Why outcross? The abandon-ship hypothesis in a facultative outcrossing/selfing fungal species.

Most species able to reproduce both sexually and asexually (facultative sexual species) invest more in sexual reproduction in stressful environment conditions. According to the abandon-ship hypothesis, plasticity for investment in sexual reproduction may have been selected in these species, allowing unfit genotypes to generate progeny carrying new advantageous allelic combinations. We tested this hypothesis in Aspergillus nidulans, a fungus able to reproduce asexually, or sexually, by outcrossing and/or haploid selfing (i.e. fusion of genetically identical haploid nuclei, causing immediate genome-wide homozygosity). We crossed various strains of A. nidulans in a non-stressful environment and a stressful environment containing a non-lethal dose of fungicide. Without stress, crosses preferentially generated haploselfed fruiting bodies, whereas stressful conditions significantly increased the outcrossing rate. Our results strongly support the abandon-ship hypothesis and suggest that, for parents with low fitness, the costs of investing in sexual reproduction may be compensated by the production of fitter progeny carrying beneficial allele combinations. Similarly, the progeny generated by outcrossing was less fit than that produced by haploid selfing in non-stressful environments, but fitter in stressful conditions, suggesting that outcrossing may have short-term advantages in stressful environments in A. nidulans.

Polygamy or subdioecy? The impact of diallelic self-incompatibility on the sexual system in Fraxinus excelsior (Oleaceae).

How flowering plants have recurrently evolved from hermaphroditism to separate sexes (dioecy) is a central question in evolutionary biology. Here, we investigate whether diallelic self-incompatibility (DSI) is associated with sexual specialization in the polygamous common ash (Fraxinus excelsior), which would ultimately facilitate the evolution towards dioecy. Using interspecific crosses, we provide evidence of strong relationships between the DSI system and sexual phenotype. The reproductive system in F. excelsior that was previously viewed as polygamy (co-occurrence of unisexuals and hermaphrodites with varying degrees of allocation to the male and female functions) and thus appears to actually behave as a subdioecious system. Hermaphrodites and females belong to one SI group and functionally reproduce as females, whereas males and male-biased hermaphrodites belong to the other SI group and are functionally males. Our results offer an alternative mechanism for the evolution of sexual specialization in flowering plants.

Effect of aperture number on pollen germination, survival and reproductive success in Arabidopsis thaliana.

Background and Aims: Pollen grains of flowering plants display a fascinating diversity of forms, including diverse patterns of apertures, the specialized areas on the pollen surface that commonly serve as the sites of pollen tube initiation and, therefore, might play a key role in reproduction. Although many aperture patterns exist in angiosperms, pollen with three apertures (triaperturate) constitutes the predominant pollen type found in eudicot species. The aim of this study was to explore whether having three apertures provides selective advantages over other aperture patterns in terms of pollen survival, germination and reproductive success, which could potentially explain the prevalence of triaperturate pollen among eudicots. Methods: The in vivo pollen germination, pollen tube growth, longevity and competitive ability to sire seeds were compared among pollen grains of Arabidopsis thaliana with different aperture numbers. For this, an arabidopsis pollen aperture series was used, which included the triaperturate wild type, as well as mutants without an aperture (inaperturate) and with more than three apertures. Key Results: Aperture number appears to influence pollen grain performance. In most germination and longevity experiments, the triaperturate and inaperturate pollen grains performed better than pollen with higher aperture numbers. In mixed pollinations, in which triaperturate and inaperturate pollen were forced to compete with each other, the triaperturate pollen outperformed the inaperturate pollen. Conclusions: Triaperturate pollen grains might provide the best trade-off among various pollen performance traits, thus explaining the prevalence of this morphological trait in the eudicot clade.

More than sixty origins of pantoporate pollen in angiosperms.

