FREQUENCY-DEPENDENT FITNESS IN SILENE VULGARIS,A GYNODIOECIOUS PLANT

In gynodioecious plants the selective processes that determine the relative number of female and hermaphroditic individuals are often frequency dependent. Frequency-dependent fitness can occur in the two sexes through a variety of mechanisms, especially given pollen limitation and inbreeding depression when hermaphrodites are rare. Frequency dependence in several components of the fitness of female and hermaphroditic Silene vulgaris was tested in experiments in which the relative numbers of the two sexes was varied among 12 artificial populations. In females, the proportion of flowers that set fruit covaried positively among populations with the frequency of hermaphrodites in two separate experiments, whereas the number of flowers/plant covaried negatively in one case. In hermaphrodites, the number of seeds/fruit covaried positively with the frequency of hermaphrodites, whereas the fitness of hermaphrodites estimated through pollen transfer covaried negatively. The results are discussed as they relate to the selective maintenance of gynodioecy in S. vulgaris and in light of a recent model of the effect of population structure on selection in gynodioecious systems.     

An association between chloroplast DNA haplotypeand gender in a plant metapopulation

Theoretical models have shown that metapopulation structure can influence the evolution of the sex ratio in gynodioecious plants when the fitness of females and/or hermaphrodites varies among populations with the local sex ratio. Such frequency-dependent fitness has been demonstrated previously in natural populations of Silene vulgaris, a gynodioecious plant in which sex determination is cytonuclear. We investigated whether there was an association between chloroplast DNA (cpDNA) haplotype and sex expression, with the assumption that cpDNA haplotypes could be associated with specific male sterility variants likely found in the mitochondrial DNA, owing to co-transmission of the two cytoplasmic genomes. Two cpDNA haplotypes were studied in a collection of 111 individuals of known sex taken from 20 natural populations found in Virginia, USA. The set of haplotype 1 individuals consisted of 71.4% hermaphrodites, where as only 7.7% of the haplotype 2 individuals were hermaphroditic; a highly statistically significant difference. By extension of a previous model it was also shown that the differential clustering of these two haplotypes into local populations contributes to among-population sex ratio variation and has the potential to lower the fitness of haplotype 2 by greater than 50%, relative to that expected with no population structure. This revised version was published online in July 2006 with corrections to the Cover Date.     

Fine scale spatial structuring of sex and mitochondria in Silene vulgaris

Fine scale spatial structure (FSSS) of cytoplasmic genes in plants is thought to be generated via founder events and can be amplified when seeds germinate close to their mother. In gynodioecious species these processes are expected to generate FSSS in sex ratio because maternally inherited cytoplasmic male sterility genes partially influence sex expression. Here we document a striking example of FSSS in both mitochondrial genetic markers and sex in roadside populations of Silene vulgaris. We show that in one population FSSS of sexes influences relative fruit production of females compared to hermaphrodites. Furthermore, FSSS in sex ratio is expected to persist into future generations because offspring sex ratios from females are female-biased whereas offspring sex ratios from hermaphrodites are hermaphrodite-biased. Earlier studies indicated that pollen limitation is the most likely mechanism underlying negative frequency dependent fitness of females. Our results support the theoretical predictions that FSSS in sex ratio can reduce female fitness by decreasing the frequency at which females experience hermaphrodites. We argue that the influence of FSSS on female fitness is complementary to the influence of larger scale population structure on female fitness, and that population structure at both scales will act to decrease female frequencies in gynodioecious species. Better comprehension of the spatial structure of genders and genes controlling sex expression at a local scale is required for future progress toward understanding sex ratio evolution in gynodioecious plants.     

SEX RATIO VARIATION AMONG GYNODIOECIOUS POPULATIONS OF SEA BEET: CAN IT BE EXPLAINED BY NEGATIVE FREQUENCY‐DEPENDENT SELECTION?

