Field of Dreams: Restitution of Pollinator Services in Restored Bird‐Pollinated Plant Populations

Ecosystem functionality is an increasingly important objective of ecological restoration. Despite this, a few studies have rigorously assessed reproductive functionality within restored plant populations, and it is largely assumed that pollinators follow restoration of plant communities—“build it and they will come.” Here, we applied an ecological genetic approach to determine the impact of spatial separation on mating in Banksia menziesii (Proteaceae), a dominant bird‐pollinated species of Banksia woodlands of Western Australia. All plants at three post‐mining restored sites (n = 72 [13 years old], n = 21 [8 years old], and n = 20 [9 years old]), as well as a sample from an adjacent natural reference site (n = 42), were genotyped at nine microsatellite loci. Seed set, mating system parameters, realized pollen dispersal through the assignment of paternity to seed, and avian pollinator species composition, abundance and behavior, were assessed. All patches displayed equivalent heterozygosity (H_e = 0.53–0.59) and very weak genetic divergence (F_ST ≤ 0.01). Seed of plants within restored sites showed complete outcrossing and relatively high seed set, 26% of which were sired by pollen donors located beyond the local patch. Similar abundance and movement of nectar‐feeding birds was observed in restored and natural sites, despite lower bird species diversity in the restored site, where a smaller, less aggressive species was dominant. Our results demonstrate the restitution of wide outcrossing in these restored Banksia patches within an active mine‐site, and suggest that restored bird‐pollinated Banksia populations are resilient to human impacts, due largely to their generalist pollinator requirements and highly‐mobile avian pollinators.     

Sex and boldness explain individual differences in spatial learning in a lizard

Understanding individual differences in cognitive performance is a major challenge to animal behaviour and cognition studies. We used the Eastern water skink (Eulamprus quoyii) to examine associations between exploration, boldness and individual variability in spatial learning, a dimension of lizard cognition with important bearing on fitness. We show that males perform better than females in a biologically relevant spatial learning task. This is the first evidence for sex differences in learning in a reptile, and we argue that it is probably owing to sex-specific selective pressures that may be widespread in lizards. Across the sexes, we found a clear association between boldness after a simulated predatory attack and the probability of learning the spatial task. In contrast to previous studies, we found a nonlinear association between boldness and learning: both ‘bold’ and ‘shy’ behavioural types were more successful learners than intermediate males. Our results do not fit with recent predictions suggesting that individual differences in learning may be linked with behavioural types via high–low-risk/reward trade-offs. We suggest the possibility that differences in spatial cognitive performance may arise in lizards as a consequence of the distinct environmental variability and complexity experienced by individuals as a result of their sex and social tactics.     

Epigenetic regulation of sex ratios may explain natural variation in self-fertilization rates

Self-fertilization (selfing) favours reproductive success when mate availability is low, but renders populations more vulnerable to environmental change by reducing genetic variability. A mixed-breeding strategy (alternating selfing and outcrossing) may allow species to balance these needs, but requires a system for regulating sexual identity. We explored the role of DNA methylation as a regulatory system for sex-ratio modulation in the mixed-mating fish Kryptolebias marmoratus. We found a significant interaction between sexual identity (male or hermaphrodite), temperature and methylation patterns when two selfing lines were exposed to different temperatures during development. We also identified several genes differentially methylated in males and hermaphrodites that represent candidates for the temperature-mediated sex regulation in K. marmoratus. We conclude that an epigenetic mechanism regulated by temperature modulates sexual identity in this selfing species, providing a potentially widespread mechanism by which environmental change may influence selfing rates. We also suggest that K. marmoratus, with naturally inbred populations, represents a good vertebrate model for epigenetic studies.     