PREMISE OF THE STUDY: Apertures in pollen grains are key structures of the wall, involved in pollen tube germination and exchanges with the environment. Aperture types in angiosperms are diverse, but pollen with one and three apertures (including monosulcate and tricolpate, respectively) are the two most common types. Here, we investigate the phylogenetic distribution in angiosperms of pollen with many round, scattered apertures called pantoporate pollen. METHODS: We constructed a morphological data set with species producing pantoporate pollen and representative angiosperm species with other pollen types, sampled from every angiosperm order, with a total of 1260 species distributed in 330 families. This data set was analyzed with parsimony to characterize the phylogenetic distribution of pantoporate pollen in angiosperms. KEY RESULTS: We show that pantoporate pollen is distributed throughout most of the angiosperm tree, including early diverging angiosperms, monocots, and eudicots. However, this pollen type is usually restricted to a few species in a given group, and is seldom fixed at large taxonomical scales, with a few notable exceptions. CONCLUSIONS: Pantoporate pollen evolved many times during angiosperm history, but the persistence of this morphology in the long term is infrequent. This distribution pattern could indicate conflicting short-term and long-term selective pressures, pantoporate pollen being selected in the short run, but eliminated in the long run. Biological hypotheses supporting this scenario are discussed, in the context of both theoretical and empirical data on pollen biology.

Evolutionary stasis in pollen morphogenesis due to natural selection.

The contribution of developmental constraints and selective forces to the determination of evolutionary patterns is an important and unsolved question. We test whether the long-term evolutionary stasis observed for pollen morphogenesis (microsporogenesis) in eudicots is due to developmental constraints or to selection on a morphological trait shaped by microsporogenesis: the equatorial aperture pattern. Most eudicots have three equatorial apertures but several taxa have independently lost the equatorial pattern and have microsporogenesis decoupled from aperture pattern determination. If selection on the equatorial pattern limits variation, we expect to see increased variation in microsporogenesis in the nonequatorial clades. Variation of microsporogenesis was studied using phylogenetic comparative analyses in 83 species dispersed throughout eudicots including species with and without equatorial apertures. The species that have lost the equatorial pattern have highly variable microsporogenesis at the intra-individual and inter-specific levels regardless of their pollen morphology, whereas microsporogenesis remains stable in species with the equatorial pattern. The observed burst of variation upon loss of equatorial apertures shows that there are no strong developmental constraints precluding variation in microsporogenesis, and that the stasis is likely to be due principally to selective pressure acting on pollen morphogenesis because of its implication in the determination of the equatorial aperture pattern.

Aperture number influences pollen survival in Arabidopsis mutants.

PREMISE OF THE STUDY: Pollen grains are subject to intense dehydration before dispersal. They rehydrate after landing on a stigma or when placed in humid environment by absorbing water from the stigma or surroundings. Resulting fluctuations in water content cause pollen grains to undergo significant changes in volume. Thus, morphological or structural adaptations might exist to help pollen adjust to sudden volume changes, though little is known about the correlation between pollen morphology and its ability to accommodate volume changes. We studied the effect of one morphological feature of pollen grains, the aperture number, on pollen wall resistance to water inflow in Arabidopsis thaliana. METHODS: We used three Arabidopsis thaliana mutants that differ in the number of apertures in their pollen (zero, four, or a mix of four to eight, respectively) and the wild type with pollen with three apertures. We tested pollen survival in solutions with various mannitol concentrations. KEY RESULTS: The number of intact pollen grains increased with increasing mannitol concentration for all pollen morphs tested. At a given mannitol concentration, however, an increase in aperture number was associated with an increase in pollen breakage. CONCLUSIONS: Aperture patterns, i.e., number, shape, and position, influence the capacity to accommodate volume variations in pollen grains. When subjected to water inflow, pollen grains with few apertures survive better than pollen with many apertures. Trade-offs between survival and germination are likely to be involved in the evolution of pollen morphology.

Evolution of a genetic polymorphism with climate change in a Mediterranean landscape.

Many species show changes in distribution and phenotypic trait variation in response to climatic warming. Evidence of genetically based trait responses to climate change is, however, less common. Here, we detected evolutionary variation in the landscape-scale distribution of a genetically based chemical polymorphism in Mediterranean wild thyme (Thymus vulgaris) in association with modified extreme winter freezing events. By comparing current data on morph distribution with that observed in the early 1970s, we detected a significant increase in the proportion of morphs that are sensitive to winter freezing. This increase in frequency was observed in 17 of the 24 populations in which, since the 1970s, annual extreme winter freezing temperatures have risen above the thresholds that cause mortality of freezing-sensitive morphs. Our results provide an original example of rapid ongoing evolutionary change associated with relaxed selection (less extreme freezing events) on a local landscape scale. In species whose distribution and genetic variability are shaped by strong selection gradients, there may be little time lag associated with their ecological and evolutionary response to long-term environmental change.

