Evolution of acuteness in pathogen metapopulations: conflicts between “classical” and invasion-persistence trade-offs

Classical life-history theory predicts that acute, immunizing pathogens should maximize between-host transmission. When such pathogens induce violent epidemic outbreaks, however, a pathogen’s short-term advantage at invasion may come at the expense of its ability to persist in the population over the long term. Here, we seek to understand how the classical and invasion-persistence trade-offs interact to shape pathogen life-history evolution as a function of the size and structure of the host population. We develop an individual-based infection model at three distinct levels of organization: within an individual host, among hosts within a local population, and among local populations within a metapopulation. We find a continuum of evolutionarily stable pathogen strategies. At one end of the spectrum—in large well-mixed populations—pathogens evolve to greater acuteness to maximize between-host transmission: the classical trade-off theory applies in this regime. At the other end of the spectrum—when the host population is broken into many small patches—selection favors less acute pathogens, which persist longer within a patch and thereby achieve enhanced between-patch transmission: the invasion-persistence trade-off dominates in this regime. Between these extremes, we explore the effects of the size and structure of the host population in determining pathogen strategy. In general, pathogen strategies respond to evolutionary pressures arising at both scales.     

A Multi-scale Analysis of Influenza A Virus Fitness Trade-offs due to Temperature-dependent Virus Persistence

Successful replication within an infected host and successful transmission between hosts are key to the continued spread of most pathogens. Competing selection pressures exerted at these different scales can lead to evolutionary trade-offs between the determinants of fitness within and between hosts. Here, we examine such a trade-off in the context of influenza A viruses and the differential pressures exerted by temperature-dependent virus persistence. For a panel of avian influenza A virus strains, we find evidence for a trade-off between the persistence at high versus low temperatures. Combining a within-host model of influenza infection dynamics with a between-host transmission model, we study how such a trade-off affects virus fitness on the host population level. We show that conclusions regarding overall fitness are affected by the type of link assumed between the within- and between-host levels and the main route of transmission (direct or environmental). The relative importance of virulence and immune response mediated virus clearance are also found to influence the fitness impacts of virus persistence at low versus high temperatures. Based on our results, we predict that if transmission occurs mainly directly and scales linearly with virus load, and virulence or immune responses are negligible, the evolutionary pressure for influenza viruses to evolve toward good persistence at high within-host temperatures dominates. For all other scenarios, influenza viruses with good environmental persistence at low temperatures seem to be favored.     

Lack of Phenotypic and Evolutionary Cross-Resistance against Parasitoids and Pathogens in Drosophila melanogaster

Background

When organisms are attacked by multiple natural enemies, the evolution of a resistance mechanism to one natural enemy will be influenced by the degree of cross-resistance to another natural enemy. Cross-resistance can be positive, when a resistance mechanism against one natural enemy also offers resistance to another; or negative, in the form of a trade-off, when an increase in resistance against one natural enemy results in a decrease in resistance against another. Using Drosophila melanogaster, an important model system for the evolution of invertebrate immunity, we test for the existence of cross-resistance against parasites and pathogens, at both a phenotypic and evolutionary level.

Methods

We used a field strain of D. melanogaster to test whether surviving parasitism by the parasitoid Asobara tabida has an effect on the resistance against Beauveria bassiana, an entomopathogenic fungus; and whether infection with the microsporidian Tubulinosema kingi has an effect on the resistance against A. tabida. We used lines selected for increased resistance to A. tabida to test whether increased parasitoid resistance has an effect on resistance against B. bassiana and T. kingi. We used lines selected for increased tolerance against B. bassiana to test whether increased fungal resistance has an effect on resistance against A. tabida.

Results/Conclusions

We found no positive cross-resistance or trade-offs in the resistance to parasites and pathogens. This is an important finding, given the use of D. melanogaster as a model system for the evolution of invertebrate immunity. The lack of any cross-resistance to parasites and pathogens, at both the phenotypic and the evolutionary level, suggests that evolution of resistance against one class of natural enemies is largely independent of evolution of resistance against the other.     

