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

Premise of Study

In a seminal body of theory, Lloyd showed that the fitness consequences of selfing will depend on its timing in anthesis. Selfing that occurs after opportunities for outcrossing or pollen dispersal can provide reproductive assurance when pollinators are limited and is expected to incur little cost, even when inbreeding depression is high. As a result, delayed selfing is often interpreted as a “best‐of‐both‐worlds” mating system that combines the advantages of selfing and outcrossing.

Methods

We surveyed 65 empirical studies of delayed selfing, recording floral mechanisms and examining information on inbreeding depression, autofertility, and other parameters to test the support for delayed selfing as a best‐of‐both‐worlds strategy.

Key Results

Phylogenetic distribution of the diverse floral mechanisms suggests that some basic floral structures may predispose plant taxa to evolve delayed selfing. Delayed selfing appears to serve as a best‐of‐both‐worlds strategy in some but not all species. While the capacity for autonomous selfing is often high, it is lower, in some cases, than in related species with earlier modes of selfing. In other delayed‐selfers, low inbreeding depression and reduced investment in corollas and pollen suggest limited benefits from outcrossing.

Conclusions

Despite a growing literature on the subject, experimental evidence for delayed selfing is limited and major gaps in knowledge remain, particularly with respect to the stability of delayed selfing and the conditions that may favor transitions between delayed and earlier selfing. Finally, we suggest a potential role of delayed selfing in facilitating transitions from self‐incompatibility to selfing.     

Does stigma curvature promote delayed selfing? An experimental investigation in Triodanis perfoliata (Campanulaceae)

• Self‐fertilisation that is delayed until after opportunities for outcrossing have ceased has been argued to provide both the reproductive assurance benefits of selfing and the genetic advantages of outcrossing. In the Campanulaceae, presentation of pollen on stylar hairs and progressive stigma curvature have been hypothesised to facilitate delayed selfing, but experimental tests are lacking. Stigma curvature is common in Campanula, a genus largely characterised by self‐incompatibility, and therefore is unlikely to have initially evolved to promote self‐fertilisation. In derived self‐compatible species, however, stigma curvature might serve the secondary function of delayed selfing.
• We investigated delayed selfing in Triodanis perfoliata, a self‐compatible relative of Campanula. Using floral manipulation experiments and pollen tube observations, we quantified the extent and timing of self‐pollination. Further, we hypothesised that, if stigma curvature provides the benefit of delayed selfing in Triodanis, selection should have favoured retention of self‐pollen through the loss of a stylar hair retraction mechanism.
• Results of a stigma removal experiment indicated that autonomous selfing produces partial seed set, but only some selfing was delayed. Pollen tube observations and a flower senescence assay also supported the finding of partial delayed selfing. Scanning electron microscopy revealed that pollen‐collecting hairs retract during anthesis, which may limit the extent of delayed selfing.
• Delayed selfing appeared to be only partially effective in T. perfoliata. The stylar hair retraction in this species would seem to contradict selection for selfing. We suggest that caution and rigour are needed in interpreting floral traits as adaptive mechanisms for delayed selfing.

     

Does selfing or outcrossing promote local adaptation?

The degree to which plants self-fertilize may impact their potential for genetic adaptation. Given that the mating system influences genetic processes within and among populations, the mating system could limit or promote local adaptation. I conducted a literature survey of published reciprocal transplant experiments in plant populations to quantify the effect of mating system on the magnitude of local adaptation. Mating system had no effect on local adaptation. I detected no effect when species were categorized as either self-compatible or self-incompatible or when accounting for environmental differences between source populations. The results suggest that, despite limited genetic variation in selfing species and greater potential for gene flow in outcrossing species, mating system has little influence on adaptation of populations.     

Fine-scale spatial genetic structure in predominantly selfing plants with limited seed dispersal:a rule or exception?

Gene flow at a fine scale is still poorly understood despite its recognized importance for plant population demographic and genetic processes.We tested the hypothesis that intensity of gene flow will be lower and strength of spatial genetic structure(SGS) will be higher in more peripheral populations because of lower population density.The study was performed on the predominantly selfing Avena sterilis and included:(1) direct measurement of dispersal in a controlled environment;and(2) analyses of SGS in three natural populations,sampled in linear transects at fixed increasing inter-plant distances.We found that in A.sterilis major seed dispersal is by gravity in close(less than 2 m) vicinity of the mother plant,with a minor additional effect of wind.Analysis of SGS with six nuclear SSRs revealed a significant autocorrelation for the distance class of 1 m only in the most peripheral desert population,while in the two core populations with Mediterranean conditions,no genetic structure was found.Our results support the hypothesis that intensity of SGS increases from the species core to periphery as a result of decreased within-population gene flow related to low plant density.Our findings also show that predominant self-pollination and highly localized seed dispersal lead to SGS at a very fine scale,but only if plant density is not too high.     

