Host-parasite Coevolution Research Articles

Soil biodiversity and microbial antagonism for suppression of plant-parasitic nematodes

Abstract Plant parasitic nematodes (PPN) cause significant economic losses in agriculture and the use of nematicides is the most common management practice applied today. However, due to the impact of such chemicals, more sustainable methods are needed. Current trends consider the exploitation of indigenous soil microbial communities. In this review we discuss some concepts required for the conservation and management of soil microorganisms, considered as a fundamental natural resource. Co-evolution and co-speciation are basic evolutionary processes of soil taxa involved in soil ecosystem services such as nematode regulation. The microorganisms showing a host-parasite co-evolution hold potential for the insurgence or re-construction of a natural equilibrium in soil, aiming at nematode regulation. The impact on soil microbial diversity of farming intensification and PPN management through nematicides is also discussed. Some examples of soil microbial resources and their impact including antagonists like nematophagous fungi (NF), aquatic parasites and bacteria are also briefly reviewed.

Optimality and extinction in a mutator model for host-parasite coevolution

We employed a mutator version of the quasispecies model to analyze the coevolution of host-parasite systems, where both are modeled with digital genomes and parasites recognize their hosts by matching. Specifically, they successfully identify the targets if their Hamming distance is sufficiently small. Mutations enable hosts to navigate through sequence space, thus evading parasite detection. We analytically solved the single-peak landscape scenario for this coevolving model. Our findings indicate that there is an optimal mutation rate for parasites that maximizes their survival, beyond which a critical mutation rate defines a threshold leading to parasite extinction.

Trade-offs between receptor modification and fitness drive host-bacteriophage co-evolution leading to phage extinction or co-existence.

Parasite-host co-evolution results in population extinction or co-existence, yet the factors driving these distinct outcomes remain elusive. In this study, Salmonella strains were individually co-evolved with the lytic phage SF1 for 30days, resulting in phage extinction or co-existence. We conducted a systematic investigation into the phenotypic and genetic dynamics of evolved host cells and phages to elucidate the evolutionary mechanisms. Throughout co-evolution, host cells displayed diverse phage resistance patterns: sensitivity, partial resistance, and complete resistance, to wild-type phage. Moreover, phage resistance strength showed a robust linear correlation with phage adsorption, suggesting that surface modification-mediated phage attachment predominates as the resistance mechanism in evolved bacterial populations. Additionally, bacterial isolates eliminating phages exhibited higher mutation rates and lower fitness costs in developing resistance compared to those leading to co-existence. Phage resistance genes were classified into two categories: key mutations, characterized by nonsense/frameshift mutations in rfaH-regulated rfb genes, leading to the removal of the receptor O-antigen; and secondary mutations, which involve less critical modifications, such as fimbrial synthesis and tRNA modification. The accumulation of secondary mutations resulted in partial and complete resistance, which could be overcome by evolved phages, whereas key mutations conferred undefeatable complete resistance by deleting receptors. In conclusion, higher key mutation frequencies with lower fitness costs promised strong resistance and eventual phage extinction, whereas deficiencies in fitness cost, mutation rate, and key mutation led to co-existence. Our findings reveal the distinct population dynamics and evolutionary trade-offs of phage resistance during co-evolution, thereby deepening our understanding of microbial interactions.

Nuts and bolts of the behavioural manipulation by Toxoplasma gondii.

In this review, I take the first-person perspective of a neuroscientist interested in Toxoplasma gondii (Nicolle et Manceaux, 1908). I reflect on the value of behavioural manipulation as a perturbation tool to understand the organisation of behaviour within the brain. Toxoplasma gondii infection reduces the aversion of rats to the olfactory cues of cat presence. This change in behaviour is one of the often-discussed exemplars of host-parasite coevolution, culminating in the manipulation of the host behaviour for the benefit of the parasite. Such coevolution also means that we can use host-parasite systems as tools to derive fundamental insights about the host brain itself.