Gametophytic vs. sporophytic control of pollen aperture number: a generational conflict.

In flowering plants, the haploid phase is reduced to the pollen grain and embryo sac. These reproductive tissues (gametophytes) are actually distinct individuals that have a different genome from the plant (sporophyte), and are more or less independent. The morphology of pollen grains, particularly the openings permitting pollen tube germination (apertures), is crucial for determining the outcome of pollen competition. Many species of flowering plants simultaneously produce pollen grains with different aperture numbers in a single individual (heteromorphism). In this paper, we show that the heteromorphic pollen aperture pattern depends on the genetic control of pollen morphogenesis. This points out a conflict of interest between genes expressed in the sporophyte and genes expressed in the gametophyte. More generally, such a conflict should exist whenever heteromorphism is an ESS resulting from a bet-hedging strategy. For pollen aperture, heteromorphism has been observed in about 40% of angiosperm species, suggesting that conflicting situations are the rule. In this context, the sporo-gametophytic conflict could be one of the factors that led to the reduction of the haploid phase in plants.

A Review of the Developmental Processes and Selective Pressures Shaping Aperture Pattern in Angiosperms.

Pollen grains of flowering plants display a fascinating diversity of forms. The observed diversity is determined by the developmental mechanisms involved in the establishment of pollen morphological features. Pollen grains are generally surrounded by an extremely resistant wall displaying apertures that play a key role in reproduction, being the places at which pollen tube growth is initiated. Aperture number, structure, and position (collectively termed 'aperture pattern') are determined during microsporogenesis, which is the earliest step of pollen ontogeny. Here, we review current knowledge about aperture pattern developmental mechanisms and adaptive significance with respect to plant reproduction and how advances in these fields shed light on our understanding of aperture pattern evolution in angiosperms.

Evaluating the probability of CRISPR-based gene drive contaminating another species.

The probability D that a given clustered regularly interspaced short palindromic repeats (CRISPR)-based gene drive element contaminates another, nontarget species can be estimated by the following Drive Risk Assessment Quantitative Estimate (DRAQUE) Equation: D = h y b + t r a n s f × e x p r e s s × c u t × f l a n k × i m m u n e × n o n e x t i n c t with hyb = probability of hybridization between the target species and a nontarget species; transf = probability of horizontal transfer of a piece of DNA containing the gene drive cassette from the target species to a nontarget species (with no hybridization); express = probability that the Cas9 and guide RNA genes are expressed; cut = probability that the CRISPR-guide RNA recognizes and cuts at a DNA site in the new host; flank = probability that the gene drive cassette inserts at the cut site; immune = probability that the immune system does not reject Cas9-expressing cells; nonextinct = probability of invasion of the drive within the population. We discuss and estimate each of the seven parameters of the equation, with particular emphasis on possible transfers within insects, and between rodents and humans. We conclude from current data that the probability of a gene drive cassette to contaminate another species is not insignificant. We propose strategies to reduce this risk and call for more work on estimating all the parameters of the formula.

Pollen dispersal in sugar beet production fields.

Pollen-mediated gene flow has important implications for biodiversity conservation and for breeders and farmers' activities. In sugar beet production fields, a few sugar beet bolters can produce pollen as well as be fertilized by wild and weed beet. Since the crop, the wild beets, and the weed beets are the same species and intercross freely, the question of pollen flow is an important issue to determine the potential dispersal of transgenes from field to field and to wild habitats. We report here an experiment to describe pollen dispersal from a small herbicide-resistant sugar beet source towards male sterile target plants located along radiating lines up to 1,200 m away. Individual dispersal functions were inferred from statistical analyses and compared. Pollen limitation, as expected in root-production fields, was confirmed at all the distances from the pollen source. The number of resistant seeds produced by bait plants best fitted a fat-tailed probability distribution curve of pollen grains (power-law) dependent on the distance from the pollen source. A literature survey confirmed that power-law function could fit in most cases. The b coefficient was lower than 2. The number of fertilized flowers by background (herbicide-susceptible) pollen grains was uniform across the whole field. Airborne pollen had a fertilization impact equivalent to that of one adjacent bolter. The individual dispersal function from different pollen sources can be integrated to provide the pollen cloud composition for a given target plant, thus allowing modeling of gene flow in a field, inter-fields in a small region, and also in seed-production area. Long-distance pollen flow is not negligible and could play an important role in rapid transgene dispersal from crop to wild and weed beets in the landscape. The removing of any bolting, herbicide-resistant sugar beet should be compulsory to prevent the occurrence of herbicide-resistant weed beet, thus preventing gene flow to wild populations and preserving the sustainable utility of the resistant varieties. Whether such a goal is attainable remains an open question and certainly would be worth a large scale experimental study.

