Estimating the impact of divergent mating phenology between residents and migrants on the potential for gene flow

Gene flow between populations can allow the spread of beneficial alleles and genetic diversity between populations, with importance to conservation, invasion biology, and agriculture. Levels of gene flow between populations vary not only with distance, but also with divergence in reproductive phenology. Since phenology is often locally adapted, arriving migrants may be reproductively out of synch with residents, which can depress realized gene flow. In flowering plants, the potential impact of phenological divergence on hybridization between populations can be predicted from overlap in flowering schedules—the daily count of flowers capable of pollen exchange—between a resident and migrant population. The accuracy of this prospective hybridization estimate, based on parental phenotypes, rests upon the assumptions of unbiased pollen transfer between resident and migrant active flowers. We tested the impact of phenological divergence on resident–migrant mating frequencies in experiments that mimicked a single large gene flow event. We first prospectively estimated mating frequencies two lines of Brassica rapaselected or early and late flowering. We then estimated realized mating frequencies retrospectively through progeny testing. The two estimates strongly agreed in a greenhouse experiment, where procedures ensured saturating, unbiased pollination. Under natural pollination in the field, the rate of resident–migrant mating, was lower than estimated by phenological divergence alone, although prospective and retrospective estimates were correlated. In both experiments, differences between residents and migrants in flowering schedule shape led to asymmetric hybridization. Results suggest that a prospective estimate of hybridization based on mating schedules can be a useful, although imperfect, tool for evaluating potential gene flow. They also illustrate the impact of mating phenology on the magnitude and symmetry of reproductive isolation.     

Effect of snowmelt timing on the genetic structure of an <Emphasis Type="Italic">Erythronium grandiflorum</Emphasis> population in an alpine environment

In alpine environments, flowering phenology can differ within local populations even at the same elevation. We assessed the effects of differences in flowering phenology due to snowmelt timing caused by local geographic heterogeneity on the genetic structure of a population of an alpine plant, Erythronium grandiflorum Pursh. We established a study plot of 250×70 m at 3,340 m above sea level in the Front Range of the Rocky Mountains, CO, USA. The flowering phenology was considerably influenced by snowmelt timing due to local geographic heterogeneity. Twenty-two patches of E. grandiflorum were recognized in the study plot and were classified into three phenological groups: early, middle, and late. To express the differentiation of flowering phenology among the patches, we defined phenological distance and analyzed the relationship between genetic and phenological distances. Additionally, since genetic distance is expected to co-vary with geographic distance, we also analyzed the relationship between genetic distance and geographic distance among patches. The results revealed not only that isolation by distance was present among patches, but also that the differences in snowmelt timing gave rise to phenologically distant patches of E. grandiflorum, which in turn determine the genetic structure caused by the limited pollen flow between patches.     

Non-Density Dependent Pollen Dispersal of Shorea maxwelliana (Dipterocarpaceae) Revealed by a Bayesian Mating Model Based on Paternity Analysis in Two Synchronized Flowering Seasons

Pollinator syndrome is one of the most important determinants regulating pollen dispersal in tropical tree species. It has been widely accepted that the reproduction of tropical forest species, especially dipterocarps that rely on insects with weak flight for their pollination, is positively density-dependent. However differences in pollinator syndrome should affect pollen dispersal patterns and, consequently, influence genetic diversity via the mating process. We examined the pollen dispersal pattern and mating system of Shorea maxwelliana, the flowers of which are larger than those of Shorea species belonging to section Mutica which are thought to be pollinated by thrips (weak flyers). A Bayesian mating model based on the paternity of seeds collected from mother trees during sporadic and mass flowering events revealed that the estimated pollen dispersal kernel and average pollen dispersal distance were similar for both flowering events. This evidence suggests that the putative pollinators – small beetles and weevils – effectively contribute to pollen dispersal and help to maintain a high outcrossing rate even during sporadic flowering events. However, the reduction in pollen donors during a sporadic event results in a reduction in effective pollen donors, which should lead to lower genetic diversity in the next generation derived from seeds produced during such an event. Although sporadic flowering has been considered less effective for outcrossing in Shorea species that depend on thrips for their pollination, effective pollen dispersal by the small beetles and weevils ensures outcrossing during periods of low flowering tree density, as occurs in a sporadic flowering event.     

