Pollen Precedence Research Articles

Pollen precedence in sexual Potentilla puberula and its role as a protective reproductive barrier against apomictic cytotypes.

Cross-pollination is a major factor determining the demographic dynamics of mixed-ploidy populations. Typically, rare cytotypes are suppressed due to reduced female fertility by losing gametes in heteroploid crosses (i.e., through minority cytotype exclusion). In species with reproductive differentiation into sexual and apomictic cytotypes, sexuals might be reproductively suppressed by apomicts (or transformed due to introgression of apomixis genes). Pollen precedence potentially acts as a post-pollination pre-fertilization barrier protecting sexuals against their apomictic counterparts. We estimated the role of pollen precedence as a barrier against cross-fertilization of tetraploid sexuals by penta- and heptaploid gametophytic apomicts in Potentilla puberula (Rosaceae) by means of controlled crosses, and inference of the paternity through DNA ploidy estimation of embryos. Individuals from five regions spanning an elevational and biogeographic gradient were used to account for the variation in the relative frequencies of reproductive modes across the study area. We tested (1) whether the application of heteroploid pollen (sexual × apomictic) causes a reduction of seed yield compared to homoploid crosses (sexual × sexual), and (2) if so, whether pollen precedence recovers the seed yield in simultaneous applications of pollen from sexuals and apomicts (mixed-ploidy). Seed yield was significantly lower in hetero- than in homoploid crosses. We found clear evidence for precedence of homoploid pollen, despite a 13% to 15% of embryos experienced a change in ploidy due to heteroploid fertilizations. Thus, our study indicates that pollen precedence operates as a barrier against intercytotype fertilization in P. puberula, promoting the integrity of the sexual cytotype and their co-existence with apomictic individuals.

Interspecific reproductive barriers between sympatric populations of wild tomato species (Solanum section Lycopersicon).

Interspecific reproductive barriers (IRBs) often prevent hybridization between closely related species in sympatry. In the tomato clade (Solanum section Lycopersicon), interspecific interactions between natural sympatric populations have not been evaluated previously. In this study, we assessed IRBs between members of the tomato clade from nine sympatric sites in Peru. Coflowering was assessed at sympatric sites in Peru. Using previously collected seeds from sympatric sites in Peru, we evaluated premating prezygotic (floral morphology), postmating prezygotic (pollen-tube growth), and postzygotic barriers (fruit and seed development) between sympatric species in common gardens. Pollen-tube growth and seed development were examined in reciprocal crosses between sympatric species. We confirmed coflowering of sympatric species at five sites in Peru. We found three types of postmating prezygotic IRBs during pollen-pistil interactions: (1) unilateral pollen-tube rejection between pistils of self-incompatible species and pollen of self-compatible species; (2) potential conspecific pollen precedence in a cross between two self-incompatible species; and (3) failure of pollen tubes to target ovules. In addition, we found strong postzygotic IRBs that prevented normal seed development in 11 interspecific crosses, resulting in seed-like structures containing globular embryos and aborted endosperm and, in some cases, overgrown endothelium. Viable seed and F1 hybrid plants were recovered from three of 19 interspecific crosses. We have identified diverse prezygotic and postzygotic IRBs that would prevent hybridization between sympatric wild tomato species, but interspecific hybridization is possible in a few cases.

Selection on plant male function genes identifies candidates for reproductive isolation of yellow monkeyflowers.