Why was there a delayed radiation after the end‐Palaeozoic extinctions?

Data from widespread dysaerobic facies, carbon/sulphur ratios and cerium anomalies suggest that the early Triassic was a time when anoxic conditions spread widely over epicontinental seas. These conditions, associated with marine transgression following the latest Permian regression, are likely to be a prime cause of the mass extinction of Palaeozoic marine faunas. The occurrence of many Lazarus taxa in the Middle and Upper Triassic indicates, however, that the extinctions at the end of the Permian were less severe than has been widely assumed, and that the turnover from Palaeozoic to Mesozoic faunas was considerably extended in time, being finally accomplished only after the end‐Triassic mass extinction event.     

Fine-scale spatial genetic structure in predominantly selfing plants with limited seed dispersal: a rule or exception?

Gene flow at a fine scale is still poorly understood despite its recognized importance for plant population demographic and genetic processes. We tested the hypothesis that intensity of gene flow will be lower and strength of spatial genetic structure (SGS) will be higher in more peripheral populations because of lower population density. The study was performed on the predominantly selfing Avena sterilis and included: (1) direct measurement of dispersal in a controlled environment; and (2) analyses of SGS in three natural populations, sampled in linear transects at fixed increasing inter plant distances. We found that in A.sterilis major seed dispersal is by gravity in close (less than 2m) vicinity of the mother plant, with a minor additional effect of wind. Analysis of SGS with six nuclear SSRs revealed a significant autocorrelation for the distance class of 1m only in the most peripheral desert population, while in the two core populations with Mediterranean conditions, no genetic structure was found. Our results support the hypothesis that intensity of SGS increases from the species core to periphery as a result of decreased within population gene flow related to low plant density. Our findings also show that predominant self pollination and highly localized seed dispersal lead to SGS at a very fine scale, but only if plant density is not too high.     

Can varying inbreeding depression select for intermediary selfing rates?

We study the evolution of the self-fertilization of an annual hermaphroditic plant under varying inbreeding depression. While classical population genetic models treat inbreeding depression as a constant parameter, recent empirical research has shown that changing environmental conditions can make inbreeding depression vary. Here, we create a simple phenotypic model, assuming variable inbreeding depression. We investigate how different types of variability (spatial, temporal, and spatiotemporal variability) affect the evolution of selfing rates in three models. Two main results, which differ from the classical predictions, emerge from this study. First, we find that fluctuating environments, which influence the magnitude of inbreeding depression, are able to select for evolutionarily stable intermediary selfing rates. Second, we show that spatiotemporal variation of inbreeding depression can lead to the development and the maintenance of polymorphic selfing rates within a population.     

Persistent mucus accumulation: a consequence of delayed bronchial mucous cell apoptosis in RAO-affected horses?

This study examined the contribution of delayed apoptosis of bronchial mucous cells to mucus accumulation in equine recurrent airway obstruction (RAO). In pilot studies, Bcl-2, an apoptosis inhibitor, was detected in airway mucous cells of RAO-affected horses in remission and during acute disease, when most mucus was secreted. To study whether delayed apoptosis results in an increase in the number of mucous cells during disease recovery, six RAO-affected and six control horses were fed hay for 5 days to induce inflammation and then pellets for 7 days to partially resolve RAO before euthanasia. RAO-affected horses had more airway obstruction and luminal mucus than control horses under both management systems. At the time of euthanasia, RAO-affected horses had more inflammation and Bcl-2-positive bronchial mucous cells than control animals. In horses with >10 and <10 neutrophils per microliter of bronchoalveolar lavage fluid, >50% and <10% of mucous cells stained positive for Bcl-2, respectively. No differences in mucous cell number or amount of stored mucosubstance were observed between RAO-affected and control horses, but in RAO-affected animals, the amount of stored mucosubstance decreased as the number of neutrophils in bronchoalveolar lavage fluid increased. Because the number of mucous cells was similar in both groups of horses but only mucous cells of RAO-affected horses expressed Bcl-2 during recovery from acute disease, a conclusive role for Bcl-2 in prolonging bronchial mucous cell life could not be determined. Future studies are needed to compare horses that are kept in remission for prolonged periods when all mucous cells are fully developed.     

Hypoparathyroidism after surgery on thyroid cancer: is there a delayed chance for recovery after a prolonged period of substitutive therapy?

