Coevolutionary interactions in a host–parasite system

Interactions between parasitic cuckoos and their hosts represent a classic example of coevolution, where adaptations in the parasite to exploit the host select for defences, which in turn select for new parasite adaptations. Current interactions between the two parties may be at an evolutionary equilibrium or, alternatively, a coevolutionary arms race may be taking place. By taking into account the effect of gene flow in 15 European magpie ( Pica pica ) populations, we studied the coevolutionary interactions with its brood parasite, the great spotted cuckoo ( Clamator glandarius ). Our results suggest that, in Europe, magpies and cuckoos are engaged in an ongoing coevolutionary process because, despite controlling for the large amounts of gene flow among different magpie populations, we still found a positive relationship between host defence (i.e. foreign egg recognition and rejection) and parasite selection pressure.     

Heterogeneous selection promotes maintenance of polymorphism in host–parasite interactions

Polymorphism in loci affecting host resistance and parasite virulence is characteristic for nearly all species and this genetic variation is considered to have profound consequences for the patterns of disease incidence, prevalence and evolution. The gene-for-gene (GFG) system is a well-characterized genetic interaction of host recognition and parasite antigenic loci for a wide range of plant-parasite interactions. Long-term maintenance of polymorphism in GFG systems has remained puzzling for both theoreticians and empiricists. Traditionally this diversity has been explained by tradeoffs with other life-history traits closely linked with fitness, yet empirical evidence for such costs has remained mixed. Here we argue that incorporating simple ecological reality – spatial structuring and gradient of environmental conditions – into host–parasite research will help us understand how polymorphism is maintained. While environmental conditions (biotic and abiotic factors) have been studied in depth in plant pathology for their influence on disease severity and plant yield, they have been rarely set into an evolutionary framework. We briefly review recent data on natural plant–parasite metapopulations and theoretical models moving from single population models towards metapopulation theory to reveal in just how many ways spatial structuring may affect the coevolutionary process. We clarify also how spatially heterogeneous selection, through G×E (or G×G×E) interactions, may be particularly important for natural host–parasite interactions and suggest that this provides the unifying ground upon which future theoretical and empirical work should be build on.     

The evolutionary dynamics of local infection and global reproduction in host–parasite interactions

A fundamental question in both evolutionary biology and parasitology is why do different levels of virulence evolve in different parasites. Here we use explicitly spatial lattice models to show how the spatial relationships of infection and host reproduction determine the degree of virulence that will occur. When the reproduction of the host acts over larger spatial scales than the infection process higher virulence is predicted. In contrast to both the mean-field and the case where infection acts over larger spatial scales than reproduction, the transmission and virulence predicted are always finite as "self-shading" of infected individuals always occurs. This process may help to explain the evolution of the high virulence of larval diseases of insects where reproduction clearly acts over greater distances than infection.     

Local adaptation and the geometry of host–parasite coevolution

Metapopulation dynamics can strongly affect the ecological and evolutionary processes involved in host–parasite interactions. Here, I analyse a deterministic host–parasite coevolutionary model and derive analytic approximations for the level of local adaptation as a function of (1) host migration rate, (2) parasite migration rate, (3) parasite specificity and (4) parasite virulence. This analysis confirms the results of previous simulation studies: the difference between host and parasite migration rates may explain the level of local adaptation of both species. I also show that both higher specificity and higher virulence generally lead to higher levels of local adaptation of the species which is already ahead in the coevolutionary arms race. The present analysis also provides a simple geometric interpretation for local adaptation which captures the complexity of the temporal dynamics of host–parasite coevolution.     