Understanding the genetic basis of reproductive isolation promises insight into speciation and the origins of biological diversity. While progress has been made in identifying genes underlying barriers to reproduction that function after fertilization (post-zygotic isolation), we know much less about earlier acting pre-zygotic barriers. Of particular interest are barriers involved in mating and fertilization that can evolve extremely rapidly under sexual selection, suggesting they may play a prominent role in the initial stages of reproductive isolation. A significant challenge to the field of speciation genetics is developing new approaches for identification of candidate genes underlying these barriers, particularly among non-traditional model systems. We employ powerful proteomic and genomic strategies to study the genetic basis of conspecific pollen precedence, an important component of pre-zygotic reproductive isolation among yellow monkeyflowers (Mimulus spp.) resulting from male pollen competition. We use isotopic labeling in combination with shotgun proteomics to identify more than 2,000 male function (pollen tube) proteins within maternal reproductive structures (styles) of M. guttatus flowers where pollen competition occurs. We then sequence array-captured pollen tube exomes from a large outcrossing population of M. guttatus, and identify those genes with evidence of selective sweeps or balancing selection consistent with their role in pollen competition. We also test for evidence of positive selection on these genes more broadly across yellow monkeyflowers, because a signal of adaptive divergence is a common feature of genes causing reproductive isolation. Together the molecular evolution studies identify 159 pollen tube proteins that are candidate genes for conspecific pollen precedence. Our work demonstrates how powerful proteomic and genomic tools can be readily adapted to non-traditional model systems, allowing for genome-wide screens towards the goal of identifying the molecular basis of genetically complex traits.

COMPONENTS OF REPRODUCTIVE ISOLATION BETWEEN ORCHIS MASCULA AND ORCHIS PAUCIFLORA

Studies of the strength and nature of reproductive isolation (RI) between species can greatly contribute to our understanding of speciation. Although the role of RI in speciation is well recognized, there is a dearth of information on the contributions of different barriers between related plant species. Here, we estimated multiple components of RI between two Mediterranean orchid sister species (Orchis mascula and Orchis pauciflora), disentangling the strength and absolute contributions of seven different isolating mechanisms. Our survey includes one prepollination, two postpollination prezygotic (pollen-stigma incompatibility, conspecific pollen precedence), two intrinsic postzygotic (embryo mortality and hybrid sterility) and two extrinsic postzygotic (hybrid habitat differentiation and hybrid pollination) isolating mechanisms. We found strong RI between the investigated species, although none of the barriers were able to completely impede gene flow. Five isolating mechanisms contributed positively to the maintenance of species boundaries. Contrary to most surveys of isolating mechanisms, our data speak against a clear predominance of prepollination or of prezygotic barriers but confirm the emerging pattern of multiple barriers contributing to the maintenance of species integrity. These findings suggest an allopatric condition during early phases of species divergence. We discuss our data in the wider context of previous studies carried out in this orchid group by using a comparative approach.

Strength and variability of postmating reproductive isolating barriers between four European white oak species

The identification and quantification of the relative importance of reproductive isolating barriers is of fundamental importance to understand species maintenance in the face of interspecific gene flow between hybridising species. Yet, such assessments require extensive experimental fertilisations that are particularly difficult when dealing with more than two hybridising and long-generation-time species such as oaks. Here, we quantify the relative contribution of four postmating reproductive isolating barriers consisting of two prezygotic barriers (gametic incompatibility, conspecific pollen precedence) and two postzygotic barriers (germination rate, early survival) from extensively controlled pollinations between four oak species (Quercus robur, Quercus petraea, Quercus pubescens and Quercus pyrenaica) that have been shown to frequently hybridise in natural populations. We found high variation in the strength of total reproductive isolation between species, ranging from total reproductive isolation to advantage toward hybrid formation. As previously found, Q. robur pollen was unable to fertilise Q. petraea due to a strong reproductive isolating mechanism. On the contrary, Q. pubescens pollen was more efficient at fertilising Q. petraea than conspecific pollen. Overall, prezygotic barriers contribute far more than postzygotic barriers to isolate species reproductively, suggesting a role for reinforcement in the development of prezygotic barriers. Conspecific pollen precedence reduced hybrid formation when pollen competition was allowed; however, presence of conspecific pollen did not totally prevent hybridization. Our results suggest that pollen competition depends on multiple ecological and environmental parameters, including species local abundance, and that it may be of uppermost importance to understand interspecific gene flow among natural multispecies populations.

