Towards a genetic theory for the evolution of the sex ratio

A genetical model is formulated in which the sex ratio in broods and the relative size of broods are determined by the genotype at an autosomal locus. The results also apply to the case in which the sex-ratio locus is sex linked and expressed in the homogametic sex and to the case in which the locus is expressed in the diploid sex of a haplodiploid organism. Fisher (1930) argued that the sex ratio evolves under natural selection to a value such that parental expenditure is equalized between the sexes. Shaw and Mohler (1953) and MacArthur (1965) proposed that the sex ratio evolves to increase a certain expression for fitness. The sex ratio suggested by Fisher (1930) is in fact identical to the sex ratio specified by these maximization principles. Further, in our model, the Fisherian sex ratio corresponds exactly to the sex ratio at certain equilibria that are approached whenever they exist.     

The evolution of sex differences in mate searching when females benefit: new theory and a comparative test

Sexual selection is thought to have led to searching as a profitable, but risky way of males obtaining mates. While there is great variation in which sex searches, previous theory has not considered search evolution when both males and females benefit from multiple mating. We present new theory and link it with data to bridge this gap. Two different search protocols exist between species in the bush-cricket genus Poecilimon (Orthoptera): females search for calling males, or males search for calling females. Poecilimon males also transfer a costly nuptial food gift to their mates during mating. We relate variations in searching protocols to variation in nuptial gift size among 32 Poecilimon taxa. As predicted, taxa where females search produce significantly larger nuptial gifts than those where males search. Our model and results show that search roles can reverse when multiple mating brings about sufficiently strong material benefits to females.     

Stabilizing selection,mutational bias,and the evolution of sex*

Stabilizing selection around a fixed phenotypic optimum is expected to disfavor sexual reproduction, since asexually reproducing organisms can maintain a higher fitness at equilibrium, while sex disrupts combinations of compensatory mutations. This conclusion rests on the assumption that mutational effects on phenotypic traits are unbiased, that is, mutation does not tend to push phenotypes in any particular direction. In this article, we consider a model of stabilizing selection acting on an arbitrary number of polygenic traits coded by bialellic loci, and show that mutational bias may greatly reduce the mean fitness of asexual populations compared with sexual ones in regimes where mutations have weak to moderate fitness effects. Indeed, mutation and drift tend to push the population mean phenotype away from the optimum, this effect being enhanced by the low effective population size of asexual populations. In a second part, we present results from individual‐based simulations showing that positive rates of sex are favored when mutational bias is present, while the population evolves toward complete asexuality in the absence of bias. We also present analytical (QLE) approximations for the selective forces acting on sex in terms of the effect of sex on the mean and variance in fitness among offspring.     

Mate choice and the operational sex ratio: an experimental test with robotic crabs

The operational sex ratio (OSR: sexually active males: receptive females) predicts the intensity of competition for mates. It is less clear, however, under what circumstances, the OSR predicts the strength of sexual selection – that is, the extent to which variation in mating success is attributable to traits that increase the bearer's attractiveness and/or fighting ability. To establish causality, experiments that manipulate the OSR are required. Furthermore, if it is possible to control for any OSR‐dependent changes in the chosen sex (e.g. changes in male courtship), we can directly test whether the OSR affects the behaviour of the choosing sex (e.g. female choice decisions). We conducted female mate choice experiments in the field using robotic models of male fiddler crabs (Uca mjoebergi). We used a novel design with two females tested sequentially per trial. As in nature, the choice of the first female to mate therefore affected the mates available to the next female. In general, we detected significant sexual selection due to female choice for ‘males’ with larger claws. Importantly, the strength of sexual selection did not vary across five different OSR/density treatments. However, as the OSR decreased (hence the number of available males declined), females chose the ‘males’ with the largest claws available significantly more often than expected by chance. Possible reasons for this mismatch between the expected and observed effects of the OSR on the strength of sexual selection are discussed.     