Patterns of self compatibility, inbreeding depression, outcrossing, and sex allocation in a marine bryozoan suggest the predominating influence of sperm competition

Sex allocation by simultaneous hermaphrodites is theoretically influenced by selfing rate, which is in turn influenced by the benefits of enhanced genomic transmission and reproductive assurance relative to the cost of inbreeding depression. The experimental investigation of these influences in seed plants has a rich pedigree, yet although such an approach is equally relevant to colonial invertebrates, which globally dominate subtidal communities on firm substrata, such studies have been scarce. We reared self‐compatible genets of the marine bryozoan Celleporella hyalina s.l. in the presence and absence of allosperm, and used molecular genetic markers for paternity analysis of progeny to test theoretical predictions that: (1) genets from focal populations with high selfing rates show less inbreeding depression than from focal populations with low selfing rates; (2) genets whose selfed progeny show inbreeding depression prefer outcross sperm (allosperm); and (3) genets bias sex allocation toward female function when reared in reproductive isolation. Offspring survivorship and paternity analysis were used to estimate levels of inbreeding depression and preference for outcrossing or selfing. Sex allocation was assessed by counting male and female zooids. As predicted, inbreeding depression was severe in selfed progeny of genets derived from the populations with low self‐compatibility rates, but, with one exception, was not detected in selfed progeny of genets derived from the populations with higher self‐compatibility rates. Also, as predicted, genets whose selfed progeny showed inbreeding depression preferred outcrossing, and a genet whose selfed progeny did not show inbreeding depression preferred selfing. Contrary to prediction, sex allocation in the majority of genets was not influenced by reproductive isolation. Lack of economy of male function may reflect the over‐riding influence of allosperm‐competition in typically dense breeding populations offering good opportunity for outcrossing. We suggest that hermaphroditism may be a plesiomorphic character of the crown group Bryozoa, prevented by phylogenetic constraint from being replaced by gonochorism and therefore not necessarily adaptive in all extant clades. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 519–531.     

Maintenance of androdioecy in the freshwater shrimp Eulimnadia texana: sexual encounter rates and outcrossing success

The clam shrimp Eulimnadia texana has a rare mating system known as androdioecy, in which males and hermaphrodites cooccur butthere are no pure females. In this species, reproduction takesplace by outcrossing between males and hermaphrodites, or byselfing within a hermaphrodite; this system provides a uniqueopportunity to examine the adaptive significance of out-crossingand selfing in animals. Our study examined mating behavior in hermaphrodites and males from two populations to understandthe propensity of these shrimp to mate and to estimate a parameterof a model developed by Otto et al. (American Naturalist 141:329-337),which predicts the conditions for stability of the mixed matingsystem in E. texana. Here we present evidence that mating frequencyis environmentally sensitive, with greater numbers of encountersand matings per male when males are rare and in younger males.However, the effects of shrimp density, relative male frequency,and shrimp age interact in a complex way to determine malemating success. Overall, mating frequency was determined bya combination of encounter rates between the sexes and theproportion of encounters resulting in mating. The mating rateswere then used to estimate one of four parameters of the Ottoet al. model, and these estimates were combined with previousestimates of the other three parameters to examine the fitof the predicted to the observed sex ratios in the two populations.     

海滨锦葵花内五柱头裂片弯曲的独自调节

海滨锦葵花柱有5柱头裂片,若传粉失败,柱头裂片向下弯曲使柱头与自身花粉接触,发生延迟自交。传粉不足条件下发生的延迟自交可能提供繁殖保障。该研究定量分析了花粉搁置和授精胚珠数对花内未授粉柱头裂片运动的影响,并测定了花粉—胚珠比及柱头可授性和花粉生活力。结果表明,花内未授粉柱头裂片的弯曲不受其他柱头接受花粉量及授精胚珠数的影响,仅响应于其自身是否接受到花粉,花粉-胚珠比值显示海滨锦葵交配系统属兼性异交;未授粉柱头经弯曲与自身花粉授触时的强柱头可授粉和高花粉生活力为自交授粉的发生提供了可能。包括柱头裂片运动在内的多个花性状有机地展示了一种新花内混合交配系统,且花内柱头裂片弯曲的独自调节为从花水平验证被广泛接受的自交进化解释——繁殖保障假说提供了可能。     

