Natural variation in host feeding behaviors impacts host disease and pathogen transmission potential

Animals ranging from mosquitoes to humans often vary their feeding behavior when infected or merely exposed to pathogens. These so‐called “sickness behaviors” are part of the innate immune response with many consequences, including avoiding orally transmitted pathogens. Fully understanding the role of this ubiquitous behavior in host defense and pathogen evolution requires a quantitative account of its impact on host and pathogen fitness across environmentally relevant contexts. Here, we use a zooplankton host and fungal pathogen as a case study to ask if infection‐mediated feeding behaviors vary across pathogen exposure levels and natural genetic variation in susceptibility to infection. Then, we connect these changes in behavior to pathogen transmission potential (spore yield) and fitness and growth costs to the host. Our results validate a protective effect of altered feeding behavior during pathogen exposure while also revealing significant variation in the magnitude of this response across host susceptibility and pathogen exposure levels. Across all four host genotypes, feeding rates were negatively correlated with susceptibility to infection and transmission potential. The most susceptible genotypes exhibited either strong anorexia, reducing food intake by 26%–42%, (“Standard”) or pronounced hyperphagia, increasing food intake by 20%–54% (“A45”). Together, these results suggest that infection‐mediated changes in host feeding behavior—which are traditionally interpreted as immunopathology— may in fact serve as crucial components of host defense strategies and warrant further investigation.     

Temporal dynamics and diversity of avian malaria parasites in a single host species

1. We have used molecular methods to unravel a remarkable diversity of parasite lineages in a long-term population study of great reed warblers Acrocephalus arundinaceus that was not foreseen from traditional microscopic examination of blood smears. This diversity includes eight Haemoproteus and 10 Plasmodium lineages of which most probably represent good biological species. 2. Contrary to expectation, the relative frequency of parasite lineages seemed not to change over the 17-year study period and we found no effects of the parasites on a male secondary sexual ornament (song repertoire size) and two measures of fitness (adult survival and production of recruited offspring). 3. We discuss whether the absence of fitness consequences of the parasites might relate to the fact that we have studied the host at the breeding sites in Europe, whereas the transmission seems to take place at the wintering sites in Africa, where the na?ve birds encounter the parasites for the first time and the resulting primary infections likely make them sicker than during the chronic phase of the infection. 4. The prevalence of the three most common lineages appeared to fluctuate in parallel with a periodicity of approximately 3-4 years. Theoretical models based on intrinsic interactions between parasite antigen and host immune genes cannot explain such dynamics, suggesting that knowledge of extrinsic parameters such as vector distribution and alternative hosts are required to understand these patterns.     

Coalescence 2.0: a multiple branching of recent theoretical developments and their applications

Population genetics theory has laid the foundations for genomic analyses including the recent burst in genome scans for selection and statistical inference of past demographic events in many prokaryote, animal and plant species. Identifying SNPs under natural selection and underpinning species adaptation relies on disentangling the respective contribution of random processes (mutation, drift, migration) from that of selection on nucleotide variability. Most theory and statistical tests have been developed using the Kingman coalescent theory based on the Wright‐Fisher population model. However, these theoretical models rely on biological and life history assumptions which may be violated in many prokaryote, fungal, animal or plant species. Recent theoretical developments of the so‐called multiple merger coalescent models are reviewed here (Λ‐coalescent, beta‐coalescent, Bolthausen‐Sznitman, Ξ‐coalescent). We explain how these new models take into account various pervasive ecological and biological characteristics, life history traits or life cycles which were not accounted in previous theories such as (i) the skew in offspring production typical of marine species, (ii) fast adapting microparasites (virus, bacteria and fungi) exhibiting large variation in population sizes during epidemics, (iii) the peculiar life cycles of fungi and bacteria alternating sexual and asexual cycles and (iv) the high rates of extinction‐recolonization in spatially structured populations. We finally discuss the relevance of multiple merger models for the detection of SNPs under selection in these species, for population genomics of very large sample size and advocate to potentially examine the conclusion of previous population genetics studies.     

Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection

Abstract.— Models of host‐parasite coevolution assume the presence of genetic variation for host resistance and parasite infectivity, as well as genotype‐specific interactions. We used the freshwater crustacean Daphnia magna and its bacterial microparasite Pasteuria ramosa to study genetic variation for host susceptibility and parasite infectivity within each of two populations. We sought to answer the following questions: Do host clones differ in their susceptibility to parasite isolates? Do parasite isolates differ in their ability to infect different host clones? Are there host clone‐parasite isolate interactions? The analysis revealed considerable variation in both host resistance and parasite infectivity. There were significant host clone‐parasite isolate interactions, such that there was no single host clone that was superior to all other clones in the resistance to every parasite isolate. Likewise, there was no parasite isolate that was superior to all other isolates in infectivity to every host clone. This form of host clone‐parasite isolate interaction indicates the potential for coevolution based on frequency‐dependent selection. Infection success of original host clone‐parasite isolate combinations (i.e., those combinations that were isolated together) was significantly higher than infection success of novel host clone‐parasite isolate combinations (i.e., those combinations that were created in the laboratory). This finding is consistent with the idea that parasites track specific host genotypes under natural conditions. In addition, correspondence analysis revealed that some host clones, although distinguishable with neutral genetic markers, were susceptible to the same set of parasite isolates and thus probably shared resistance genes.     

Parasite-driven genetic change in a natural population of Daphnia

A substantial body of theory indicates that parasites may mould the population genetic structure of their hosts, but few empirical studies have directly linked parasitism to genetic dynamics. We used molecular markers (allozymes) to investigate genotype frequency changes in a natural population of the crustacean Daphnia magna in relation to an epidemic of the bacterial pathogen Pasteuria ramosa. The population experienced a severe epidemic during the study period in which parasite prevalence reached 100% of the adult portion of the population. The parasite epidemic was associated with genetic change in the host population. Clonal diversity was observed to decrease as parasite prevalence increased in the population, and tests for differences in the clonal composition of the population before, during, and after the epidemic indicated that significant change had occurred. A laboratory infection experiment showed that the genotypes which were more common following the peak of the parasite epidemic were also the most resistant to parasite infection. Thus, this study provides an illustration of parasite-mediated selection in the wild.     

Experimental evolution of field populations of Daphnia magna in response to parasite treatment

Although there is little doubt that hosts evolve to reduce parasite damage, little is known about the evolutionary time scale on which host populations may adapt under natural conditions. Here we study the effects of selection by the microsporidian parasite Octosporea bayeri on populations of Daphnia magna. In a field study, we infected replicated populations of D. magna with the parasite, leaving control populations uninfected. After two summer seasons of experimental evolution (about 15 generations), the genetic composition of infected host populations differed significantly from the control populations. Experiments revealed that hosts from the populations that had evolved with the parasite had lower mortality on exposure to parasite spores and a higher competitive ability than hosts that had evolved without the parasite. In contrast, the susceptibility of the two treatment groups to another parasite, the bacterium Pasteuria ramosa, which was not present during experimental evolution of the populations, did not differ. Fitness assays in the absence of parasites revealed a higher fitness for the control populations, but only under low population density with high resource availability. Overall, our results show that, under natural conditions, Daphnia populations are able to adapt rapidly to the prevailing conditions and that this evolutionary change is specific to the environment.     

Rapid laboratory evolution of adult wing area in Drosophila melanogaster in response to humidity

Abstract We examined the evolutionary response of wing area (a trait highly correlated with other measures of body size) to relative humidity (RH), temperature, and their interaction in Drosophila melanogaster , using replicated lines that had been allowed to evolve at low or high humidity at 18°C or at 25°C. We found that after 20 weeks of selection (5–10 generations), low RH lines had significantly greater wing areas than high RH lines in both sexes. This evolutionary response may have resulted from selection of larger flies with a smaller surface area for water loss relative to their weight, or as a correlated response to selection on some other unidentified trait. There were no evolutionary effects of temperature on wing area or cell density. This may have been due to the short duration of the selection experiment, and/or counteracting selection pressures on body size at warm temperature.     