No evidence of adaptive tolerance of parasitism in a cavity-nesting brood parasite host

Abstract Acceptance of avian brood parasitism by hosts is one of the most enigmatic aspects of brood parasite–host coevolution. The most common explanation for acceptance of parasitism by hosts of the brown-headed cowbird (Molothrus ater) is evolutionary lag, which suggests that hosts have not had enough time to evolve defenses against parasitism. Alternatively, acceptance may be the optimal strategy when the costs of rejecting parasitism exceed the benefits. The lack of nest site hypothesis applies to secondary cavity-nesting birds that cannot excavate their own nests and predicts that hosts accept parasitism instead of deserting a parasitized nest when there are no vacant nest sites available in which to renest. I tested this hypothesis using the prothonotary warbler (Pronotaria citrea), a commonly parasitized, cavity-nesting cowbird host. I used a paired nest box design and predicted that if hosts accept parasitism because of a lack of alternative nest sites, they should desert parasitized nests and renest in the vacant nest box on their territory. I recorded 37 cases where a nest was parasitized and warblers only deserted 2 parasitized nest boxes for a vacant nest box. Both desertions were attributable to factors other than parasitism and the rate of desertion did not differ from controls that only had a single nest box. Moreover, 7 of the warblers initiated clutches in nest boxes that already contained cowbird egg despite having vacant nest boxes available on their territories. These results indicate that warblers do not accept parasitism because of tolerance, but likely due to evolutionary lag.

Isospora pichororei n. sp. (Chromista: Apicomplexa: Eimeriidae) from rufous-capped spinetails Synallaxis ruficapilla Vieillot, 1819 (Passeriformes: Furnariidae: Synallaxiinae) in South America

Spinetails are a suboscine passerines of the genus Synallaxis Vieillot, 1818 which have great interest for ornithology, given the wide diversity of 37 species that are distributed throughout the Neotropical region. Despite this wide diversity and distribution, Synallaxis spp. have never been recorded as hosts of coccidian parasites. In this context, the current study describes a new species of Isospora Schneider, 1881 from rufous-capped spinetails Synallaxis ruficapilla Vieillot, 1819 captured in the Itatiaia National Park, which is a federal conservation unit in Southeastern Brazil. The oocysts of Isospora pichororei Genovez-Oliveira & Berto n. sp. are subspheroidal to ovoidal, measuring on average 25 by 21 μm. Micropyle is present, but discrete. Oocyst residuum absent, but one or two polar granules are present. Sporocysts are ellipsoidal with slightly pointed posterior end, measuring on average 17 by 10 μm. Stieda and sub-Stieda bodies are present. Sporocyst residuum is clustered among the vermiform sporozoites, which have striations, refractile bodies and nucleus. This morphology was different from the other Isospora spp. recorded in the host family Furnariidae. Molecular identification was targeted by the amplification and sequencing of a locus of the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene. This sequence had the highest similarity of 99.5% with a sequence deposited for Isospora oliveirai Ortúzar-Ferreira & Berto, 2020, which is a coccidian species that parasitizes suboscine tityrids Schiffornis virescens (Lafresnaye, 1838), also in the Itatiaia National Park. Phylogenetic analysis grouped some species in subclades, including I. pichororei with I. oliveirai; however, it was inconclusive in an expectation of parasite-host coevolution. Finally, I. pichororei is established as new to science, being the first description from Synallaxinae and the third description from Furnariidae. Furthermore, this is the first Isospora sp. from the host family Furnariidae to have a molecular supplementation by sequencing a locus of the cox1 gene of the mitochondrial genome.

Environmental conditions influence host-parasite interactions and host fitness in a migratory passerine.

The study of host-parasite co-evolution is a central topic in evolutionary ecology. However, research is still fragmented and the extent to which parasites influence host life history is debated. One reason for this incomplete picture is the frequent omission of environmental conditions in studies analyzing host-parasite dynamics, which may influence the exposure to or effects of parasitism. To contribute to elucidating the largely unresolved question of how environmental conditions are related to the prevalence and intensity of infestation and their impact on hosts, we took advantage of 25 years of monitoring of a breeding population of pied flycatchers, Ficedula hypoleuca, in a Mediterranean area of central Spain. We investigated the influence of temperature and precipitation during the nestling stage at a local scale on the intensity of blowfly (Protocalliphora azurea) parasitism during the nestling stage. In addition, we explored the mediating effect of extrinsic and intrinsic factors and blowfly parasitism on breeding success (production of fledglings) and offspring quality (nestling mass on day 13). The prevalence and intensity of blowfly parasitism were associated with different intrinsic (host breeding date, brood size) and extrinsic (breeding habitat, mean temperature) factors. Specifically, higher average temperatures during the nestling phase were associated with lower intensities of parasitism, which may be explained by changes in blowflies' activity or larval developmental success. In contrast, no relationship was found between the prevalence of parasitism and any of the environmental variables evaluated. Hosts that experienced high parasitism intensities in their broods produced more fledglings as temperature increased, suggesting that physiological responses to severe parasitism during nestling development might be enhanced in warmer conditions. The weight of fledglings was, however, unrelated to the interactive effect of parasitism intensity and environmental conditions. Overall, our results highlight the temperature dependence of parasite-host interactions and the importance of considering multiple fitness indicators and climate-mediated effects to understand their complex implications for avian fitness and population dynamics.