Coevolution of daily activity timing in a host–parasite system

Coevolutionary theories applied in the study of host–parasite systems indicate that lineages exhibit progressive trends in response to reciprocal selective pressures. Avian brood parasites have generated intense interest as models for coevolutionary processes. Similar to avian cuckoos, Polistes wasp social parasites usurp a nest and exploit the parental care of a congeneric species to rear their own brood. In the present study, we show a coevolutionary arms race in the daily activity pattern in a Polistes host–parasite pair. We measured the daily activity rate, in constant laboratory conditions, of both host and parasite females during the period in which nest usurpations occur. The parasites showed a hyperkinesis in the middle of the day. As the field observations suggested, this mid-day activity is used to perform host nest usurpation attempts. Timing the usurpations allows the parasite to maximize its usurpation attempts during daytime when the host defence is lower. A field comparison of host presence on the nest in two populations with different parasitism rates showed that populations under strong parasitic pressure exhibit timing counteradaptations to optimize nest defence. This study provides the first example of a mutual coadaptation in timing activity in a parasite–host system.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 399–405.     

Host parasite interactions and pathophysiology in Giardia infections

Giardia is a protozoan parasite of the small intestine, and a leading cause of diarrhoeal disease worldwide in a variety of animals, including humans. The host-parasite interaction and pathophysiological processes of giardiasis remain incompletely understood. Current research suggests that Giardia-induced diarrhoeal disease is mediated by small intestinal malabsorption and maldigestion, chloride hypersecretion and increased rates of small intestinal transit. Small intestinal malabsorption and maldigestion results from the CD8+ lymphocyte-induced diffuse shortening of brush border microvilli. Activation of CD8+ lymphocytes occurs secondary to small intestinal barrier dysfunction, which results from heightened rates of enterocyte apoptosis and disruption of epithelial tight junctions. Both host and parasite factors contribute to the pathogenesis of giardiasis and ongoing research in this field may elucidate genotype/assemblage-specific pathogenic mechanisms. Giardia infections can result in chronic gastrointestinal disorders such as post-infectious Irritable Bowel Syndrome and symptoms may manifest at extra-intestinal sites, even though the parasite does not disseminate beyond the gastrointestinal tract. The infection can cause failure to thrive in children. Furthermore, there is now evidence suggesting that Giardia symptoms may vary between industrialised and developing areas of the world, for reasons that remain obscure. More research is needed to improve our understanding of this parasitic infection which was recently included in the World Health Organisation “Neglected Disease Initiative”.     

Molecular characteristics and physiology of microsporidia

A survey of the molecular features of microsporidia is presented which attempts to comment on unresolved questions concerning the physiology of these amitochondrial intracellular parasites. Various transports of host-derived molecules can be predicted and trehalose appears as a potential reserve of glucose for energy metabolism. Significant insights into membrane lipids, polyamine metabolism and sporogony-specific proteins have been gained. Some species, such as Encephalitozoon cuniculi, are heterogeneous entities and harbor a small genome. Although showing a variation in genome size of 8.5-fold, microsporidia share reduced rDNA genes. Finally, data on gene organization and a possible evolutionary relationship with fungi are considered.     

Relatedness and spatial proximity as determinants of host–parasite interactions in the brood parasitic Barrow's goldeneye (Bucephala islandica)

Recent studies, which have found evidence for kin-biased egg donation, have sparked interest in re-assessing the parasitic nature of conspecific brood parasitism (CBP). Since host–parasite kinship is essential for mutual benefits to arise from CBP, we explored the role of relatedness in determining the behaviour of conspecific nest parasites and their hosts in nesting female Barrow's goldeneyes ( Bucephala islandica ), a duck in which CBP is common. The results revealed that the amount of parasitism increased with host–parasite relatedness, the effect of which was independent of geographical proximity of host and parasite nests. Proximity per se was also positively associated with the amount of parasitism. Furthermore, while hosts appeared to reduce their clutch size as a response to the presence of parasitic eggs, the magnitude of host clutch reduction also tended to increase with increasing relatedness to the parasite. Hence, our results indicate that both relatedness and spatial proximity are important determinants of CBP, and that host clutch reduction may be an adaptation to nest parasitism, modulated by host–parasite relatedness. Taken together, the results provide a demonstration that relatedness influences host and parasite behaviour in Barrow's goldeneyes, resulting in kin-biased egg donation.     

