Variation in sexual dimorphism in a wind-pollinated plant: The influence of geographical context and life-cycle dynamics

Understanding the mechanisms causing phenotypic differences between females and males has long fascinated evolutionary biologists. An extensive literature exists on animal sexual dimorphism but less information is known about sex differences in plants, particularly the extent of geographical variation in sexual dimorphism and its life‐cycle dynamics. Here, we investigated patterns of genetically based sexual dimorphism in vegetative and reproductive traits of a wind‐pollinated dioecious plant, Rumex hastatulus, across three life‐cycle stages using open‐pollinated families from 30 populations spanning the geographic range and chromosomal variation (XY and XY1Y2) of the species. The direction and degree of sexual dimorphism was highly variable among populations and life‐cycle stages. Sex‐specific differences in reproductive function explained a significant amount of temporal change in sexual dimorphism. For several traits, geographical variation in sexual dimorphism was associated with bioclimatic parameters, likely due to the differential responses of the sexes to climate. We found no systematic differences in sexual dimorphism between chromosome races. Sex‐specific trait differences in dioecious plants largely result from a balance between sexual and natural selection on resource allocation. Our results indicate that abiotic factors associated with geographical context also play a role in modifying sexual dimorphism during the plant life‐cycle

Sexual Dimorphism of Staminate- and Pistillate-Phase Flowers of Saponaria officinalis (Bouncing Bet) Affects Pollinator Behavior and Seed Set

The sequential separation of male and female function in flowers of dichogamous species allows for the evolution of differing morphologies that maximize fitness through seed siring and seed set. We examined staminate- and pistillate-phase flowers of protandrous Saponaria officinalis for dimorphism in floral traits and their effects on pollinator attraction and seed set. Pistillate-phase flowers have larger petals, greater mass, and are pinker in color, but due to a shape change, pistillate-phase flowers have smaller corolla diameters than staminate-phase flowers. There was no difference in nectar volume or sugar content one day after anthesis, and minimal evidence for UV nectar guide patterns in staminate- and pistillate-phase flowers. When presented with choice arrays, pollinators discriminated against pistillate-phase flowers based on their pink color. Finally, in an experimental garden, in 2012 there was a negative correlation between seed set of an open-pollinated, emasculated flower and pinkness (as measured by reflectance spectrometry) of a pistillate-phase flower on the same plant in plots covered with shade cloth. In 2013, clones of genotypes chosen from the 2012 plants that produced pinker flowers had lower seed set than those from genotypes with paler flowers. Lower seed set of pink genotypes was found in open-pollinated and hand-pollinated flowers, indicating the lower seed set might be due to other differences between pink and pale genotypes in addition to pollinator discrimination against pink flowers. In conclusion, staminate- and pistillate-phase flowers of S. officinalis are dimorphic in shape and color. Pollinators discriminate among flowers based on these differences, and individuals whose pistillate-phase flowers are most different in color from their staminate-phase flowers make fewer seeds. We suggest morphological studies of the two sex phases in dichogamous, hermaphroditic species can contribute to understanding the evolution of sexual dimorphism in plants without the confounding effects of genetic differences between separate male and female individuals

Two's Company, Three's a Crowd: Experimental Evaluation of the Evolutionary Maintenance of Trioecy in Mercurialis annua (Euphorbiaceae)

