The spatial distribution of plant populations, disease dynamics and evolution of resistance

Empirical studies of the interaction between the anther smut fungus Microbotryum violaceum and its host plant Lychnis alpina were combined with modelling approaches to investigate how variation in the spatial distribution of host populations influences disease dynamics and variation in resistance. Patterns of disease incidence and prevalence were surveyed in three contrasting systems of natural L . alpina populations where there is substantial variation in spatial structure, ranging from large continuous populations through to small isolated patches. Disease incidence (fraction of populations where disease was present) was highest in the continuous situation, and lowest in the most isolated populations. The reverse was true for prevalence (fraction of individuals diseased). To better understand the long-term ecological and evolutionary consequences of differences in among population spatial structure, we developed a two-dimensional spatially explicit simulation model in which host-population spacing was modelled by varying the percentage of sites suitable for the host. The general patterns of disease incidence and prevalence generated in the simulations corresponded well with the patterns observed in natural populations of L. alpina and M. violaceum ; i.e. the fraction of sites with disease increased while the average disease prevalence in diseased populations decreased when host populations became more connected. One likely explanation for the differences in disease incidence and prevalence seen in natural populations is that the evolution of host resistance varies as a function of the degree of fragmentation. This is supported by simulation results that were qualitatively similar to the survey data when resistance was allowed to vary, but not when hosts were assumed to be uniformly susceptible. In the former, the frequency of resistance increased markedly as host populations became more connected.     

Pathogens as potential selective agents in the wild

Pathogens are considered a serious threat to which wild populations must adapt, most particularly under conditions of rapid environmental change. One way host adaptation has been studied is through genetic population structure at the major histocompatibility complex (MHC), a complex of adaptive genes involved in pathogen resistance in vertebrates. However, while associations between specific pathogens and MHC alleles or diversity have been documented from laboratory studies, the interaction between hosts and pathogens in the wild is more complex. As such, identifying selective agents and understanding underlying co-evolutionary mechanisms remains a major challenge. In this issue of Molecular Ecology , Evans & Neff (2009) characterized spatial and temporal variation in the bacterial parasite community infecting Chinook salmon ( Oncorhynchus tshawytscha ) fry from five populations in British Columbia, Canada. They used a 16S rDNA sequencing-based approach to examine the prevalence of bacterial infection in kidney and looked for associations with MHC class I and II genetic variability. The authors found a high diversity of bacteria infecting fry, albeit at low prevalence. It was reasoned that spatial variability in infection rate and bacterial community phylogenetic similarity found across populations may represent differential pathogen-mediated selection pressures. The study revealed some evidence of heterozygote advantage at MHC class II, but not class I, and preliminary associations between specific MHC alleles and bacterial infections were uncovered. This research adds an interesting perspective to the debate on host–pathogen co-evolutionary mechanisms and emphasizes the importance of considering the complexity of pathogen communities in studies of host local adaptation.     

中国板栗居群间等位酶基因频率的空间分布

中国板栗21个自然群间等位酶遗传变异的空间自相关分析及F－统计分析结果表明：其多数等位基因频率在居群间呈随机分布模式,缺乏一定的空间结构;而部分等位基因表现为渐变或双向渐变的非随机分布模式,又具有特定空间结构。中国板栗遗传变异空间结构模式的形成可能是长距离基因流、自然气候、人类活动、地理距离隔离等诸因素综合作用的结果。文中还就居群等位基因分布格局的成因进行了讨论：在第四纪冰川后,中国板栗以长江流域中下游的孑遗中心为起点,等位基因分别沿着向北和向南的不同方向迁移形成现在的居群结构;季风气候和人类活动干扰是削弱居群分化的主要因素,而基于环境梯度的选择,是形成由北向南渐变分布的原因。     

Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia

Drosophila melanogaster invaded Australia around 100 years ago, most likely through a northern invasion. The wide range of climatic conditions in eastern Australia across which D. melanogaster is now found provides an opportunity for researchers to identify traits and genes that are associated with climatic adaptation. Allozyme studies indicate clinal patterns for at least four loci including a strong linear cline in Adh and a non-linear cline in alpha-Gpdh. Inversion clines were initially established from cytological studies but have now been validated with larger sample sizes using molecular markers for breakpoints. Recent collections indicate that some genetic markers (Adh and In(3R)Payne) have changed over the last 20 years reflecting continuing evolution. Heritable clines have been established for quantitative traits including wing length/area, thorax length and cold and heat resistance. A cline in egg size independent of body size and a weak cline in competitive ability have also been established. Postulated clinal patterns for resistance to desiccation and starvation have not been supported by extensive sampling. Experiments under laboratory and semi-natural conditions have suggested selective factors generating clinal patterns, particularly for reproductive patterns over winter. Attempts are being made to link clinal variation in traits to specific genes using QTL analysis and the candidate locus approach, and to identify the genetic architecture of trait variation along the cline. This is proving difficult because of inversion polymorphisms that generate disequilibrium among genes. Substantial gaps still remain in linking clines to field selection and understanding the genetic and physiological basis of the adaptive shifts. However D. melanogaster populations in eastern Australia remain an excellent resource for understanding past and future evolutionary responses to climate change.     

Pleiotropic Effects of Immune Responses Explain Variation in the Prevalence of Fibroproliferative Diseases

Many diseases are differentially distributed among human populations. Differential selection on genetic variants in ancestral environments that coincidentally predispose to disease can be an underlying cause of these unequal prevalence patterns. Selected genes may be pleiotropic, affecting multiple phenotypes and resulting in more than one disease or trait. Patterns of pleiotropy may be helpful in understanding the underlying causes of an array of conditions in a population. For example, several fibroproliferative diseases are more prevalent and severe in populations of sub-Saharan ancestry. We propose that this disparity is due to selection for an enhanced Th2 response that confers resistance to helminthic infections, and concurrently increases susceptibility to fibrosis due to the profibrotic action of Th2 cytokines. Many studies on selection of Th2-related genes for host resistance to helminths have been reported, but the pleiotropic impact of this selection on the distribution of fibrotic disorders has not been explicitly investigated. We discuss the disproportionate occurrence of fibroproliferative diseases in individuals of African ancestry and provide evidence that adaptation of the immune system has shaped the genetic structure of these human populations in ways that alter the distribution of multiple fibroproliferative diseases.     

The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication

Wild and cultivated plants represent very different habitats for pathogens, especially when cultivated plants bear qualitative resistance genes. Here, we investigated to what extent the population genetic structure of a plant pathogenic fungus collected on its wild host can be impacted by the deployment of resistant cultivars. We studied one of the main poplar diseases, poplar rust, caused by the fungus Melampsora larici‐populina. A thousand and fifty individuals sampled from several locations in France were phenotyped for their virulence profile (ability to infect or not the most deployed resistant cultivar ‘Beaupré’), and a subset of these was genotyped using 25 microsatellite markers. Bayesian assignment tests on genetic data clustered the 476 genotyped individuals into three genetic groups. Group 1 gathered most virulent individuals and displayed evidence for selection and drastic demographic changes resulting from breakdown of the poplar cultivar ‘Beaupré’. Group 2 comprised individuals corresponding to ancestral populations of M. larici‐populina naturally occurring in the native range. Group 3 displayed the hallmarks of strict asexual reproduction, which has never previously been demonstrated in this species. We discuss how poplar cultivation has influenced the spatial and genetic structure of this plant pathogenic fungus, and has led to the spread of virulence alleles (gene swamping) in M. larici‐populina populations evolving on the wild host.     

The cause of parasitic infection in natural populations of Daphnia (Crustacea: Cladocera): the role of host genetics.

Disease patterns in nature may be determined by genetic variation for resistance or by factors, genetic or environmental, which influence the host-parasite encounter rate. Elucidating the cause of natural infection patterns has been a major pursuit of parasitologists, but it also matters for evolutionary biologists because host resistance genes must influence the expression of disease if parasite-mediated selection is to occur. We used a model system in order to disentangle the strict genetic component from other causes of infection in the wild. Using the crustacean Daphnia magna and its sterilizing bacterial parasite Pasteuria ramosa, we tested whether genetic variation for resistance, as determined under controlled conditions, accounted for the distribution of infections within natural populations. Specifically, we compared whether the clonally produced great-granddaughters of those individuals that were infected in field samples (but were subsequently 'cured' with antibiotics) were more susceptible than were the great-granddaughters of those individuals that were healthy in field samples. High doses of parasite spores led to increased infection in all four study populations, indicating the importance of encounter rate. Host genetics appeared to be irrelevant to natural infection patterns in one population. However, in three other populations hosts that were healthy in the field had greater genetic-based resistance than hosts that were infected in the field, unambiguously showing the effect of host genetic factors on the expression of disease in the wild.     

Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales

Natural plant populations are often found to be extremely diverse in their resistance to pathogens. While the potential of pathogens in driving the evolution of resistance in hosts has been widely recognized, empirical evidence linking disease dynamics to host population genetic structure has remained scarce. Here I show that current coevolutionary selection for resistance can be divergent even on a very fine spatial scale. In a natural plant-pathogen metapopulation, disease occurrence patterns were highly aggregated over space and time within host populations. A laboratory inoculation experiment showed higher resistance within areas of the host populations where encounter rates with the pathogen have been high. Higher resistance to sympatric than to allopatric strains of the pathogen suggests that this change has taken place as a response to local selection. These results constitute evidence of adaptive microevolution of resistance resulting from disease epidemics in natural plant-pathogen associations, and highlight the importance of finding the relevant scale at which to address questions of current coevolutionary selection.     

Contrasting epidemic histories reveal pathogen-mediated balancing selection on class II MHC diversity in a wild songbird

The extent to which pathogens maintain the extraordinary polymorphism at vertebrate Major Histocompatibility Complex (MHC) genes via balancing selection has intrigued evolutionary biologists for over half a century, but direct tests remain challenging. Here we examine whether a well-characterized epidemic of Mycoplasmal conjunctivitis resulted in balancing selection on class II MHC in a wild songbird host, the house finch (Carpodacus mexicanus). First, we confirmed the potential for pathogen-mediated balancing selection by experimentally demonstrating that house finches with intermediate to high multi-locus MHC diversity are more resistant to challenge with Mycoplasma gallisepticum. Second, we documented sequence and diversity-based signatures of pathogen-mediated balancing selection at class II MHC in exposed host populations that were absent in unexposed, control populations across an equivalent time period. Multi-locus MHC diversity significantly increased in exposed host populations following the epidemic despite initial compromised diversity levels from a recent introduction bottleneck in the exposed host range. We did not observe equivalent changes in allelic diversity or heterozygosity across eight neutral microsatellite loci, suggesting that the observations reflect selection rather than neutral demographic processes. Our results indicate that a virulent pathogen can exert sufficient balancing selection on class II MHC to rescue compromised levels of genetic variation for host resistance in a recently bottlenecked population. These results provide evidence for Haldane's long-standing hypothesis that pathogens directly contribute to the maintenance of the tremendous levels of genetic variation detected in natural populations of vertebrates.     

Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation

Antagonistic coevolution is a critical force driving the evolution of diversity, yet the selective processes underpinning reciprocal adaptive changes in nature are not well understood. Local adaptation studies demonstrate partner impacts on fitness and adaptive change, but do not directly expose genetic processes predicted by theory. Specifically, we have little knowledge of the relative importance of fluctuating selection vs. arms-race dynamics in maintaining polymorphism in natural systems where metapopulation processes predominate. We conducted cross-year epidemiological, infection and genetic studies of multiple wild host and pathogen populations in the Linum-Melampsora association. We observed asynchronous phenotypic fluctuations in resistance and infectivity among demes. Importantly, changes in allelic frequencies at pathogen infectivity loci, and in host recognition of these genetic variants, correlated with disease prevalence during natural epidemics. These data strongly support reciprocal coevolution maintaining balanced resistance and infectivity polymorphisms, and highlight the importance of characterising spatial and temporal dynamics in antagonistic interactions.     

Genetic and phenotypic variation in a colourful treefrog across five geographic barriers

Aim Understanding the patterns and processes underlying phenotype in a polytypic species provides key insights into microevolutionary mechanisms of diversification. The red‐eyed treefrog, Agalychnis callidryas, exhibits strong regional differentiation in colour pattern, corresponding to five admixed mitochondrial DNA clades. We evaluated spatial diversity patterns across multiple, putative barriers to examine the fine‐scale processes that mediate phenotypic divergence between some regions while maintaining homogeneity between others. Location We examined patterns of phenotypic diversification among 17 sites that span five putative biogeographic barriers in lower Central America (Costa Rica and Panama). Methods We tested the extent to which genetic distance (F_ST) derived from six multilocus nuclear genotypes covaried with measures of phenotypic distance (leg coloration) within and between biogeographic regions. We used linear regression analyses to determine the role of geographic and genetic factors in structuring spatial patterns of phenotypic diversity. Results The factors that best explained patterns of phenotypic diversity varied among biogeographic regions. We identified one geographic barrier that impeded gene exchange and resulted in concordant phenotypic divergence across the Continental Divide, isolating Caribbean and Pacific populations. Across Caribbean Costa Rican populations, one barrier structured phenotypic but not genetic diversity patterns, indicating a role for selection. In other regions, the putative barriers had no determining effect on either genetic or leg colour structure. Main conclusions The processes mediating the distribution and diversification of colour pattern in this polytypic, wide‐ranging treefrog varied among biogeographic regions. Spatially varying selection combined with the isolating effects of geographic factors probably resulted in the patchy distribution of colour diversity across Costa Rican and Panamanian populations.     

