the joint likelihood approach shows substantially improved estimates when dominant or a mixture of dominant and codominant markers are used. This is because the joint likelihood implicitly finds the optimal weights among different classes of data, while the former method does not accurately predict the information from crosses involving dominant markers. Application of our method is illustrated by the construction of a linkage map for Linanthus using both backcrosses and the F2 of a cross between Linanthus jepsonii and L. bicolor, assayed with amplified fragment length polymorphisms (AFLP).