Diplostigmaty in plants: a novel mechanism that provides reproductive assurance

Differentiation of female sexual organs in flowering plants is rare and contrasts with the wide range of male reproductive strategies. An unusual example involves diplostigmaty, the possession of spatially and temporally distinct stigmas in Sebaea (Gentianaceae). Here, the single pistil within a flower has an apical stigma, as occurs in most flowering plants, but also a secondary stigma that occurs midway down the style, which is physically discrete and receptive several days after the apical stigma. We examined the function of diplostigmaty in Sebaea aurea, an insect-pollinated species of the Western Cape of South Africa. Floral manipulations and measurements of fertility and mating patterns provided evidence that basal stigmas function to enable autonomous delayed self-pollination, without limiting opportunities for outcrossing and thus avoiding the costs of seed discounting. We suggest that delayed selfing serves as a mechanism of reproductive assurance in populations with low plant density. The possession of dimorphic stigma function provides a novel example of a flexible mixed-mating strategy in plants that is responsive to changing demographic conditions.     

Ovule discounting in an outcrossing, cryptically dioecious tree

Ovule discounting denotes the reduction in the number of ovules available for cross-fertilization due to the interference of inferior pollen. Traditionally, ovule discounting has been discussed solely from the perspective of compromised outcrossing opportunities as a result of selfing, but the principle is more general. Here, we extend its applicability beyond the simple contrast between selfing and outcrossing by showing that, in the cryptically dioecious tree species Fraxinus ornus, ovule discounting through frequent outcrossing with inferior fathers also constitutes a substantial cost of mating. In F. ornus, hermaphrodites produce pollen capable of siring offspring, but these offspring are less viable than those sired by males and are inferred to produce few, if any, surviving progeny. In this paper, we used microsatellite markers to analyze the mating system and paternity in a wild population of F. ornus. We found that the effective number of sires per mother was low (N(ep) = 2.93 to 4.95), and that paternity was correlated among progeny sampled from the same mother, but not among progeny sampled from neighboring mothers. Despite the existence of a local spatial genetic structure (up to 30 m), we found no evidence of biparental inbreeding. There was negligible selfing by hermaphrodites, but they sired approximately one fourth of the seeds produced by other hermaphrodites. Given that these progeny are not inferred to reach reproductive maturity, this constitutes a substantial cost of ovule discounting in the broad sense. We discuss the possible reasons for why hermaphrodites invest resources into inferior pollen.     

Pollinator specialization increases with a decrease in a mass‐flowering plant in networks inferred from DNA metabarcoding

相似文献   

Contrasting variation within and covariation between gender-related traits in autogamous versus outcrossing species: Alternative evolutionary predictions

We present several predictions concerning the expression of genetic variation in, and covariation among, gender-related traits in perfect-flowered plant taxa with different breeding systems. We start with the inference that the pollen:ovule (P/O) ratio in obligately autogamous species (in which the ovules in a flower are fertilized only by the pollen it produces) should be under much stronger stabilizing selection than in outcrossing taxa. Consequently, we predict that obligately autogamous taxa should exhibit lower genetic coefficients of variation in the P/O ratio. Nevertheless, genetic variation in both pollen and ovule production per flower might persist within autogamous as well as outcrossing populations. In autogamous taxa, genotypes with relatively few pollen grains and ovules per flower (but producing relatively high numbers of flowers) and genotypes with comparatively high numbers of gametes per flower (but producing relatively few flowers) could co-exist if lifetime flower production is selectively neutral. In contrast, in outcrossers, the maintenance of genetic variation in ovule and pollen production per flower might result predominantly from their ability to maintain variation in phenotypic and functional gender. Given genetic variation in primary sexual traits, we predict that the genetic correlation between investment in male and female gametes per flower should qualitatively differ between selfers and outcrossers. We predict a positive genetic correlation between pollen and ovule production per flower in obligately autogamous taxa, primarily because strong stabilizing selection on the P/O ratio should select against the gender specialists that would be necessary to effect a negative genetic correlation between mean pollen and ovule production per flower. Moreover, the fact that autogamous individuals are 50% female and 50% male means that gender-biased phenotypes cannot be functionally gender-biased, preventing selection from favouring phenotypic extremes. In contrast, in outcrossing taxa, in which functionally male- and female-biased genotypes may co-exist, the maintenance of contrasting genders could contribute to the expression of negative genetic correlations between pollen and ovule production per flower. We discuss these and a number of corollary predictions, and we provide a preliminary empirical test of the first prediction. This revised version was published online in July 2006 with corrections to the Cover Date.     