This study is devoted to assess sex ratio variation among 33 populations of the gynodioecious Beta vulgaris ssp. maritima in Brittany (France) and to explore the causes of this variation. We showed that three different CMS (cytoplasmic male sterility) cytotypes occurred in populations, but strongly differed for their frequencies and the frequency of their associated nuclear restorer alleles (which counteract the effect of CMS and restore male fertility). No correlation was found between CMS and restorer frequencies within populations, which has been previously interpreted as a result of stochasticity. However, neutral genetic variation did not indicate recent population bottlenecks in studied populations. Moreover, no significant correlation was found between female frequency or variance and current population size. Consequently, stochastic processes could not be the major cause of sex ratio variation. Alternatively, empirical estimations of the variation of females, CMS genes and nuclear restorer allele's frequencies were compared to theoretical predictions based on a frequency‐dependent selection model of gynodioecy. In particular, we showed that an absence of correlation between CMS and restorer frequencies could also occur without stochasticity. The large variation of sex ratio in Beta vulgaris could thus be explained by frequency‐dependent selection acting on CMS genes and restorer alleles.     

Constrained evolution of the sex comb in Drosophila simulans

Male fitness is dependent on sexual traits that influence mate acquisition (precopulatory sexual selection) and paternity (post‐copulatory sexual selection), and although many studies have documented the form of selection in one or the other of these arenas, fewer have done it for both. Nonetheless, it appears that the dominant form of sexual selection is directional, although theoretically, populations should converge on peaks in the fitness surface, where selection is stabilizing. Many factors, however, can prevent populations from reaching adaptive peaks. Genetic constraints can be important if they prevent the development of highest fitness phenotypes, as can the direction of selection if it reverses across episodes of selection. In this study, we examine the evidence that these processes influence the evolution of the multivariate sex comb morphology of male Drosophila simulans. To do this, we conduct a quantitative genetic study together with a multivariate selection analysis to infer how the genetic architecture and selection interact. We find abundant genetic variance and covariance in elements of the sex comb. However, there was little evidence for directional selection in either arena. Significant nonlinear selection was detected prior to copulation when males were mated to nonvirgin females, and post‐copulation during sperm offence (again with males mated to nonvirgins). Thus, contrary to our predictions, the evolution of the D. simulans sex comb is limited neither by genetic constraints nor by antagonistic selection between pre‐ and post‐copulatory arenas, but nonlinear selection on the multivariate phenotype may prevent sex combs from evolving to reach some fitness maximizing optima.     

Optimal age of maturity in fluctuating environments under r‐ and K‐selection

Optimality models for evolution of life histories have shown that increased environmental stochasticity promotes early age of maturity. Here we argue that if r‐selection for early maturation implies a tradeoff making those phenotypes more sensitive to a change in population size than phenotypes maturing at older ages, K‐selection can favor delayed onset of maturation. We analyze a general stochastic Leslie‐matrix model with a simplified density regulation affecting all survivals equally through a function of the population vector, often called the ‘critical age class’. We show that the outcome of such an age‐dependent r‐ and K‐selection is that the expected value of the ‘critical age class’ is maximized by evolution, a strategy strongly influenced by the magnitude of the environmental stochasticity. We also demonstrate that evolution caused by such density‐dependent selection influences the population dynamics, showing a possible reciprocal effect between ecology and evolution in age‐structured populations. This modeling approach reveals that changes in population size affecting the fitness of phenotypes with different age of maturity may be an important selective agent for variation in onset of reproduction in fluctuating environments. This provides a testable hypothesis for how patterns in the population dynamics should affect life history variation.     

Sex ratio in populations of Silene otites in relation to vegetation cover,population size and fungal infection

Abstract. In contrast to populations of most dioecious Silene species (which usually are female-biased), populations of Silene otites have been frequently reported to be male-biased. We describe sex ratio variation in 34 natural S. otites populations in Central Germany in relation to vegetation cover, population size and fungal infection. The overall sex ratio was unbiased in 1994 and only slightly male-biased in 1995. Sex ratio varied among the populations from 26.6 % to 72.6 % females. The sex ratio of small populations varied strongly due to stochastic processes. Furthermore, we found that populations in habitats with high vegetation cover contained a higher percentage of females. Hermaphroditic plants, theoretically, could increase male bias as they only produce male or hermaphroditic offspring. Their frequency in the populations, however, was far too low to affect sex ratio. In 1994 12.1 % and in 1995 17.0 % of the plants were infected by the smut fungus Ustilago major. Disease incidence in the population was not related to sex ratio, suggesting equal susceptibility of males and females. The sex ratio of partially infected plants did not deviate from the population sex ratio, both under field conditions and in a greenhouse laboratory experiment. The results suggest that the frequently reported male bias in Silene otites populations is not a general pattern, but is mainly caused by environmental conditions.     