Differences in surface-dwelling beetles of grasslands invaded and non-invaded by goldenrods (Solidago canadensis,S. gigantea) with special reference to Carabidae

We evaluated surface-dwelling Coleoptera with special reference to ground beetles (Coleoptera: Carabidae) using pitfall traps across fourteen stands of grasslands invaded and non-invaded by invasive goldenrods (Solidago canadensis L. and S. gigantea Ait.) over a 3 year period. We analysed differences in assemblages of invaded and non-invaded grasslands and tested responses of surface-dwelling beetles and carabids to invasion of goldenrods. We identified 29 Coleoptera families and 91 Carabidae species. Solidago invaded grasslands showed significantly higher activity-abundance of rove and carrion beetles and supported greater diversity and significantly higher evenness of surface-dwelling Coleoptera and the number of sampled families and individuals was higher too. We found lower taxonomic richness and significantly lower activity-abundance of carabids across goldenrods stands. Several less common Carabidae species and significantly higher representation of stenotopic brachypterous habitat specialists were also observed within invaded stands. We confirmed that differences in plant cover connected with invasion of goldenrods, soil moisture and abandonment of invaded habitats are the driving mechanisms of changes in surface-dwelling Coleoptera and ground beetles assemblages composition across Solidago invaded grasslands. Overall, changes of grassland biotopes connected with invasion of goldenrods significantly alter Coleoptera families and Carabidae assemblages, but not necessarily reduce diversity.     

Patterns of Privet: Urbanizing Watersheds,Invasive Ligustrum sinense,and Performance of Native Plant Species in Piedmont Floodplain Forests

Floodplain forests in rapidly changing landscapes with increased urbanization may reshape habitat conditions to the detriment of native biota and favor invasive species. We assessed whether introduced Ligustrum sinense distribution and abundance are causally linked to urbanization and whether mechanisms that promote L. sinense cause the demise of native plant species. We surveyed vegetation in 12 independent floodplain forests along an urban to rural gradient in South Carolina, USA. We then used a seedling transplant experiment in nine watersheds to assess how increased urban development affects survival and growth of L. sinense and three native species over two growing seasons. Urban development ranged from 1 to 45% and L. sinense cover was positively associated with development. However, in our transplant experiment, growth and survival of L. sinense did not differ significantly among watersheds. Native species were able to survive at all sites, but performance varied greatly among sites and species but not as a function of urban development. Our results suggest that although L. sinense invasion and urbanization are related (likely due to proximity of propagules from urban sources), the demise of native species cannot be explained by increased urbanization or changes in edaphic conditions and points to L. sinense as an agent of change in our floodplain forests. These results indicate that all floodplain forests are at risk of invasion if propagules arrive and that land managers need to be vigilant against new species introductions regardless of the proximity to urban areas.     

Female and male genetic contributions to post-mating immune defence in female Drosophila melanogaster

Post-mating reduction in immune defence is common in female insects, and a trade-off between mating and immunity could affect the evolution of immunity. In this work, we tested the capacity of virgin and mated female Drosophila melanogaster to defend against infection by four bacterial pathogens. We found that female D. melanogaster suffer post-mating immunosuppression in a pathogen-dependent manner. The effect of mating was seen after infection with two bacterial pathogens (Providencia rettgeri and Providencia alcalifaciens), though not after infection with two other bacteria (Enterococcus faecalis and Pseudomonas aeruginosa). We then asked whether the evolution of post-mating immunosuppression is primarily a ‘female’ or ‘male’ trait by assaying for genetic variation among females for the degree of post-mating immune suppression they experience and among males for the level of post-mating immunosuppression they elicit in their mates. We also assayed for an interaction between male and female genotypes to test the specific hypothesis that the evolution of a trade-off between mating and immune defence in females might be being driven by sexual conflict. We found that females, but not males, harbour significant genetic variation for post-mating immunosuppression, and we did not detect an interaction between female and male genotypes. We thus conclude that post-mating immune depression is predominantly a ‘female’ trait, and find no evidence that it is evolving under sexual conflict.     