Limited pollen dispersal and biparental inbreeding in Symphonia globulifera in French Guiana

In this paper, we report a study of the mating system and gene flow of Symphonia globulifera, a hermaphroditic, mainly bird-pollinated tree species with a large geographic distribution in the tropical Americas and Africa. Using three microsatellites, we analysed 534 seeds of 28 open pollinated families and 164 adults at the experimental site 'Paracou' in French Guiana. We observed, compared to other tropical tree species, relatively high values for the effective number of alleles. Significant spatial genetic structure was detected, with trees at distances up to 150 m more genetically similar than expected at random. We estimated parameters of the mating system and gene flow by using the mixed mating model and the TwoGener approach. The estimated multilocus outcrossing rate, tm, was 0.920. A significant level of biparental inbreeding and a high proportion of full-sibs were estimated for the 28 seed arrays. We estimated mean pollen dispersal distances between 27 and 53 m according to the dispersal models used. Although the adult population density of S. globulifera in Paracou was relatively high, the joint estimation of pollen dispersal and density of reproductive trees gave effective density estimates of 1.6 and 1.3 trees/ha. The parameters of the mating system and gene flow are discussed in the context of spatial genetic and demographic structures, flowering phenology and pollinator composition and behaviour.     

Mating patterns and contemporary gene flow by pollen in a large continuous and a small isolated population of the scattered forest tree Sorbus torminalis

The influence of population size and spatial isolation on contemporary gene flow by pollen and mating patterns in temperate forest trees are not well documented, although they are crucial factors in the life history of plant species. We analysed a small, isolated population and a large, continuous population of the insect-pollinated tree species Sorbus torminalis in two consecutive years. The species recently experienced increased habitat fragmentation due to altered forest management leading to forests with closed canopies. We estimated individual plant size, percentage of flowering trees, intensity of flowering, degree of fruiting and seed set per fruit, and we determined mating patterns, pollen flow distances and external gene flow in a genetic paternity analysis based on microsatellite markers. We found clear effects of small population size and spatial isolation in S. torminalis. Compared with the large, continuous population, the small and isolated population harboured a lower percentage of flowering trees, showed less intense flowering, lower fruiting, less developed seeds per fruit, increased selfing and received less immigrant pollen. However, the negative inbreeding coefficients (F(IS)) of offspring indicated that this did not result in inbred seed at the population level. We also show that flowering, fruiting and pollen flow patterns varied among years, the latter being affected by the size of individuals. Though our study was unreplicated at the factor level (i.e. isolated vs non-isolated populations), it shows that small and spatially isolated populations of S. torminalis may also be genetically isolated, but that their progeny is not necessarily more inbred.     

Flowering phenology, display size, and fruit set in an understory dioecious shrub, Aucuba japonica (Cornaceae)

I investigated the effects of display size and flowering phenology on fruit set in Aucuba japonica, an understory dioecious shrub pollinated by opportunistic insects. Natural variations in display size, flowering phenology, and fruit set were monitored in 1997. A hand-pollination experiment was also conducted to check whether pollen limitation was a factor in fruit set in the field. Increases in floral display size did not affect fruit set; the proportion of flowers that set fruit was almost constant irrespective of the total number of flowers per inflorescence, the total number of inflorescences per plant, and the total number of flowers per plant. The hand-pollination experiment showed that fruit set was not pollen limited despite the low mating probability that resulted from the combination of dioecism and the species' dependence on opportunistic pollinators. This was due, in part, to the fact that female flowers did not have a predetermined period of receptivity, but instead remained receptive until they received pollen. In contrast, flowering phenology did affect fruit set. Fruit set was most abundant when male and female flowering was most abundant. This suggests there was some degree of pollen limitation during the part of the flowering season when male flowers were scarce.     

