Trade-off between virulence and vertical transmission and the maintenance of a virulent plant pathogen

The continuum hypothesis predicts that parasites should evolve reduced virulence if they have higher opportunity for vertical transmission. However, when there is a trade-off between virulence and vertical transmission, selection may favor horizontal transmission and higher virulence. Atkinsonella hypoxylon is a fungal pathogen that reduces Danthonia fitness by 50% or more when it completely castrates hosts' chasmogamous inflorescences, despite the high opportunity for vertical transmission through cleistogamous seeds. Sporadically, infected hosts with partially castrated inflorescences (which have higher fecundity than completely castrated hosts) are observed in natural populations. Why are partially castrated plants rare if selection favors reduced virulence? We investigated whether there was genetic diversity for virulence among A. hypoxylon genotypes and the relationship between virulence and vertical transmission. We found that the fungal genotype significantly affects the occurrence of partial castration in Danthonia compressa. The proportion of seedlings that were vertically infected by their maternal plant was lower for partially castrated than for completely castrated plants. Our results demonstrate a trade-off between virulence and vertical transmission, explaining the maintenance of more virulent, completely castrating fungal genotypes in natural populations, and suggest that vertical transmission in plants is more complex than what is considered in current models.     

Microsporidian life cycles and diversity: the relationship between virulence and transmission

The microsporidia are obligate intracellular parasites which have diverse life cycles involving both horizontal and vertical transmission and parasitise a wide range of vertebrate and invertebrate hosts. In this paper we consider the life cycles and diversity of the microsporidia. We focus in particular on the relationship between parasite transmission and virulence and its implications for host-parasite coevolution. The use of horizontal and vertical routes of transmission varies between species and there is a strong link between transmission and virulence. Horizontal transmission is characterised by a high parasite burden and associated pathogenicity. In contrast, vertical transmission is characterised by low virulence, which has led to under-reporting of this important transmission route. Vertically transmitted microsporidia may also cause male killing or feminisation of their host, with implications for host population sex ratio and stability. Phylogenetic analysis shows that vertical transmission occurs in diverse branches of the Microspora. We find that there is evidence for vertical transmission in both vertebrate and invertebrate hosts and conclude that it is a common or possibly even ubiquitous transmission route within this phylum.     

Nest desertion: a trade-off between current and future reproduction

Life history theory predicts that parents should desert a reproductive attempt if the costs of rearing this brood exceed the expected benefits. Thus, if the value of the current breeding attempt is reduced, for example through an unexpected reduction in size, parents are expected to reconsider whether it is worth continuing investing in their brood. With regard to nest desertion behaviour two predictions can be made: individuals are (1) more likely to desert if the reduction in clutch size is large and (2) less likely to desert if the reduction is at a late stage of breeding. We investigated the threshold at which nest desertion takes place by experimentally reducing great tit, Parus major, clutches to different sizes and at different stages of the incubation period. The results were in accordance with the predictions: clutch desertion rates were negatively related to the number of eggs that remained in the nest, and nest desertion was less likely nearer the end of the incubation period. In addition, we estimated the fitness consequences of nest desertion behaviour. For this purpose we made one group of birds desert in favour of a replacement clutch and another group rear a reduced brood. The latter were more likely to produce a second clutch after the first-brood fledglings had left the nest. As a consequence, the number of fledglings produced over the entire breeding season did not differ between the two experimental groups. We also counted the number of recruits and breeding adults in the following breeding season and found that the experimental groups did not differ in local recruitment and adult survival. Therefore, the results did not indicate that parents improved their fitness by deserting a reduced clutch.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Fitness optimization of Daphnia in a trade-off between food and temperature

In thermally stratified lakes with a deep chlorophyll maximum (DCM), Daphnia face a trade-off between food availability and optimum development temperatures. We hypothesize that Daphnia optimize their fitness by allocating the time spent in the different vertical habitats depending on the distribution of algal resources and the temperature gradient. We used the plankton towers (large indoor mesocosms) to study the vertical distribution of a population of Daphnia hyalina×galeata in three different temperature gradients with a DCM. Additionally, we determined the fitness of Daphnia in the epilimnion and hypolimnion by transferring water from these layers into flow-through systems where we raised Daphnia and assessed their juvenile growth rate as a measure of fitness. The fitness distribution was correlated with the vertical distribution. The vertical distribution most likely reflected the proportions of time Daphnia allocated to dwelling in the two vertical habitats.     