Spatial heterogeneity and the stability of host-parasite coexistence

Spatially heterogeneous environments can theoretically promote more stable coexistence of hosts and parasites by reducing the risk of parasite attack either through providing permanent spatial refuges or through providing ephemeral refuges by reducing dispersal. In experimental populations of Pseudomonas aeruginosa and the bacteriophage PP7, spatial heterogeneity promoted stable coexistence of host and parasite, while coexistence was significantly less stable in the homogeneous environment. Phage populations were found to be persisting on subpopulations of sensitive bacteria. Transferring populations to fresh microcosms every 24 h prevented the development of permanent spatial refuges. However, the lower dispersal rates in the heterogeneous environment were found to reduce parasite transmission thereby creating ephemeral refuges from phage attack. These results suggest that spatial heterogeneity can stabilize an otherwise unstable host-parasite interaction even in the absence of permanent spatial refuges.     

The evolution and diversification of oakleaf butterflies

1. Download : Download high-res image (192KB)
2. Download : Download full-size image

     

Genetic parallelism of protein polymorphism in nature: ecological test of the neutral theory of molecular evolution

We have conducted an ecological test of protein polymorphism in 13 unrelated genera of plants, invertebrates and vertebrates, involving 21 species, 142 populations and 5474 individuals. Each was tested, on average, for 27 enzymatic gene loci. These species varied in population size and structure, life histories and biogeographical origins, but they largely share a geographically short (260 km) and ecologically stressful gradient of increasing aridity in Israel, both eastward and (mainly) southward. We found genetic parallelism across most taxa, and most loci. Observed average heterozygosity, H , and gene diversity, He , were positively and overall significantly correlated with rainfall variation. This result corroborates the environmental theory of genetic diversity, primarily the niche-width variation hypothesis in both space and time. Our results are inconsistent with the neutral theory of molecular evolution and suggest that natural selection appears to be an important differentiating evolutionary force at the protein level.     

Rapid genome‐wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools

There is increasing evidence that evolution can occur rapidly in response to selection. Recent advances in sequencing suggest the possibility of documenting genetic changes as they occur in populations, thus uncovering the genetic basis of evolution, particularly if samples are available from both before and after selection. Here, we had a unique opportunity to directly assess genetic changes in natural populations following an evolutionary response to a fluctuation in climate. We analysed genome‐wide differences between ancestors and descendants of natural populations of Brassica rapa plants from two locations that rapidly evolved changes in multiple phenotypic traits, including flowering time, following a multiyear late‐season drought in California. These ancestor‐descendant comparisons revealed evolutionary shifts in allele frequencies in many genes. Some genes showing evolutionary shifts have functions related to drought stress and flowering time, consistent with an adaptive response to selection. Loci differentiated between ancestors and descendants (F_ST outliers) were generally different from those showing signatures of selection based on site frequency spectrum analysis (Tajima's D), indicating that the loci that evolved in response to the recent drought and those under historical selection were generally distinct. Very few genes showed similar evolutionary responses between two geographically distinct populations, suggesting independent genetic trajectories of evolution yielding parallel phenotypic changes. The results show that selection can result in rapid genome‐wide evolutionary shifts in allele frequencies in natural populations, and highlight the usefulness of combining resurrection experiments in natural populations with genomics for studying the genetic basis of adaptive evolution.     

The design and function of birds' nests

All birds construct nests in which to lay eggs and/or raise offspring. Traditionally, it was thought that natural selection and the requirement to minimize the risk of predation determined the design of completed nests. However, it is becoming increasingly apparent that sexual selection also influences nest design. This is an important development as while species such as bowerbirds build structures that are extended phenotypic signals whose sole purpose is to attract a mate, nests contain eggs and/or offspring, thereby suggesting a direct trade‐off between the conflicting requirements of natural and sexual selection. Nest design also varies adaptively in order to both minimize the detrimental effects of parasites and to create a suitable microclimate for parents and developing offspring in relation to predictable variation in environmental conditions. Our understanding of the design and function of birds' nests has increased considerably in recent years, and the evidence suggests that nests have four nonmutually exclusive functions. Consequently, we conclude that the design of birds' nests is far more sophisticated than previously realized and that nests are multifunctional structures that have important fitness consequences for the builder/s.     