Individual and Temporal Variation in Outcrossing Rates and Pollen Flow Patterns in Ceiba pentandra (Malvaceae: Bombacoidea)

Ceiba pentandra is a tropical tree with high rates of selfing in some populations. In mixed‐mating species, variation in selfing is due to changes in adult density or variability of incompatibility systems. The effect of spatial isolation and phenology on selfing rates and pollen flow distances was analyzed using microsatellites in a fragmented population of Ceiba pentandra, in southern Costa Rica. Adult trees within a heterogeneous landscape were classified as grouped or isolated. We compared selfing rates at the individual level, between isolation conditions and 2 yr (2007, 2009), which differed in the number of flowering individuals. Mixed mating was estimated in both years (t_m = 0.624–0.759). Trees mated predominantly by outcrossing, while only a few trees reproduced through selfing. Spatial isolation did not significantly affect outcrossing rates. The progeny of grouped trees was mostly sired by near‐neighbors (<1 km) and by long‐distance pollen flow events in isolated trees. A reduction in the number of flowering individuals in 2009 reduced near‐neighbor matings, increased selfing in grouped trees, and decreased the number of unsampled sires in the progeny. Comparing selfing rates on individuals that flowered in both reproductive periods suggests a flexible mating system. Variation in self‐fertilization rates in this population appears to depend on variation of individual traits, such as genetic variability in self‐incompatibility genes, but it is independent of landscape heterogeneity. In contrast, pollen flow distances depend on local tree density as bats concentrate their foraging between near individuals to maximize energy efficiency.     

Pollination ecology and inbreeding depression control individual flowering phenologies and mixed mating

We analyze evolution of individual flowering phenologies by combining an ecological model of pollinator behavior with a genetic model of inbreeding depression for plant viability. The flowering phenology of a plant genotype determines its expected daily floral display which, together with pollinator behavior, governs the population rate of geitonogamous selfing (fertilization among flowers on the same plant). Pollinators select plant phenologies in two ways: they are more likely to visit plants displaying more flowers per day, and they influence geitonogamous selfing and consequent inbreeding depression via their abundance, foraging behavior, and pollen carry‐over among flowers on a plant. Our model predicts two types of equilibria at stable intermediate selfing rates for a wide range of pollinator behaviors and pollen transfer parameters. Edge equilibria occur at maximal or minimal selfing rates and are constrained by pollinators. Internal equilibria occur between edge equilibria and are determined by a trade‐off between pollinator attraction to large floral displays and avoidance of inbreeding depression due to selfing. We conclude that unavoidable geitonogamous selfing generated by pollinator behavior can contribute to the common occurrence of stable mixed mating in plants.     

The effect of segregation of flowering time on fine-scale spatial genetic structure in an alpine-snowbed herb Primula cuneifolia

The flowering phenology of alpine-snowbed plants varies widely depending on the time of snowmelt. This variation may cause spatial and temporal heterogeneity in pollen dispersal, which in turn may influence genetic structure. We used spatial autocorrelation analyses to evaluate relative effect of segregation in flowering time and physical distance on fine-scale spatial genetic structure (SGS) of a snowbed herb Primula cuneifolia sampled in 10-m grids within a continuous snow patch (110 x 250 m) using nine allozyme loci. Although the individual flower lasts for 相似文献   

Testing the 'assortative mating' hypothesis on a variation maintenance mechanism for flowering time within a forest-floor population of Primula sieboldii

Flowering phenology and allozyme variation were studied to test the existence of positive assortative mating for flowering time in a natural population of Primula sieboldii E. Morren, a heterostylous perennial herb, consisting of approximately 180 genets in a deciduous forest. There was significant variation in flowering date among genets, but not between heterostylous morphs. The temporal order of the flowering time of genets was fairly constant for the two years of the study. The spatial heterogeneity of light availability at the study site was small during the flowering season of the species. In order to analyze the extent of genetic differentiation between early- and late-flowering genet groups, allozyme diversities were analyzed with 10 loci. The G_ST between the early- and late-flowering groups was not significantly different from zero. Evidence of positive assortative mating for flowering time was not detected. Prolongation of flowering duration due to pollen limitation may be one important factor preventing the genetic differentiation of early- and late-flowering groups by enhancing the overlap of flowering time among genets.     