Potential trade-off between vocal ornamentation and spatial ability in a songbird

Bird song is hypothesized to be a reliable indicator of cognition because it depends on brain structure and function. Song features have been found to correlate positively with measures of cognition, but the relationship between song and cognition is complicated because not all cognitive abilities are themselves positively correlated. If cognition is not a unitary trait, developmental constraints on brain growth could generate trade-offs between some aspects of cognition and song. To further clarify the relationship between song and cognition in song sparrows (Melospiza melodia), we examined repertoire size and performance on a spatial task. We found an inverse relationship between repertoire size and speed of spatial learning and suggest that a developmental trade-off between the hippocampus and song control nuclei could be responsible for this relationship. By attending to male song, females may learn about a suite of cognitive abilities; this study suggests that females may glean information about a male''s cognitive weaknesses as well as his strengths.     

A trade-off between growth and starvation endurance in a pit-building antlion

Trade-offs have a central role in evolutionary ecology and life-history theory. Here, we present evidence for the existence of a rarely studied trade-off between growth rate and starvation endurance in larvae of a pit-building antlion. We first manipulated antlions’ feeding regime and obtained a spectrum of growth rates. Next, we starved the antlions and documented their rate of mass loss. Antlions growing faster during the feeding phase also lost mass faster during the successive starvation period, implying the existence of an induced trade-off between fast growth and starvation endurance. Finally, we fed all antlions with prey items of similar mass and measured both the giving-up prey mass (i.e. the remaining body mass of the prey that was not converted into predator body mass), and growth efficiency of antlions (i.e. proportion of prey consumed, negatively correlated with giving-up prey mass). The giving-up mass was negatively correlated with the growth rate of the antlions during the feeding phase, and positively correlated with their growth rate during the starvation phase (the opposite pattern was evident when examining growth efficiency), incongruently with the common phenomenon of growth compensation (i.e. extracting more of the prey after a starvation period). We suggest that antlion larvae can adopt a physiological mode bounded by two extremes: one extreme is adapted to starvation, involving reduced metabolic rates but also reduced capability to exploit prey, while the other is adapted to fast growth, allowing an efficient exploitation of prey, but at the expense of lowered starvation endurance.     

Seasonal migration determined by a trade-off between predator avoidance and growth

Migration is a common phenomenon in many organisms, terrestrial as well as aquatic, and considerable effort has been spent to understand the evolution of migratory behaviour and its consequences for population and community dynamics. In aquatic systems, studies on migration have mainly been focused on commercially important fish species, such as salmon and trout. However, seasonal mass-migrations may occur also among other freshwater fish, e.g. in cyprinids that leave lakes and migrate into streams and wetlands in the fall and return back to the lake in spring. In a conceptual model, we hypothesized that this is an adaptive behaviour in response to seasonal changes in predation (P) and growth (G) and that migrating fish change habitat so as to minimise the ratio between predation mortality and growth rate (P/G). Estimates from bioenergetic modelling showed that seasonal changes in the ratio between predator consumption rate and prey growth rate followed the predictions from the conceptual model and also gave more precise predictions for the timing of the habitat change. By quantifying the migration of more than 1800 individually marked fish, we showed that actual migration patterns followed predictions with a remarkable accuracy, suggesting that migration patterns have evolved in response to seasonally fluctuating trade-offs between predator avoidance and foraging gains. Thus, the conceptual model provides a mechanistic understanding to mass-migration in prey fish. Further, we also show that the dominant prey fish is actually absent from the lake during a major part of the year, which should have strong implications for the dynamics of the lake ecosystem through direct and indirect food-web interactions.     

No evidence for a trade-off between reproductive investment and immunity in a rodent

