An analysis of mating biases in trees

Assortative mating is a deviation from random mating based on phenotypic similarity. As it is much better studied in animals than in plants, we investigate for trees whether kinship of realized mating pairs deviates from what is expected from the set of potential mates and use this information to infer mating biases that may result from kin recognition and/or assortative mating. Our analysis covers 20 species of trees for which microsatellite data is available for adult populations (potential mates) as well as seed arrays. We test whether mean relatedness of observed mating pairs deviates from null expectations that only take pollen dispersal distances into account (estimated from the same data set). This allows the identification of elevated as well as reduced kinship among realized mating pairs, indicative of positive and negative assortative mating, respectively. The test is also able to distinguish elevated biparental inbreeding that occurs solely as a result of related pairs growing closer to each other from further assortativeness. Assortative mating in trees appears potentially common but not ubiquitous: nine data sets show mating bias with elevated inbreeding, nine do not deviate significantly from the null expectation, and two show mating bias with reduced inbreeding. While our data sets lack direct information on phenology, our investigation of the phenological literature for each species identifies flowering phenology as a potential driver of positive assortative mating (leading to elevated inbreeding) in trees. Since active kin recognition provides an alternative hypothesis for these patterns, we encourage further investigations on the processes and traits that influence mating patterns in trees.     

Variation in floral longevity in the genus Leptosiphon: mating system consequences

Pollination or fertilisation trigger floral senescence in a wide range of flowering plants, and yet little attention has been given to the implications of this phenomenon to mating system evolution. We examined the effects of pollination on floral senescence in the genus Leptosiphon. Species in the genus exhibit a wide range of breeding systems. In all cases, compatible pollination induced senescence; emasculated flowers lived longer than hand‐outcrossed flowers. In the self‐compatible species, Leptosiphon acicularis and L. bicolor, and in one highly selfing population of L. jepsonii, unmanipulated flowers had reduced longevity compared to emasculated flowers, suggesting that autonomous self‐pollination limits floral longevity in these species. Limited floral longevity in these highly selfing taxa may reduce opportunities for male outcross success, representing a possible source of selection on the mating system. In turn, the mating system might influence how selection acts on floral longevity; obligately outcrossing taxa are expected to benefit from longer floral longevities to maximise opportunities for pollination, while selfing taxa might benefit from earlier floral senescence to reduce resource expenditure. Overall, the longevity of unpollinated flowers increased with the level of outcrossing in the genus Leptosiphon. Our results taken together with those of a previous study and similar results in other species suggest that floral longevity may represent a largely unexamined role in mating system evolution.     

EVALUATING A SIMPLE APPROXIMATION TO MODELING THE JOINT EVOLUTION OF SELF‐FERTILIZATION AND INBREEDING DEPRESSION

A comprehensive understanding of plant mating system evolution requires detailed genetic models for both the mating system and inbreeding depression, which are often intractable. A simple approximation assuming that the mating system evolves by small infrequent mutational steps has been proposed. We examine its accuracy by comparing the evolutionarily stable selfing rates it predicts to those obtained from an explicit genetic model of the selfing rate, when inbreeding depression is caused by partly recessive deleterious mutations at many loci. Both models also include pollen limitation and pollen discounting. The approximation produces reasonably accurate predictions with a low or moderate genomic mutation rate to deleterious alleles, on the order of U = 0.02–0.2. However, for high mutation rates, the predictions of the full genetic model differ substantially from those of the approximation, especially with nearly recessive lethal alleles. This occurs because when a modifier allele affecting the selfing rate is rare, homozygous modifiers are produced mainly by selfing, which enhances the opportunity for purging nearly recessive lethals and increases the marginal fitness of the allele modifying the selfing rate. Our results confirm that explicit genetic models of selfing rate and inbreeding depression are required to understand mating system evolution.     