INTRODUCTION: Transient and persistent hypoparathyroidism (HPT) belong to the well known complications of total thyroidectomy performed because of thyroid carcinoma. The true frequency of persistent hypoparathyroidism is often higher than estimated in the reports published by the specialized centers with low rate of complications. THE AIM OF THE STUDY: Investigation whether the repeated check-up, performed over 2 years post thyroidectomy, reveals some cases of recovery in patients diagnosed with persistent HPT post thyroid cancer surgery. MATERIAL AND METHODS: In total, 115 patients were included into the study, all of them treated with vitamin D derivatives and calcium supplementation. In 17 of them a diagnosis of transient hypoparathyroidism was made on the basis of evaluation performed 6 months after surgery, the remaining 98 were diagnosed with persistent HPT. Parathyroid (PTH) function was reevaluated after withdrawal of active vitamin D derivatives for 10 days and of calcium carbonate for two days during the hospital stay in patients admitted for radioiodine scan, thus after thyroxine withdrawal. The control group consisted of 123 DTC (differentiated thyroid carcinoma) patients without parathyroid dysfunction. On the basis of intact PTH serum level and calcium and phosphorus estimations HPT was unequivocally confirmed in 49 patients (50%). The remaining 49 patients exhibited normal PTH level and in 43 (86%) of them Ca(2+) level was also within normal range, thus delayed, recovery from HPT was stated. RESULTS: Our results indicate that reevaluation of hypoparathyroidism post total thyreoidectomy is necessary, as delayed recover of parathyroid dysfunction is a frequent phenomenon. We also propose criteria of reevaluation of HTP in patients on chronic substitutive therapy.     

Multiple periodic solutions of a delayed predator–prey model with non-monotonic functional response and stage structure

The paper studies a periodic and delayed predator–prey system with non-monotonic functional responses and stage structure. In the system, both the predator and prey are divided into immature individuals and mature individuals by two fixed ages. It is assumed that the immature predators cannot attack preys, and the case of the mature predators attacking the immature preys is also ignored. Based on Mawhin's coincidence degree, sufficient conditions are obtained for the existence of two positive periodic solutions of the system. An example is presented to illustrate the feasibility of the main results.     

Do selfing species have greater niche breadth? Support from ecological niche modeling

We explore the relationship between plant mating system (selfing or outcrossing) and niche breadth to gain new insights into processes that drive species distributions. Using a comparative approach with highly selfing versus highly outcrossing sister species, we test the extent to which: (1) species pairs have evolved significant niche divergence and less niche overlap, (2) selfers have wider niche breadths than outcrossers or vice versa, and (3) niches of selfers and outcrossers are defined by significant differences in environmental variables. We applied predictive ecological niche modeling approaches to estimate and contrast niche divergence, overlap and breadth, and to identify key environmental variables associated with each species’ niche for seven sister species with divergent mating systems. Data from 4862 geo-referenced herbarium occurrence records were compiled for 14 species in Collinsia and Tonella (Plantaginaceae) and 19 environmental variables associated with each record. We found sister species display significant niche divergence, though not as a function of divergence time, and overall, selfers have significantly wider niche breadths compared to their outcrossing sisters. Our results suggest that a selfing mating system likely contributes to the greater capacity to reach, reproduce, establish, and adapt to new habitats, which increases niche breadth of selfers.     

Does selfing provide reproductive assurance in the perennial herb Bulbine vagans (Asphodelaceae)?

Selection for selfing to provide reproductive assurance depends on the balance between increased reproductive output when pollinators or potential mates are scarce and the extent that inbreeding depression erodes such fertility gains. We use glasshouse and field experiments to examine the benefits of autonomous and facilitated selfing in Bulbine vagans . Autonomous selfing was delayed until after opportunities for outcrossing and reproductive output was 0.67 relative to manual selfing and open pollination. Values less than one probably reflected insufficient autonomous deposition of self pollen. In the field, reproductive output of emasculated flowers was 0.50 relative to intact flowers that could both outcross and self, indicating that outcross pollen was limited and that selfing boosted reproductive output. Because all pollen was removed from anthers before intact flowers closed, facilitated selfing rather than autonomous selfing occurred. In the glasshouse, inbreeding depression was 0.45, but under natural conditions would probably exceed 0.5. Values greater than 0.5 negate the automatic gene transmission advantage afforded by selfing and increasingly erode the benefits of reproductive assurance. We conclude that in B. vagans delayed and facilitated selfing can confer reproductive assurance, providing the latter does not usurp ovules that could be outcrossed.     