Cytoplasmic and nuclear markers reveal contrasting patterns of spatial genetic structure in a natural Ipomopsis hybrid zone

Spatial variation in natural selection may play an important role in determining the genetic structure of hybridizing populations. Previous studies have found that F1 hybrids between naturally hybridizing Ipomopsis aggregata and Ipomopsis tenuituba in central Colorado differ in fitness depending on both genotype and environment: hybrids had higher survival when I. aggregata was the maternal parent, except in the centre of the hybrid zone where both hybrid types had high survival. Here, we developed both maternally (cpDNA PCR-RFLP) and biparentally inherited (nuclear AFLP) species-diagnostic markers to characterize the spatial genetic structure of the natural Ipomopsis hybrid zone, and tested the prediction that the majority of natural hybrids have I. aggregata cytoplasm, except in areas near the centre of the hybrid zone. Analyses of 352 individuals from across the hybrid zone indicate that cytoplasmic gene flow is bidirectional, but contrary to expectation, most plants in the hybrid zone have I. tenuituba cytoplasm. This cytotype distribution is consistent with a hybrid zone in historical transition, with I. aggregata nuclear genes advancing into the contact zone. Further, nuclear data show a much more gradual cline than cpDNA markers that is consistent with morphological patterns across the hybrid populations. A mixture of environment- and pollinator-mediated selection may contribute to the current genetic structure of this hybrid system.     

INFECTIOUS DISEASES OF MAZZAELLA LAMINARIOIDES (RHODOPHYTA): CHANGES IN INFECTION PREVALENCE AND DISEASE EXPRESSION ASSOCIATED WITH SEASON,LOCALITY, AND WITHIN-SITE LOCATION1

This study addresses the issues of infection prevalence and disease expression in two wild populations of the red algal host Mazzaella laminarioides and their variability associated with locality, season, and spatial location of the host in the intertidal zone. Our results demonstrated that Endophyton ramosum is the most frequent infective pathogen affecting M. laminarioides in Matanzas and Pucatrihue. This situation prevailed through the year and across the high-to-low intertidal gradient. Although there was a general trend for lower levels of infection in late winter and early spring, only in a few, cases was well-defined seasonality detected. Furthermore, clear seasonal patterns, as displayed by deformative disease in the high intertidal zone of Pucatrihue, were attenuated in the middle and lower intertidal zones. Differences in levels of infection in M. laminarioides between the high intertidal zones of Matanzas and Pucatrihue diminished toward the low intertidal zone. Thus, effects of seasonality and locality on infection prevalence may be influenced, at least in part, by the position of the hosts an the intertidal zone. Spatial distribution of the diseased individuals also varied along the beach. This pattern was consistent between the two sites and seemed related to wave exposure and the specific pathogen. Comparisons of the size distribution of noninfected fronds with their infected counterparts showed that infections by Endophyton ramosum and Pleurocapsa sp. more frequently affected medium-and large-sized fronds. This pattern was consistent temporally and similar in the two localities. Finally, a clear association between maturity and prevalence of infection was detected. This association resulted in most fronds of the noninfected segment of the host population being immature, whereas most mature fronds were infected. In conclusion, infectious diseases affecting the red alga Mazzaella laminarioides are a persistent phenomenon in wild populations of the host, although only a small segment of the infected populations displays the full expression of the disease. In spite of the suggested role of factors such as season, latitude, and spatial location of the host on disease prevalence and expression, additional studies are needed to understand fully the dynamics of infectious diseases in wild populations of algal hosts.     