Mechanisms of reproductive isolation of interspecific hybridization between Trillium camschatcense and T. tschonoskii (Melanthiaceae)

AbstractReproductive isolation plays a significant role in the prevention of gene flow between different plant species. Isolation factors can vary, acting either pre‐ or postzygotically. Trillium camschatcense and T. tschonoskii are herbaceous perennials which frequently grow together in Hokkaido, Japan. Natural hybrid formation, T. × hagae, between these species is common, and occurs asymmetrically with T. camschatcense as the maternal parent and T. tschonoskii as the paternal. Here, we examined the efficiency of each reproductive isolation factor to clarify which factor was responsible for the frequency and asymmetry of the hybridization. We found that prezygotic barriers, self fertilization and conspecific pollen precedence, are major isolation factors in both parental species, and that T. tschonoskii as a maternal parent has more effective prezygotic barriers than T. camschatcense. In addition, hybrids with T. tschonoskii as the maternal parent were not observed to reach the flowering stage. We concluded that prezygotic isolation factors in the both species act as main barriers to prevent natural hybridization, and that asymmetry of the isolating barriers between these species would promote T. camschatcense as the maternal parent of the hybrids.

Genome duplication and the evolution of conspecific pollen precedence.

Conspecific pollen precedence can be a strong reproductive barrier between polyploid and diploid species, but the role of genome multiplication in the evolution of this barrier has not been investigated. Here, we examine the direct effect of genome duplication on the evolution of pollen siring success in tetraploid Chamerion angustifolium. To separate the effects of genome duplication from selection after duplication, we compared pollen siring success of synthesized tetraploids (neotetraploids) with that of naturally occurring tetraploids by applying 2x, 4x (neo or established) or 2x + 4x pollen to diploid and tetraploid flowers. Seed set increased in diploids and decreased in both types of tetraploids as the proportion of pollen from diploid plants increased. Based on offspring ploidy from mixed-ploidy pollinations, pollen of the maternal ploidy always sired the majority of offspring but was strongest in established tetraploids and weakest in neotetraploids. Pollen from established tetraploids had significantly higher siring rates than neotetraploids when deposited on diploid (4x(est) = 47.2%, 4x(neo) = 27.1%) and on tetraploid recipients (4x(est) = 91.9%, 4x(neo) = 56.0%). Siring success of established tetraploids exceeded that of neotetraploids despite having similar pollen production per anther and pollen diameter. Our results suggest that, while pollen precedence can arise in association with the duplication event, the strength of polyploid siring success evolves after the duplication event.

Asymmetrical conspecific seed-siring advantage between Silene latifolia and S. dioica.

Silene dioica and S. latifolia experience only limited introgression despite overlapping flowering phenologies, geographical distributions, and some pollinator sharing. Conspecific pollen precedence and other reproductive barriers operating between pollination and seed germination may limit hybridization. This study investigates whether barriers at this stage contribute to reproductive isolation between these species and, if so, which mechanisms are responsible. Pollen-tube lengths for pollen of both species in styles of both species were compared. Additionally, both species were pollinated with majority S. latifolia and majority S. dioica pollen mixes; then seed set, seed germination rates and hybridity of the resulting seedlings were determined using species-specific molecular markers. The longest pollen tubes were significantly longer for conspecific than heterospecific pollen in both species, indicating conspecific pollen precedence. Seed set but not seed germination was lower for flowers pollinated with pure heterospecific versus pure conspecific pollen. Mixed-species pollinations resulted in disproportionately high representation of nonhybrid offspring for pollinations of S. latifolia but not S. dioica flowers. The finding of conspecific pollen precedence for pollen-tube growth but not seed siring in S. dioica flowers may be explained by variation in pollen-tube growth rates, either at different locations in the style or between leading and trailing pollen tubes. Additionally, this study finds a barrier to hybridization operating between pollination and seed germination against S. dioica but not S. latifolia pollen. The results are consistent with the underlying cause of this barrier being attrition of S. dioica pollen tubes or reduced success of heterospecifically fertilized ovules, rather than time-variant mechanisms. Post-pollination, pre-germination barriers to hybridization thus play a partial role in limiting introgression between these species.