Male interference with pollination efficiency in a hermaphroditic orchid

Hermaphroditism can lead to both intra‐ and intersexual conflict between male and female gender functions. However, the effect that such gender conflicts have on pollination efficiency has seldom been investigated. By artificially reducing the number of available male gametes on an individual, we quantified whether male interference with pollination efficiency occurs in the self‐compatible, moth‐pollinated orchid Satyrium longicauda. We partially emasculated S. longicauda inflorescences and compared pollination success and fecundity in these plants to intact controls. Pollen in both groups of plants was colour‐labelled so that its dispersal by pollinators could be tracked directly in the field. Intact flowers on partially emasculated inflorescences exported more pollen and received more cross‐pollen and less self‐pollen than those on intact inflorescences. Proportion of fruit set per plant was similar between the two treatments; however, fruits on partially emasculated plants had proportionally more viable seeds than those on intact controls. These results provide empirical evidence that male interference with pollination efficiency can occur in a hermaphroditic plant and that such interference can compromise fecundity. The most likely mechanism for such male interference is competition for placement on the proboscis of hawkmoth pollinators. Consequently, male competition for siring success may influence the evolution of sexual systems in hermaphroditic pollinator‐dependent plants.     

Complex patterns of mating revealed in a Eucalyptus regnans seed orchard using allozyme markers and the neighbourhood model

The neighbourhood model apportions offspring of individual mother plants to self-fertilization, outcrossing to males within a circumscribed area around the mother plant (the neighbourhood), and outcrossing to males outside the neighbourhood. Formerly the model was applied only to haploid pollen gametes in the offspring of conifers, but is extended so that it can be used with genotypic data from diploid offspring of both angiosperms and gymnosperms. In addition, it is shown that the mating parameters can be estimated without independent estimates of allele frequencies in the pollen pools outside the neighbourhood; thus the model might be applied effectively to natural populations exposed to unknown external pollen sources. Parameters of the neighbourhood mating model were estimated for a 10-year-old seed orchard population of the insect-pollinated tree, Eucalyptus regnans, in southeast Australia, which contained a mixture of two geographical provenances (Victoria and Tasmania). The mating patterns revealed were complex. Crosses between trees of the same provenance occurred three times more often than crosses between trees of different provenances. Levels of self-fertilization and patterns of mating within neighbourhoods were influenced by provenance origin, crop fecundity and orchard position (central vs. edge) of mother trees. Gene dispersal, however, was extensive, with approximately 50% of effective pollen gametes coming from males more than 40 m away from mother trees (average distance between neighbouring trees was 7.4 m). Thus, insect pollinators are efficient promoters of cross-fertilization in this orchard, with the result that the effective number of males mating with each female is large.     

Increased selfing and correlated paternity in a small population of a predominantly outcrossing conifer, Pinus sylvestris

Outcrossing rate, the rates of ovule and seed abortion, and levels of correlated paternity were estimated in a small population of Pinus sylvestris, a predominantly outcrossing conifer, and were compared with estimates from two widely dispersed woodlands of the same species, showing a range of densities. On average, seed trees of the small population showed an eight-fold higher selfing rate (25 vs. 3%) and a 100-fold greater incidence of correlated paternity (19.6 vs. 0.2%) than did trees from the large populations. No evidence was found of pollen limitation within the remnant stand, as suggested by ovule abortion rates. Investigation of the mating patterns in the small population, based on the unambiguous genealogy of 778 open-pollinated seeds, showed a large departure from random mating. Only 8% of the possible mating pairs within the stand were observed. Correlated paternity rate within a maternal sibship was negatively associated (rs = -0.398, P < 0.050) with the distance to the nearest neighbour, and shared paternity among maternal sibships was negatively correlated (rs = -0.704, P < 0.001) with the distance between seed trees. Numerical simulations, based on the estimated individual pollen dispersal kernel, suggest that restricted dispersal might have been the key factor affecting mating patterns in the small population and, together with low population density, may account for the observed mating system variation between the small and the large populations. The results of this study show that a severe size reduction may substantially affect the mating system of a wind-pollinated, typically outcrossed plant species.     

Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. IV. Whole interindividual variance of male fecundity estimated jointly with the dispersal kernel

Interindividual variance of male reproductive success (MRS) contributes to genetic drift, which in turn interacts with selection and migration to determine the short-term response of populations to rapid changes in their environment. Individual relative MRS can be estimated through paternity analysis and can be further dissected into fecundity and spatial components. Existing methods to achieve this decomposition either rely on the strong assumption of a random distribution of pollen donors (TwoGener) or estimate only the part of the variance of male fecundity that is explained by few covariates. We developed here a method to estimate jointly the whole variance of male fecundity and the pollen dispersal curve from the genotypic information of sampled seeds and their putative fathers and geographical information of all individuals in the study area. We modelled the relative individual fecundities as a log-normally distributed random effect. We used a Bayesian approach, well suited to the hierarchical nature of the model, to estimate these fecundities. When applied to Sorbus torminalis , the estimated variance of male fecundity corresponded to an effective density of trees 13 times lower than the observed density ( d_obs / d_ep ~  13). This value is between the value ( ~ 2) estimated with a classical mating model including three covariates (neighbourhood density, diameter, flowering intensity) that affect fecundity and the value ( ~ 30) estimated with TwoGener. The estimated dispersal kernel was close to previous results. This approach allows fine monitoring of ongoing genetic drift in natural populations, and quantitative dissection of the processes contributing to drift, including human actions.     

Pollen transfer dynamics and the evolution of gametophytic self-incompatibility

Recent studies of mating system evolution have attempted to include aspects of pollination biology in analysis of both theoretical models and experimental systems. In light of this growing trend, we propose a simple population genetic model for the evolution of gametophytic self-incompatibility, incorporating parameters for pollen discounting and pollen export/capture. In this model, we consider several cases that span the spectrum for dominance of the mutant self-incompatibility allele and for the degree of incompatibility conferred by the allele. We confirm earlier results that inbreeding depression is required for successful invasion of the self-incompatibility allele and we demonstrate that, unless pollen discounting is very low, the level of inbreeding depression must be very high for an allele conferring self-incompatibility to become established. Finally, we show that the dominance of the mutant allele has a greater impact on the fate of a newly arisen self-incompatibility allele than the strength of the incompatibility conferred by the allele. In particular, the more recessive the self-incompatibility expression in heterozygote stigmas and the weaker the response induced, the easier it is for a self-incompatibility allele to invade.     

Genomic Signatures of Sexual Selection on Pollen-Expressed Genes in Arabis alpina

Fertilization in angiosperms involves the germination of pollen on the stigma, followed by the extrusion of a pollen tube that elongates through the style and delivers two sperm cells to the embryo sac. Sexual selection could occur throughout this process when male gametophytes compete for fertilization. The strength of sexual selection during pollen competition should be affected by the number of genotypes deposited on the stigma. As increased self-fertilization reduces the number of mating partners, and the genetic diversity and heterozygosity of populations, it should thereby reduce the intensity of sexual selection during pollen competition. Despite the prevalence of mating system shifts, few studies have directly compared the molecular signatures of sexual selection during pollen competition in populations with different mating systems. Here we analyzed whole-genome sequences from natural populations of Arabis alpina, a species showing mating system variation across its distribution, to test whether shifts from cross- to self-fertilization result in molecular signatures consistent with sexual selection on genes involved in pollen competition. We found evidence for efficient purifying selection on genes expressed in vegetative pollen, and overall weaker selection on sperm-expressed genes. This pattern was robust when controlling for gene expression level and specificity. In agreement with the expectation that sexual selection intensifies under cross-fertilization, we found that the efficacy of purifying selection on male gametophyte-expressed genes was significantly stronger in genetically more diverse and outbred populations. Our results show that intra-sexual competition shapes the evolution of pollen-expressed genes, and that its strength fades with increasing self-fertilization rates.     