Variation in resistance and virulence in the interaction between Arabidopsis thaliana and a bacterial pathogen

We examined patterns of variation and the extent of local adaptation in the interaction between the highly selfing annual weed Arabidopsis thaliana and its foliar bacterial pathogen Pseudomonas viridiflava by cross-infecting 23 bacterial isolates with 35 plant lines collected from six fallow or cultivated fields in the Midwest, USA. We used two measures of resistance and virulence: bacterial count in the leaf and symptom development four days after infection. We found variation in resistance in A. thaliana and virulence in P. viridiflava, as well as a significant difference in symptoms between two distinct genetic clades within P. viridiflava. We also observed that both resistance and plant development rate varied with field type of origin (cultivated or fallow), possibly through age-related resistance, a developmentally regulated general form of resistance. Finally, we did not observe local adaptation by host or pathogen, rather we found patterns of variation across populations that depended in part on P. viridiflava clade. These data suggest that the interaction between A. thaliana and P. viridiflava varies across space and is mediated by the selection regime of the host populations and differential performance of the P. viridiflava clades. This is one of a very limited number of studies examining a bacterial pathogen of wild plant populations and one of a few studies to examine patterns of variation in a plant-pathogen association that is not a highly specialized gene-for-gene interaction.     

Genomic and resistance gene homolog diversity of the dominant tallgrass prairie species across the U.S. Great Plains precipitation gradient

Background

Environmental variables such as moisture availability are often important in determining species prevalence and intraspecific diversity. The population genetic structure of dominant plant species in response to a cline of these variables has rarely been addressed. We evaluated the spatial genetic structure and diversity of Andropogon gerardii populations across the U.S. Great Plains precipitation gradient, ranging from approximately 48 cm/year to 105 cm/year.

Methodology/Principal Findings

Genomic diversity was evaluated with AFLP markers and diversity of a disease resistance gene homolog was evaluated by PCR-amplification and digestion with restriction enzymes. We determined the degree of spatial genetic structure using Mantel tests. Genomic and resistance gene homolog diversity were evaluated across prairies using Shannon''s index and by averaging haplotype dissimilarity. Trends in diversity across prairies were determined using linear regression of diversity on average precipitation for each prairie. We identified significant spatial genetic structure, with genomic similarity decreasing as a function of distance between samples. However, our data indicated that genome-wide diversity did not vary consistently across the precipitation gradient. In contrast, we found that disease resistance gene homolog diversity was positively correlated with precipitation.

Significance

Prairie remnants differ in the genetic resources they maintain. Selection and evolution in this disease resistance homolog is environmentally dependent. Overall, we found that, though this environmental gradient may not predict genomic diversity, individual traits such as disease resistance genes may vary significantly.     

HOST-PATHOGEN INTERACTIONS IN NATURAL POPULATIONS OF LINUM MARGINALE AND MELAMPSORA LINI: II. LOCAL AND REGIONAL VARIATION IN PATTERNS OF RESISTANCE AND RACIAL STRUCTURE

Spatial variation in the resistance structure of Linum marginale (wild flax) populations to the rust fungus Melampsora lini, and in the racial structure of this pathogen, was investigated by sampling 10 populations distributed throughout the Kosciusko National Park, New South Wales, Australia. Considerable differences were found among populations in the structure of both host and pathogen. Host populations were divided into three broad categories: (1) populations susceptible to all testing races; (2) populations containing a strictly limited number of resistant phenotypes; and (3) populations with a considerable diversity of resistant phenotypes. The pathogen populations also showed a range of diversity. The major differences between these populations were determined by the occurrence and frequency of four common races of pathogen (races A, E, K, and N). These differences were apparent both at a regional spatial scale (over the 100 km separation of the most distant populations) and at a local scale where major differences were detected between two populations only 300 m apart. The distribution of the four common races of M. lini was consistent with the hypothesis that a fitness cost was associated with unnecessary virulence. In general, however, differences in the structure of pathogen populations from genetically very similar host populations implied that, in addition to host resistance genes, other evolutionary forces are also important in determining the genetic structure of individual pathogen populations.     

Genome‐wide analysis of allele frequency change in sunflower crop–wild hybrid populations evolving under natural conditions

Crop‐wild hybridization occurs in numerous plant species and could alter the genetic structure and evolutionary dynamics of wild populations. Studying crop‐derived alleles in wild populations is also relevant to assessing/mitigating the risks associated with transgene escape. To date, crop‐wild hybridization has generally been examined via short‐term studies, typically within a single generation, focusing on few traits or genetic markers. Little is known about patterns of selection on crop‐derived alleles over multiple generations, particularly at a genome‐wide scale. Here, we documented patterns of natural selection in an experimental crop × wild sunflower population that was allowed to evolve under natural conditions for two generations at two locations. Allele frequencies at a genome‐wide collection of SNPs were tracked across generations, and a common garden experiment was conducted to compare trait means between generations. These data allowed us to identify instances of selection on crop‐derived alleles/traits and, in concert with QTL mapping results, test for congruence between our genotypic and phenotypic results. We found that natural selection overwhelmingly favours wild alleles and phenotypes. However, crop alleles in certain genomic regions can be favoured, and these changes often occurred in parallel across locations. We did not, however, consistently observe close agreement between our genotypic and phenotypic results. For example, when a trait evolved towards the wild phenotype, wild QTL alleles associated with that trait did not consistently increase in frequency. We discuss these results in the context of crop allele introgression into wild populations and implications for the management of GM crops.     