Phenological match drives pollen‐mediated gene flow in a temporally dimorphic tree

• Variation in flowering phenology is common in natural populations, and is expected to be, together with inter‐mate distance, an important driver of effective pollen dispersal. In populations composed of plants with temporally separated sexual phases (i.e. dichogamous or heterodichogamous populations), pollen‐mediated gene flow is assumed to reflect phenological overlap between complementary sexual phases. In this study, we conducted paternity analyses to test this hypothesis in the temporally dimorphic tree Acer opalus.
• We performed spatially explicit analyses based on categorical and fractional paternity assignment, and included tree size, pair‐wise genetic relatedness and morph type as additional predictors. Because differences between morphs in flowering phenology may also influence pollination distances, we modelled separate pollen dispersal kernels for the two morphs.
• Extended phenological overlap between male and female phases (mainly associated with inter‐morph crosses) resulted in higher siring success after accounting for the effects of genetic relatedness, morph type and tree size, while reduced phenological overlap (mainly associated with intra‐morph crosses) resulted in longer pollination distances achieved. Siring success also increased in larger trees.
• Mating patterns could not be predicted by phenology alone. However, as heterogeneity in flowering phenology was the single morph‐specific predictor of siring success, it is expected to be key in maintaining the temporal dimorphism in A. opalus, by promoting not only a prevalent pattern of inter‐morph mating, but also long‐distance pollination resulting from intra‐morph mating events.

     

Pollination Biology of Distylous Rubiaceae in the Atlantic Rain Forest, SE Brazil

Abstract: Data on pollination biology constitute important clues for the comprehension of pollen flow and genetic differentiation in plant populations. Pollinator type, availability and behaviour may modify morphological and mating patterns in populations of typically distylous species. This study investigates the pollination biology of four distylous species of Rubiaceae in the Atlantic rain forest, SE Brazil. Data on flowering phenology, floral lifespan, stigmatic receptivity, pollen availability, nectar volume and concentration, and pollinator activity were collected. The species studied flower sequentially throughout the wet season, and produce terminal inflorescences which bear small, tubular, diurnal, nectariferous flowers. Despite these similarities, some of the species studied are pollinated by different groups of pollinators, probably due to their distribution, availability of flowers and corolla length. On the other hand, pollinator specificity does not seem to be so important for distylous species. Long mouthparts, like those of most of the recorded pollinators, may reach lower sexual organs and, together with the self- and intramorph-incompatibilities observed, be sufficient to perform legitimate pollination and maintain levels of intermorph mating.     

外来入侵植物意大利苍耳的传粉生态学特性

从开花物候、花粉活力、柱头可受性、传粉媒介、花粉散布距离、雄性、雌性功能以及繁育系统等方面系统地研究了意大利苍耳的传粉生态学特性,旨在为揭示该物种成功入侵的机理提供科学依据。研究结果显示:意大利苍耳种群的花期较长,雌花花期可达40d,雄花花期可达30d。其雄性和雌性功能都很强,意大利苍耳单株雄花序和花粉量分别高达3847个/株和37903037粒/株,单株雌花序和单株胚珠数高达3847个/株和7694枚/株,种群平均结实率高达80.59%,即平均每株个体能形成6200枚成熟的果实。花粉活力的日变化呈单峰型曲线,早晨和傍晚的花粉活力最低,14:00时的活力高达99%。雌蕊柱头一经伸出总苞即具有可受性,可受期长达7d,开花后的3—4d柱头的可受性最强。意大利苍耳为风媒传粉植物,在4.5km/h的微风条件下,其花粉的散布距离可达45m,大量的花粉集中分布在距花粉源0—20m的范围内,这对于往往高密度连片分布的意大利苍耳种群来说无疑是一种高效的传粉策略。意大利苍耳的交配系统灵活多样,盛花期自然结实率达到100%,套袋试验结果表明该植物自交亲和,自株自然授粉的结实率高达93%。表明较长的花期、大量的雌雄花序及花粉数量、较高的花粉活力、较长的柱头可授期、较远的花粉风媒散布距离、混合交配系统、以及较高的结实率是意大利苍耳繁殖成功的重要保障,也是其成功入侵的重要原因。     

On the potential strength and consequences for nonrandom gene flow caused by local adaptation in flowering time