Males as somatic investment in a parthenogenetic nematode.

We report the reproductive strategy of the nematode Mesorhabditis belari This species produces only 9% males, whose sperm is necessary to fertilize and activate the eggs. However, most of the fertilized eggs develop without using the sperm DNA and produce female individuals. Only in 9% of eggs is the male DNA utilized, producing sons. We found that mixing of parental genomes only gives rise to males because the Y-bearing sperm of males are much more competent than the X-bearing sperm for penetrating the eggs. In this previously unrecognized strategy, asexual females produce few sexual males whose genes never reenter the female pool. Here, production of males is of interest only if sons are more likely to mate with their sisters. Using game theory, we show that in this context, the production of 9% males by M. belari females is an evolutionary stable strategy.

Mixing of propagules from discrete sources at long distance: comparing a dispersal tail to an exponential.

BACKGROUND: Rare long distance dispersal events impact the demography and the genetic structure of populations. When dispersal is modelled via a dispersal kernel, one possible characterisation of long-distance dispersal is given by the shape of the tail of the kernel, i.e. its type of decay. This characteristic is known to directly act on the speed and pattern of colonization, and on the spatial structure of genetic diversity during colonization. In particular, colonization waves behave differently depending on whether the kernel decreases faster or slower than an exponential (i.e. is thin-tailed vs. fat-tailed). To interpret and extend published results on the impact of long-distance dispersal on the genetic structure of populations, we examine a classification of dispersal kernels based on the shape of their tails and formally demonstrate qualitative differences among them that can influence the predicted diversity of a propagule pool sampled far from two distinct sources. RESULTS: We show that a fat-tailed kernel leads asymptotically to a diverse propagule pool containing a balanced mixing of the propagules from the two sources, whereas a thin-tailed kernel results in all propagules originating from the closest source. We further show that these results hold for biologically relevant distances under certain circumstances, and in particular if the number of propagules is large enough, as would be the case for pollen or seeds. CONCLUSION: To understand the impact of long-distance dispersal on the structure and dynamics of a metapopulation, it might be less important to precisely estimate an average dispersal distance than to determine if the tail of the dispersal kernel is fatter or thinner than that of an exponential function. Depending solely on this characteristic, a metapopulation will behave similarly to an island model with a diverse immigrant pool or to a stepping-stone model with migrants from closest populations. Our results further help to understand why thin-tailed dispersal kernels lead to a colonization wave of constant speed, whereas fat-tailed dispersal kernels lead to a wave of increasing speed. Our results also suggest that the diversity of the pollen cloud of a mother plant should increase with increasing isolation for fat-tailed kernels, whereas it should decrease for thin-tailed kernels.

Reproductive system and colonizing strategy of two species of Carduus (compositae).

Carduus pycnocephalus and C. tenuiflorus are two important weed species in mediterranean-type ecosystems. They were studied in their native habitat in southern France from April to December 1981.These species both produce two types of seed (achenes) in each capitulum. Those in the center are not dormant and are easily dispersed, while the outer ones can be dormant and have no apparent means of dispersal. Our observations on pollen transfer and self fertilization show that the dispersable, non dormant seeds have a low probability of inbreeding, while the potentially dormant, non dispersed seeds have a high probability of inbreeding. The significance of this dimorphism is discussed.

Lineage Selection and the Maintenance of Sex.