Pollinator individual‐based networks reveal the specialized plant–pollinator mutualism in two biodiverse communities

Generalization of pollination systems is widely accepted by ecologists in the studies of plant–pollinator interaction networks at the community level, but the degree of generalization of pollination networks remains largely unknown at the individual pollinator level. Using potential legitimate pollinators that were constantly visiting flowers in two alpine meadow communities, we analyzed the differences in the pollination network structure between the pollinator individual level and species level. The results showed that compared to the pollinator species‐based networks, the linkage density, interaction diversity, interaction evenness, the average plant linkage level, and interaction diversity increased, but connectance, degree of nestedness, the average of pollinator linkage level, and interaction diversity decreased in the pollinator individual‐based networks, indicating that pollinator individuals had a narrower food niche than their counterpart species. Pollination networks at the pollinator individual level were more specialized at the network level (H′₂) and the plant species node level (d′) than at the pollinator species‐level networks, reducing the chance of underestimating levels of specialization in pollination systems. The results emphasize that research into pollinator individual‐based pollination networks will improve our understanding of the pollination networks at the pollinator species level and the coevolution of flowering plants and pollinators.     

Widespread functional android in Mercurialis annua L. (Euphorbiaceae)

The widespread coexistence of male and monoecious (cosexual) plants in Spanish, Portuguese and Moroccan populations of Mercurialis annua , an annual wind-pollinated ruderal, represents an important case of functional androdioecy, a rare breeding system in plants and animals. In M. annua , both males and cosexes disperse fully competent pollen. Quantitative gender varies discontinuously between males and cosexes, with males producing a mean of 6.09 times as much pollen as cosexes. It appears that gender is determined by a simple developmental switch, with male and cosexual inflorescences differing markedly in morphology: staminate flowers are borne on erect peduncles in males and in tight spiral clusters around a subsessile pistillate flower in cosexes. Males do not differ from cosexes in their biomass, but they are significantly taller, principally as a result of their greater internode lengths. The cosexual inflorescence is strongly protogynous so that outcrossing is favoured in dense stands, but seed-set is assured in cosexes isolated from prospective mates because of their ability to self-fertilize. Males typically occur at frequencies of less than about 30% in androdioecious populations, in accordance with theoretical predictions for functional androdioecy. In the genus Mercurialis , dioecy is the ancestral condition and monoecy and androdioecy, which occur in polyploid populations of M. annua , are derived. I argue here that androdioecy is most likely to evolve in plants (1) from dioecy, (2) in wind-pollinated species, and (3) in species with a colonizing habit. These predictions are also consistent with the limited published data available for other species.     

Dichogamy correlates with outcrossing rate and defines the selfing syndrome in the mixed-mating genus Collinsia

Background and Aims

How and why plants evolve to become selfing is a long-standing evolutionary puzzle. The transition from outcrossing to highly selfing is less well understood in self-compatible (SC) mixed-mating (MM) species where potentially subtle interactions between floral phenotypes and the environment are at play. We examined floral morphological and developmental traits across an entire SC MM genus, Collinsia, to determine which, if any, predict potential autonomous selfing ability when pollinators are absent (AS) and actual selfing rates in the wild, s_m, and to best define the selfing syndrome for this clade.

Methods

Using polymorphic microsatellite markers, we obtained 30 population-level estimates of s_m across 19 Collinsia taxa. Species grand means for the timing of herkogamy (stigma–anther contact) and dichogamy (stigmatic receptivity, SR), AS, floral size, longevity and their genetic correlations were quantified for 22 taxa.

Key Results

Species fell into discrete selfing and outcrossing groups based on floral traits. Loss of dichogamy defines Collinsia''s selfing syndrome. Floral size, longevity and herkogamy also differ significantly between these groups. Most taxa have high AS rates (>80 %), but AS is uncorrelated with any measured trait. In contrast, s_m is significantly correlated only with SR. High variance in s_m was observed in the two groups.