Gene flow is generally considered a random process, that is the loci under consideration have no effect on dispersal success. Edelaar and Bolnick (Trends Ecol Evol, 27, 2012 659) recently argued that nonrandom gene flow could exert a significant evolutionary force. It can, for instance, ameliorate the maladaptive effects of immigration into locally adapted populations. I examined the potential strength for nonrandom gene flow for flowering time genes, a trait frequently found to be locally adapted. The idea is that plants that successfully export pollen into a locally adapted resident population will be a genetically biased subset of their natal population – they will have resident‐like flowering times. Reciprocally, recipients will be more migrant‐like than the resident population average. I quantified the potential for biased pollen exchange among three populations along a flowering time cline in Brassica rapa from southern California. A two‐generation line cross experiment demonstrated genetic variance in flowering time, both within and among populations. Calculations based on the variation in individual flowering schedules showed that resident plants with the most migrant‐like flowering times could expect to have up to 10 times more of the their flowers pollinated by immigrant pollen than the least migrant‐like. Further, the mean flowering time of the pollen exporters that have access to resident mates differs by up to 4 weeks from the mean in the exporters’ natal population. The data from these three populations suggest that the bias in gene flow for flowering time cuts the impact on the resident population by as much as half. This implies that when selection is divergent between populations, migrants with the highest mating success tend to be resident‐like in their flowering times, and so, fewer maladaptive alleles will be introduced into the locally adapting gene pool.     

High paternal diversity in the self-incompatible herb Arabidopsis halleri despite clonal reproduction and spatially restricted pollen dispersal

The number of sires fertilizing a given dam is a key parameter of the mating system in species with spatially restricted offspring dispersal, since genetic relatedness among maternal sibs determines the intensity of sib competition. In flowering plants, the extent of multiple paternity is determined by factors such as floral biology, properties of the pollen vector, selfing rate, spatial organization of the population, and genetic compatibility between neighbours. To assess the extent of multiple paternity and identify ecological factors involved, we performed a detailed study of mating patterns in a small population of a self-incompatible clonal herb, Arabidopsis halleri . We mapped and genotyped 364 individuals and 256 of their offspring at 12 microsatellite loci and jointly analysed the level of multiple paternity, pollen and seed dispersal, and spatial genetic structure. We found very low levels of correlated paternity among sibs ( P _full-sib = 3.8%) indicating high multiple paternity. Our estimate of the outcrossing rate was 98.7%, suggesting functional self-incompatibility. The pollen dispersal distribution was significantly restricted (mean effective pollen dispersal distance: 4.42 m) but long-distance successful pollination occurred and immigrating pollen was at most 10% of all pollination events. Patterns of genetic structure indicated little extent of clonal reproduction, and a low but significant spatial genetic structure typical for a self-incompatible species. Overall, in spite of restricted pollen dispersal, the multiple paternity in this self-incompatible species was very high, a result that we interpret as a consequence of high plant density and high pollinator service in this population.     

ASSORTATIVE MATING AND NATURAL SELECTION IN AN IRIS HYBRID ZONE

The phenology of different genotypes and the distribution of genetic variation among flowering plants and their progeny were examined to assess the levels of assortative mating and selection in a hybrid population of Iris. This study and a previous survey of RAPD nuclear markers and chloroplast markers indicate that the population consists of parental genotypes and recombinant hybrid genotypes that are similar to the parental species (I. fulva and I. brevicaulis), although lacking intermediate genotypes. Early in the season only I. fulva genotypes produced flowers, but as flowering in these plants decreased, the hybrid genotypes and I. brevicaulis genotypes began flowering, resulting in a 24-d period of coincidental flowering. The genotypic distribution of seeds produced during the period of flowering overlap contained a high frequency of intermediate genotypes that were not present in the adult generation. The degree of effective assortative mating was examined by comparing the observed progeny genotypic distributions with expected distributions from a mixed-mating model. The model included selfing and random outcrossing to the nearest plants that had pollen-bearing flowers on the day the recipient flower was receptive. The observed genotypic distribution of progeny from plants with I. brevicaulis chloroplast DNA (cpDNA) was not significantly different from the expected distribution. For I. fulva genotypes, however, there were higher than expected frequencies in the extreme genotypic classes, although intermediate genotypes were absent, indicating that these plants were preferentially mating with similar genotypes. Compared with the extreme genotypes, a larger proportion of the intermediate seed progeny produced were aborted, indicating that intermediate genotypes have lower viability. On the basis of the observed progeny genotypes and genetic disequilibria estimates for the adults and the progeny, there appears to be a pattern of effective asymmetrical mating in this population. This asymmetry is most likely due to pollen-style interactions that reduce the fertilization ability of genetically dissimilar pollen, or preferential abortion of genetically intermediate zygotes by I. fulva-like genotypes. The lack of any apparent discrimination by I. brevicaulis-like genotypes creates a directional exchange of nuclear genetic elements that will have implications for introgression and the evolution of hybrid genotypes.     