Rapid contemporary evolution and clonal food web dynamics

Character evolution that affects ecological community interactions often occurs contemporaneously with temporal changes in population size, potentially altering the very nature of those dynamics. Such eco-evolutionary processes may be most readily explored in systems with short generations and simple genetics. Asexual and cyclically parthenogenetic organisms such as microalgae, cladocerans and rotifers, which frequently dominate freshwater plankton communities, meet these requirements. Multiple clonal lines can coexist within each species over extended periods, until either fixation occurs or a sexual phase reshuffles the genetic material. When clones differ in traits affecting interspecific interactions, within-species clonal dynamics can have major effects on the population dynamics. We first consider a simple predator–prey system with two prey genotypes, parametrized with data from a well-studied experimental system, and explore how the extent of differences in defence against predation within the prey population determine dynamic stability versus instability of the system. We then explore how increased potential for evolution affects the community dynamics in a more general community model with multiple predator and multiple prey genotypes. These examples illustrate how microevolutionary ‘details’ that enhance or limit the potential for heritable phenotypic change can have significant effects on contemporaneous community-level dynamics and the persistence and coexistence of species.     

Using experimental evolution to explore natural patterns between bacterial motility and resistance to bacteriophages

Resistance of bacteria to phages may be gained by alteration of surface proteins to which phages bind, a mechanism that is likely to be costly as these molecules typically have critical functions such as movement or nutrient uptake. To address this potential trade-off, we combine a systematic study of natural bacteria and phage populations with an experimental evolution approach. We compare motility, growth rate and susceptibility to local phages for 80 bacteria isolated from horse chestnut leaves and, contrary to expectation, find no negative association between resistance to phages and bacterial motility or growth rate. However, because correlational patterns (and their absence) are open to numerous interpretations, we test for any causal association between resistance to phages and bacterial motility using experimental evolution of a subset of bacteria in both the presence and absence of naturally associated phages. Again, we find no clear link between the acquisition of resistance and bacterial motility, suggesting that for these natural bacterial populations, phage-mediated selection is unlikely to shape bacterial motility, a key fitness trait for many bacteria in the phyllosphere. The agreement between the observed natural pattern and the experimental evolution results presented here demonstrates the power of this combined approach for testing evolutionary trade-offs.     

Modularity and the units of evolution

Summary While many developmental processes (e. g., gene networks or signaling pathways) are astonishingly conserved during evolution, they may be employed differently in different metazoan taxa or may be used multiply in different contexts of development. This suggests that these processes belong to building blocks or modules, viz., highly integrated parts of the organism, which develop and/or function relatively independent from other parts. Such modules may be relatively easy to dissociate from other modules and, therefore, could also serve as units of evolution. However, in order to further explore the implications of modularity for evolution, the vague notion of “modularity” as well as its relation to concepts like “unit of evolution” need to be more precisely specified. Here, a module is characterized as a certain type of dynamic pattern of couplings among the constituents of a process. It may or may not form a spatially contiguous unit. A unit of selection is defined as a unit of those constituents of a reproducing process/system, which exists in different variants and acts as a non-decomposable unit of fitness and variant reproduction during a particular selection process. The more general notion of a unit of evolution is characterized as a nondecomposable unit of constituents with reciprocal fitness dependence, be it due to fitness epistasis or due to the lack of independent variability. Because such fitness dependence may only be observed for some combinations of variants, several constituents may act as a unit of evolution only with a certain probability (coevolution probability). It is argued, that under certain conditions modules are likely to act as units of evolution with high coevolution probabilities, because there is likely to be a close tie between the pattern of couplings of the constituents of a reproducing system and their interdependent fitness contributions. Moreover and contrary to the traditional dichotomy of genes versus organisms as units of selection, modules tend to be more important in delimiting actual units of selection than either organisms or genes, because they are less easily disrupted by recombination than organisms, while having less contextsensitive fitness values than genes. Finally, it is suggested that the evolution of modularity is self-reinforcing, because the flexibility of intermodular connections facilitates the recombination among modules and their multiple employment in new contexts.     

Parasite-mediated selection and the role of sex and diapause in Daphnia

To gain insight into parasite-mediated natural selection, we studied a natural population of the crustacean Daphnia magna during a severe epidemic of the bacterial parasite Pasteuria ramosa. We also investigated the relationship between susceptibility and the production of resting eggs, which are only produced during the sexual phase of reproduction. Live host samples were taken before and after this epidemic and resistance to P. ramosa was examined in the laboratory. Host clones collected after the epidemic were more resistant to P. ramosa than were those collected pre-epidemic, which is consistent with parasite-mediated selection. In our study population, asexually reproducing females were observed across the entire study period, but females carrying resting eggs were observed only prior to the epidemic. For hosts isolated in this pre-epidemic period, we found evidence that those carrying resting eggs (at the time of collection) were more susceptible than those that were reproducing asexually. This was especially apparent for measures of parasite growth, although not all measures of infection success conclusively supported this pattern. Nevertheless, the data suggest that some genotypes invest heavily in diapause at the expense of immunocompetence. Sex could therefore inhibit the evolution of resistance because each spring new genotypes will hatch from resting eggs that are relatively susceptible as they were not exposed to the previous years bout of parasite-mediated selection.     