Life history theory assumes there are trade-offs between competing functions such as reproduction and immunity. Although well studied in birds, studies of the trade-offs between reproduction and immunity in small mammals are scarce. Here we examined whether reduced immunity is a consequence of reproductive effort in lactating Brandt's voles (Lasiopodomys brandtii). Specifically, we tested the effects of lactation on immune function (Experiment I). The results showed that food intake and resting metabolic rate (RMR) were higher in lactating voles (6≤ litter size ≤8) than that in non-reproductive voles. Contrary to our expectation, lactating voles also had higher levels of serum total Immunoglobulin G (IgG) and anti-keyhole limpet hemocyanin (KLH) IgG and no change in phytohemagglutinin (PHA) response and anti-KLH Immunoglobulin M (IgM) compared with non-reproductive voles, suggesting improved rather than reduced immune function. To further test the effect of differences in reproductive investment on immunity, we compared the responses between natural large (n≥8) and small litter size (n≤6) (Experiment II) and manipulated large (11-13) and small litter size (2-3) (Experiment III). During peak lactation, acquired immunity (PHA response, anti-KLH IgG and anti-KLH IgM) was not significantly different between voles raising large or small litters in both experiments, despite the measured difference in reproductive investment (greater litter size, litter mass, RMR and food intake in the voles raising larger litters). Total IgG was higher in voles with natural large litter size than those with natural small litter size, but decreased in the enlarged litter size group compared with control and reduced group. Our results showed that immune function is not suppressed to compensate the high energy demands during lactation in Brandt's voles and contrasting the situation in birds, is unlikely to be an important aspect mediating the trade-off between reproduction and survival.     

Living off a fish: a trade-off between parasites and the immune system

Research in fish immune system and parasite invasion mechanisms has advanced the knowledge of the mechanisms whereby parasites evade or cope with fish immune response. The main mechanisms of immune evasion employed by fish parasites are reviewed and considered under ten headings. 1) Parasite isolation: parasites develop in immuno-privileged host tissues, such as brain, gonads, or eyes, where host barriers prevent or limit the immune response. 2) Host isolation: the host cellular immune response isolates and encapsulates the parasites in a dormant stage without killing them. 3) Intracellular disguise: typical of intracellular microsporidians, coccidians and some myxosporeans. 4) Parasite migration, behavioural and environmental strategies: parasites migrate to host sites the immune response has not yet reached or where it is not strong enough to kill them, or they accommodate their life cycles to the season or the age in which the host immune system is down-regulated. 5) Antigen-based strategies such as mimicry or masking, variation and sharing of parasite antigens. 6) Anti-immune mechanisms: these allow parasites to resist innate humoral factors, to neutralize host antibodies or to scavenge reactive oxygen species within macrophages. 7) Immunodepression: parasites either suppress the fish immune systems by reducing the proliferative capacity of lymphocytes or the phagocytic activity of macrophages, or they induce apoptosis of host leucocytes. 8) Immunomodulation: parasites secrete or excrete substances which modulate the secretion of host immune factors, such as cytokines, to their own benefit. 9) Fast development: parasites proliferate faster than the ability of the host to mount a defence response. 10) Exploitation of the host immune reaction. Knowledge of the evasion strategies adopted by parasites will help us to understand host-parasite interactions and may therefore help in the discovery of novel immunotherapeutic agents or targeted vaccines, and permit the selection of host-resistant strains.     

Natural variation in a testosterone-mediated trade-off between mating effort and parental effort

Male birds frequently face a trade-off between acquiring mates and caring for offspring. Hormone manipulation studies indicate that testosterone often mediates this trade-off, increasing mating effort while decreasing parental effort. Little is known, however, about individual covariation between testosterone and relevant behavior on which selection might act. Using wild, male dark-eyed juncos (Junco hyemalis), we measured individual variation in testosterone levels before and after standardized injections of gonadotropin-releasing hormone (GnRH). The GnRH challenges have been shown to produce short-term testosterone increases that are similar to those produced naturally in response to social stimuli, repeatable in magnitude, and greater in males with more attractive ornaments. We correlated these testosterone increases with behavioral measures of mating and parental effort (aggressive response to a simulated territorial intrusion and nestling feeding, respectively). Males that showed higher postchallenge testosterone displayed more territorial behavior, and males that produced higher testosterone increases above initial levels displayed reduced parental behavior. Initial testosterone levels were positively but nonsignificantly correlated with aggression but did not predict parental behavior. These relationships suggest that natural variation in testosterone, specifically the production of short-term increases, may underlie individual variation in the mating effort/parental effort trade-off. We discuss the implications of these results for the evolution of hormonally mediated trade-offs.     

