The role of epistasis on the evolution of recombination in host-parasite coevolution

Antagonistic coevolution between hosts and parasites is known to affect selection on recombination in hosts. The Red Queen Hypothesis (RQH) posits that genetic shuffling is beneficial for hosts because it quickly creates resistant genotypes. Indeed, a large body of theoretical studies have shown that for many models of the genetic interaction between host and parasite, the coevolutionary dynamics of hosts and parasites generate selection for recombination or sexual reproduction. Here we investigate models in which the effect of the host on the parasite (and vice versa) depend approximately multiplicatively on the number of matched alleles. Contrary to expectation, these models generate a dynamical behavior that strongly selects against recombination/sex. We investigate this atypical behavior analytically and numerically. Specifically we show that two complementary equilibria are responsible for generating strong linkage disequilibria of opposite sign, which in turn causes strong selection against sex. The biological relevance of this finding stems from the fact that these phenomena can also be observed if hosts are attacked by two parasites that affect host fitness independently. Hence the role of the Red Queen Hypothesis in natural host parasite systems where infection by multiple parasites is the rule rather than the exception needs to be reevaluated.     

A host-parasite model yielding heterogeneous parasite loads

Many models of parasitic infections lead to an approximately Poisson distribution of parasites among hosts, in stark contrast to the highly over-dispersed distributions that are usually encountered in practice. In this paper, a model is analyzed which, while assuming all individuals to be alike, can still lead to a very heterogeneous distribution of parasites among the host population. The model can be viewed as a very simple mean field interacting particle system, with the particles corresponding to the individual hosts, which behaves like an associated deterministic system when the number of hosts is large. The deterministic system describes the evolution over time of the proportions of the population with different parasite loads, and its equilibria are interpreted as typical distributions of parasites among hosts. Despite its simplicity, the model is complicated enough mathematically to leave a number of open problems.This work was supported in part by Schweiz. Nationalfonds Grants Nos 21-25579.88 and 20-31262.91, and by NSF Grant DMS 90-05833     

A schistosomiasis model with mating structure and time delay

A system of homogeneous equations with a time delay is used to model the population dynamics of schistosomes. The model includes the parasite’s mating structure, multiple resistant schistosome strains, and biological complexity associated with the parasite’s life cycle. Invasion criteria of resistant strains and coexistence threshold conditions are derived. These results are used to explore the impact of drug treatment on resistant strain survival. Numerical simulations indicate that the dynamical behaviors of the current model are not qualitatively different from those derived from an earlier model that ignores the impact of time delays associated with the multiple stages in parasite’s life cycle. However, quantitatively the time delays make it more likely for drug-resistant strains to invade in a parasite population.     

Stabilizing factors interact in promoting host-parasite coexistence

Understanding the mechanisms that promote coexistence among species is a fundamental problem in evolutionary ecology. Such mechanisms include environmental noise, spatial population structure, density dependence, and genetic variation. In natural populations such factors may exert combined effects on coexistence. Thus, to disentangle the contribution of several factors to coexistence, their effects have to be considered simultaneously. Here we investigate the effects of Ricker-type density dependence, genetic variation, and the frequency of sex on host-parasite coexistence, using Nicholson-Bailey models with and without host density dependence. Interestingly, a low frequency of sex (and the genetic variation induced by sex) is the most important factor in explaining the stability of the host-parasite interaction. However, the carrying capacity K and the frequency of sex interact in affecting coexistence. If K is low (strong density regulation), coexistence is easily attained in the density-dependent model, independently of the frequency of sex. In contrast, for high values of K (weak density regulation), low frequencies of sex considerably improve coexistence. Thus, our results suggest that coexistence among species may strongly depend on interactions among several stabilizing factors. These results seem to be robust since they remain qualitatively unchanged if one assumes (1) Beverton-Holt-type or genotype-specific rather than Ricker-type density dependence in the host, or (2) different genotype-specific susceptibilities of hosts to their parasites, or if one adds (3) moderate levels of environmental stochasticity.     

