Melinda Pickup

Comparative analyses of sex-ratio variation in dioecious flowering plants.

Dioecious plant species commonly exhibit deviations from the equilibrium expectation of 1:1 sex ratio, but the mechanisms governing this variation are poorly understood. Here, we use comparative analyses of 243 species, representing 123 genera and 61 families to investigate ecological and genetic correlates of variation in the operational (flowering) sex ratio. After controlling for phylogenetic nonindependence, we examined the influence of growth form, clonality, fleshy fruits, pollen and seed dispersal vector, and the possession of sex chromosomes on sex‐ratio variation. Male‐biased flowering sex ratios were twice as common as female‐biased ratios. Male bias was associated with long‐lived growth forms (e.g., trees) and biotic seed dispersal and fleshy fruits, whereas female bias was associated with clonality, especially for herbaceous species, and abiotic pollen dispersal. Female bias occurred in species with sex chromosomes and there was some evidence for a greater degree of bias in those with heteromorphic sex chromosomes. Although the role of interactions among these correlates require further study, our results indicate that sex‐based differences in costs of reproduction, pollen and seed dispersal mechanisms and sex chromosomes can each play important roles in affecting flowering sex ratios in dioecious plants.

Ecological genetics of sex ratios in plant populations

In many angiosperm species, populations are reproductively subdivided into distinct sexual morphs including females, males and hermaphrodites. Sexual polymorphism is maintained by frequency-dependent selection, leading to predictable sex ratios at equilibrium. Charles Darwin devoted much of his book ‘The Different Forms of Flowers on Plants of the Same Species’ (1877) to investigating plant sexual polymorphisms and laid the foundation for many problems addressed today by integrating theory with empirical studies of the demography and genetics of populations. Here, we summarize our recent work on the ecological and genetic mechanisms influencing variation in sex ratios and their implications for evolutionary transitions among sexual systems. We present the results of a survey of sex ratios from 126 species from 47 angiosperm families and then address two general problems using examples from diverse angiosperm taxa: (i) the mechanisms governing biased sex ratios in dioecious species; (ii) the origins and maintenance of populations composed of females, males and hermaphrodites. Several themes are emphasized, including the importance of non-equilibrium conditions, the role of life history and demography in affecting sex ratios, the value of theory for modelling the dynamics of sex ratio variation, and the utility of genetic markers for investigating evolutionary processes in sexually polymorphic plant populations.

Population size, self-incompatibility and genetic rescue in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae)

Self-incompatibility systems function to prevent inbreeding, and work effectively in large, genetically diverse populations. However, a decrease in population size can reduce genetic diversity at the self-incompatibility locus, which leads to a reduction in mate availability and has important demographic implications for small populations. Currently, little is known about the response of self-incompatible polyploid species to a reduction in population size. In Rutidosis leptorrhynchoides there was a significant decrease in the within-population probability of fertilization with a decline in population size for diploid populations and a marginally significant relationship for tetraploid populations, suggesting that in small populations of both chromosome races fertilization success is reduced due to a decrease in self-incompatibility allele (S-allele) diversity. There was no significant difference between the slopes of the fertility–population size relationship for diploid and tetraploid populations which indicates a similar rate of decline in fertilization success with population size for both chromosome races. Fertilization success increased when crosses were undertaken between populations and this was significantly related to population size for diploid and tetraploid populations, indicating that small populations gain the greatest benefit to fertilization success from crossing between populations. For tetraploid populations the benefits of crossing between populations tended to decline more rapidly with increasing population size. These results suggest that for small populations that have reduced fertilization success, genetic rescue by introducing new genetic material from other populations is an important means of ameliorating mate limitation issues associated with reduced S-allele diversity in both diploid and tetraploid races.