Sex predominates in eukaryotes, despite its short-term disadvantage when compared to asexuality. Myriad models have suggested that short-term advantages of sex may be sufficient to counterbalance its twofold costs. However, despite decades of experimental work seeking such evidence, no evolutionary mechanism has yet achieved broad recognition as explanation for the maintenance of sex. We explore here, through lineage-selection models, the conditions favouring the maintenance of sex. In the first model, we allowed the rate of transition to asexuality to evolve, to determine whether lineage selection favoured species with the strongest constraints preventing the loss of sex. In the second model, we simulated more explicitly the mechanisms underlying the higher extinction rates of asexual lineages than of their sexual counterparts. We linked extinction rates to the ecological and/or genetic features of lineages, thereby providing a formalisation of the only figure included in Darwin's "The origin of species". Our results reinforce the view that the long-term advantages of sex and lineage selection may provide the most satisfactory explanations for the maintenance of sex in eukaryotes, which is still poorly recognized, and provide figures and a simulation website for training and educational purposes. Short-term benefits may play a role, but it is also essential to take into account the selection of lineages for a thorough understanding of the maintenance of sex.

Sex expression and reproductive biology in a tree species, Fraxinus excelsior L.

We investigated Fraxinus excelsior breeding system using field data collected in a natural population and in a seed orchard. First, we attested functional trioecy (co-occurrence of males, hermaphrodites and females), with males producing pollen, hermaphrodites producing both pollen and seeds simultaneously, and females producing seeds. Second, we found that the reproductive system of F. excelsior was not labile, as sex expression seemed to be stable through time. Third, gender is genetically determined since different trees belonging to the same clone in the orchard exhibit similar sexual phenotypes.

Microsporogenesis variation in Codiaeum producing inaperturate pollen grain.

A study of microsporogenesis (the earliest stage of pollen ontogeny) was undertaken in seven cultivars of Codiaeum variegatum var. pictum, a eudicot species that produces inaperturate pollen grains. Microsporogenesis appears highly variable for the developmental events suspected to be implicated in the determination of aperture pattern. Most eudicots have tri-aperturate pollen grains and microsporogenesis is described as highly conserved in this clade. The observed burst of variation in C. variegatum therefore appears especially remarkable. A plausible hypothesis to explain the variation is that the pollen being inaperturate, the selective forces applying on the ontogeny of the aperture pattern are relaxed.

Constraints and selection: insights from microsporogenesis in Asparagales.

Developmental constraints have been proposed to interfere with natural selection in limiting the available set of potential adaptations. Whereas this concept has long been debated on theoretical grounds, it has been investigated empirically only in a few studies. In this article, we evaluate the importance of developmental constraints during microsporogenesis (male meiosis in plants), with an emphasis on phylogenetic patterns in Asparagales. Different developmental constraints were tested by character reshuffling or by simulated distributions. Among the different characteristics of microsporogenesis, only cell wall formation appeared as constrained. We show that constraints may also result from biases in the correlated occurrence of developmental steps (e.g., lack of successive cytokinesis when wall formation is centripetal). We document such biases and their potential outcomes, notably the establishment of intermediate stages, which allow development to bypass such constraints. These insights are discussed with regard to potential selection on pollen morphology.

Arming the enemy: the evolution of resistance to self-proteins.

A remarkable range of novel antibiotics is attracting increasing interest as a major new weapon in the campaign against bacterial infection. They are based on the toxic peptides that provide the innate immune system of animals, and it is claimed that bacteria will be unable to evolve resistance to them because they attack the 'Achilles' heel' of bacterial membrane structure. Both experimental evidence and theoretical arguments suggest that this claim is doubtful. If so, the introduction of these substances into general use may provoke the evolution of resistance to our own defence proteins and thus compromise our natural defences against infection.

POLLEN APERTURE POLYMORPHISM AND GAMETOPHYTE PERFORMANCE IN VIOLA DIVERSIFOLIA.

Pollen aperture polymorphism is studied in Viola diversifolia, where all plants produce three- and four-apertured pollen grains. We tested whether there are genetic differences among plants for the proportions of the different pollen morphs, and whether the morphs differ in gametophytic performance. Results show that the more apertures a pollen grain has, the more quickly it germinates but that few-apertured pollen grains have faster growing pollen tubes and longer life expectancies. The proportions of the different pollen morphs, together with pollen tube growth rates, may be inherited traits based on differences among maternal families. These results suggest that the different pollen morphs are favored in different pollination ecology situations. The production of several pollen morphs by the same individual could therefore be evolutionarily advantageous.