Effects of Limb Length,Body Mass,Gender, Gravidity,and Elevation on Escape Speed in the Lizard Psammodromus algirus

Most animals rely on their escape speed to flee from predators. Here, we test several hypotheses on the evolution of escape speed in the lizard Psammodromus algirus. We test that: (1) Longer limbs should improve speed sprint. (2) Heavier lizards should be impaired regarding their sprint speed ability, suggesting a trade-off between fat storage and escape capability. (3) Males should achieve faster speeds due to their higher exposure to predators. (4) Gravid females, with increased body mass, should perform lower speed than non-gravid females. And (5) there are inter-population differences in sprint speed across an elevational gradient. We measured lizards sprint speed in a lineal raceway in the laboratory, filming races in standardized conditions and then calculating their maximal speed. We found that hind limb length greatly determined maximal sprint speed, lizards with longer limbs being faster. In parallel, higher body masses reduced maximal speed, which points to a trade-off between fat storage and escaping capability. Sexual differences also arose, as males were faster than females, as a consequence of males having longer limbs. Regarding females, gravidity did not impair maximal sprint speed, suggesting adaptations which compensate for the increased body mass. Finally, we found no elevational trend in both limbs length and sprint speed. In any case, this study suggests that selection on escape capacity may cast morphological evolution, and affect other life-history traits, such as fat storage and reproduction.     

Structural and functional analysis of the anti-malarial drug target prolyl-tRNA synthetase

Aminoacyl-tRNA synthetases (aaRSs) drive protein translation in cells and hence these are essential enzymes across life. Inhibition of these enzymes can halt growth of an organism by stalling protein translation. Therefore, small molecule targeting of aaRS active sites is an attractive avenue from the perspective of developing anti-infectives. Febrifugine and its derivatives like halofuginone (HF) are known to inhibit prolyl-tRNA synthetase of malaria parasite Plasmodium falciparum. Here, we present functional and crystallographic data on P. falciparum prolyl-tRNA synthetase (PfPRS). Using immunofluorescence data, we show that PfPRS is exclusively resident in the parasite cytoplasm within asexual blood stage parasites. The inhibitor HF interacts strongly with PfPRS in a non-competitive binding mode in presence or absence of ATP analog. Intriguingly, the two monomers that constitute dimeric PfPRS display significantly different conformations in their active site regions. The structural analyses presented here provide a framework for development of febrifugine derivatives that can seed development of new anti-malarials.     

Vector-Borne Pathogen and Host Evolution in a Structured Immuno-Epidemiological System

Vector-borne disease transmission is a common dissemination mode used by many pathogens to spread in a host population. Similar to directly transmitted diseases, the within-host interaction of a vector-borne pathogen and a host’s immune system influences the pathogen’s transmission potential between hosts via vectors. Yet there are few theoretical studies on virulence–transmission trade-offs and evolution in vector-borne pathogen–host systems. Here, we consider an immuno-epidemiological model that links the within-host dynamics to between-host circulation of a vector-borne disease. On the immunological scale, the model mimics antibody-pathogen dynamics for arbovirus diseases, such as Rift Valley fever and West Nile virus. The within-host dynamics govern transmission and host mortality and recovery in an age-since-infection structured host-vector-borne pathogen epidemic model. By considering multiple pathogen strains and multiple competing host populations differing in their within-host replication rate and immune response parameters, respectively, we derive evolutionary optimization principles for both pathogen and host. Invasion analysis shows that the \({\mathcal {R}}_0\) maximization principle holds for the vector-borne pathogen. For the host, we prove that evolution favors minimizing case fatality ratio (CFR). These results are utilized to compute host and pathogen evolutionary trajectories and to determine how model parameters affect evolution outcomes. We find that increasing the vector inoculum size increases the pathogen \({\mathcal {R}}_0\), but can either increase or decrease the pathogen virulence (the host CFR), suggesting that vector inoculum size can contribute to virulence of vector-borne diseases in distinct ways.     