Differential proteomics reveals novel insights into Nosema–honey bee interactions

Host manipulation is a common strategy by parasites to reduce host defense responses, enhance development, host exploitation, reproduction and, ultimately, transmission success. As these parasitic modifications can reduce host fitness, increased selection pressure may result in reciprocal adaptations of the host. Whereas the majority of studies on host manipulation have explored resistance against parasites (i.e. ability to prevent or limit an infection), data describing tolerance mechanisms (i.e. ability to limit harm of an infection) are scarce. By comparing differential protein abundance, we provide evidence of host-parasite interactions in the midgut proteomes of N. ceranae-infected and uninfected honey bees from both Nosema-tolerant and Nosema-sensitive lineages. We identified 16 proteins out of 661 protein spots that were differentially abundant between experimental groups. In general, infections of Nosema resulted in an up-regulation of the bee's energy metabolism. Additionally, we identified 8 proteins that were differentially abundant between tolerant and sensitive honey bees regardless of the Nosema infection. Those proteins were linked to metabolism, response to oxidative stress and apoptosis. In addition to bee proteins, we also identified 3 Nosema ceranae proteins. Interestingly, abundance of two of these Nosema proteins were significantly higher in infected Nosema-sensitive honeybees relative to the infected Nosema-tolerant lineage. This may provide a novel candidate for studying the molecular interplay between N. ceranae and its honey bee host in more detail.     

Independent effects of familiarity and mating preferences for ornamental traits on mating decisions in guppies

The avoidance of familiar individuals as mates can act to maximizethe benefits of polyandry or might help to minimize inbreedingin small or highly philopatric populations. As previous matesare also familiar, the effects of familiarity and mating historycan often be confounded. Here, we disentangle these effectson mating decisions in the guppy, Poecilia reticulata, and examinetheir influence on sexual selection. In 3 experiments, malesand females were 1) able to mate, 2) had visual and olfactorycontact, or 3) had visual contact only. Familiarity was successfullyacquired via visual cues, and females were in all cases morelikely to mate with unfamiliar than with familiar males, indicatingthat familiarity is a more important determinant of mating outcomethan mating history. Males did not court unfamiliar femalesany more than familiar females and did not differentially allocatesperm. Familiarity did not alter the strength of sexual selectionon male coloration: we found overall positive selection forbright, large males. Female preferences for unfamiliar malesand ornamental traits may therefore be largely independent.     

Prezygotic isolation,mating preferences,and the evolution of chromosomal inversions

Chromosomal inversions are frequently implicated in isolating species. Models have shown how inversions can evolve in the context of postmating isolation. Inversions are also frequently associated with mating preferences, a topic that has not been studied theoretically. Here, we show how inversions can spread by capturing a mating preference locus and one or more loci involved with epistatic incompatibilities. Inversions can be established under broad conditions ranging from near panmixis to nearly complete speciation. These results provide a hypothesis to explain the growing number of examples of inversions associated with premating isolating mechanisms.     

Leishmania donovani flagellum-specific epitopes mediating host-parasite interactions

Abstract Monoclonal antibodies were developed against flagellar components of promastigotes of Leishmania donovani . The monoclonal antibody produced by clone A₁₁ (mAb A₁₁) recognised epitopes in the polypeptides with molecular weights of 86, 66 and weakly 53 kDa. These epitopes were found to be distributed along the flagellum and at the anterior end of promastigotes. The mAb A₁₁ of IgG₁ isotype strongly agglutinated the promastigotes of L. donovani . The prior treatment of promastigotes of L. donovani with mAb A₁₁ resulted in a significant ( P < 0.001) reduction in the attachment of promastigotes to cultured mouse peritoneal macrophages of line J774G8. The affinity-purified epitopes identified by mAb A₁₁ were recognised by human sera of cases of visceral leishmaniasis. The present study suggest that flagellar-specific epitopes mediate host-parasite interactions and, therefore, the role of these epitopes in the disease process is speculated.     

Female mating preferences determine system-level evolution in a gene network model

Environmental patterns of directional, stabilizing and fluctuating selection can influence the evolution of system-level properties like evolvability and mutational robustness. Intersexual selection produces strong phenotypic selection and these dynamics may also affect the response to mutation and the potential for future adaptation. In order to to assess the influence of mating preferences on these evolutionary properties, I modeled a male trait and female preference determined by separate gene regulatory networks. I studied three sexual selection scenarios: sexual conflict, a Gaussian model of the Fisher process described in Lande (in Proc Natl Acad Sci 78(6):3721–3725, 1981) and a good genes model in which the male trait signalled his mutational condition. I measured the effects these mating preferences had on the potential for traits and preferences to evolve towards new states, and mutational robustness of both the phenotype and the individual’s overall viability. All types of sexual selection increased male phenotypic robustness relative to a randomly mating population. The Fisher model also reduced male evolvability and mutational robustness for viability. Under good genes sexual selection, males evolved an increased mutational robustness for viability. Females choosing their mates is a scenario that is sufficient to create selective forces that impact genetic evolution and shape the evolutionary response to mutation and environmental selection. These dynamics will inevitably develop in any population where sexual selection is operating, and affect the potential for future adaptation.     