A priori and a posteriori methods in comparative evolutionary studies of host–parasite associations

Brooks parsimony analysis (BPA) and reconciliation methods in studies of host–parasite associations differ fundamentally, despite using the same null hypothesis. Reconciliation methods may eliminate or modify input data to maximize fit of single parasite clades to a null hypothesis of cospeciation, by invoking different a priori assumptions, including a known host phylogeny. By examining the degree of phylogenetic congruence among multiple parasite clades, using hosts as analogs of taxa but not presuming a host phylogeny or any degree of cospeciation a priori, BPA modifies the null hypothesis of cospeciation if necessary to maintain the integrity of the input data. Two exemplars illustrate critical empirical differences between reconciliation methods and BPA: (1) reconciliation methods rather than BPA may select the incorrect general host cladogram for a set of data from different clades of parasites, (2) BPA rather than reconciliation methods provides the most parsimonious interpretation of all available data, and (3) secondary BPA, proposed in 1990, when applied to data sets in which host‐switching produces hosts with reticulate histories, provides the most parsimonious and biologically realistic interpretations of general host cladograms. The extent to which these general host cladograms, based on cospeciation among different parasite clades inhabiting the same hosts, correspond to host phylogeny can be tested, a posteriori, by comparison with a host phylogeny generated from nonparasite data. These observations lead to the conclusion that BPA and reconciliation methods are designed to implement different research programs based on different epistemologies. BPA is an a posteriori method that is designed to assess the host context of parasite speciation events, whereas reconciliation methods are a priori methods that are designed to fit parasite phylogenies to a host phylogeny. Host‐switching events are essential for explaining complex histories of host–parasite associations. BPA assumes coevolutionary complexity (historical contingency), relying on parsimony as an a posteriori explanatory tool to summarize complex results, whereas reconciliation methods, which embody formalized assumptions of maximum cospeciation, are based on a priori conceptual parsimony. Modifications of basic reconciliation methods, embodied in TreeMap 1.0 and TreeMap 2.02, represent the addition of weighting schemes in which the researcher specifies allowed departures from cospeciation a priori, with the result that TreeMap results more closely agree with BPA results than do reconciled tree analysis results.     

Horizontal gene transfer: sustaining pathogenicity and optimizing host–pathogen interactions

Successful host–pathogen interactions require the presence, maintenance and expression of gene cassettes called 'pathogenicity islands' (PAIs) and 'metabolic islands' (MAIs) in the respective pathogen. The products of these genes confer on the pathogen the means to recognize their host(s) and to efficiently evade host defences in order to colonize, propagate within the host and eventually disseminate from the host. Virulence effectors secreted by type III and type IV secretion systems, among others, play vital roles in sustaining pathogenicity and optimizing host–pathogen interactions. Complete genome sequences of plant pathogenic bacteria have revealed the presence of PAIs and MAIs. The genes of these islands possess mosaic structures with regions displaying differences in nucleotide composition and codon usage in relation to adjacent genome structures, features that are highly suggestive of their acquisition from a foreign donor. These donors can be other bacteria, as well as lower members of the Archaea and Eukarya. Genes that have moved from the domains Archaea and Eukarya to the domain Bacteria are true cases of horizontal gene transfer. They represent interdomain genetic transfer. Genetic exchange between distinct members of the domain Bacteria, however, represents lateral gene transfer, an intradomain event. Both horizontal and lateral gene transfer events have been used to facilitate survival fitness of the pathogen.     