Evolution under pH stress and high population densities leads to increased density-dependent fitness in the protist Tetrahymena thermophila

Abiotic stress is a major force of selection that organisms are constantly facing. While the evolutionary effects of various stressors have been broadly studied, it is only more recently that the relevance of interactions between evolution and underlying ecological conditions, that is, eco-evolutionary feedbacks, have been highlighted. Here, we experimentally investigated how populations adapt to pH-stress under high population densities. Using the protist species Tetrahymena thermophila, we studied how four different genotypes evolved in response to stressfully low pH conditions and high population densities. We found that genotypes underwent evolutionary changes, some shifting up and others shifting down their intrinsic rates of increase (r₀). Overall, evolution at low pH led to the convergence of r₀ and intraspecific competitive ability (α) across the four genotypes. Given the strong correlation between r₀ and α, we argue that this convergence was a consequence of selection for increased density-dependent fitness at low pH under the experienced high density conditions. Increased density-dependent fitness was either attained through increase in r₀, or decrease of α, depending on the genetic background. In conclusion, we show that demography can influence the direction of evolution under abiotic stress.     

POPULATION SEX STRUCTURE AND REPRODUCTIVE FITNESS IN GYNODIOECIOUS SIDALCEA MALVIFLORA MALVIFLORA (MALVACEAE)

The spatial distribution of females and hermaphrodites within gynodioecious populations is expected to exert considerable selective pressure on gender fitness through pollen limitation of seed set. If pollen flow is predominantly local, seed set in individual plants may be sensitive to the proximity of pollen donors; pollen limitation of seed set may occur if hermaphrodites are locally rare. Under such circumstances, female fitness will be negatively frequency dependent and hermaphrodite fitness will be positively frequency dependent. Given local seed dispersal, a nonrandom clumped distribution of the genders is expected in gynodioecious populations due to the heritability of gender in gynodioecious species. If gender fitness is frequency dependent, such structure should favor hermaphrodites and select against females. To test this hypothesis, I quantified the distribution of the genders in terms of nearest neighbors and neighborhood sex ratio in two populations of gynodioecious Sidalcea malviflora malviflora. I then measured the effect of neighborhood sex ratio on open-pollinated seed set and pollen limitation in both manipulated and unmanipulated neighborhoods. Results indicate that the genders have a patchy distribution and that both genders are pollen limited and show an increase in seed set with an increase in neighborhood hermaphrodite frequency. The observed population sex structure favors hermaphrodites and disadvantages females. These results highlight the importance that population-level traits can have in determining individual fitness and the evolution of sex ratios in gynodioecious species.     

Genomic admixture increases fitness during a biological invasion

Abstract During biological invasions, multiple introductions can provide opportunities for admixture among genetically distinct lineages. Admixture is predicted to contribute to invasion success by directly increasing fitness through hybrid vigour or by enhancing evolutionary potential within populations . Here, we demonstrate genome‐wide admixture during an invasion that substantially boosted fitness in the cosmopolitan weed, Silene vulgaris. We identified three divergent demes in the native European range that expanded from glacial refugia and experienced historical admixture in a well‐known suture zone. During recent invasion of North America, multiple introductions created additional opportunities for admixture. In common garden experiments, recombinant genotypes from North America experienced a two‐fold increase in fitness relative to nonrecombinants, whereas recombinant genotypes from Europe showed no lasting fitness benefits. This contrast implicates hybrid vigour behind the boost in fitness and supports the hypothesis that admixture can lead to fitness increases that may catapult invasion into a new range.     