Ecological context and metapopulation dynamics affect sex-ratio variation among dioecious plant populations

BACKGROUND AND AIMS Populations of dioecious flowering plants commonly exhibit heterogeneity in sex ratios and deviations from the equilibrium expectation of equal numbers of females and males. Yet the role of ecological and demographic factors in contributing towards biased sex ratios is currently not well understood. METHODS Species-level studies from the literature were analysed to investigate ecological correlates of among-population sex-ratio variation and metapopulation models and empirical data were used to explore the influence of demography and non-equilibrium conditions on flowering sex ratios. KEY RESULTS The survey revealed significant among-population heterogeneity in sex ratios and this was related to the degree of sampling effort. For some species, sex-ratio bias was associated with the proportion of non-reproductive individuals, with greater male bias in populations with a lower proportion of individuals that were flowering. Male-biased ratios were also found at higher altitudes and latitudes, and in more xeric sites. Simulations and empirical data indicated that clonal species exhibited greater heterogeneity in sex ratios than non-clonal species as a result of their slower approach to equilibrium. The simulations also indicated the importance of interactions between reproductive mode and founder effects, with greater departures from equilibrium in clonal populations with fewer founding individuals. CONCLUSIONS The results indicate that sex-based differences in costs of reproduction and non-equilibrium conditions can each play important roles in affecting flowering sex ratios in populations of dioecious plants.

Source population characteristics affect heterosis following genetic rescue of fragmented plant populations

Understanding the relative importance of heterosis and outbreeding depression over multiple generations is a key question in evolutionary biology and is essential for identifying appropriate genetic sources for population and ecosystem restoration. Here we use 2455 experimental crosses between 12 population pairs of the rare perennial plant Rutidosis leptorrhynchoides (Asteraceae) to investigate the multi-generational (F1, F2, F3) fitness outcomes of inter-population hybridization. We detected no evidence of outbreeding depression, with inter-population hybrids and backcrosses showing either similar fitness or significant heterosis for fitness components across the three generations. Variation in heterosis among population pairs was best explained by characteristics of the foreign source or home population, and was greatest when the source population was large, with high genetic diversity and low inbreeding, and the home population was small and inbred. Our results indicate that the primary consideration for maximizing progeny fitness following population augmentation or restoration is the use of seed from large, genetically diverse populations.

Reversal of height dimorphism promotes pollen and seed dispersal in a wind-pollinated dioecious plant

Variation in the timing of reproductive functions in dioecious organisms may result in adaptive changes in the direction of sexual dimorphism during the breeding season. For plants in which both pollen and seeds are wind-dispersed, it may be advantageous for male plants to be taller when pollen is dispersed and female plants to be taller when seeds are dispersed. We examined the dynamics of height dimorphism in Rumex hastatulus, an annual, wind-pollinated, dioecious plant from the southern USA. A field survey of seven populations indicated that females were significantly taller than males at seed maturity. However, a glasshouse experiment revealed a more complex pattern of height growth during the life cycle. No dimorphism was evident prior to reproduction for six of seven populations, but at flowering, males were significantly taller than females in all populations. This pattern was reversed at reproductive maturity, consistent with field observations. Males flowered later than females and the degree of height dimorphism was greater in populations with a later onset of male flowering. We discuss the potential adaptive significance of temporal changes in height dimorphism for pollen and seed dispersal, and how this may be optimized for the contrasting reproductive functions of the sexes.

The influence of demography and local mating environment on sex ratios in a wind-pollinated dioecious plant

Negative frequency-dependent selection should result in equal sex ratios in large populations of dioecious flowering plants, but deviations from equality are commonly reported. A variety of ecological and genetic factors can explain biased sex ratios, although the mechanisms involved are not well understood. Most dioecious species are long-lived and/or clonal complicating efforts to identify stages during the life cycle when biases develop. We investigated the demographic correlates of sex-ratio variation in two chromosome races of Rumex hastatulus, an annual, wind-pollinated colonizer of open habitats from the southern USA. We examined sex ratios in 46 populations and evaluated the hypothesis that the proximity of males in the local mating environment, through its influence on gametophytic selection, is the primary cause of female-biased sex ratios. Female-biased sex ratios characterized most populations of R. hastatulus (mean sex ratio = 0.62), with significant female bias in 89% of populations. Large, high-density populations had the highest proportion of females, whereas smaller, low-density populations had sex ratios closer to equality. Progeny sex ratios were more female biased when males were in closer proximity to females, a result consistent with the gametophytic selection hypothesis. Our results suggest that interactions between demographic and genetic factors are probably the main cause of female-biased sex ratios in R. hastatulus. The annual life cycle of this species may limit the scope for selection against males and may account for the weaker degree of bias in comparison with perennial Rumex species.