Long-term balancing selection for pathogen resistance maintains trans-species polymorphisms in a planktonic crustacean

Balancing selection is an evolutionary process that maintains genetic polymorphisms at selected loci and strongly reduces the likelihood of allele fixation. When allelic polymorphisms that predate speciation events are maintained independently in the resulting lineages, a pattern of trans-species polymorphisms may occur. Trans-species polymorphisms have been identified for loci related to mating systems and the MHC, but they are generally rare. Trans-species polymorphisms in disease loci are believed to be a consequence of long-term host-parasite coevolution by balancing selection, the so-called Red Queen dynamics. Here we scan the genomes of three crustaceans with a divergence of over 15 million years and identify 11 genes containing identical-by-descent trans-species polymorphisms with the same polymorphisms in all three species. Four of these genes display molecular footprints of balancing selection and have a function related to immunity. Three of them are located in or close to loci involved in resistance to a virulent bacterial pathogen, Pasteuria, with which the Daphnia host is known to coevolve. This provides rare evidence of trans-species polymorphisms for loci known to be functionally relevant in interactions with a widespread and highly specific parasite. These findings support the theory that specific antagonistic coevolution is able to maintain genetic diversity over millions of years.

Characterizing genetic variation on the Z chromosome in Schistosoma japonicum reveals host-parasite co-evolution

BackgroundSchistosomiasis is a neglected tropical disease that afflicts millions of people worldwide; it is caused by Schistosoma, the only dioecious flukes with ZW systems. Schistosoma japonicum is endemic to Asia; the Z chromosome of S. japonicum comprises one-quarter of the entire genome. Detection of positive selection using resequencing data to understand adaptive evolution has been applied to a variety of pathogens, including S. japonicum. However, the contribution of the Z chromosome to evolution and adaptation is often neglected.MethodsWe obtained 1,077,526 high-quality SNPs on the Z chromosome in 72 S. japonicum using re-sequencing data publicly. To examine the faster Z effect, we compared the sequence divergence of S. japonicum with two closely related species, Schistosoma haematobium and S. mansoni. Genetic diversity was compared between the Z chromosome and autosomes in S. japonicum by calculating the nucleotide diversity (π) and Dxy values. Population structure was also assessed based on PCA and structure analysis. Besides, we employed multiple methods including Tajima’s D, FST, iHS, XP-EHH, and CMS to detect positive selection signals on the Z chromosome. Further RNAi knockdown experiments were performed to investigate the potential biological functions of the candidate genes.ResultsOur study found that the Z chromosome of S. japonicum showed faster evolution and more pronounced genetic divergence than autosomes, although the effect may be smaller than the variation among genes. Compared with autosomes, the Z chromosome in S. japonicum had a more pronounced genetic divergence of sub-populations. Notably, we identified a set of candidate genes associated with host-parasite co-evolution. In particular, LCAT exhibited significant selection signals within the Taiwan population. Further RNA interference experiments suggested that LCAT is necessary for S. japonicum survival and propagation in the definitive host. In addition, we identified several genes related to the specificity of the intermediate host in the C-M population, including Rab6 and VCP, which are involved in adaptive immune evasion to the host.ConclusionsOur study provides valuable insights into the adaptive evolution of the Z chromosome in S. japonicum and further advances our understanding of the co-evolution of this medically important parasite and its hosts.Graphical

High parasite diversity maintained after an alga-virus coevolutionary arms race.

