The Red Queen Process does not Select for High Recombination Rates in Haplodiploid Hosts

Kidner, Jonathan; Moritz, Robin F. A.

doi:10.1007/s11692-012-9221-4

Cited by 8 publications

(7 citation statements)

References 36 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The Red Queen hypothesis of host–parasite coevolution predicts that the evolution of resistance and counter‐resistance traits will result in oscillations of haplotype frequency (van Valen, ; Kidner & Moritz, ), which track the oscillation of the relative frequency and virulence of parasite lineages and select for increased genetic diversity, recombination and evolutionary rates in the more slowly reproducing host (Maynard Smith, ; Hamilton et al ., ; Kidner & Moritz, ). However, in haplodiploid lineages such as the Hymenoptera, some models suggest that the link between sex, recombination and the evolution of resistance traits is weaker than when the host is diploid (Kidner & Moritz, ).…”

Section: Introductionmentioning

confidence: 99%

The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones

Conlon

Frey

Rosenkranz

et al. 2018

J of Evolutionary Biology

View full text Add to dashboard Cite

The Red Queen hypothesis predicts that host-parasite coevolutionary dynamics can select for host resistance through increased genetic diversity, recombination and evolutionary rates. However, in haplodiploid organisms such as the honeybee (Apis mellifera), models suggest the selective pressure is weaker than in diploids. Haplodiploid sex determination, found in A. mellifera, can allow deleterious recessive alleles to persist in the population through the diploid sex with negative effects predominantly expressed in the haploid sex. To overcome these negative effects in haploid genomes, epistatic interactions have been hypothesized to play an important role. Here, we use the interaction between A. mellifera and the parasitic mite Varroa destructor to test epistasis in the expression of resistance, through the inhibition of parasite reproduction, in haploid drones. We find novel loci on three chromosomes which explain over 45% of the resistance phenotype. Two of these loci interact only additively, suggesting their expression is independent of each other, but both loci interact epistatically with the third locus. With drone offspring inheriting only one copy of the queen's chromosomes, the drones will only possess one of two queen alleles throughout the years-long lifetime of the honeybee colony. Varroa, in comparison, completes its highly inbred reproductive cycle in a matter of weeks, allowing it to rapidly evolve resistance. Faced with the rapidly evolving Varroa, a diversity of pathways and epistatic interactions for the inhibition of Varroa reproduction could therefore provide a selective advantage to the high levels of recombination seen in A. mellifera. This allows for the remixing of phenotypes despite a fixed queen genotype.

show abstract

Section: Introductionmentioning

confidence: 99%

The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones

Conlon

Frey

Rosenkranz

et al. 2018

J of Evolutionary Biology

View full text Add to dashboard Cite

show abstract

“…In the context of plant necrotrophic parasites, this model is also confusingly named 'inverse gene-for-gene' (Peters et al 2019). Thirdly, the inverse-matching-allele (IMA) model was proposed to reflect the adaptive immune system of vertebrates, where the host resists through recognition of the parasite and infections occur when the parasite mismatches the host (Kidner and Moritz 2013;Thrall et al 2016). The IMA model was defined in the context of multi-allelic series of resistance and pathogenicity genes.…”

Section: Introductionmentioning

confidence: 99%

The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions

Moury¹,

Audergon²,

Baudracco-Arnas³

et al. 2021

Preprint

View full text Add to dashboard Cite

Understanding the relationships between host range and pathogenicity for parasites, and between the efficiency and scope of immunity for hosts are essential to implement efficient disease control strategies. In the case of plant parasites, most studies have focused on describing qualitative interactions and a variety of genetic and evolutionary models has been proposed in this context. Although plant quantitative resistance benefits from advantages in terms of durability, we presently lack models that account for quantitative interactions between plants and their parasites and the evolution of these interactions. Nestedness and modularity are important features to unravel the overall structure of host-parasite interaction matrices. Here, we analysed these two features on 32 matrices of quantitative pathogenicity trait data gathered from 15 plant-parasite pathosystems consisting of either annual or perennial plants along with fungi or oomycetes, bacteria, nematodes, insects and viruses. The performance of several nestedness and modularity algorithms was evaluated through a simulation approach, which helped interpretation of the results. We observed significant modularity in only six of the 32 matrices, with two or three modules detected. For three of these matrices, modules could be related to resistance quantitative trait loci present in the host. In contrast, we found high and significant nestedness in 30 of the 32 matrices. Nestedness was linked to other properties of plant-parasite interactions. First, pathogenicity trait values were explained in majority by a parasite strain effect and a plant accession effect, with no parasite-plant interaction term. Second, correlations between the efficiency and scope of the resistance of plant genotypes, and between the host range breadth and pathogenicity level of parasite strains were overall positive. This latter result questions the efficiency of strategies based on the deployment of several genetically-differentiated cultivars of a given crop species in the case of quantitative plant immunity.

show abstract

“…The conflicting fitness optima between host and parasite mean that an adaptation in one is expected to lead to a counter‐adaptation in the other (Bell, ). This, in turn, is expected to drive fluctuations in haplotype frequency, selecting for those which are most effective against the most common virulence or resistance trait (Bell, ; Kidner & Moritz, ). With the concentration of resources in social insect colonies making them attractive targets for parasites, these fluctuations in the fitness of different defensive traits have typically resulted in social insects evolving a range of anti‐parasite defences (Kurze, Routtu, & Moritz, ).…”

Section: Introductionmentioning

confidence: 99%

A gene for resistance to the Varroa mite (Acari) in honey bee (Apis mellifera) pupae

et al. 2019

View full text Add to dashboard Cite

Social insect colonies possess a range of defences which protect them against highly virulent parasites and colony collapse. The host–parasite interaction between honey bees (Apis mellifera) and the mite Varroa destructor is unusual, as honey bee colonies are relatively poorly defended against this parasite. The interaction has existed since the mid‐20th Century, when Varroa switched host to parasitize A. mellifera. The combination of a virulent parasite and relatively naïve host means that, without acaricides, honey bee colonies typically die within 3 years of Varroa infestation. A consequence of acaricide use has been a reduced selective pressure for the evolution of Varroa resistance in honey bee colonies. However, in the past 20 years, several natural‐selection‐based breeding programmes have resulted in the evolution of Varroa‐resistant populations. In these populations, the inhibition of Varroa's reproduction is a common trait. Using a high‐density genome‐wide association analysis in a Varroa‐resistant honey bee population, we identify an ecdysone‐induced gene significantly linked to resistance. Ecdysone both initiates metamorphosis in insects and reproduction in Varroa. Previously, using a less dense genetic map and a quantitative trait loci analysis, we have identified Ecdysone‐related genes at resistance loci in an independently evolved resistant population. Varroa cannot biosynthesize ecdysone but can acquire it from its diet. Using qPCR, we are able to link the expression of ecdysone‐linked resistance genes to Varroa's meals and reproduction. If Varroa co‐opts pupal compounds to initiate and time its own reproduction, mutations in the host's ecdysone pathway may represent a key selection tool for honey bee resistance and breeding.

show abstract

The Red Queen Process does not Select for High Recombination Rates in Haplodiploid Hosts

Cited by 8 publications

References 36 publications

The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones

The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones

The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions

A gene for resistance to the Varroa mite (Acari) in honey bee (Apis mellifera) pupae

Contact Info

Product

Resources

About