Mathematical and computational approaches can complement experimental studies of host–pathogen interactions

In addition to traditional and novel experimental approaches to study host–pathogen interactions, mathematical and computer modelling have recently been applied to address open questions in this area. These modelling tools not only offer an additional avenue for exploring disease dynamics at multiple biological scales, but also complement and extend knowledge gained via experimental tools. In this review, we outline four examples where modelling has complemented current experimental techniques in a way that can or has already pushed our knowledge of host–pathogen dynamics forward. Two of the modelling approaches presented go hand in hand with articles in this issue exploring fluorescence resonance energy transfer and two-photon intravital microscopy. Two others explore virtual or ' in silico ' deletion and depletion as well as a new method to understand and guide studies in genetic epidemiology. In each of these examples, the complementary nature of modelling and experiment is discussed. We further note that multi-scale modelling may allow us to integrate information across length (molecular, cellular, tissue, organism, population) and time (e.g. seconds to lifetimes). In sum, when combined, these compatible approaches offer new opportunities for understanding host–pathogen interactions.     

A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems

Aim  To integrate ecological fitting, the oscillation hypothesis and the taxon pulse hypothesis into a coherent null model for the evolution of complex host–parasite associations.
Location  Global.
Methods  This paper reviews and synthesizes literature that focuses on phylogenetic analyses and reciprocal mapping of a model system of hosts and their parasites to determine patterns of host–parasite associations and geographical distributions through time.
Results  Host-switching and geographical dispersal of parasites are common phenomena, occurring on many temporal and spatial scales. Diversification involving both co-evolution and colonization explains complex host–parasite associations. Across the expanse of Earth history, the major radiations in host–parasite assemblages have been preceded by ecological disruption, ecological breakdown and host-switching in a context that can be defined by the concept of ecological fitting. This cyclical process sets the stage for co-diversification during periods of relative stability, punctuated by host-switching during episodes of regional to global environmental disruption and climatological change.
Main conclusions  Most observed host–parasite associations can be explained by an historical interaction between ecological fitting, oscillation (episodes of increasing host range alternating with isolation on particular hosts) and taxon pulses (cyclical episodes of expansion and isolation in geographical range). Major episodes of environmental change appear to be the main drivers for both the persistence and diversification of host–parasite systems, creating opportunities for host-switching during periods of geographical expansion and allowing for co-evolution and co-speciation during periods of geographical isolation.     

Not everything is everywhere: the distance decay of similarity in a marine host–parasite system

Aim We test the similarity–distance decay hypothesis on a marine host–parasite system, inferring the relationships from abundance data gathered at the lowest scale of parasite community organization (i.e. that of the individual host). Location Twenty‐two seasonal samples of the bogue Boops boops (Teleostei: Sparidae) were collected at seven localities along a coastal positional gradient from the northern North‐East Atlantic to the northern Mediterranean coast of Spain. Methods We used our own, taxonomically consistent, data on parasite communities. The variations in parasite composition and structure with geographical and regional distance were examined at two spatial scales, namely local parasite faunas and component communities, using both presence–absence (neighbour joining distance) and abundance (Mahalanobis distance) data. The influence of geographical and regional distance on faunal/community divergence was assessed through the permutation of distance matrices. Results Our results revealed that: (1) geographical and regional distances do not affect the species composition in the system under study at the higher scales; (2) geographical distance between localities contributes significantly to the decay of similarity estimated from parasite abundance at the lowest scale (i.e. the individual host); (3) the structured spatial patterns are consistent in time but not across seasons; and (4) a restricted clade of species (the ‘core’ species of the bogue parasite fauna) contributes substantially to the observed patterns of both community homogenization and differentiation owing to the strong relationship between local abundance and regional distribution of species. Main conclusions The main factors that tend to homogenize the composition of parasite communities of bogue at higher regional scales are related to the dispersal of parasite colonizers across host populations, which we denote as horizontal neighbourhood colonization. In contrast, the spatial structure detectable in quantitative comparisons only, is related to a vertical neighbourhood colonization associated with larval dispersal on a local level. The stronger decline with distance in the spatial synchrony of the assemblages of the ‘core’ species indicates a close‐echoing environmental synchrony that declines with distance. Our results emphasize the importance of the parasite supracommunity (i.e. parasites that exploit all hosts in the ecosystem) to the decay of similarity with distance.