Rapid evolution of the intersexual genetic correlation for fitness in Drosophila melanogaster

Sexual antagonism (SA) arises when male and female phenotypes are under opposing selection, yet genetically correlated. Until resolved, antagonism limits evolution toward optimal sex‐specific phenotypes. Despite its importance for sex‐specific adaptation and existing theory, the dynamics of SA resolution are not well understood empirically. Here, we present data from Drosophila melanogaster, compatible with a resolution of SA. We compared two independent replicates of the “LH_M” population in which SA had previously been described. Both had been maintained under identical, controlled conditions, and separated for around 200 generations. Although heritabilities of male and female fitness were similar, the intersexual genetic correlation differed significantly, being negative in one replicate (indicating SA) but close to zero in the other. Using population sequencing, we show that phenotypic differences were associated with population divergence in allele frequencies at nonrandom loci across the genome. Large frequency changes were more prevalent in the population without SA and were enriched at loci mapping to genes previously shown to have sexually antagonistic relationships between expression and fitness. Our data suggest that rapid evolution toward SA resolution has occurred in one of the populations and open avenues toward studying the genetics of SA and its resolution.     

Scale dependence of sex ratio in wild plant populations: implications for social selection

Social context refers to the composition of an individual''s social interactants, including potential mates. In spatially structured populations, social context can vary among individuals within populations, generating the opportunity for social selection to drive differences in fitness functions among individuals at a fine spatial scale. In sexually polymorphic plants, the local sex ratio varies at a fine scale and thus has the potential to generate this opportunity. We measured the spatial distribution of two wild populations of the gynodioecious plant Silene vulgaris and show that there is fine‐scale heterogeneity in the local distribution of the sexes within these populations. We demonstrate that the largest variance in sex ratio is among nearest neighbors. This variance is greatly reduced as the spatial scale of social interactions increases. These patterns suggest the sex of neighbors has the potential to generate fine‐scale differences in selection differentials among individuals. One of the most important determinants of social interactions in plants is the behavior of pollinators. These results suggest that the potential for selection arising from sex ratio will be greatest when pollen is shared among nearest neighbors. Future studies incorporating the movement of pollinators may reveal whether and how this fine‐scale variance in sex ratio affects the fitness of individuals in these populations.     

Negative frequency‐dependent selection maintains coexisting genotypes during fluctuating selection

Natural environments are rarely static; rather selection can fluctuate on timescales ranging from hours to centuries. However, it is unclear how adaptation to fluctuating environments differs from adaptation to constant environments at the genetic level. For bacteria, one key axis of environmental variation is selection for planktonic or biofilm modes of growth. We conducted an evolution experiment with Burkholderia cenocepacia, comparing the evolutionary dynamics of populations evolving under constant selection for either biofilm formation or planktonic growth with populations in which selection fluctuated between the two environments on a weekly basis. Populations evolved in the fluctuating environment shared many of the same genetic targets of selection as those evolved in constant biofilm selection, but were genetically distinct from the constant planktonic populations. In the fluctuating environment, mutations in the biofilm‐regulating genes wspA and rpfR rose to high frequency in all replicate populations. A mutation in wspA first rose rapidly and nearly fixed during the initial biofilm phase but was subsequently displaced by a collection of rpfR mutants upon the shift to the planktonic phase. The wspA and rpfR genotypes coexisted via negative frequency‐dependent selection around an equilibrium frequency that shifted between the environments. The maintenance of coexisting genotypes in the fluctuating environment was unexpected. Under temporally fluctuating environments, coexistence of two genotypes is only predicted under a narrow range of conditions, but the frequency‐dependent interactions we observed provide a mechanism that can increase the likelihood of coexistence in fluctuating environments.     

