Models of mating-system evolution emphasize the importance of frequency-dependent interactions among mating partners. It is also known that outcross siring success and the selfing rate in self-compatible hermaphrodites can be density dependent. Here, we use array experiments to show that the mating system (i.e., the outcrossing rate) and the siring success of morphs with divergent sex allocation strategies are both density dependent and frequency dependent in androdioecious populations of the wind-pollinated, annual plant Mercurialis annua. In particular, the outcrossing rate is a decreasing function of the mean interplant distance, regulated by a negative exponential pollen fall-off curve. Our results indicate that pollen dispersed from a male inflorescence are over 60% more likely to sire outcrossed progeny than equivalent pollen dispersed from hermaphrodites, likely due to the fact that males, but not hermaphrodites, disperse their pollen from erect inflorescence stalks. Because of this difference, and because males of M.annua produce much more pollen than hermaphrodites, the presence of males in the experimental arrays reduced both the selfing rate and the outcross siring success of hermaphrodites. We use our results to infer a density threshold below which males are unable to persist with hermaphrodites but above which they can invade hermaphroditic populations. We discuss our findings in the context of a metapopulation model, in which males can only persist in well-established populations but are excluded from small, sparse populations, for example, in the early stages of colonization.
Sexual reproduction in non-vascular plants requires unicellular free-motile sperm to travel from male to female reproductive structures across the terrestrial landscape. Recent data suggest that microarthropods can disperse sperm in mosses. However, little is known about the chemical communication, if any, that is involved in this interaction or the relative importance of microarthropod dispersal compared to abiotic dispersal agents in mosses. Here we show that tissues of the cosmopolitan moss Ceratodon purpureus emit complex volatile scents, similar in chemical diversity to those described in pollination mutualisms between flowering plants and insects, that the chemical composition of C. purpureus volatiles are sex-specific, and that moss-dwelling microarthropods are differentially attracted to these sex-specific moss volatile cues. Furthermore, using experimental microcosms, we show that microarthropods significantly increase moss fertilization rates, even in the presence of water spray, highlighting the important role of microarthropod dispersal in contributing to moss mating success. Taken together, our results indicate the presence of a scent-based 'plant-pollinator-like' relationship that has evolved between two of Earth's most ancient terrestrial lineages, mosses and microarthropods.
Which conditions favour the evolution of hermaphroditism or separate sexes? One classical hypothesis states that an organism’s mode of locomotion (if any) when searching for a mate should influence breeding system evolution. We used published phylogenies to reconstruct evolutionary changes in adult mate‐search efficiency and breeding systems among multicellular organisms. Employing maximum‐likelihood analyses, we found that changes in adult mate‐search efficiency are significantly correlated with changes in breeding system, and this result is robust to uncertainties in the phylogenies. These data provide the first statistical support, across a broad range of taxa, for the hypothesis that breeding systems and mate‐search efficiency did not evolve independently. We discuss our results in context with other causal factors, such as inbreeding avoidance and sexual specialization, likely to affect breeding system evolution.
Bias in the adult sex ratio of a population, if not due to a biased primary sex ratio, may be due to differential mortality of males and females, which can occur during any life history stage. Yet, although adult sex-ratio bias is common in dioecious plant species, little is known about the demography of prereproductive individuals. Using a RAPD-PCR (randomly amplified polymorphic DNA) marker that co-segregates with female phenotype, I studied juvenile demography in the saltmarsh grass Distichlis spicata, which exhibits within-population sex-ratio variation (spatial segregation of the sexes) and has genetic sex determination. First, I surveyed populations of D. spicata to ascertain whether any environmental factor co-varies with local sex ratio, and I found that habitats with female majorities are located at significantly lower elevations in the marsh than are habitats with male majorities. In randomly collected seeds, the sex ratio was significantly biased toward females, but male and female seeds did not differ in mass. Using a subsample of these seeds, I conducted greenhouse and field experiments to examine whether differences in seed germination or seedling survival between the sexes explain sex-ratio variation along the micro-elevation gradient in the marsh. In greenhouse treatments designed to mimic field habitats with female majorities, more male seeds germinated than did female seeds. In habitats with female majorities in the field, significantly more female seedlings survived an extreme high tide than did male seedlings (25.17% of females vs. 13.49% of males). These results suggest that, in habitats with female majorities, gender-specific bias in seedling survivorship, rather than seed germination, is a causal factor in the underlying sex-ratio bias. In habitats with male majorities, seed germination and seedling survival did not differ between the sexes. This study is the first to document environment-dependent differential seed germination and seedling mortality between males and females in a dioecious plant species.
If males and females of a species differ in their effect on intraspecific competition then this can have significant ecological and evolutionary consequences because it can lead to size and mortality disparities between the sexes, and thus cause biased population sex ratios. If the degree of sexual dimorphism of competitive effect varies across environments then this variation can generate sex ratio variation within and between populations. In a California population of Distichlis spicata, a dioecious grass species exhibiting extreme within-population sex ratio variation (spatial segregation of the sexes), I evaluated the intraspecific competitive effects of male and female D. spicata seedlings in three soil types. The sex of seedlings was determined using a RAPD-PCR marker co-segregating with female phenotype. Distichlis spicata seedlings, regardless of sex, were six times larger when grown with male versus female conspecific seedlings in soil from microsites where the majority of D. spicata plants are female, and this sexual dimorphism of competitive effect was weaker or did not occur in other soil types. This study suggests that it is not just the higher costs of female versus male reproduction itself that cause spatial segregation of the sexes in D. spicata, but that differences in competitive abilities between the sexes--which occur as early as the seedling stage--can generate sex ratio variation.
Self-fertilization is a key difference of adaptive significance between species with combined versus separate sexes. In haploid-dominant species such as mosses and ferns, species with either combined or separate sexes (monoicous and dioicous, respectively) have the potential to self-fertilize (intergametophytic selfing), but being monoicous allows an additional mode of selfing (intragametophytic selfing). We used allozyme electrophoresis to estimate deviations from expected levels of heterozygosity under Hardy-Weinberg equilibrium to infer selfing rates in 10 moss species from 36 New Zealand populations. We found that while there were deficiencies of heterozygotes compared to expectation in both monoicous and dioicous mosses, monoicous species had significantly higher levels of heterozygote deficiency than dioicous species (F IS ¼ 0.8970.12 and 0.4170.11, respectively). Estimated selfing rates suggest that selfing occurs frequently in monoicous populations, and rarely in dioicous populations. However, in two dioicous species (Polytrichadelphus magellanicus and Breutelia pendula), we found significant indications of mixed mating or biparental inbreeding in a handful of populations. These data provide the first analysis of heterozygote deficiency and selfing among haploid-dominant species with breeding system variation, and we discuss our results with respect to the consequences of inbreeding depression and the evolution of breeding systems.
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