The evolution of parasite virulence and transmission rate in a spatially structured population

If the transmission occurs through local contact of the individuals in a spatially structured population, the evolutionarily stable (ESS) traits of parasite might be quite different from what the classical theory with complete mixing predicts. In this paper, we theoretically study the ESS virulence and transmission rate of a parasite in a lattice-structured host population, in which the host can send progeny only to its neighboring vacant site, and the transmission occurs only in between the infected and the susceptible in the nearest-neighbor sites. Infected host is assumed to be infertile. The analysis based on the pair approximation and the Monte Carlo simulation reveal that the ESS transmission rate and virulence in a lattice-structured population are greatly reduced from those in completely mixing population. Unlike completely mixing populations, the spread of parasite can drive the host to extinction, because the local density of the susceptible next to the infected can remain high even when the global density of host becomes very low. This demographic viscosity and group selection between self-organized spatial clusters of host individuals then leads to an intermediate ESS transmission rate even if there is no tradeoff between transmission rate and virulence. The ESS transmission rate is below the region of parasite-driven extinction by a finite amount for moderately large reproductive rate of host; whereas, the evolution of transmission rate leads to the fade out of parasite for small reproductive rate, and the extinction of host for very large reproductive rate.     

Microhabitat selection in a grassland butterfly: a trade-off between microclimate and food availability

Understanding the factors that determine habitat quality is vital to ensuring appropriate habitat management. The main objective of this study was to assess the microhabitat preferences of egg-depositing females of the Grizzled Skipper (Pyrgus malvae) in calcareous grasslands of the Diemel Valley (Central Germany) for defining habitat quality. Based on this knowledge, we make management recommendations for the conservation of this threatened species. P. malvae generally preferred open and warm oviposition sites. However, there were considerable differences in the environmental conditions, depending on the selected host plant. On the small Potentilla tabernaemontani plants that grew in sparse vegetation with low-growing turf, mostly only one egg was found per plant. In contrast, occupied Agrimonia eupatoria host plants were larger and more prominent, regularly having more than one egg, and grew at sites with a taller and denser vegetation. The observed oviposition pattern reflects a trade-off between microclimate and food availability: Usually, occupied P. tabernaemontani plants grow under favourable microclimatic conditions. However, during hot years the risk of desiccation is high, leading to food shortage. In contrast, A. eupatoria generally provides more biomass, thrives on deeper soils and the vegetation has a cooler microclimate: hence, food shortage is somewhat unlikely. To meet the described habitat requirements of P. malvae, traditional rough grazing by sheep and goats seemed to be the most appropriate land management strategy. The re-introduction of coppicing in woodlands, particularly adjacent to calcareous grasslands, would also be beneficial.     

Evolution of virulence when transmission occurs before disease

Most models of virulence evolution assume that transmission and virulence are constant during an infection. In many viral (HIV and influenza), bacterial (TB) and prion (BSE and CWD) systems, disease-induced mortality occurs long after the host becomes infectious. Therefore, we constructed a model with two infected classes that differ in transmission rate and virulence in order to understand how the evolutionarily stable strategy (ESS) depends on the relative difference in transmission and virulence between classes, on the transition rate between classes and on the recovery rate from the second class. We find that ESS virulence decreases when expressed early in the infection or when transmission occurs late in an infection. When virulence occurred relatively equally in each class and there was disease recovery, ESS virulence increased with increased transition rate. In contrast, ESS virulence first increased and then decreased with transition rate when there was little virulence early in the infection and a rapid recovery rate. This model predicts that ESS virulence is highly dependent on the timing of transmission and pathology after infection; thus, pathogen evolution may either increase or decrease virulence after emergence in a new host.     

Evidence for a trade-off between growth and body reserves in northern white-tailed deer

We contrasted patterns of growth and accumulation of body reserves in autumn between two high-density (HD) white-tailed deer populations facing winters of different severity and length. Both populations occurred in the absence of effective predators and suffered from some forage competition based on reduced body masses. A third population living at low density (LD) and confronting long and severe winters (SW) served to distinguish the influence of food competition and winter severity on growth and body reserves. We estimated body components (water, protein, fat and ash) of deer during the first half of November and compared growth patterns between sexes and regions. HD-SW males continuted growth to an older age than HD males facing short and mild winters (MW) but females of both regions reached adult body mass at the same age. LD-SW deer exhibited a growth pattern similar to that of HD-SW animals but were the heaviest and the largest, suggesting that growth patterns are related to winter harshness (or length of the growing season) and that final body size is related to forage competition in summer. Sexual dimorphism became evident at an older age in the HD-SW population than in the HD-MW population, demonstrating that winter harshness does not affect immature males and females in the same manner. Fawns from the HD-SW population had proportionally longer legs and a higher percentage of body fat. Adaptations of immature deer to long and severe winters suggest that survival during the first winter represents the most critical step in the life span of northern white-tailed deer.     