Impaired TGF-β signaling and a defect in resolution of inflammation contribute to delayed wound healing in a female rat model of type 2 diabetes

Wound healing (WH) impairment is a well-documented phenomenon in clinical and experimental diabetes. Sex hormones, in addition to a number of signaling pathways including transforming growth factor-β1 (TGF-β1)/Smads and TNF-α/NF-κB in macrophages and fibroblasts, appear to play a cardinal role in determining the rate and nature of WH. We hypothesized that a defect in resolution of inflammation and an enhancement in TNF-α/NF-κB activity induced by estrogen deficiency contribute to the impairment of TGF-β signaling and delayed WH in diabetes models. Goto-Kakizaki (GK) rats and full thickness excisional wounds were used as models for type 2 diabetes (T2D) and WH, respectively. Parameters related to the various stages of WH were assessed using histomorphometry, western blotting, real-time PCR, immunofluorescence microscopy and ELISA-based assays. Retarded re-epithelialization, suppressed angiogenesis, delayed wound closure, reduced estrogen level and heightened states of oxidative stress were characteristic features of T2D wounds. These abnormalities were associated with a defect in resolution of inflammation, shifts in macrophage phenotypes, increased β3-integrin expression, impaired wound TGF-β1 signaling (↓p-Smad2/↑Smad7) and enhanced TNF-α/NFκB activity. Human/rat dermal fibroblasts of T2D, compared to corresponding control values, displayed resistance to TGF-β-mediated responses including cell migration, myofibroblast formation and p-Smad2 generation. A pegylated form of soluble TNF receptor-1 (PEG-sTNF-RI) or estrogen replacement therapy significantly improved re-epithelialization and wound contraction, enhanced TGFβ/Smad signaling, and polarized the differentiation of macrophages toward an M2 or "alternatively" activated phenotype, while limiting secondary inflammatory-mediated injury. Our data suggest that reduced estrogen levels and enhanced TNF-α/NF-κB activity delayed WH in T2D by attenuating TGFβ/Smad signaling and impairing the resolution of inflammation; most of these defects were ameliorated with estrogen and/or PEG-sTNF-RI therapy.     

Can females benefit from selfing avoidance? Genetic associations and the evolution of plant gender

Evolutionary stability of dioecy and nuclear gynodioecy in higher plants requires that females produce over twice as many successful seeds as hermaphrodites. This fitness differential is widely thought to derive primarily from the advantages of outcrossing caused by high selfing rates and inbreeding depression in the hermaphrodite. This study hypothesized that (i) extraordinarily high deleterious mutation rates are necessary to double female seed success due to outcrossing, and (ii) the large difference in outcrossing rates between sex morphs causes differential purging of these mutations, resulting in additional genetic selection on male sterility. Using genetically explicit models, I showed that the phenotypic outcrossing advantage requires at least one new highly recessive deleterious mutation per genome per generation, regardless of selection coefficient. However, under this mutational regime, differential purging created strong genetic selection against recessive male sterility that overwhelmed the phenotypic selection in favour of outcrossing. In very small populations and for dominant male sterility, this genetic selection was weaker or absent. This first genetically explicit study of the outcrossing advantage of unisexual females may shed new light on both the genetic and selective conditions for the evolution of gynodioecy and dioecy.     

Is there direct and delayed density dependent variation in population structure in a temperate European cyclic vole population?

Population structure, in terms of the body mass, condition, sex and reproductive status of individuals, has been found to vary in phase with population density in cyclic populations of microtine rodents. Because sustained population cycles involve delayed density dependent changes in the population growth rate, we would expect at least some life history traits also to depend on past densities. Detailed, long-term studies of changes in vole life history traits are however few, and are largely restricted to northern Europe. In view of the uncertainty as to whether the cyclic microtine populations of western Europe represent the same phenomenon as those of northern Europe, we studied temporal variation in the structure of a clearly cyclic population of the common vole Microtus arvalis Pallas, in the cereal plains of mid-western France. Our data set contains seasonal, individual-level data from long-term, large-scale trapping covering four entire population cycles. We found considerable cyclic variation in population structure in spring (April), but less so in summer (June). In spring of post-peak years, animals were of low body weight and body condition (particularly females), litter sizes were smaller and there was a reduction in the proportion of breeders. All of these could be proximal drivers of increased mortality rates, or decreased birth rates, contributing to the population declines. Few life history traits, however, showed direct density dependent variation, and none of the traits studied here showed delayed density dependence. We have shown declines in the fecundity and body condition of voles from a western European population that coincides with, and may be a proximal cause of, cyclic declines in population density. Closer attention to proximal causes, by which ecological processes drive cycles, could clarify the extent to which microtine cycles across Europe represent a single phenomenon.     

Hereditary retinoblastoma: delayed mutation or host resistance?

Evidence is presented from the literature that there is little need to postulate delayed mutation for the retinoblastoma locus. Both penetrance and expressivity in the gene carrier can be defined as a variable determined by genetic and environmental factors, not by a Poisson distribution of tumors formed. Of individuals who received a new mutation from a healthy parent, approximately 13% do not manifest retinoblastoma, and the heritability of the host resistance is estimated at about 90%. The nonhereditary form of retinoblastoma may occur in the most susceptible group of the population.