Arms race dynamics are a common outcome of host-parasite coevolution. While they can theoretically be maintained indefinitely, realistic arms races are expected to be finite. Once an arms race has ended, for example due to the evolution of a generalist-resistant host, the system may transition into coevolutionary dynamics that favour long-term diversity. In microbial experiments, host-parasite arms races often transition into a stable coexistence of generalist-resistant hosts, (semi-)susceptible hosts, and parasites. While long-term host diversity is implicit in these cases, parasite diversity is usually overlooked. In this study, we examined parasite diversity after the end of an experimental arms race between a unicellular alga (Chlorella variabilis) and its lytic virus (PBCV-1). First, we isolated virus genotypes from multiple time points from two replicate microcosms. A time-shift experiment confirmed that the virus isolates had escalating host ranges, i.e., that arms races had occurred. We then examined the phenotypic and genetic diversity of virus isolates from the post-arms race phase. Post-arms race virus isolates had diverse host ranges, survival probabilities, and growth rates; they also clustered into distinct genetic groups. Importantly, host range diversity was maintained throughout the post-arms race phase, and the frequency of host range phenotypes fluctuated over time. We hypothesize that this dynamic polymorphism was maintained by a combination of fluctuating selection and demographic stochasticity. Together with previous work in prokaryotic systems, our results link experimental observations of arms races to natural observations of long-term host and parasite diversity.

Genome Evolution and Introgression in the New Zealand mud Snails Potamopyrgus estuarinus and Potamopyrgus kaitunuparaoa.

We have sequenced, assembled, and analyzed the nuclear and mitochondrial genomes and transcriptomes of Potamopyrgus estuarinus and Potamopyrgus kaitunuparaoa, two prosobranch snail species native to New Zealand that together span the continuum from estuary to freshwater. These two species are the closest known relatives of the freshwater species Potamopyrgus antipodarum-a model for studying the evolution of sex, host-parasite coevolution, and biological invasiveness-and thus provide key evolutionary context for understanding its unusual biology. The P. estuarinus and P. kaitunuparaoa genomes are very similar in size and overall gene content. Comparative analyses of genome content indicate that these two species harbor a near-identical set of genes involved in meiosis and sperm functions, including seven genes with meiosis-specific functions. These results are consistent with obligate sexual reproduction in these two species and provide a framework for future analyses of P. antipodarum-a species comprising both obligately sexual and obligately asexual lineages, each separately derived from a sexual ancestor. Genome-wide multigene phylogenetic analyses indicate that P. kaitunuparaoa is likely the closest relative to P. antipodarum. We nevertheless show that there has been considerable introgression between P. estuarinus and P. kaitunuparaoa. That introgression does not extend to the mitochondrial genome, which appears to serve as a barrier to hybridization between P. estuarinus and P. kaitunuparaoa. Nuclear-encoded genes whose products function in joint mitochondrial-nuclear enzyme complexes exhibit similar patterns of nonintrogression, indicating that incompatibilities between the mitochondrial and the nuclear genome may have prevented more extensive gene flow between these two species.

How flexible parasites can outsmart their hosts for evolutionary dominance

Antagonistic coevolution between hosts and parasites substantially impacts community structure, with parasites displaying fluctuating selection or arms race dynamics during coevolution. The traditional matching alleles (MA) and gene-for-gene (GFG) models have been used to describe the dynamics and interaction of host-parasite coevolution, with these models assuming that parasites adopt a single strategy when competing with other parasites. We present a nonlinear dynamic population model that challenges this assumption, showing how a parasite that is disadvantaged under either the MA or the GFG model can win the competition by switching between the two losing strategies based on an external environmental cue, internal processes, or stochastic decision-making. This counterintuitive outcome is analogous to Parrondo's paradox, a game-theoretic concept that shows how alternating between two losing strategies can result in a winning outcome. Our numerical experiments support the validity of this model, suggesting that parasites can greatly benefit from maximum flexibility in their interactions with hosts. The flexibility of successful parasites puts an extra burden on the host defenses that have to adapt to different strategies of the parasites. These findings contribute to a deeper understanding of the coevolution of parasites and hosts, with broad implications for the evolution of complex ecological systems. Published by the American Physical Society 2024

Ectopical expression of bacterial collagen-like protein supports its role as adhesin in host-parasite coevolution.

For a profound understanding of antagonistic coevolution, it is necessary to identify the coevolving genes. The bacterium Pasteuria and its host, the microcrustacean Daphnia, are a well-characterized paradigm for co-evolution, but the underlying genes remain largely unknown. A genome-wide association study suggested a Pasteuria collagen-like protein 7 (Pcl7) as a candidate mediating parasite attachment and driving its coevolution with the host. Since Pasteuria ramosa cannot currently be genetically manipulated, we used Bacillus thuringiensis to express a fusion protein of a Pcl7 carboxy-terminus from P. ramosa and the amino-terminal domain of a B. thuringiensis collagen-like protein (CLP). Mutant B. thuringiensis (Pcl7-Bt) spores but not wild-type B. thuringiensis (WT-Bt) spores attached to the same site of susceptible hosts as P. ramosa. Furthermore, Pcl7-Bt spores attached readily to susceptible host genotypes, but only slightly to resistant host genotypes. These findings indicated that the fusion protein was properly expressed and folded and demonstrated that indeed the C-terminus of Pcl7 mediates attachment in a host genotype-specific manner. These results provide strong evidence for the involvement of a CLP in the coevolution of Daphnia and P. ramosa and open new avenues for genetic epidemiological studies of host-parasite interactions.