Evidence for a trade-off between early growth and tooth wear in Svalbard reindeer

Ruminants depend on efficient physical degradation of forage through chewing to increase the surface area of the food particles presented to the microflora. Fossil evidence suggests that increased molar height is an adaptation for wear tolerance in dry ecosystems with sparse vegetation, but no study has shown selection pressure for hypsodonty in contemporary ruminants. We explored the relationships between particle size in rumen, tooth wear (scanned molar occlusal topography), age and body mass of female Svalbard reindeer living in an arctic desert at 78 degrees latitude on Svalbard. We predicted that (H1) if the rumen particle size is determined mainly by constraints due to tooth wear, and if tooth wear is mainly a function of age, average particle size in rumen should increase with age. From allometric relations it is known that larger individuals can survive on a lower-quality diet, we therefore predicted (H2) larger particle sizes with increases in (ln) body mass, irrespective of age and wear. Lastly, if there is a trade-off between growth and tooth wear in dry ecosystems (a selection pressure for hypsodonty), we predicted (H3) that teeth of heavier animals should be more worn than those of lighter animals of the same age. The proportion of small particles (<1.0 mm) decreased rapidly with increasing age (consistent with H1). Heavier females within an age class had more worn teeth (consistent with H3) than lighter ones. A close-to-isometric relationship between particle size and body mass suggested that heavier animals partly compensated for reduced tooth efficiency by chewing more. We provide the first evidence of a trade-off between fast early growth and wear (a somatic cost) of a senescence-related trait--the structure and height of the molar--in a wild ruminant inhabiting an arctic desert where selection pressure for increased tooth height is expected. This suggests that foraging conditions are more extreme than the environment in which the species originally evolved.     

Evidence for a trade-off between host-range breadth and host-use efficiency in aphid parasitoids

"The jack-of-all-trades is a master of none" describes the widely held belief that engaging in many tasks comes at the cost of being unable to do those tasks well. However, empirical evidence for generalist fitness costs remains scarce. We used published data from a long-term field survey of aphid parasitoids to determine whether relative specialists are more abundant than generalists on their shared hosts, a pattern that would be expected if generalists suffer a trade-off between host-range breadth and host-use efficiency. Relative specialists were more abundant than generalists on their shared hosts, but only when we used a measure of specialization that accounts for the taxonomic differences among parasitoids' hosts. These results suggest that a generalist-specialist trade-off exists within this group of parasitoids and that the generalist fitness cost depends on the taxonomic breadth, rather than the number, of host species that are used.     

There is no trade-off between speed and force in a dynamic lever system

Lever systems within a skeleton transmit force with a capacity determined by the mechanical advantage, A. A is the distance from input force to a joint, divided by the distance from the joint to the output force. A lever with a relatively high A in static equilibrium has a great capacity to generate force but moves a load over a small distance. Therefore, the geometry of a skeletal lever presents a trade-off between force and speed under quasi-static conditions. The present study considers skeletal dynamics that do not assume static equilibrium by modelling kicking by a locust leg, which is powered by stored elastic energy. This model predicts that the output force of this lever is proportional to A, but its maximum speed is independent of A. Therefore, no trade-off between force and velocity exists in a lever system with spring-mass dynamics. This demonstrates that the motion of a skeleton depends on the major forces that govern its dynamics and cannot be inferred from skeletal geometry alone.     

A trade-off between scale and precision in resource foraging

Summary There is widespread uncertainty about the nature and role of morphological plasticity in resource competition in plant communities. We have assayed the foraging characteristics of leaf canopies and root systems of eight herbaceous plants of contrasted ecology using new techniques to create controlled patchiness in light and mineral nutrient supply. The results are compared with those of a conventional competition experiment. Measurements of dry matter partitioning and growth in patchy conditions indicate a consistent positive association between the foraging characteristics of roots and shoots, supporting the hypothesis of strong interdependence of competitive abilities for light and mineral nutrients. Differences are identified in the abilities of dominant and subordinate plants to forage on coarse and fine scalcs. It is suggested that a trade-off exists in the scale (“high” in dominants) and precision (high in subordinates) with which resources are intercepted and that this trade-off contributes to diversity in communities of competing plants.