A gene with major phenotypic effects as a target for selection vs. homogenizing gene flow

Genes with major phenotypic effects facilitate quantifying the contribution of genetic vs. plastic effects to adaptive divergence. A classical example is Ectodysplasin (Eda), the major gene controlling lateral plate phenotype in three‐spined stickleback. Completely plated marine stickleback populations evolved repeatedly towards low‐plated freshwater populations, representing a prime example of parallel evolution by natural selection. However, many populations remain polymorphic for lateral plate number. Possible explanations for this polymorphism include relaxation of selection, disruptive selection or a balance between divergent selection and gene flow. We investigated 15 polymorphic stickleback populations from brackish and freshwater habitats in coastal North‐western Europe. At each site, we tracked changes in allele frequency at the Eda gene between subadults in fall, adults in spring and juveniles in summer. Eda genotypes were also compared for body size and reproductive investment. We observed a fitness advantage for the Eda allele for the low morph in freshwater and for the allele for the complete morph in brackish water. Despite these results, the differentiation at the Eda gene was poorly correlated with habitat characteristics. Neutral population structure was the best predictor of spatial variation in lateral plate number, suggestive of a substantial effect of gene flow. A meta‐analysis revealed that the signature of selection at Eda was weak compared to similar studies in stickleback. We conclude that a balance between divergent selection and gene flow can maintain stickleback populations polymorphic for lateral plate number and that ecologically relevant genes may not always contribute much to local adaptation, even when targeted by selection.     

Female frequencies and fitness components between sex phenotypes among gynodioecious populations of the colonizing species Trifolium hirtum All. in California

Summary Male sterility has been recently discovered in Californian populations of rose clover (Trifolium hirtum). This study describes the frequency distribution of male sterility in Turkish and Californian populations, and compares fitness components of hermaphrodites and females. As male-steriles were found in Turkey, it is likely that they were introduced to California during the 1940's with the original material derived from Turkey. The spread of male-sterile genotypes in California has given rise to an asymmetrical frequency distribution of male sterility with positive skewness. The frequency of females has not exceeded fifty percent and it appears to be temporally stable in most of the Californian populations. The hypothesis that female frequencies and fitness differences between phenotypes are correlated was tested by comparing sex phenotypes in seven populations with contrasting levels of male sterility. The analysis of those populations showed no evidence for such a correlation as no significant differences were found between sex phenotypes for fecundity and seed germination. The hypothesis that females are maintained due to fitness differences in the progeny of hermaphrodites and females was experimentally tested in the population with maximum frequency of male-steriles. The results showed no significant differences in the demographic performance of the progenies of hermaphrodites and females. The present results are discussed in terms of the possible mechanism of maintenance of gynodioecy in rose clover.     

Sex ratio and gamete size across eastern North America in Dictyostelium discoideum,a social amoeba with three sexes

Theory indicates that numbers of mating types should tend towards infinity or remain at two. The social amoeba, Dictyostelium discoideum, however, has three mating types. It is therefore a mystery how this species has broken the threshold of two mating types, but has not increased towards a much higher number. Frequency‐dependent selection on rare types in combination with isogamy, a form of reproduction involving gametes similar in size, could explain the evolution of multiple mating types in this system. Other factors, such as drift, may be preventing the evolution of more than three. We first looked for evidence of isogamy by measuring gamete size associated with each type. We found no evidence of size dissimilarities between gametes. We then looked for evidence of balancing selection, by examining mating type distributions in natural populations and comparing genetic differentiation at the mating type locus to that at more neutral loci. We found that mating type frequency varied among the three populations we examined, with only one of the three showing an even sex ratio, which does not support balancing selection. However, we found more population structure at neutral loci than the mating type locus, suggesting that the three mating types are indeed maintained at intermediate frequencies by balancing selection. Overall, the data are consistent with balancing selection acting on D. discoideum mating types, but with a sufficiently weak rare sex advantage to allow for drift, a potential explanation for why these amoebae have only three mating types.     