Mating unplugged: a model for the evolution of mating plug (dis-)placement

Mating plugs are male-derived structures that may impede female remating by physically obstructing the female genital tract. Although mating plugs exist in many taxa, the forces shaping their evolution are poorly understood. A male can clearly benefit if his mating plug secures his paternity. It is unclear, however, how plug efficacy can be maintained over evolutionary time in the face of counteracting selection on males' ability to remove any plugs placed by their rivals. Here, I present a game-theory model and a simulation model to address this problem. The models predict that evolutionarily stable levels of mating-plug efficacy should be high when (1) the number of mating attempts per female is low; (2) the sex ratio is male-biased, and (3) males are sperm-limited. I discuss these results in the light of empirical data.     

The major histocompatibility complex and mating preferences in wild house mice (mus domesticus)

This study examined the relationship between the major histocompatibilitycomplex (MHC) genes and mate choice by wild house mice in acontrolled laboratory setting in an attempt to understand themechanisms maintaining natural MHC diversity. Three rearinggroups of wild test mice were produced: nonfostered controlmice, mice fostered into families of an inbred laboratory mousestrain, and mice fostered into families of a second mouse straindiffering genetically from the first only within the MHC region.At maturity, test mice were given a choice of two opposite-sexstimulus mice of the two MHC-congenic strains used for fostering.Test mice were scored for several measures of preference includingamount of time spent with either stimulus mouse, and ejaculationwith a stimulus mouse. Females in two of three rearing groupsspent more time with one MHC type regardless of rearing environment,suggesting that females did not prefer mates dissimilar fromfamily MHC type. Time preferences tended to be stronger in femalesthan in males. Male test mice ejaculated indiscriminantly. Femalewild mice mated to ejaculation more often in longer trials,but these matings were still too infrequent to assess preferences.Fostering had little or no effect on MHC-based mate preferencesof wild house mice, and no evidence suggested that MHC was usedto avoid inbreeding. Wild female mice may still choose matesbased on MHC haplotypes (but do not necessarily prefer MHC-dissimilarmates); other cues are probably also used. Based on these results,inbreeding avoidance does not seem a strong mechanism for maintainingnatural MHC diversity     

Convergent host-parasite codon usage between honeybee and bee associated viral genomes

By correlating the codon usage in four insects (the honeybee, red flour beetle, mosquito and fruit fly) with six honeybee host specific viruses, we found that the codon usage patterns of the bee viruses were strongly related to that of the honeybee and only weakly related to the red flour beetle. The insects shared varying degrees of codon usage similarity which roughly follow the known phylogenetic relatedness. All of the codon usage similarity can be described by relatedness-by-descent except for the high codon usage similarity between the honeybee and honeybee associated viruses. This evidence for the convergent evolution of the honeybee viruses toward the codon usage of the honeybee suggests that small host specific viral genomes have the freedom to quickly optimize codon usage to successfully parasitize their preferred host. The codon usage co-evolution of the six host specific honeybee viruses towards the codon usage of the honeybee described in this paper is the first evidence for codon usage correlation between an insect host and a single stranded RNA virus.     

Male mating strategies and the mating system of great-tailed grackles

Great-tailed grackles (Quiscalus mexicanus) are sexually dimorphic,dichromatic, colonially nesting blackbirds. In this study, males pursued three basic types of conditional mating strategies,each of which employed a different set of mating tactics. Territorialmales defended one or more trees in which several females nested.They achieved reproductive success by siring the offspringof their social mates and through extrapair fertilization.Resident males lived in the colony but did not defend territoriesor have social mates. Transient males passed through the colony, staying no more than a few days, and probably visited more thanone colony. Residents appeared to queue for access to territories,but transients did not. Residents and transients gained allpaternity through extrapair fertilizations and provided noparental care. Territorial males sired the majority of offspring,but residents and transients also sired small numbers of nestlings. Territorial males were larger and had longer tails than nonterritorialmales. The number of social mates was related to body size,and males that sired nestlings were heavier and had longertails than males with no genetic reproductive success. Malesthat gained paternity through extrapair fertilization wereheavier and had longer tails than males that did not. The matingsystem of great-tailed grackles can best be categorized as "non-faithful-female frank polygyny."     

Evolution of disassortative and assortative mating preferences based on imprinting

A two-locus haploid model of sexual selection is investigated to explore evolution of disassortative and assortative mating preferences based on imprinting. In this model, individuals imprint on a genetically transmitted trait during early ontogeny and choosy females later use those parental images as a criterion of mate choice. It is assumed that the presence or absence of the female preference is determined by a genetic locus. In order to incorporate such mechanisms as inbreeding depression and heterozygous advantage into our haploid framework, we assume that same-type matings are less fertile than different-type mating. The model suggests that: if all the females have a disassortative mating preference a viability-reducing trait may be maintained even without the fertility cost of same-type matings; a disassortative mating preference can be established even if it is initially rare, when there is a fertility cost of same-type matings. Further, an assortative mating preference is less likely to evolve than a disassortative mating preference. The model may be applicable to the evolution of MHC-disassortative mating preferences documented in house mice and humans.     