DOES INTERFERENCE COMPETITION AMONG POLLEN GRAINS OCCUR IN WILD RADISH?

Interest in the possibility of sexual selection in plants has focused primarily on competition among pollen donors based on the speed of pollen-tube growth. However, when pollen arrives on stigmas, there is the opportunity for both races for access to ovules (exploitation competition) and interference with the germination and growth of pollen from other donors (interference competition). We considered whether this second form of competition might occur among pollen grains of wild radish in two experiments. In the first, interference likely occurred because the amount of pollen germination was less in mixed-donor than in single-donor pollinations. This result was duplicated in a second experiment, which also showed that interference occurred only when pollen grains from different donors were in direct contact with each other. In addition, in the second experiment, the opportunity for interference affected the frequency of seeds sired by different pollen donors. Because pollen loads are often mixed in nature, interference competition among pollen grains may be important in the ecology and evolution of plant reproduction.     

丹东蒲公英专性无融合生殖特性

采用田间去雄套袋、花粉活性与花粉管萌发观测等交配系统实验,辅以染色体分析、胚囊发育观察以及流式细胞仪检测,对丹东蒲公英(Taraxacum antungense)生殖特性进行系统研究。结果表明,去雄套袋情况下,结籽率高达96%,由此证明交配系统具有极高的无融合发生率;自花授粉不能萌发,花粉活性仅为20.6%,异花授粉虽可萌发,但生长缓慢,花粉在到达子房前,花粉管已停止生长并消失;二分体时期,合子端大孢子发育为功能性大孢子,珠孔端大孢子退化消失,经蓼型发育,形成7细胞8核,卵细胞继续发育形成原胚,中央细胞形成胚乳,其它细胞退化消失,花未开放前,已形成球形胚。此外,丹东蒲公英为三倍体。流式细胞仪检测结果表明,丹东蒲公英为专性无融合生殖,胚乳自主发育。综合以上研究结果,说明丹东蒲公英具专性无融合生殖特性。     

Pollen-size comparisons among animal-pollinated angiosperms with different pollination characteristics

Pollen volume varies among angiosperm species over five orders of magnitude, presumably because the functional advantages of pollen size depend on each species' particular pollination and fertilization conditions. This paper reports two studies that assess whether animal-pollinated species with different pollination systems differ correspondingly in pollen size, as would be expected if pollen size affected pollen transport. Analysis of nine Pedicularis species detected significant interspecific variation in pollen size; however, the overall mean pollen volume of species pollinated primarily by nectar-collecting bees did not differ significantly from that of species pollinated by pollen-collecting bees. Similarly, comparison of bee- and bird-pollinated congeners in 16 genera (nine families) from Australia and North America found considerable variation in pollen diameter within and between genera, but this variation was not associated consistency with differences in primary pollinator type (bee>bird for three genera, bee > bird for five genera, bee相似文献   

On the evolutionary costs of self-incompatibility: incomplete reproductive compensation due to pollen limitation

Pollen limitation affects plants with diverse reproductive systems and ecologies. In self-incompatible (SI) species, pollen limitation may preclude full reproductive compensation for prezygotic rejection of pollen. We present a model designed to explore the effects of incomplete reproductive compensation on evolutionary changes at a modifier locus that regulates the level of SI expression. Our results indicate that incomplete reproductive compensation greatly increases the evolutionary costs of SI, particularly in populations with low S-allele diversity. The evolutionary fate of modifiers of SI expression depends on the rate at which they are transmitted to future generations as well as the effects of SI on offspring number and quality. Partial SI expression can represent a stable condition rather than an evolutionarily transient state between full expression and full suppression. This unanticipated result provides the first theoretical support for the evolutionary stability of such mixed mating systems, the existence of which has recently been documented.     