Conclusions

Collinsia species exhibit clear morphological and developmental traits diagnostic of ‘selfing’ or ‘outcrossing’ groups. However, many species in both the ‘selfing’ and the ‘outcrossing’ groups were MM, pointing to the critical influence of the pollination environment, the timing of AS and outcross pollen prepotency on s_m. Flower size is a poor predictor of Collinsia species'' field selfing rates and this result may apply to many SC species. Assessment of the variation in the pollination environment, which can increase selfing rates in more ‘outcrossing’ species but can also decrease selfing rates in more ‘selfing’ species, is critical to understanding mating system evolution of SC MM taxa.     

Rapid loss of self‐incompatibility in experimental populations of the perennial outcrossing plant Linaria cavanillesii

Transitions from self‐incompatibility to self‐compatibility in angiosperms may be frequently driven by selection for reproductive assurance when mates or pollinators are rare, and are often succeeded by loss of inbreeding depression by purging. Here, we use experimental evolution to investigate the spread of self‐compatibility from one such population of the perennial plant Linaria cavanillesii into self‐incompatible (SI) populations that still have high inbreeding depression. We introduced self‐compatible (SC) individuals at different frequencies into replicate experimental populations of L. cavanillesii that varied in access to pollinators. Our experiment revealed a rapid shift to self‐compatibility in all replicates, driven by both greater seed set and greater outcross siring success of SC individuals. We discuss our results in the light of computer simulations that confirm the tendency of self‐compatibility to spread into SI populations under the observed conditions. Our study illustrates the ease with which self‐compatibility can spread among populations, a requisite for species‐wide transitions from self‐incompatibility to self‐compatibility.     

Sibling competition, size variation and frequency-dependent outcrossing advantage in Plantago coronopus

Many plants display limited seed dispersal, thereby creating an opportunity for sibling competition, i.e. fitness-determined interactions between related individuals. Here I investigated the consequences of intra-specific competition, by varying density and genetic composition of neighbors, on the performance of seedlings derived by selfing or outcrossing of the partially self-fertilizing plant Plantago coronopus (L.). Seedlings from eight plants, randomly selected from an area of about 50 m² in a natural population, were used in (i) a density series with either one, four or eight siblings of each cross type per pot and (ii) a replacement series with eight plants per pot where selfed and outcrossed siblings were grown intermixed in varying frequencies. Density had a pronounced effect on plant performance. But, except for singly grown individuals, no differences were detected between selfed and outcrossed progenies in vegetative and reproductive biomass. When grown intermixed, selfed offspring were always inferior to their outcrossed relatives. The magnitude of reduction in performance was dependent on the number of outcrossed relatives a selfed seedling had to compete with, giving rise to a frequency-dependent fitness advantage to outcrossed seedlings. The major result of this study is (i) that the relative fitness of inbred progeny is strongly affected by the type of competitors (inbred or outbred) and (ii) that inbreeding depression varies according to the density and frequency of outbred plants and could be considered as a density- and frequency-dependent phenomenon. It is argued that sibling competition, due to the small genetic neighborhood of P. coronopus, might be an important selective force in natural populations of this species.     

Low outcrossing rates and shift in pollinators in New Zealand pohutukawa (Metrosideros excelsa; Myrtaceae)

New Zealand pohutukawa (Metrosideros excelsa), a member of the Myrtaceae, is a large, mass-flowering tree endemic to northern New Zealand coastlines. Mainland populations have been reduced to fragmented stands, and the original suite of bird pollinators has been largely replaced by introduced species. The native pollinator fauna on several offshore islands is largely intact and includes three species of the New Zealand honeyeaters (Meliphagidae) and native, solitary bees. We estimated multilocus outcrossing rates for three mainland and two island populations and found that they were among the lowest in the Myrtaceae (t(m) = 0.22-0.53). The shift in pollinators had no measurable effect on the mating system. Mass-flowering facilitates geitonogamous selfing, and inbreeding depression in seedling height was detectable at 6 mo of growth. F(s) [Wright's (1965) Fixation Index] was consistently higher than F(m) in all populations, indicating that selection may eliminate selfed offspring from populations prior to achieving reproductive maturity. Results suggest that increased selfing in mainland populations due to pollinator changes is not responsible for current patterns of poor regeneration of this species.