TOWARD THE EVOLUTIONARY GENOMICS OF GAMETOPHYTIC DIVERGENCE: PATTERNS OF TRANSMISSION RATIO DISTORTION IN MONKEYFLOWER (MIMULUS) HYBRIDS REVEAL A COMPLEX GENETIC BASIS FOR CONSPECIFIC POLLEN PRECEDENCE

Conspecific pollen precedence (CPP) is a major component of reproductive isolation between many flowering plant taxa and may reveal mechanisms of gametophytic evolution within species, but little is known about the genetic basis and evolutionary history of CPP. We systematically investigated the genetic architecture of CPP using patterns of transmission ratio distortion (TRD) in F2 and backcross hybrids between closely related species of Mimulus (Phrymaceae) with divergent mating systems. We found that CPP in Mimulus hybrids was polygenic and was the majority source of interspecific TRD genome-wide, with at least eight genomic regions contributing to the transmission advantage of M. guttatus pollen grains on M. guttatus styles. In aggregate, these male-specific transmission ratio distorting loci (TRDLs) were more than sufficient to account for the 100% precedence of pure M. guttatus pollen over M. nasutus pollen in mixed pollinations of M. guttatus. All but one of these pollen TRDLs were style-dependent; that is, we observed pollen TRD in F(1) and/or M. guttatus styles, but not in M. nasutus styles. These findings suggest that species-specific differences in pollen tube performance accumulate gradually and may have been driven by coevolution between pollen and style in the predominantly outcrossing M. guttatus.

ECOLOGICAL DIVERGENCE ASSOCIATED WITH MATING SYSTEM CAUSES NEARLY COMPLETE REPRODUCTIVE ISOLATION BETWEEN SYMPATRIC MIMULUS SPECIES

Speciation often involves the evolution of numerous prezygotic and postzygotic isolating barriers between divergent populations. Detailed knowledge of the strength and nature of those barriers provides insight into ecological and genetic factors that directly or indirectly influenced their origin, and may help predict whether they will be maintained in the face of sympatric hybridization and introgression. We estimated the magnitude of pre- and postzygotic barriers between naturally occurring sympatric populations of Mimulus guttatus and M. nasutus. Prezygotic barriers, including divergent flowering phenologies, differential pollen production, mating system isolation, and conspecific pollen precedence, act asymmetrically to completely prevent the formation of F(1) hybrids among seeds produced by M. guttatus (F(1)g), and reduce F(1) hybrid production among seeds produced by M. nasutus (F(1)n) to only about 1%. Postzygotic isolation is also asymmetric: in field experiments, F(1)g but not F(1)n hybrids had significantly reduced germination rates and survivorship compared to parental species. Both hybrid classes had flower, pollen, and seed production values within the range of parental values. Despite the moderate degree of F(1)g hybrid inviability, postzygotic isolation contributes very little to the total isolation between these species in the wild. We also found that F(1) hybrid flowering phenology overlapped more with M. guttatus than M. nasutus. These results, taken together, suggest greater potential for introgression from M. nasutus to M. guttatus than for the reverse direction. We also address problems with commonly used indices of isolation, discuss difficulties in calculating meaningful measures of reproductive isolation when barriers are asymmetric, and propose novel measures of prezygotic isolation that are consistent with postzygotic measures.

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.

Conspecific Sperm and Pollen Precedence and Speciation

▪ Abstract The evolution of reproductive isolation is perhaps the most significant stage in the process of species formation, and the study of reproductive barriers currently dominates investigations of speciation. The discovery that conspecific sperm and pollen precedence play an important role in the reproductive isolation of some closely related animals and plants is one of the real surprises to emerge from this field in recent years. This review begins with a brief history of the study of reproductive isolation with the aim of understanding why conspecific sperm and pollen precedence were generally overlooked in early work on reproductive barriers. It then examines: case studies, the prevalence of conspecific sperm and pollen precedence, the isolating potential of this class of reproductive barriers, the mechanisms that account for the operation of these barriers, and potential explanations for the rapid divergence of populations in traits related to fertilization. Conspecific sperm and pollen precedence appear to be quite effective in limiting gene exchange; these barriers are widespread although not universal in animals and plants, and they operate through a number of different mechanisms. Much more work remains to be done on a number of fronts to elucidate the processes responsible for the evolution of these reproductive barriers.