Trioecy is an uncommon sexual system in which males, females, and hermaphrodites co-occur as three clearly different gender classes. The evolutionary stability of trioecy is unclear, but would depend on factors such as hermaphroditic sex allocation and rates of outcrossing vs. selfing. Here, trioecious populations of Mercurialis annua are described for the first time. We examined the frequencies of females, males and hermaphrodites across ten natural populations and evaluated the association between the frequency of females and plant densities. Previous studies have shown that selfing rates in this species are density-dependent and are reduced in the presence of males, which produce substantially more pollen than hermaphrodites. Accordingly, we examined the evolutionary stability of trioecy using an experiment in which we (a) indirectly manipulated selfing rates by altering plant densities and the frequency of males in a fully factorial manner across 20 experimental plots and (b) examined the effect of these manipulations on the frequency of the three sex phenotypes in the next generation of plants. In the parental generation, we measured the seed and pollen allocations of hermaphrodites and compared them with allocations by unisexual plants. In natural populations, females occurred at higher frequencies in denser patches, a finding consistent with our expectations. Under our experimental conditions, however, no combination of plant densities and male frequencies was associated with increased frequencies of females. Our results suggest that the factors that regulate female frequencies in trioecious populations of M. annua are independent of those regulating male frequencies (density), and that the stable co-existence of all three sex phenotypes within populations is unlikely

Evolution of sex-biased gene expression in a dioecious plant

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A temporal dimension to the influence of pollen rewards on bee behaviour and fecundity in Aloe tenuior

The net effect of pollen production on fecundity in plants can range from negative – when self-pollen interferes with fecundity due to incompatibility mechanisms, to positive – when pollen availability is associated with increased pollinator visitation and fecundity due to its utilization as a reward. We investigated the responses of bees to pollen and nectar rewards, and the effects of these rewards on pollen deposition and fecundity in the hermaphroditic succulent shrub Aloe tenuior. Self-pollinated plants failed to set fruit, but their ovules were regularly penetrated by self-pollen tubes, which uniformly failed to develop into seeds as expected from ovarian self-incompatibility (or strong early inbreeding depression). Bees consistently foraged for pollen during the morning and early afternoon, but switched to nectar in the late afternoon. As a consequence of this differential foraging, we were able to test the relative contribution to fecundity of pollen- versus nectar-collecting flower visitors. We exposed emasculated and intact flowers in either the morning or late afternoon to foraging bees and showed that emasculation reduced pollen deposition by insects in the morning, but had little effect in the afternoon. Despite the potential for self-pollination to result in ovule discounting due to late-acting self-sterility, fecundity was severely reduced in artificially emasculated plants. Although there were temporal fluctuations in reward preference, most bee visits were for pollen rewards. Therefore the benefit of providing pollen that is accessible to bee foragers outweighs any potential costs to fitness in terms of gender interference in this species

What explains rare and conspicuous colours in a snail? A test of time-series data against models of drift, migration or selection

It is intriguing that conspicuous colour morphs of a prey species may be maintained at low frequencies alongside cryptic morphs. Negative frequency-dependent selection by predators using search images ('apostatic selection') is often suggested without rejecting alternative explanations. Using a maximum likelihood approach we fitted predictions from models of genetic drift, migration, constant selection, heterozygote advantage or negative frequency-dependent selection to time-series data of colour frequencies in isolated populations of a marine snail (Littorina saxatilis), re-established with perturbed colour morph frequencies and followed for >20 generations. Snails of conspicuous colours (white, red, banded) are naturally rare in the study area (usually <10%) but frequencies were manipulated to levels of ~50% (one colour per population) in 8 populations at the start of the experiment in 1992. In 2013, frequencies had declined to ~15-45%. Drift alone could not explain these changes. Migration could not be rejected in any population, but required rates much higher than those recorded. Directional selection was rejected in three populations in favour of balancing selection. Heterozygote advantage and negative frequency-dependent selection could not be distinguished statistically, although overall the results favoured the latter. Populations varied idiosyncratically as mild or variable colour selection (3-11%) interacted with demographic stochasticity, and the overall conclusion was that multiple mechanisms may contribute to maintaining the polymorphisms.Heredity advance online publication, 21 September 2016; doi:10.1038/hdy.2016.77

R-gene variation across Arabidopsis lyrata subspecies: effects of population structure, selection and mating system.