Rapid courtship evolution in grouse (Tetraonidae): contrasting patterns of acceleration between the Eurasian and North American polygynous clades

Sexual selection is thought to be a powerful diversifying force, based on large ornamental differences between sexually dimorphic species. This assumes that unornamented phenotypes represent evolution without sexual selection. If sexual selection is more powerful than other forms of selection, then two effects would be: rapid divergence of sexually selected traits and a correlation between these divergence rates and variance in mating success in the ornamented sex. I tested for these effects in grouse (Tetraonidae). For three species pairs, within and among polygynous clades, male courtship characters had significantly greater divergence than other characters. This was most pronounced for two species in Tympanuchus. In the Eurasian polygynous clade, relative courtship divergence gradually increased with nucleotide divergence, suggesting a less dramatic acceleration. Increase in relative courtship divergence was associated with mating systems having higher variance in male mating success. These results suggest that sexual selection has accelerated courtship evolution among grouse, although the microevolutionary details appear to vary among clades.     

Parasite diversity drives rapid host dynamics and evolution of resistance in a bacteria‐phage system

Host–parasite evolutionary interactions are typically considered in a pairwise species framework. However, natural infections frequently involve multiple parasites. Altering parasite diversity alters ecological and evolutionary dynamics as parasites compete and hosts resist multiple infection. We investigated the effects of parasite diversity on host–parasite population dynamics and evolution using the pathogen Pseudomonas aeruginosa and five lytic bacteriophage parasites. To manipulate parasite diversity, bacterial populations were exposed for 24 hours to either phage monocultures or diverse communities containing up to five phages. Phage communities suppressed host populations more rapidly but also showed reduced phage density, likely due to interphage competition. The evolution of resistance allowed rapid bacterial recovery that was greater in magnitude with increases in phage diversity. We observed no difference in the extent of resistance with increased parasite diversity, but there was a profound impact on the specificity of resistance; specialized resistance evolved to monocultures through mutations in a diverse set of genes. In summary, we demonstrate that parasite diversity has rapid effects on host–parasite population dynamics and evolution by selecting for different resistance mutations and affecting the magnitude of bacterial suppression and recovery. Finally, we discuss the implications of phage diversity for their use as biological control agents.     

A two level mutation-selection model of cultural evolution and diversity

Cultural evolution is a complex process that can happen at several levels. At the level of individuals in a population, each human bears a set of cultural traits that he or she can transmit to its offspring (vertical transmission) or to other members of his or her society (horizontal transmission). The relative frequency of a cultural trait in a population or society can thus increase or decrease with the relative reproductive success of its bearers (individual’s level) or the relative success of transmission (called the idea’s level). This article presents a mathematical model on the interplay between these two levels. The first aim of this article is to explore when cultural evolution is driven by the idea’s level, when it is driven by the individual’s level and when it is driven by both. These three possibilities are explored in relation to (a) the amount of interchange of cultural traits between individuals, (b) the selective pressure acting on individuals, (c) the rate of production of new cultural traits, (d) the individual’s capacity to remember cultural traits and to the population size. The aim is to explore the conditions in which cultural evolution does not lead to a better adaptation of individuals to the environment. This is to contrast the spread of fitness-enhancing ideas, which make individual bearers better adapted to the environment, to the spread of “selfish” ideas, which spread well simply because they are easy to remember but do not help their individual bearers (and may even hurt them). At the same time this article explores in which conditions the adaptation of individuals is maximal. The second aim is to explore how these factors affect cultural diversity, or the amount of different cultural traits in a population. This study suggests that a larger interchange of cultural traits between populations could lead to cultural evolution not improving the adaptation of individuals to their environment and to a decrease of cultural diversity.