The impact of sterility-mortality tolerance and recovery-transmission trade-offs on host-parasite coevolution.

Understanding the coevolutionary dynamics of hosts and their parasites remains a major focus of much theoretical literature. Despite empirical evidence supporting the presence of sterility-mortality tolerance trade-offs in hosts and recovery-transmission trade-offs in parasites, none of the current models have explored the potential outcomes when both trade-offs are considered within a coevolutionary framework. In this study, we consider a model where the host evolves sterility tolerance at the cost of increased mortality and the parasite evolves higher transmission rate at the cost of increased recovery rate (reduced infection duration), and use adaptive dynamics to predict the coevolutionary outcomes under such trade-off assumptions. We particularly aim to understand how our coevolutionary dynamics compare with single species evolutionary models. We find that evolutionary branching in the host can drive the parasite population to branch, but that cycles in the population dynamics can prevent the coexisting strains from reaching their extremes. We also find that varying crowding does not impact the recovery rate when only the parasite evolves, yet coevolution reduces recovery as crowding intensifies. We conclude by discussing how different host and parasite trade-offs shape coevolutionary outcomes, underscoring the pivotal role of trade-offs in coevolution.

Host switch by honey bee parasitic mites leads to symbiont diversification

Host-parasite co-evolution is a reciprocal genetic change; however, the parasite may switch to a novel host, deviating from conventional co-evolution. Varroa destructor is a native parasite of the honey bee Apis cerana, and the mite has established infestation in another honey bee, Apis mellifera, causing colony failure. When mites switched to the novel host, they formed a distinct population from mites that remained on the native host. Consequently, this led to divergence in the microbiota associated with mites in two host populations. The microbes were conserved at the species level reflected by alpha diversity, with substantial relative abundance variance. Microbes found in mites were distinct from the bee microbiota. They mainly were pathogenic with antibiotic resistance, while a few bacterial taxa were previously found in honey bees, including Klebsiella pneumoniae and Pseudomanas aeruginosa. These symbionts may transfer between the mites and honey bees.

Host‐switching events are not always the driver of speciation in social parasites: a case study in Temnothorax (Myrmoxenus) ants (Hymenoptera, Formicidae)

AbstractHost–parasite systems, including social parasites that exploit resources of the host colonies, are fascinating objects for evolutionary biologists mainly due to the dynamic and often rapid host–parasite coevolution. Host‐switching events are believed to induce rapid speciation of parasitic species. The socially parasitic ant lineage Myrmoxenus, which corresponds to the monophyletic Temnothorax corsicus group, counts in total a dozen species. Most Myrmoxenus species utilize a single host species, but a few others, like Myrmoxenus ravouxi (André, 1896) and M. gordiagini Ruzsky, 1902, are known to use multiple host taxa. Myrmoxenus zaleskyi (Sadil, 1953) was described as a putative congener of M. ravouxi based on its distinct host selection. In this paper, we investigate the diversity of the widely distributed European lineages M. ravouxi and M. zaleskyi from multiple and complementary perspectives to understand whether the host preference exhibited by these two forms implies speciation. We integrated evidence from molecular genetics using mitochondrial CO I/CO II genes, including the tLeu‐region, and multivariate analyses of morphometric data collected from workers and female sexuals (gynes). Although there is substantial regional host species specificity, results suggest that host switching did not result in phylogenetic or morphological divergence and that the central European M. zaleskyi can be considered the junior synonym of M. ravouxi. As the lineage Myrmoxenus has been the subject of considerable evolutionary research, these results are essential to achieve a more accurate picture of host–parasite systems in the future and further strengthen the justification of an integrative approach in studying similarly complex systems. We advise against describing new parasitic species based on host preference unless coupled with marked heritable phenotypic adaptations.

Host-Parasite Coevolution in Continuous Space Leads to Variation in Local Adaptation across Spatial Scales.