THE INFLUENCE OF POLLINATION INTENSITY ON FERTILIZATION SUCCESS, PROGENY SEX RATIO, AND FITNESS IN A WIND-POLLINATED, DIOECIOUS PLANT

Variation in pollination intensity can influence the degree of gametophytic competition with diverse consequences for plant fitness. Such effects should be particularly important in wind-pollinated plants because they commonly possess uniovulate flowers. In several dioecious species, competition between female- and male-determining microgametophytes has been proposed as a cause of female-biased sex ratios. Here, we examine functional relations among pollination intensity, seed set, sex ratios, and sporophyte vigor in Rumex hastatulus, a wind-pollinated, dioecious plant. Using controlled pollinations, we applied a range of pollen grain numbers (1–71) to female flowers. Pollination intensity significantly predicted percent seed set, which was >80% when more than 15 pollen grains were added to stigmas. We estimated that the proportion of pollen grains participating in fertilization was 0.28 and the proportion of fertilized ovules developing into seed was 0.89. Overall, progeny sex ratios were female biased (0.62), with an increased probability of female offspring over the range of 1–15 pollen grains. We detected no effect of pollination intensity on sporophytic vigor. Our study is the first to investigate the relation between pollination intensity and female fertility in a wind-pollinated species and provides support for the contribution of gametophytic competition to sex ratio variation in plants.

Predicting local adaptation in fragmented plant populations: implications for restoration genetics.

Understanding patterns and correlates of local adaptation in heterogeneous landscapes can provide important information in the selection of appropriate seed sources for restoration. We assessed the extent of local adaptation of fitness components in 12 population pairs of the perennial herb Rutidosis leptorrhynchoides (Asteraceae) and examined whether spatial scale (0.7–600 km), environmental distance, quantitative (QST) and neutral (FST) genetic differentiation, and size of the local and foreign populations could predict patterns of adaptive differentiation. Local adaptation varied among populations and fitness components. Including all population pairs, local adaptation was observed for seedling survival, but not for biomass, while foreign genotype advantage was observed for reproduction (number of inflorescences). Among population pairs, local adaptation increased with QST and local population size for biomass. QST was associated with environmental distance, suggesting ecological selection for phenotypic divergence. However, low FST and variation in population structure in small populations demonstrates the interaction of gene flow and drift in constraining local adaptation in R. leptorrhynchoides. Our study indicates that for species in heterogeneous landscapes, collecting seed from large populations from similar environments to candidate sites is likely to provide the most appropriate seed sources for restoration.

The dynamics of resource allocation and costs of reproduction in a sexually dimorphic, wind‐pollinated dioecious plant

Sexual dimorphism in resource allocation is expected to change during the life cycle of dioecious plants because of temporal differences between the sexes in reproductive investment. Given the potential for sex-specific differences in reproductive costs, resource availability may contribute to variation in reproductive allocation in females and males. Here, we used Rumex hastatulus, a dioecious, wind-pollinated annual plant, to investigate whether sexual dimorphism varies with life-history stage and nutrient availability, and determine whether allocation patterns differ depending on reproductive commitment. To examine if the costs of reproduction varied between the sexes, reproduction was either allowed or prevented through bud removal, and biomass allocation was measured at maturity. In a second experiment to assess variation in sexual dimorphism across the life cycle, and whether this varied with resource availability, plants were grown in high and low nutrients and allocation to roots, aboveground vegetative growth and reproduction were measured at three developmental stages. Males prevented from reproducing compensated with increased above- and belowground allocation to a much larger degree than females, suggesting that male reproductive costs reduce vegetative growth. The proportional allocation to roots, reproductive structures and aboveground vegetative growth varied between the sexes and among life-cycle stages, but not with nutrient treatment. Females allocated proportionally more resources to roots than males at peak flowering, but this pattern was reversed at reproductive maturity under low-nutrient conditions. Our study illustrates the importance of temporal dynamics in sex-specific resource allocation and provides support for high male reproductive costs in wind-pollinated plants.