Similarity selection and the evolution of sex: revisiting the red queen

For over 25 years, many evolutionary ecologists have believed that sexual reproduction occurs because it allows hosts to change genotypes each generation and thereby evade their coevolving parasites. However, recent influential theoretical analyses suggest that, though parasites can select for sex under some conditions, they often select against it. These models assume that encounters between hosts and parasites are completely random. Because of this assumption, the fitness of a host depends only on its own genotype (“genotypic selection”). If a host is even slightly more likely to encounter a parasite transmitted by its mother than expected by random chance, then the fitness of a host also depends on its genetic similarity to its mother (“similarity selection”). A population genetic model is presented here that includes both genotypic and similarity selection, allowing them to be directly compared in the same framework. It is shown that similarity selection is a much more potent force with respect to the evolution of sex than is genotypic selection. Consequently, similarity selection can drive the evolution of sex even if it is much weaker than genotypic selection with respect to fitness. Examination of explicit coevolutionary models reveals that even a small degree of mother–offspring parasite transmission can cause parasites to favor sex rather than oppose it. In contrast to previous predictions, the model shows that weakly virulent parasites are more likely to favor sex than are highly virulent ones. Parasites have figured prominently in discussions of the evolution of sex, but recent models suggest that parasites often select against sex rather than for it. With the inclusion of small and realistic exposure biases, parasites are much more likely to favor sex. Though parasites alone may not provide a complete explanation for sex, the results presented here expand the potential for parasites to contribute to the maintenance of sex rather than act against it.     

On sex, mate selection and the red queen.

The widespread occurrence of sexual reproduction despite the two-fold disadvantage of producing males, is still an unsolved mystery in evolutionary biology. One explanatory theory, called the "Red Queen" hypothesis, states that sex is an adaptation to escape from parasites. A more recent hypothesis, the mate selection hypothesis, assumes that non-random mating, possible only with sex, accelerates the evolution of beneficial traits. This paper tests these two hypotheses, using an agent-based or "micro-analytic" evolutionary algorithm where host-parasite interaction is simulated adhering to biological reality. While previous simpler models testing the "Red Queen" hypothesis considered mainly haploid hosts, stable population density, random mating and simplified expression of fitness, our more realistic model allows diploidy, mate selection, live history constraints and variable population densities. Results suggest that the Red Queen hypothesis is not valid for more realistic evolutionary scenarios and that each of the two hypotheses tested seem to explain partially but not exhaustively the adaptive value of sex. Based on the results we suggest that sexual populations in nature should avoid both, maximizing outbreeding or maximizing inbreeding and should acquire mate selection strategies which favour optimal ranges of genetic mixing in accordance with environmental challenges.     

The red queen coupled with directional selection favours the evolution of sex

Why sexual reproduction has evolved to be such a widespread mode of reproduction remains a major question in evolutionary biology. Although previous studies have shown that increased sex and recombination can evolve in the presence of host-parasite interactions (the 'Red Queen hypothesis' for sex), many of these studies have assumed that multiple loci mediate infection vs. resistance. Data suggest, however, that a major locus is typically involved in antigen presentation and recognition. Here, we explore a model where only one locus mediates host-parasite interactions, but a second locus is subject to directional selection. Even though the effects of these genes on fitness are independent, we show that increased rates of sex and recombination are favoured at a modifier gene that alters the rate of genetic mixing. This result occurs because of selective interference in finite populations (the 'Hill-Robertson effect'), which also favours sex. These results suggest that the Red Queen hypothesis may help to explain the evolution of sex by contributing a form of persistent selection, which interferes with directional selection at other loci and thereby favours sex and recombination.     

Catching a red herring: autumn colours and aphids

The purpose of this note is not to support any particular hypothesis explaining the evolution of red coloured autumn leaves, but to present evidence that shows existing knowledge does not support one such hypothesis – that red coloured leaves evolved as a signal to protect trees from aphids feeding and laying eggs on them in autumn. An alternative hypothesis is that autumn-feeding aphids are senescence-feeders, evolved to feed only on senescing leaves. These aphids are programmed to detect and feed on such leaves when they are still green and yellow and actively exporting their nutrients. Aphids reject or ignore red leaves because they are no longer good food, not because they are protecting the trees from the aphids.     

