Virulence‐driven trade‐offs in disease transmission: A meta‐analysis*

The virulence–transmission trade‐off hypothesis proposed more than 30 years ago is the cornerstone in the study of host–parasite co‐evolution. This hypothesis rests on the premise that virulence is an unavoidable and increasing cost because the parasite uses host resources to replicate. This cost associated with replication ultimately results in a deceleration in transmission rate because increasing within‐host replication increases host mortality. Empirical tests of predictions of the hypothesis have found mixed support, which cast doubt about its overall generalizability. To quantitatively address this issue, we conducted a meta‐analysis of 29 empirical studies, after reviewing over 6000 published papers, addressing the four core relationships between (1) virulence and recovery rate, (2) within‐host replication rate and virulence, (3) within‐host replication and transmission rate, and (4) virulence and transmission rate. We found strong support for an increasing relationship between replication and virulence, and replication and transmission. Yet, it is still uncertain if these relationships generally decelerate due to high within‐study variability. There was insufficient data to quantitatively test the other two core relationships predicted by the theory. Overall, the results suggest that the current empirical evidence provides partial support for the trade‐off hypothesis, but more work remains to be done.     

Functional trait trade‐off and species abundance: insights from a multi‐decadal study

Phylogenetically informed trait comparisons across entire communities show promise in advancing community ecology. We use this approach to better understand the composition of a community of winter annual plants with multiple decades of monitoring and detailed morphological, phenological and physiological measurements. Previous research on this system revealed a physiological trade‐off among dominant species that accurately predicts population and community dynamics. Here we expanded our investigation to 51 species, representing 96% of individual plants recorded over 30 years, and analysed trait relationships in the context of species abundance and phylogenetic relationships. We found that the functional‐trait trade‐off scales to the entire community, albeit with diminished strength. It is strongest for dominant species and weakens as progressively rarer species are included. The trade‐off has been consistently expressed over three decades of environmental change despite some turnover in the identity of dominant species.     

Gene duplications circumvent trade‐offs in enzyme function: Insect adaptation to toxic host plants

Herbivorous insects and their adaptations against plant toxins provide striking opportunities to investigate the genetic basis of traits involved in coevolutionary interactions. Target site insensitivity to cardenolides has evolved convergently across six orders of insects, involving identical substitutions in the Na,K‐ATPase gene and repeated convergent gene duplications. The large milkweed bug, Oncopeltus fasciatus, has three copies of the Na,K‐ATPase α‐subunit gene that bear differing numbers of amino acid substitutions in the binding pocket for cardenolides. To analyze the effect of these substitutions on cardenolide resistance and to infer possible trade‐offs in gene function, we expressed the cardenolide‐sensitive Na,K‐ATPase of Drosophila melanogaster in vitro and introduced four distinct combinations of substitutions observed in the three gene copies of O. fasciatus. With an increasing number of substitutions, the sensitivity of the Na,K‐ATPase to a standard cardenolide decreased in a stepwise manner. At the same time, the enzyme's overall activity decreased significantly with increasing cardenolide resistance and only the least substituted mimic of the Na,K‐ATPase α1C copy maintained activity similar to the wild‐type enzyme. Our results suggest that the Na,K‐ATPase copies in O. fasciatus have diverged in function, enabling specific adaptations to dietary cardenolides while maintaining the functionality of this critical ion carrier.     

Functional diversity and trade‐offs in divergent antipredator morphologies in herbivorous insects

Predator–prey interactions may be responsible for enormous morphological diversity in prey species. We performed predation experiments with morphological manipulations (ablation) to investigate the defensive function of dorsal spines and explanate margins in Cassidinae leaf beetles against three types of predators: assassin bugs (stinger), crab spiders (biter), and tree frogs (swallower). There was mixed support for the importance of primary defense mechanisms (i.e., preventing detection or identification). Intact spined prey possessing dorsal spines were more likely to be attacked by assassin bugs and tree frogs, while intact armored prey possessing explanate margins were likely to avoid attack by assassin bugs. In support of the secondary defense mechanisms (i.e., preventing subjugation), dorsal spines had a significant physical defensive function against tree frogs, and explanate margins protected against assassin bugs and crab spiders. Our results suggest a trade‐off between primary and secondary defenses. Dorsal spines improved the secondary defense but weakened the primary defense against tree frogs. We also detected a trade‐off in which dorsal spines and explanate margins improved secondary defenses against mutually exclusive predator types. Adaptation to different predatory regimes and functional trade‐offs may mediate the diversification of external morphological defenses in Cassidinae leaf beetles.     

Life history trade‐offs and evidence for hierarchical resource allocation in two monocarpic perennials

The evolution of floral display is thought to be constrained by trade‐offs between the size and number of flowers; however, empirical evidence for the trade‐off is inconsistent. We examined evidence for trade‐offs and hierarchical allocation of resources within and between two populations each of the monocarpic perennials, Cardiocrinum cordatum and C. giganteum. Within all populations, flower size–number trade‐offs were evident after accounting for variation in plant size. In addition, variation in flower size explained much variation in flower‐level allocation to attraction, and female and male function, a pattern consistent with hierarchical allocation. However, between population differences in flower size (C. cordatum) and number (C. giganteum) were not consistent with size–number trade‐offs or hierarchical allocation. The population‐level difference in C. cordatum likely reflects the combined influence of a time lag between initiation and maturation of flowers, and higher light levels in one population. Thus, our study highlights one mechanism that may account for the apparent independence of flower size and number in many studies. A prediction of sex allocation theory was also supported. In C. giganteum: plants from one population invested more mass in pistils and less in stamens than did plants from the other population. Detection of floral trade‐offs in Cardiocrinum may be facilitated by monocarpic reproduction, production of a single inflorescence and ease of measuring plant size.     