Positive effects of flower abundance and synchronous flowering on pollination success,and pollinia dispersal in rewardless Changnienia amoena (Orchidaceae)

Pollination success and pollen dispersal in natural populations depend on the spatial‐temporal variation of flower abundance. For plants that lack rewards for pollinators, pollination success is predicted to be negatively related to flower density and flowering synchrony. We investigated the relationships between pollination success and flower abundance and flowering synchrony, and estimated pollinia dispersal distance in a rewardless species, Changnienia amoena (Orchidaceae). The results obtained in the present study revealed that male pollination success was negatively influenced by population size but was positively affected by population density, whereas female pollination success was independent of both population size and density. Phenotypic analysis suggested that highly synchronous flowering was advantageous through total pollination success, which is in contrast to previous studies. These results indicate that pollination facilitation rather than competition for pollinator visits occurs in this rewardless plant. The median distance of pollinia dispersal was 11.5 m (mean distance = 17.5 m), which is comparable to that of other rewardless plants but longer than for rewarding plants. However, pollen transfer occured mainly within populations; pollen import was a rare event. Restricted gene flow by pollinia and seeds probably explains the previous population genetic reporting a high degree of genetic differentiation between populations. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 477–488.     

Direct and indirect assortative mating: a multivariate approach to plant flowering schedules

This paper develops methods to partition the phenotypic correlation between mates for a focal trait--the standard measure for assortative mating--into a direct component and additional indirect components. Indirect assortative mating occurs when a nonassorting trait is correlated within individuals to a directly assorting trait. Direct and indirect assortative mating is assessed for flowering phenology in Brassica rapa. The flowering time of pollen recipients (mothers) was strongly correlated (rho=0.67) to that of potential pollen donors (fathers). Similarly, recipients and donors were correlated for duration of their flowering periods (rho=0.32) and stem diameters (rho=0.52). A partitioning of between-mate correlations revealed direct assortative mating for flowering time and period duration. However, assortment for stem diameter is explained solely through its correlation to flowering time. Examination of standard quantitative genetic theory shows that indirect assortative mating inflates genetic variance in a focal trait and the genetic covariance between focal and phenotypically correlated traits.     

Patterns of pollen dispersal in a small population of the Canarian endemic palm (Phoenix canariensis)

The genetic diversity of small populations is greatly influenced by local dispersal patterns and genetic connectivity among populations, with pollen dispersal being the major component of gene flow in many plants species. Patterns of pollen dispersal, mating system parameters and spatial genetic structure were investigated in a small isolated population of the emblematic palm Phoenix canariensis in Gran Canaria island (Canary Islands). All adult palms present in the study population (n=182), as well as 616 seeds collected from 22 female palms, were mapped and genotyped at 8 microsatellite loci. Mating system analysis revealed an average of 5.8 effective pollen donors (N_ep) per female. There was strong variation in correlated paternity rates across maternal progenies (ranging from null to 0.9) that could not be explained by the location and density of local males around focal females. Paternity analysis revealed a mean effective pollen dispersal distance of ∼71 m, with ∼70% of effective pollen originating from a distance of <75 m, and 90% from <200 m. A spatially explicit mating model indicated a leptokurtic pollen dispersal kernel, significant pollen immigration (12%) from external palm groves and a directional pollen dispersal pattern that seems consistent with local altitudinal air movement. No evidence of inbreeding or genetic diversity erosion was found, but spatial genetic structure was detected in the small palm population. Overall, the results suggest substantial pollen dispersal over the studied population, genetic connectivity among different palm groves and some resilience to neutral genetic erosion and subsequently to fragmentation.