Chitinases of fungi and plants: their involvement in morphogenesis and host-parasite interaction

Abstract: There has been a considerable amount of recent research aimed at elucidating the roles of chitinase in fungi and plants. In filamentous fungi and yeasts, chitinase is involved integrally in cell wall morphogenesis. Chitinase is also involved in the early events of host-parasite interactions of biotrophic and necrotrophic mycoparasites, entomopathogenic fungi and vesicular arbuscular mycorrhizal fungi. In plants, induction of chitinase and other hydrolytic enzymes is one of a coordinated, often complex and multifaceted defense mechanism triggered in response to phytopathogen attack. Chitinase induction in plants is not considered solely as an antifungal resistance mechanism. Plant chitinases can be induced by various abiotic factors as well and there is some circumstantial evidence to suggest a morphogenetic role despite the apparent absence of the substrate in plant cells. Finally, some chitinases and other chitin-binding proteins including some plant lectins share chitin-binding domains as part of their molecular structure and provide fuel for the so-called 'lectin-chitinase' debate and speculation for the origin of chitinase in plants.     

Assortative mating for a quantitative character

Phenotypic assortative mating is investigated for a character determined by additive loci without dominance and a stochastically independent environment. Conditional-expectation arguments are used to calculate the equilibrium values of the phenotypic variance and the correlation between sundry relatives. For the latter, it suffices to suppose that the regressions of an individual's genotype on his phenotype and of his phenotype on that of his mate are linear. For the former, linearity of the regression of the allelic effects on the phenotype is also posited. The biological implications of these assumptions are discussed.Supported by National Science Foundation Grant DEB81-03530     

Inbreeding under a cyclical mating system

Summary General recursion formulae for the coefficient of inbreeding under a cyclical mating system were derived in which one male and one female are selected from each of the n families per generation (population size N = 2 n). Each male is given the family number of his sire in each generation, while his mate comes from another family, varying systematically in different generations. Males of the r-th family in generations 1, 2, 3,..., t = n–1 within each cycle mate with females from families r+1, r+2, r+3,..., r+t to produce generations 2, 3, 4,..., t+1=1, respectively. The change in heterozygosity shows a cyclical pattern of rises and falls, repeating in cycles of n–1 generations. The rate of inbreeding oscillates between <-3% to >6% in different generations within each cycle, irrespective of the population size. The average rate of inbreeding per generation is approximately 1/[4 N-(Log₂N+1)], which is the rate for the maximum avoidance of inbreeding. The average inbreeding effective population size is approximately 2 N–2.     

Host‐associated pre‐mating reproductive isolation between host races of Acrocercops transecta: mating site preferences and effect of host presence on mating

• 1. A correlation between habitat and mating site preference is crucial for reproductive isolation between populations with different ecological requirements in the absence of any other barriers to gene flow. In phytophagous insects, host‐plant preference of ovipositing females has been postulated to directly influence the extent of assortative mating.
• 2. Although this pleiotropic effect of host preference is commonly postulated in both theoretical and empirical studies in phytophagous insects, few studies have assessed the mating site preferences of both sexes. In herbivorous insects, it is crucial whether males have the same host preference as ovipositing females.
• 3. This study examines whether males and females have preferences for mating sites and assesses the effects of host presence on mating activity in a leaf‐mining moth, Acrocercops transecta Meyrick (Gracillariidae). This species consists of two host races, which are associated with Juglans ailanthifolia Carr. (Juglandaceae) and Lyonia ovalifolia (Wall.) Drude (Ericaceae). The two host races clearly differ in host preferences of ovipositing females.
• 4. In an experiment of mating site selection, Lyonia‐associated host race females significantly preferred Lyonia, while males of the Lyonia‐associated host race and both sexes of the Juglans‐associated host race did not show a preference for either plant. The mating activity of the Lyonia‐associated host race was not reduced in the absence of host plants. In the Juglans‐associated host race, however, the proportion of successful matings was significantly reduced when the host was absent.
• 5. These laboratory experiments provide empirical evidence that the different host associations in A. transecta do not directly lead to host‐induced assortative mating between the two host races as a pleiotropic effect. However, the present results suggest that the combined effects of the mating‐site preference of Lyonia‐associated females and the mating propensity of Juglans‐associated females could contribute to reproductive isolation between the two host races.