Evaluating the influence of different aspects of habitat fragmentation on mating patterns and pollen dispersal in the bird-pollinated Banksia sphaerocarpa var. caesia

Habitat fragmentation can significantly affect mating and pollen dispersal patterns in plant populations, although the differential effects of the various aspects of fragmentation are poorly understood. In this study, we used eight microsatellite loci to investigate the effect of fragmentation on the mating system and pollen dispersal within one large and eight small population remnants of Banksia sphaerocarpa var. caesia, a bird-pollinated shrub in the southern agricultural region of Western Australia. The large population had a much larger neighbourhood size and lower selfing rate, maternal pollen pool differentiation and within-plot mean pollen dispersal distance than the small populations. Outcrossing was consistently high and ranged from 85.7% ± 2.6 to 98.5% ± 0.9, and mating patterns suggested nearest-neighbour pollination. Pollen immigration into small populations ranged from 2.8% ± 1.8 to 16.5% ± 3.2. Using the small populations, we tested for correlations between various fragmentation variables and mating system and pollen dispersal parameters. We found significant negative linear relationships between population isolation and outcrossing rate; population shape and neighbourhood size; and conspecific density and mean pollen dispersal distance. There were significant positive linear relationships between population shape and pollen pool differentiation and between population size and number of different fathers per seed crop. Our results suggest that birds may use a series of fragmented populations as a vegetation corridor while foraging across the landscape and that population connectivity is a critical determinant of pollinator visitation. Our results also suggest that the effect of a linear population shape on the mating system and pollen dispersal is routinely underestimated.     

Mating patterns and pollinator mobility are critical traits in forest fragmentation genetics

Most woody plants are animal-pollinated, but the global problem of habitat fragmentation is changing the pollination dynamics. Consequently, the genetic diversity and fitness of the progeny of animal-pollinated woody plants sired in fragmented landscapes tend to decline due to shifts in plant-mating patterns (for example, reduced outcrossing rate, pollen diversity). However, the magnitude of this mating-pattern shift should theoretically be a function of pollinator mobility. We first test this hypothesis by exploring the mating patterns of three ecologically divergent eucalypts sampled across a habitat fragmentation gradient in southern Australia. We demonstrate increased selfing and decreased pollen diversity with increased fragmentation for two small-insect-pollinated eucalypts, but no such relationship for the mobile-bird-pollinated eucalypt. In a meta-analysis, we then show that fragmentation generally does increase selfing rates and decrease pollen diversity, and that more mobile pollinators tended to dampen these mating-pattern shifts. Together, our findings support the premise that variation in pollinator form contributes to the diversity of mating-pattern responses to habitat fragmentation.     

Divergence in pollen performance between Clarkia sister species with contrasting mating systems supports predictions of sexual selection

Animal taxa that differ in the intensity of sperm competition often differ in sperm production or swimming speed, arguably due to sexual selection on postcopulatory male traits affecting siring success. In plants, closely related self‐ and cross‐pollinated taxa similarly differ in the opportunity for sexual selection among male gametophytes after pollination, so traits such as the proportion of pollen on the stigma that rapidly enters the style and mean pollen tube growth rate (PTGR) are predicted to diverge between them. To date, no studies have tested this prediction in multiple plant populations under uniform conditions. We tested for differences in pollen performance in greenhouse‐raised populations of two Clarkia sister species: the predominantly outcrossing C. unguiculata and the facultatively self‐pollinating C. exilis. Within populations of each taxon, groups of individuals were reciprocally pollinated (n = 1153 pollinations) and their styles examined four hours later. We tested for the effects of species, population, pollen type (self vs. outcross), the number of competing pollen grains, and temperature on pollen performance. Clarkia unguiculata exhibited higher mean PTGR than C. exilis; pollen type had no effect on performance in either taxon. The difference between these species in PTGR is consistent with predictions of sexual selection theory.