Investigation of antibacterial activity of Bacillus spp. isolated from the feces of Giant Panda and characterization of their antimicrobial gene distributions

Bacillus group is a prevalent community of Giant Panda’s intestinal flora, and plays a significant role in the field of biological control of pathogens. To understand the diversity of Bacillus group from the Giant Panda intestine and their functions in maintaining the balance of the intestinal microflora of Giant Panda, this study isolated a significant number of strains of Bacillus spp. from the feces of Giant Panda, compared the inhibitory effects of these strains on three common enteric pathogens, investigated the distributions of six universal antimicrobial genes (ituA, hag, tasA, sfp, spaS and mrsA) found within the Bacillus group by PCR, and analyzed the characterization of antimicrobial gene distributions in these strains using statistical methods. The results suggest that 34 strains of Bacillus spp. were isolated which has not previously been detected at such a scale, these Bacillus strains could be classified into five categories as well as an external strain by 16S rRNA; Most of Bacillus strains are able to inhibit enteric pathogens, and the antimicrobial abilities may be correlated to their categories of 16S rRNA; The detection rates of six common antimicrobial genes are between 20.58 %(7/34) and 79.41 %(27/34), and genes distribute in three clusters in these strains. We found that the antimicrobial abilities of Bacillus strains can be one of the mechanisms by which Giant Panda maintains its intestinal microflora balance, and may be correlated to their phylogeny.     

Reproduction and survival of a solitary bee along native and exotic floral resource gradients

Native bee abundance has long been assumed to be limited by floral resources. This paradigm has been established in large measure because more bees are often found in areas supporting greater floral abundance. This could result from attraction to resource-rich sites as well as greater local demographic performance in sites supporting high floral abundance; however, demographic performance is usually unknown. Factors other than floral resources such as availability of nest sites, pressure from natural enemies, or whether floral resources are from a mixed native or mostly monodominant exotic assemblage might influence survival or fecundity and hence abundance. We examined how the survival and fecundity of the native solitary bee Osmia lignaria varied along a gradient in floral resource abundance. We released bees alongside a nest block at 27 grassland sites in Montana (USA) that varied in floral abundance and the extent of invasion by exotic forbs. We monitored nest construction and the fate of offspring within each nest. The number of nests established was positively related to native forb abundance and was negatively related to exotic forb species richness. Fecundity was positively related to native forb species richness; however, offspring mortality caused by the brood parasite Tricrania stansburyi was significantly greater in native-dominated sites. These results suggest that native floral resources can positively influence bee populations, but that the relationship between native floral resources and bee population performance is not straightforward. Rather, bees may face a trade-off between high offspring production and low offspring survival in native-dominated sites.     

Rotifer nutrition using supplemented monoxenic cultures

The evolution of rotifer feeding/ nutritional studies is discussed together with their relevance to ecological observations. Aseptic conditions and initially synxenic cultures are regarded as a basis for nutritional work. The marine rotifer Encentrum linnhei requires the amino acid dl-tryptophan as a supplement to the food-alga Brachiomonas submarina. Observations on feeding rotifers in natural water samples, together with the morphology of their feeding mechanisms, show Encentrum to be an omnivore; a natural source of tryptophan is suggested. Vitamin B₁₂ and thiamine requirements of Encentrum and Brachionus plicatilis are examined and evidence shown for the quantitative control of the former vitamin by the rotifer's food algae. Axenic cultivation of rotifers is discussed and restricted growth of Brachionus reported under such conditions.     

Aggregation and cnidae development as early defensive strategies in Favia fragum and Porites astreoides

To survive, corals possess a variety of active and passive defenses. This study examined the effectiveness of aggregation and cnidae development as defensive strategies in enhancing post-settlement survival and growth of two brooding corals, Favia fragum and Porites astreoides, in Bermuda. Growth and survival of solitary and aggregated spat were monitored over seven weeks; cnidae were extracted from surviving spat. F. fragum aggregated spat had higher mortality, slower growth, and more cnidae than solitary spat. On the other hand, aggregation proved beneficial for P. astreoides spat, which had significantly lower mortality, faster growth, and fewer cnidae. Aggregated and solitary F. fragum spat displayed negative correlations between cnidae density and growth, suggesting a trade-off between defense and growth; however, P. astreoides spat did not demonstrate such a trade-off. These differing responses suggest that early patterns of survivorship and defensive strategies are highly species specific and complex.     