BACKGROUND: Examining allelic variation of R-genes in closely related perennial species of Arabidopsis thaliana is critical to understanding how population structure and ecology interact with selection to shape the evolution of innate immunity in plants. We finely sampled natural populations of Arabidopsis lyrata from the Great Lakes region of North America (A. l. lyrata) and broadly sampled six European countries (A. l. petraea) to investigate allelic variation of two R-genes (RPM1 and WRR4) and neutral genetic markers (Restriction Associated DNA sequences and microsatellites) in relation to mating system, phylogeographic structure and subspecies divergence. RESULTS: Fine-scale sampling of populations revealed strong effects of mating system and population structure on patterns of polymorphism for both neutral loci and R-genes, with no strong evidence for selection. Broad geographic sampling revealed evidence of balancing selection maintaining polymorphism in R-genes, with elevated heterozygosity and diversity compared to neutral expectations and sharing of alleles among diverged subspecies. Codon-based tests detected both positive and purifying selection for both R-genes, as commonly found for animal immune genes. CONCLUSIONS: Our results highlight that combining fine and broad-scale sampling strategies can reveal the multiple factors influencing polymorphism and divergence at potentially adaptive genes such as R-genes

Pollen Competition as a Reproductive Isolation Barrier Represses Transgene Flow between Compatible and Co-Flowering Citrus Genotypes

Background/Objective: Despite potential benefits granted by genetically modified (GM) fruit trees, their release and commercialization raises concerns about their potential environmental impact, and the transfer via pollen of transgenes to cross-compatible cultivars is deemed to be the greatest source for environmental exposure. Information compiled from field trials on GM trees is essential to propose measures to minimize the transgene dispersal. We have conducted a field trial of seven consecutive years to investigate the maximum frequency of pollen-mediated crop-to-crop transgene flow in a citrus orchard, and its relation to the genetic, phenological and environmental factors involved. Methodology/Principal Findings: Three different citrus genotypes carrying the uidA (GUS) tracer marker gene (pollen donors) and a non-GM self-incompatible contiguous citrus genotype (recipient) were used in conditions allowing natural entomophilous pollination to occur. The examination of 603 to 2990 seeds per year showed unexpectedly low frequencies (0.17-2.86%) of transgene flow. Paternity analyses of the progeny of subsets of recipient plants using 10 microsatellite (SSR) loci demonstrated a higher mating competence of trees from another non-GM pollen source population that greatly limited the mating chance of the contiguous cross-compatible and flowering-synchronized transgenic pollen source. This mating superiority could be explained by a much higher pollen competition capacity of the non-GM genotypes, as was confirmed through mixed-hand pollinations. Conclusions/Significance: Pollen competition strongly contributed to transgene confinement. Based on this finding, suitable isolation measures are proposed for the first time to prevent transgene outflow between contiguous plantings of citrus types that may be extendible to other entomophilous transgenic fruit tree species. (Résumé d'auteur

A rare exception to Haldane's rule: are X chromosomes key to hybrid incompatibilities?

This work was funded by NERC (NE/G014906/1, NE/L011255/1, NE/I027800/1). Additional funding from the Orthopterists’ Society to PM is also gratefully acknowledged.The prevalence of Haldane’s rule suggests that sex chromosomes commonly have a key role in reproductive barriers and speciation. However, the majority of research on Haldane’s rule has been conducted in species with conventional sex determination systems (XY and ZW) and exceptions to the rule have been understudied. Here we test the role of X-linked incompatibilities in a rare exception to Haldane’s rule for female sterility in field cricket sister species (Teleogryllus oceanicus and T. commodus). Both have an XO sex determination system. Using three generations of crosses, we introgressed X chromosomes from each species onto different, mixed genomic backgrounds to test predictions about the fertility and viability of each cross type. We predicted that females with two different species X chromosomes would suffer reduced fertility and viability compared with females with two parental X chromosomes. However, we found no strong support for such X-linked incompatibilities. Our results preclude X–X incompatibilities and instead support an interchromosomal epistatic basis to hybrid female sterility. We discuss the broader implications of these findings, principally whether deviations from Haldane’s rule might be more prevalent in species without dimorphic sex chromosomes.PostprintPeer reviewe