A comparative test of a theory for the evolution of anisogamy

Why are sperm small and eggs large? The dominant explanation for the evolution of gamete size dimorphism envisages two opposing selection pressures acting on gamete size: small gametes are favoured because many can be produced, whereas large gametes contribute to a large zygote with consequently increased survival chances. This model predicts disruptive selection on gamete size (i.e. selection for anisogamy) if increases in zygote size confer disproportional increases in fitness (at least over part of its size range). It therefore predicts that increases in adult size should be accompanied by stronger selection for anisogamy. Using data from the green algal order Volvocales, we provide the first phylogenetically controlled test of the model''s predictions using a published phylogeny and a new phylogeny derived by a different method. The predictions that larger organisms should (i) have a greater degree of gamete dimorphism and (ii) have larger eggs are broadly upheld. However, the results are highly sensitive to the phylogeny and the mode of analysis used.     

Fitness effects of beneficial mutations: the mutational landscape model in experimental evolution

The mutational landscape model is a theoretical model describing sequence evolution in natural populations. However, recent experimental work has begun to test its predictions in laboratory populations of microbes. Several of these studies have focused on testing the prediction that the effects of beneficial mutations should be roughly exponentially distributed. The prediction appears to be borne out by most of these studies, at least qualitatively. Another study showed that a modified version of the model was able to predict, with reasonable accuracy, which of a ranked set of beneficial alleles will be fixed next. Although it remains to be seen whether the mutational landscape model adequately describes adaptation in organisms other than microbes, together these studies suggest that adaptive evolution has surprisingly general properties that can be successfully captured by theoretical models.     

Parasites and sex: Catching the red queen

One version of the Red Queen hypothesis suggests that sexual reproduction may be an advantage in a coevolutionary arms race. Antagonistic biotic interactions, especially those between parasite and host, are thought to represent a sufficient evolutionary force to counterbalance the supposed inefficiency of sexual reproduction. Recent experimental studies demonstrate negative frequency-dependent selection, increased parasite load in parthenogenetic races relative to sympatric sexual conspecifics and correlations between recombination rate and frequency of parasitic chromosomes. These studies provide strong empirical evidence that there is an important role for parasites in maintaining sex.     

High-model abundance may permit the gradual evolution of Batesian mimicry: an experimental test

In Batesian mimicry, a harmless species (the ‘mimic’) resembles a dangerous species (the ‘model’) and is thus protected from predators. It is often assumed that the mimetic phenotype evolves from a cryptic phenotype, but it is unclear how a population can transition through intermediate phenotypes; such intermediates may receive neither the benefits of crypsis nor mimicry. Here, we ask if selection against intermediates weakens with increasing model abundance. We also ask if mimicry has evolved from cryptic phenotypes in a mimetic clade. We first present an ancestral character-state reconstruction showing that mimicry of a coral snake (Micrurus fulvius) by the scarlet kingsnake (Lampropeltis elapsoides) evolved from a cryptic phenotype. We then evaluate predation rates on intermediate phenotypes relative to cryptic and mimetic phenotypes under conditions of both high- and low-model abundances. Our results indicate that where coral snakes are rare, intermediate phenotypes are attacked more often than cryptic and mimetic phenotypes, indicating the presence of an adaptive valley. However, where coral snakes are abundant, intermediate phenotypes are not attacked more frequently, resulting in an adaptive landscape without a valley. Thus, high-model abundance may facilitate the evolution of Batesian mimicry.     

Gametocyte sex ratio of a malaria parasite: experimental test of heritability

The gametocyte sex ratio of Plasmodium mexicanum, a malaria parasite of western fence lizards, was studied in a modified garden experiment. Each of 6 naturally infected lizards was used to initiate 20 replicate-infections in naive western fence lizards. A significant donor effect was observed for the sex ratios of recipient infections at their maximal parasitemia, and this effect was associated with the sex ratio of the donor infection. In 20 infections in which sex ratio was followed during the course of the infection, 9 revealed constant sex ratios and 11 showed an increase in proportion of males over time. Recipient sex ratio was correlated with another life-history trait, a composite of rate of asexual replication and peak parasitemia, such that higher Rate-Peak scores were associated with infections with less female-biased sex ratios. These results are placed into the context of sex ratio theory that concludes that the degree of selfing of parasite genotypes (number of parasite clones) within the vector will influence the evolution of gametocyte sex ratio. The theory predicts that the sex ratio should be under some genetic control and thus be heritable as observed in the experiment. Clonal diversity should also influence the life-history trait, Rate-Peak, which was found to be correlated with sex ratio.     