Why and how might genetic and phylogenetic diversity be reflected in the identification of key biodiversity areas?

‘Key biodiversity areas'' are defined as sites contributing significantly to the global persistence of biodiversity. The identification of these sites builds from existing approaches based on measures of species and ecosystem diversity and process. Here, we therefore build from the work of Sgró et al. (2011 Evol. Appl. 4, 326–337. (doi:10.1111/j.1752-4571.2010.00157.x)) to extend a framework for how components of genetic diversity might be considered in the identification of key biodiversity areas. We make three recommendations to inform the ongoing process of consolidating a key biodiversity areas standard: (i) thresholds for the threatened species criterion currently consider a site''s share of a threatened species'' population; expand these to include the proportion of the species'' genetic diversity unique to a site; (ii) expand criterion for ‘threatened species'' to consider ‘threatened taxa’ and (iii) expand the centre of endemism criterion to identify as key biodiversity areas those sites holding a threshold proportion of the compositional or phylogenetic diversity of species (within a taxonomic group) whose restricted ranges collectively define a centre of endemism. We also recommend consideration of occurrence of EDGE species (i.e. threatened phylogenetic diversity) in key biodiversity areas to prioritize species-specific conservation actions among sites.     

Chromosome numbers,polyploidy, and hybridization in castilleja (scrophulariaceae ) of the Great Basin and Rocky Mountains

Chromosome numbers are reported for 190 collections ofCastilleja of the Great Basin-Rocky Mountains and adjacent regions in western North America. Polyploidy has played a major role in evolu tion of this genus. Of the 35 taxa represented, 14 are exclusively diploid (n =12). The remaining 21 taxa exhibit polyploidy: eight are tetraploid only, two are octopIoid only, while 11 of the more wide-ranging species have two or more levels of polyploidy. BothC. rhexifolia andC. sulphured have diploid, tetraploid, and octoploid races while the widespreadC. miniata has four (2x, 4x, 8x, and 10x). Where appropriate, the role of polyploidy and hybridization inCastilleja evolution and their relevance to taxonomy are discussed for individual species.     

Transmission Fitness in Co-colonization and the Persistence of Bacterial Pathogens

Humans are often colonized by polymorphic bacteria such as Streptococcus pneumoniae, Bordetella pertussis, Staphylococcus Aureus, and Haemophilus influenzae. Two co-colonizing pathogen clones may interact with each other upon host entry and during within-host dynamics, ranging from competition to facilitation. Here we examine the significance of these exploitation strategies for bacterial spread and persistence in host populations. We model SIS epidemiological dynamics to capture the global behavior of such multi-strain systems, focusing on different parameters of single and dual colonization. We analyze the impact of heterogeneity in clearance and transmission rates of single and dual colonization and find the criteria under which these asymmetries enhance endemic persistence. We obtain a backward bifurcation near \(R_0 = 1\) if the reproductive value of the parasite in dually infected hosts is sufficiently higher than that in singly infected ones. In such cases, the parasite is able to persist even in sub-threshold conditions, and reducing the basic reproduction number below 1 would be insufficient for elimination. The fitness superiority in co-colonized hosts can be attained by lowering net parasite clearance rate (\(\gamma _\mathrm{{d}}\)), by increasing transmission rate (\(\beta _\mathrm{{d}}\)), or both, and coupling between these traits critically constrains opportunities of pathogen survival in the \(R_0<1\) regime. Finally, using an adaptive dynamics approach, we verify that despite their importance for sub-threshold endemicity, traits expressed exclusively in coinfection should generally evolve independently of single infection traits. In particular, for \(\beta _\mathrm{{d}}\) a saturating parabolic or hyperbolic function of \(\gamma _\mathrm{{d}}\), co-colonization traits evolve to an intermediate optimum (evolutionarily stable strategy, ESS), determined only by host lifespan and the trade-off parameters linking \(\beta _\mathrm{{d}}\) and \(\gamma _\mathrm{{d}}\). Our study invites more empirical attention to the dynamics and evolution of parasite life-history traits expressed exclusively in coinfection.