Parasites and deleterious mutations: interactions influencing the evolutionary maintenance of sex

The restrictive assumptions associated with purely genetic and purely ecological mechanisms suggest that neither of the two forces, in isolation, can offer a general explanation for the evolutionary maintenance of sex. Consequently, attention has turned to pluralistic models (i.e. models that apply both ecological and genetic mechanisms). Existing research has shown that combining mutation accumulation and parasitism allows restrictive assumptions about genetic and parasite parameter values to be relaxed while still predicting the maintenance of sex. However, several empirical studies have shown that deleterious mutations and parasitism can reduce fitness to a greater extent than would be expected if the two acted independently. We show how interactions between these genetic and ecological forces can completely reverse predictions about the evolution of reproductive modes. Moreover, we demonstrate that synergistic interactions between infection and deleterious mutations can render sex evolutionarily stable even when there is antagonistic epistasis among deleterious mutations, thereby widening the conditions for the evolutionary maintenance of sex.     

Parasites and mate choice in red jungle fowl

Captive flocks of red jungle fowl (Gallus gallus) experimentallyinfected with the intestinal nematode Ascaridia galli were usedto test Hamilton and Zuk's (1982) hypothesis that parasitesadversely affect male secondary sex characters and that femalesprefer unparasitized over parasitized males. Infected chicksgrew more slowly than uninfected controls, with the effect particularlypronounced on comb length rather than tarsus length or bodyweight. At sexual maturity, infected roosters had duller combsand eyes, shorter combs and tail feathers, and paler hacklefeathers than control roosters. In experimental mate choicetests, females preferred unparasitized over parasitized roostersby about 2: 1, and an analysis of covariance revealed that thehens were using the traits on which the two groups differedto make their mate choice decisions. Finally, in a test of anextension of the Hamilton and Zuk hypothesis, control and infectedmales were not distinguishable based on non sexually-selectedcharacters such as bill size, suggesting that parasites havea disproportionately larger effect on ornamental traits.     

Epidemiology of a Daphnia-multiparasite system and its implications for the red queen

The Red Queen hypothesis can explain the maintenance of host and parasite diversity. However, the Red Queen requires genetic specificity for infection risk (i.e., that infection depends on the exact combination of host and parasite genotypes) and strongly virulent effects of infection on host fitness. A European crustacean (Daphnia magna)--bacterium (Pasteuria ramosa) system typifies such specificity and high virulence. We studied the North American host Daphnia dentifera and its natural parasite Pasteuria ramosa, and also found strong genetic specificity for infection success and high virulence. These results suggest that Pasteuria could promote Red Queen dynamics with D. dentifera populations as well. However, the Red Queen might be undermined in this system by selection from a more common yeast parasite (Metschnikowia bicuspidata). Resistance to the yeast did not correlate with resistance to Pasteuria among host genotypes, suggesting that selection by Metschnikowia should proceed relatively independently of selection by Pasteuria.     

Non-progressive evolution,the red queen hypothesis,and the balance of nature

The Red Queen hypothesis, or the ability organisms have to control and regulate the available trophic energy, is a recently proposed parameter for measuring fitness. Firstly, this hypothesis is analysed in terms of its heuristic power. Secondly, the claimed causal dependence between this parameter and a, still controversial, law of constant extinction is judged to be unjustified, however reasonable such a claim appears to be. Finally, the ubiquity of competition in nature which is seemingly required by the Red Queen and supposedly realized at the expense of a mutualistic alternative, is deemed to be a questionable assumption.     

Nutritional factors affecting the egg sex ratio adjustment by a honeybee queen

Summary. To determine whether and how honeybee (Apis mellifera L.) queens control the proportion of male reproductives, experiments were done with colonies under two nutritional conditions at two seasons. During the reproductive season the proportion of male eggs laid by queens under insufficiently-food-supplied conditions was lower than that under sufficiently-food-supplied conditions. The smaller proportion of male egg production could not be accounted for by cannibalization of male eggs by workers. The workers' allocation to male cell construction did not differ between sufficiently- and insufficiently-food-supplied conditions. During the non-reproductive season, however, queens showed much reduced or nearly no production of male eggs, even if the colonies were sufficiently supplied with food. These results suggest that the honeybee queen adjusts the egg sex ratio by referring to both the nutritional resources and their own intrinsic seasonal factors.     