Abundance-variance and abundance-occupancy relationships in a marine host-parasite system: the importance of taxonomy and ecology of transmission

Abundance-occupancy and abundance-variance relationships are two of the most general macroecological patterns capturing essential fundamentals of the structuring of species distributions and are widely documented for free-living animal and plant species populations at different spatial scales. However, empirical data for parasites have been gathered using appropriate sampling designs only recently. We performed analyses across species of the variation in infection parameters and patterns of aggregation of the most widespread parasites in the marine sparid fish Boops boops across seven localities of two marine biogeographical regions, the North East Atlantic and the Mediterranean. We used a large dataset of multiple population samples replicated over time for 20 parasite species and carried out assessments both intraspecifically and interspecifically, across taxonomic and ecological groupings. This taxonomically diverse complex of species representing five major metazoan higher taxa with differing transmission ecologies allowed us to assess the effect of taxonomic and ecological determinants on the abundance-occupancy and abundance-variance relationships in the model marine host-parasite system. The results revealed that: (i) a power function, relating spatial variance to mean abundance, represents a suitable model for the spatial distribution of the species; (ii) prevalence, abundance and the degree of spatial heterogeneity are true species characteristics and differ consistently between higher level taxonomic groupings; (iii) infection parameters and abundance-variance relationship are dependent on host specificity and regional distribution patterns of the parasites; and (iv) the observed infection parameters agree well with predictions from the epidemiological negative binomial abundance-occupancy model built on parameters of Taylor's power law both within and across species.     

Natural selection in the water: freshwater invasion and adaptation by water colour in the Amazonian pufferfish

Natural selection and ecological adaptation are ultimately responsible for much of the origin of biodiversity. Yet, the identification of divergent natural selection has been hindered by the spatial complexity of natural systems, the difficulty in identifying genes under selection and their relationship to environment, and the confounding genomic effects of time. Here, we employed genome scans, population genetics and sequence-based phylogeographic methods to identify divergent natural selection on population boundaries in a freshwater invader, the Amazonian pufferfish, Colomesus asellus. We sampled extensively across markedly different hydrochemical settings in the Amazon Basin and use 'water colour' to test for ecological isolation. We distinguish the relative contribution of natural selection across hydrochemical gradients from biogeographic history in the origin and maintenance of population boundaries within a single species and across a complex ecosystem. We show that spatially distinct population structure generated by multiple forces (i.e. water colour and vicariant biogeographic history) can be identified if the confounding effects of genetic drift have not accumulated between selective populations. Our findings have repercussions for studies aimed at identifying engines of biodiversity and assessing their temporal progression in understudied and ecologically complex tropical ecosystems.     

The genetic architecture of disease resistance in plants and the maintenance of recombination by parasites

Parasites represent strong selection on host populations because they are ubiquitous and can drastically reduce host fitness. It has been hypothesized that parasite selection could explain the widespread occurrence of recombination because it is a coevolving force that favours new genetic combinations in the host. A review of deterministic models for the maintenance of recombination reveals that for recombination to be favoured, multiple genes that interact with each other must be under selection. To evaluate whether parasite selection can explain the maintenance of recombination, we review 85 studies that investigated the genetic architecture of plant disease resistance and discuss whether they conform to the requirements that emerge from theoretical models. General characteristics of disease resistance in plants and problems in evaluating resistance experimentally are also discussed. We found strong evidence that disease resistance in plants is determined by multiple loci. Furthermore, in most cases where loci were tested for interactions, epistasis between loci that affect resistance was found. However, we found weak support for the idea that specific allelic combinations determine resistance to different host genotypes and there was little data on whether epistasis between resistance genes is negative or positive. Thus, the current data indicate that it is possible that parasite selection can favour recombination, but more studies in natural populations that specifically address the nature of the interactions between resistance genes are necessary. The data summarized here suggest that disease resistance is a complex trait and that environmental effects and fitness trade-offs should be considered in future models of the coevolutionary dynamics of host and parasites.