Sex‐biased oviposition by a nursery pollinator on a gynodioecious host plant: Implications for breeding system evolution and evolution of mutualism

Dioecy, a breeding system where individual plants are exclusively male or female, has evolved repeatedly. Extensive theory describes when dioecy should arise from hermaphroditism, frequently through gynodioecy, where females and hermaphrodites coexist, and when gynodioecy should be stable. Both pollinators and herbivores often prefer the pollen‐bearing sex, with sex‐specific fitness effects that can affect breeding system evolution. Nursery pollination, where adult insects pollinate flowers but their larvae feed on plant reproductive tissues, is a model for understanding mutualism evolution but could also yield insights into plant breeding system evolution. We studied a recently established nursery pollination interaction between native Hadena ectypa moths and introduced gynodioecious Silene vulgaris plants in North America to assess whether oviposition was biased toward females or hermaphrodites, which traits were associated with oviposition, and the effect of oviposition on host plant fitness. Oviposition was hermaphrodite‐biased and associated with deeper flowers and more stems. Sexual dimorphism in flower depth, a trait also associated with oviposition on the native host plant (Silene stellata), explained the hermaphrodite bias. Egg‐receiving plants experienced more fruit predation than plants that received no eggs, but relatively few fruits were lost, and egg receipt did not significantly alter total fruit production at the plant level. Oviposition did not enhance pollination; egg‐receiving flowers usually failed to expand and produce seeds. Together, our results suggest that H. ectypa oviposition does not exert a large fitness cost on host plants, sex‐biased interactions can emerge from preferences developed on a hermaphroditic host species, and new nursery pollination interactions can arise as negative or neutral rather than as mutualistic for the plant.     

Modeling and quantifying frequency‐dependent fitness in microbial populations with cross‐feeding interactions

Coexistence of two or more populations by frequency‐dependent selection is common in nature, and it often arises even in well‐mixed experiments with microbes. If ecology is to be incorporated into models of population genetics, then it is important to represent accurately the functional form of frequency‐dependent interactions. However, measuring this functional form is problematic for traditional fitness assays, which assume a constant fitness difference between competitors over the course of an assay. Here, we present a theoretical framework for measuring the functional form of frequency‐dependent fitness by accounting for changes in abundance and relative fitness during a competition assay. Using two examples of ecological coexistence that arose in a long‐term evolution experiment with Escherichia coli, we illustrate accurate quantification of the functional form of frequency‐dependent relative fitness. Using a Monod‐type model of growth dynamics, we show that two ecotypes in a typical cross‐feeding interaction—such as when one bacterial population uses a byproduct generated by another—yields relative fitness that is linear with relative frequency.     

THE GENETIC STRUCTURE OF A GYNODIOECIOUS PLANT: NUCLEAR AND CYTOPLASMIC GENES

Sex expression in gynodioecious plants is often determined by an interaction between biparentally and maternally inherited genes. Their relative rates of gene flow should be considered when modeling the evolution of the sex ratio in structured populations. In order to understand patterns of gene flow in Silene vulgaris, a gynodioecious plant, genetic structure was estimated from biparentally inherited genetic markers (allozymes) and a maternally inherited marker (chloroplast DNA) using Wright's F_st. Based on data from 16 local populations, chloroplast DNA showed considerably more genetic structure than did allozymes (F_st values of 0.62 and 0.22, respectively). This suggests that the rate of gene flow is about three times greater for nuclear genes.     

Legacy of prior host and soil selection on rhizobial fitness in planta

Measuring selection acting on microbial populations in natural or even seminatural environments is challenging because many microbial populations experience variable selection. The majority of rhizobial bacteria are found in the soil. However, they also live symbiotically inside nodules of legume hosts and each nodule can release thousands of daughter cells back into the soil. We tested how past selection (i.e., legacies) by two plant genotypes and by the soil alone affected selection and genetic diversity within a population of 101 strains of Ensifer meliloti. We also identified allelic variants most strongly associated with soil‐ and host‐dependent fitness. In addition to imposing direct selection on rhizobia populations, soil and host environments had lasting effects across host generations. Host presence and genotype during the legacy period explained 22% and 12% of the variance in the strain composition of nodule communities in the second cohort, respectively. Although strains with high host fitness in the legacy cohort tended to be enriched in the second cohort, the diversity of the strain community was greater when the second cohort was preceded by host rather than soil legacies. Our results indicate the potential importance of soil selection driving the evolution of these plant‐associated microbes.