Parasites and the evolution of extravagant male characters: Anolis lizards on Caribbean islands as a test of the Hamilton-Zuk hypothesis

Anolis lizards from Puerto Rico (five species from one site), Curaçao and Aruba in the southern Caribbean (2 populations), and 22 populations from 14 islands in the eastern Caribbean were surveyed for blood parasites (two species of Plasmodium and haemogregarines). Literature records for gut helminths from nine of these populations were added to the data set. Dorsal body color and dewlap color of males were also observed and classified into objective classes with no subjective view of showiness. These data were used to test the among-species prediction of the Hamilton-Zuk hypothesis which states that species harboring more harmful parasites over their evolutionary history will be more likely to evolve extravagant sexually dimorphic traits. Critics have noted important shortcomings in previous tests of the prediction; here we corrected for these errors. Parasite loads (prevalence and number of species) and dorsal and dewlap color varied substantially among the populations sampled. However, there was no association of parasite load with color either in a broad analysis or when correcting for phylogenetic relationships among the lizard species.     

Parasites and the blackcap's tail: implications for the evolution of feather ornaments

Although parasites may impair the expression of tail ornaments in birds, the importance of parasitism in driving the evolution of the initial stages of tail ornamentation is not well understood. Parasites could have negatively affected the expression of nonexaggerated, functional traits before these evolved ornaments, or they could have played a relevant role only after tails became ornamental and hence too costly to produce. To shed light on this issue, we studied the correlation between the abundance of feather mites (Acari, Proctophyllodidae) and the size, quality, growth rate and symmetry of tail feathers of blackcaps ( Sylvia atricapilla ), a non-ornamented passerine. Tail length was not correlated with mite load, yet blackcaps holding many mites at the moment of feather growth (fledglings) had lighter and more asymmetric feathers that grew at relatively lower rates. In blackcaps whose mite load was measured one year after feather growth (adults), only the negative correlation between mite intensity and feather symmetry remained significant. Changes in mite load since the moult season could have erased the correlation between condition-dependent feather traits and current parasite load in adults. Our results support the idea that different traits of non-ornamental feathers can signal parasite resistance. Therefore, parasitism could have played a central role in the evolution of tail ornamentation ever since its initial stages.  © 2002 The Linnean Society of London. Biological Journal of the Linnean Society , 2002, 76 , 481–492.     

Long-term experimental evolution of HIV-1 reveals effects of environment and mutational history

An often-returning question for not only HIV-1, but also other organisms, is how predictable evolutionary paths are. The environment, mutational history, and random processes can all impact the exact evolutionary paths, but to which extent these factors contribute to the evolutionary dynamics of a particular system is an open question. Especially in a virus like HIV-1, with a large mutation rate and large population sizes, evolution is expected to be highly predictable if the impact of environment and history is low, and evolution is not neutral. We investigated the effect of environment and mutational history by analyzing sequences from a long-term evolution experiment, in which HIV-1 was passaged on 2 different cell types in 8 independent evolutionary lines and 8 derived lines, 4 of which involved a switch of the environment. The experiments lasted for 240–300 passages, corresponding to approximately 400–600 generations or almost 3 years. The sequences show signs of extensive parallel evolution—the majority of mutations that are shared between independent lines appear in both cell types, but we also find that both environment and mutational history significantly impact the evolutionary paths. We conclude that HIV-1 evolution is robust to small changes in the environment, similar to a transmission event in the absence of an immune response or drug pressure. We also find that the fitness landscape of HIV-1 is largely smooth, although we find some evidence for both positive and negative epistatic interactions between mutations.

Analysis of the longest evolutionary experiment with HIV-1 to-date reveals continuous viral adaptation over several years. The authors quantify the environment-specific mutations that arise and determine the fraction of mutations that co-occur with significantly different frequencies than expected by chance.     