Floral evolution and male reproductive success: Optimal dispensing schedules for pollen dispersal by animal-pollinated plants

Selection favouring an outcrossing plant's ability to sire seeds generally promotes floral characters that increase (1) the frequency of pollinator visits, (2) the number of pollen grains dispersed to other plants by each pollinator and (3) the probability of a pollen grain successfully fertilizing an ovule after reaching a stigma. Flowers influence pollen dispersal and fertilization probabilities by determining the pattern of pollen removal during a series of visits (dispensing schedule). We model male reproductive success to identify optimal dispensing schedules, which characteristically involve monotonic increases in the proportion of remaining pollen removed during successive visits. These schedules balance the benefits of restricted removal, which counteracts the diminishing returns associated with animal pollination (e.g. pollinator grooming, local mate competition), with the advantages of increased removal to avoid time-dependent losses in fertilization ability (e.g. pollen precedence, declining viability). Because pollinator availability mediates this balance, the most effective dispensing schedule allows dynamic adjustment of removal to the prevailing frequency of visits experienced by individual plants. As an example of such dynamic removal we demonstrate that the dispensing mechanism ofLupinus sericeus flowers allows facultative adjustment of removal to the interval between visits. Because optimal control of pollen removal can increase a plant's mating opportunities by an order of magnitude, dispensing mechanisms should be a common component of floral design.

Pollen precedence and stigma closure: a mechanism of competition for pollination between Delphinium nelsonii and Ipomopsis aggregata.

Previous experiments showed that the sympatric herbs Delphinium nelsonii and Ipomopsis aggregata compete for hummingbird pollination and that deleterious effects of the former species on seed set of the latter involve interspecific pollen transfer. However, seed set was not reduced when pollen of both species was applied simultaneously to I. aggregata stigmas. Hence a competitive effect may require arrival of foreign pollen before conspecific pollen. To explore this possibility we subjected I. aggregata flowers to a "competition" treatment in which they received D. nelsonii pollen 6 h before I. aggregata pollen, or to a "control" in which they received only the conspecific pollen. Foreign pollen precedence decreased mean seed set by almost 50%, which is consistent with effects observed in previous experiments. Reduced seed set can be explained by the fact that foreign pollen often caused stigma lobes to close together within 1.5-6 h, reducing subsequent receptivity. Stigma closure was also elicited by conspecific pollen, but not by mechanical stimulation, and was influenced by size of the pollen load and identity of the plant being pollinated.

An Ecologic View of the Species Conception. I. Past and Present Practise in Species-Making

Previous articleNext article FreeSymposium: Aspects of the Species QuestionAn Ecologic View of the Species Conception. I. Past and Present Practise in Species-MakingFrederic E. ClementsFrederic E. Clements Search for more articles by this author PDFPDF PLUS Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The American Naturalist Volume 42, Number 496Apr., 1908 Published for The American Society of Naturalists Article DOIhttps://doi.org/10.1086/278930 Views: 44Total views on this site Citations: 6Citations are reported from Crossref PDF download Crossref reports the following articles citing this article:B.R. Erick Peirson Plasticity, stability, and yield: The origins of Anthony David Bradshaw's model of adaptive phenotypic plasticity, Studies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences 50 (Apr 2015): 51–66.https://doi.org/10.1016/j.shpsc.2015.01.005Daniel J. Howard Conspecific Sperm and Pollen Precedence and Speciation, Annual Review of Ecology and Systematics 30, no.11 (Nov 1999): 109–132.https://doi.org/10.1146/annurev.ecolsys.30.1.109Malcolm Nicolson Henry Allan Gleason and the individualistic hypothesis: The structure of a botanist’s career, The Botanical Review 56, no.22 (Apr 1990): 91–161.https://doi.org/10.1007/BF02858533Joel B. Hagen THE DEVELOPMENT OF EXPERIMENTAL METHODS IN PLANT TAXONOMY, 1920‐1950, TAXON 32, no.33 (Jun 2019): 406–416.https://doi.org/10.2307/1221497William M. Hiesey Environmental influence and transplant experiments, The Botanical Review 6, no.55 (May 1940): 181–203.https://doi.org/10.1007/BF02882482C. L. Shear, F. E. Clements The Condition and Needs of Systematic Mycology, Science 63, no.16331633 (Apr 1926): 393–395.https://doi.org/10.1126/science.63.1633.393