AbstractPrevious host-parasite coevolutionary theory has focused on understanding the determinants of local adaptation using spatially discrete models. However, these studies fall short of describing patterns of host-parasite local adaptation across spatial scales. In contrast, empirical work demonstrates that patterns of adaptation depend on the scale at which they are measured. Here, we propose a mathematical model of host-parasite coevolution in continuous space that naturally leads to a scale-dependent definition of local adaptation. In agreement with empirical research, we find that patterns of adaptation vary across spatial scales. In some cases, not only the magnitude of local adaptation but also the identity of the locally adapted species will depend on the spatial scale at which measurements are taken. Building on our results, we suggest a way to consistently measure parasite local adaptation when continuous space is the driver of cross-scale variation. We also describe a way to test whether continuous space is driving cross-scale variation. Taken together, our results provide a new perspective that can be used to understand empirical observations previously unexplained by theoretical expectations and deepens our understanding of the mechanics of host-parasite local adaptation.

The maintenance of genetic diversity under host-parasite coevolution in finite, structured populations.

As a corollary to the Red Queen hypothesis, host-parasite coevolution has been hypothesized to maintain genetic variation in both species. Recent theoretical work, however, suggests that reciprocal natural selection alone is insufficient to maintain variation at individual loci. As highlighted by our brief review of the theoretical literature, models of host-parasite coevolution often vary along multiple axes (e.g. inclusion of ecological feedbacks or abiotic selection mosaics), complicating a comprehensive understanding of the effects of interacting evolutionary processes on diversity. Here we develop a series of comparable models to explore the effect of interactions between spatial structures and antagonistic coevolution on genetic diversity. Using a matching alleles model in finite populations connected by migration, we find that, in contrast to panmictic populations, coevolution in a spatially structured environment can maintain genetic variation relative to neutral expectations with migration alone. These results demonstrate that geographic structure is essential for understanding the effect of coevolution on biological diversity.

Parasite manipulation of host phenotypes inferred from transcriptional analyses in a trematode-amphipod system.

Manipulation of host phenotypes by parasites is hypothesized to be an adaptive strategy enhancing parasite transmission across hosts and generations. Characterizing the molecular mechanisms of manipulation is important to advance our understanding of host-parasite coevolution. The trematode (Levinseniella byrdi) is known to alter the colour and behaviour of its amphipod host (Orchestia grillus) presumably increasing predation of amphipods which enhances trematode transmission through its life cycle. We sampled 24 infected and 24 uninfected amphipods from a salt marsh in Massachusetts to perform differential gene expression analysis. In addition, we constructed novel genomic tools for O. grillus including a de novo genome and transcriptome. We discovered that trematode infection results in upregulation of amphipod transcripts associated with pigmentation and detection of external stimuli, and downregulation of multiple amphipod transcripts implicated in invertebrate immune responses, such as vacuolar ATPase genes. We hypothesize that suppression of immune genes and the altered expression of genes associated with coloration and behaviour may allow the trematode to persist in the amphipod and engage in further biochemical manipulation that promotes transmission. The genomic tools and transcriptomic analyses reported provide new opportunities to discover how parasites alter diverse pathways underlying host phenotypic changes in natural populations.

Host–parasite coevolution and the stability of genetic kin recognition

Crozier's paradox suggests that genetic kin recognition will not be evolutionarily stable. The problem is that more common tags (markers) are more likely to be recognized and helped. This causes common tags to increase in frequency, eliminating the genetic variability that is required for genetic kin recognition. Two potential solutions to this problem have been suggested: host-parasite coevolution and multiple social encounters. We show that the host-parasite coevolution hypothesis does not work as commonly assumed. Host-parasite coevolution only stabilizes kin recognition at a parasite resistance locus if parasites adapt rapidly to hosts and cause intermediate or high levels of damage (virulence). Additionally, when kin recognition is stabilized at a parasite resistance locus, this can have an additional cost of making hosts more susceptible to parasites. However, we show that if the genetic architecture is allowed to evolve, meaning natural selection can choose the recognition locus, genetic kin recognition is more likely to be stable. The reason for this is that host-parasite coevolution can maintain tag diversity at another (neutral) locus by genetic hitchhiking, allowing that other locus to be used for genetic kin recognition. These results suggest a way that host-parasite coevolution can resolve Crozier's paradox, without making hosts more susceptible to parasites. However, the opportunity for multiple social encounters may provide a more robust resolution of Crozier's paradox.