Predicting epistasis: an experimental test of metabolic control theory with bacterial transcription and translation

Epistatic interactions between mutations are thought to play a crucial role in a number of evolutionary processes, including adaptation and sex. Evidence for epistasis is abundant, but tests of general theoretical models that can predict epistasis are lacking. In this study, I test the ability of metabolic control theory to predict epistasis using a novel experimental approach that combines phenotypic and genetic perturbations of enzymes involved in gene expression and protein synthesis in the bacterium Pseudomonas aeruginosa. These experiments provide experimental support for two key predictions of metabolic control theory: (i) epistasis between genes involved in the same pathway is antagonistic; (ii) epistasis becomes increasingly antagonistic as mutational severity increases. Metabolic control theory is a general theory that applies to any set of genes that are involved in the same linear processing chain, not just metabolic pathways, and I argue that this theory is likely to have important implications for predicting epistasis between functionally coupled genes, such as those involved in antibiotic resistance. Finally, this study highlights the fact that phenotypic manipulations of gene activity provide a powerful method for studying epistasis that complements existing genetic methods.     

Phenotypic plasticity of hermaphrodite sex allocation promotes the evolution of separate sexes: an experimental test of the sex-differential plasticity hypothesis using Sagittaria latifolia (Alismataceae)

Separate sexes can evolve under nuclear inheritance when unisexuals have more than twice the reproductive fitness of hermaphrodites through one sex function (e.g., when females have more than twice the seed fertility of hermaphrodites). Because separate sexes are thought to evolve most commonly via a gynodioecious intermediate (i.e., populations in which females and hermaphrodites cooccur), the conditions under which females can become established in populations of hermaphrodites are of considerable interest. It has been proposed that resource-poor conditions could promote the establishment of females if hermaphrodites are plastic in their sex allocation and allocate fewer resources to seed production under these conditions. If this occurs, the seed fertility of females could exceed the doubling required for the evolution of unisexuality under low-, but not high-resource conditions (the sex-differential plasticity hypothesis). We tested this hypothesis using replicate experimental arrays of the aquatic herb Sagittaria latifolia grown under two fertilizer treatments. The results supported the sex-differential plasticity hypothesis, with females having more than twice the seed fertility of hermaphrodites under low-, but not high-fertilizer conditions. Our findings are consistent with the idea that separate sexes are more likely to evolve under unfavorable conditions.     

Local adaptation and effect of host genotype on the rate of pathogen evolution: an experimental test in a plant pathosystem

Abstract Virulence is thought to be a driving force in host–pathogen coevolution. Theoretical models suggest that virulence is an unavoidable consequence of pathogens evolving towards a high rate of intrahost reproduction. These models predict a positive correlation between the reproductive fitness of a pathogen and its level of virulence. Theoretical models also suggest that the demography and genetic structure of a host population can influence the evolution of virulence. If evolution occurs faster in pathogen populations than in host populations, the predicted result is local adaptation of the pathogen population. In our studies, we used a combination of molecular and physiological markers to test these hypotheses in an agricultural system. We isolated five strains of the fungal pathogen Mycosphaerella graminicola from each of two wheat cultivars that differed in their level of resistance to this pathogen. Each of the 10 fungal strains had distinct genotypes as indicated by different DNA fingerprints. These fungal strains were re‐inoculated onto the same two host cultivars in a field experiment and their genotype frequencies were monitored over several generations of asexual reproduction. We also measured the virulence of these 10 fungal strains and correlated it to the reproductive fitness of each fungal strain. We found that host genotypes had a strong impact on the dynamics of the pathogen populations. The pathogen population collected from the moderately resistant cultivar Madsen showed greater stability, higher genotype diversity, and smaller selection coefficients than the pathogen populations collected from the susceptible cultivar Stephens or a mixture of the two host cultivars. The pathogen collection from the mixed host population was midway between the two pure lines for most parameters measured. Our results also revealed that the measures of reproductive fitness and virulence of a pathogen strain were not always correlated. The pathogen strains varied in their patterns of local adaptation, ranging from locally adapted to locally maladapted.