Homage to the red queen. I. Coevolution of predators and their victims

In this paper we develop a model to describe the coevolution of a two-species predator-victim ecosystem. Evolution among the predators acts to displace the predators' zero growth isocline, J, to the left, whereas victim evolution has the opposite effect. More important, we show that for many such systems, there is a value of J, J1, at which the rate of predator evolution exactly equals the rate of victim evolution. This value of J turns out to be a coevolutionary steady state (CSS) which is stable to perturbations. It is suggested that this analysis permits qualitative understanding of why certain real world predator-prey systems oscillate, whereas others do not.     

Parasites, sex, and clonal diversity in natural snail populations

Under the Red Queen hypothesis, host-parasite coevolution selects against common host genotypes. Although this mechanism might underlie the persistence of sexual reproduction, it might also maintain high clonal diversity. Alternatively, clonal diversity might be maintained by multiple origins of parthenogens from conspecific sexuals, a feature in many animal groups. Herein, we addressed the maintenance of overall genetic diversity by coevolving parasites, as predicted by the Red Queen hypothesis. We specifically examined the contribution of parasites to host clonal diversity and the frequency of sexually reproducing individuals in natural stream populations of Potamopyrgus antipodarum snails. We also tested the alternative hypothesis that clonal diversity is maintained by the input of clones by mutation from sympatric sexuals. Clonal diversity and the frequency of sexual individuals were both positively related to infection frequency. Surprisingly, although clones are derived by mutation from sexual snails, parasites explained more of the genotypic variation among parthenogenetic subpopulations. Our findings thus highlight the importance of parasites as drivers of clonal diversity, as well as sex.     

Parasites and mutational load: an experimental test of a pluralistic theory for the evolution of sex

Ecological and mutational explanations for the evolution of sexual reproduction have usually been considered independently. Although many of these explanations have yielded promising theoretical results,experimental support for their ability to overcome a twofold cost of sex has been limited. For this reason, it has recently been argued that a pluralistic approach, combining effects from multiple models, may be necessary to explain the apparent advantage of sex. One such pluralistic model proposes that parasite load and synergistic epistasis between deleterious mutations might interact to create an advantage for recombination.Here, we test this proposal by comparing the fitness functions of parasitized and parasite-free genotypes of Escherichia coli bearing known numbers of transposon-insertion mutations. In both classes, we failed to detect any evidence for synergistic epistasis. However, the average effect of deleterious mutations was greater in parasitized than parasite-free genotypes. This effect might broaden the conditions under which another proposed model combining parasite-host coevolutionary dynamics and mutation accumulation can explain the maintenance of sex. These results suggest that, on average, deleterious mutations act multiplicatively with each other but in synergy with infection in determining fitness.     

Homage to the red queen. II. Coevolutionary response to enrichment of exploitation ecosystems

The model of predator-victim coevolution developed in the preceding paper (Schaffer and Rosenzweig, 1978) is used to analyze the coevolutionary response to ecosystem enrichment. It is shown that coevolution tends to oppose the destabilization that results from the enrichment itself. In the circumstance that the victims' r and K are proportional, gradual enrichment followed by coevolutionary adjustment actually enhances ecosystem stability.     

Parasites and the avian spleen: helminths

A comparative analysis of the relationship between the spleen–a major organ of immunity and helminths was undertaken with bird species, using the phylogenetic regression technique. Species in which many individuals are infected with nematodes relative to the number of individuals examined for the presence of helminths (termed 'relative nematode presence') have significantly larger spleens, for a given body weight, in females (though not in males). There was little indication that this relationship depends on incidental ecological indices, the weights of other organs, or the 'relative presences' of trematodes, cestodes or haematozoa. Combined with previous, experimental, work it suggests that the avian spleen is important in resisting nematodes. Body weight is correlated with the relative presence of helminths; but even after removing body size effects, bird species which tend to be infected with trematodes are also more likely to be infected with cestodes. This paper indicates that the spleens of wild bird species are associated with macroparasites in the natural environment.