Not attackable or not crackable—How pre‐ and post‐attack defenses with different competition costs affect prey coexistence and population dynamics

It is well‐known that prey species often face trade‐offs between defense against predation and competitiveness, enabling predator‐mediated coexistence. However, we lack an understanding of how the large variety of different defense traits with different competition costs affects coexistence and population dynamics. Our study focusses on two general defense mechanisms, that is, pre‐attack (e.g., camouflage) and post‐attack defenses (e.g., weaponry) that act at different phases of the predator—prey interaction. We consider a food web model with one predator, two prey types and one resource. One prey type is undefended, while the other one is pre‐ or post‐attack defended paying costs either by a higher half‐saturation constant for resource uptake or a lower maximum growth rate. We show that post‐attack defenses promote prey coexistence and stabilize the population dynamics more strongly than pre‐attack defenses by interfering with the predator's functional response: Because the predator spends time handling “noncrackable” prey, the undefended prey is indirectly facilitated. A high half‐saturation constant as defense costs promotes coexistence more and stabilizes the dynamics less than a low maximum growth rate. The former imposes high costs at low resource concentrations but allows for temporally high growth rates at predator‐induced resource peaks preventing the extinction of the defended prey. We evaluate the effects of the different defense mechanisms and costs on coexistence under different enrichment levels in order to vary the importance of bottom‐up and top‐down control of the prey community.     

Evidence of trade‐offs shaping virulence evolution in an emerging wildlife pathogen

In the mid‐1990s, the common poultry pathogen Mycoplasma gallisepticum (MG) made a successful species jump to the eastern North American house finch Haemorhous mexicanus (HM). Subsequent strain diversification allows us to directly quantify, in an experimental setting, the transmission dynamics of three sequentially emergent geographic isolates of MG, which differ in the levels of pathogen load they induce. We find significant among‐strain variation in rates of transmission as well as recovery. Pathogen strains also differ in their induction of host morbidity, measured as the severity of eye lesions due to infection. Relationships between pathogen traits are also investigated, with transmission and recovery rates being significantly negatively correlated, whereas transmission and virulence, measured as average eye lesion score over the course of infection, are positively correlated. By quantifying these disease‐relevant parameters and their relationships, we provide the first analysis of the trade‐offs that shape the evolution of this important emerging pathogen.     

The role of climate and plant functional trade‐offs in shaping global biome and biodiversity patterns

Aim Two of the oldest observations in plant geography are the increase in plant diversity from the poles towards the tropics and the global geographic distribution of vegetation physiognomy (biomes). The objective of this paper is to use a process‐based vegetation model to evaluate the relationship between modelled and observed global patterns of plant diversity and the geographic distribution of biomes. Location The global terrestrial biosphere. Methods We implemented and tested a novel vegetation model aimed at identifying strategies that enable plants to grow and reproduce within particular climatic conditions across the globe. Our model simulates plant survival according to the fundamental ecophysiological processes of water uptake, photosynthesis, reproduction and phenology. We evaluated the survival of an ensemble of 10,000 plant growth strategies across the range of global climatic conditions. For the simulated regional plant assemblages we quantified functional richness, functional diversity and functional identity. Results A strong relationship was found (correlation coefficient of 0.75) between the modelled and the observed plant diversity. Our approach demonstrates that plant functional dissimilarity increases and then saturates with increasing plant diversity. Six of the major Earth biomes were reproduced by clustering grid cells according to their functional identity (mean functional traits of a regional plant assemblage). These biome clusters were in fair agreement with two other global vegetation schemes: a satellite image classification and a biogeography model (kappa statistics around 0.4). Main conclusions Our model reproduces the observed global patterns of plant diversity and vegetation physiognomy from the number and identity of simulated plant growth strategies. These plant growth strategies emerge from the first principles of climatic constraints and plant functional trade‐offs. Our study makes important contributions to furthering the understanding of how climate affects patterns of plant diversity and vegetation physiognomy from a process‐based rather than a phenomenological perspective.     

Geographical variation in reproductive traits and trade‐offs between size and number of eggs in the king ratsnake,Elaphe carinata

We collected gravid king ratsnakes (Elaphe carinata) from three geographically separated populations in Chenzhou (CZ), Lishui (LS) and Dinghai (DH) of China to study the geographical variation in female reproductive traits and trade‐offs between the size and number of eggs. Not all reproductive traits varied among the three populations. Of the traits examined, five (egg‐laying date, post‐oviposition body mass, clutch size, egg mass and egg width) differed among the three populations. The egg‐laying date, ranging from late June to early August, varied among populations in a geographically continuous trend, with females at the most northern latitude (DH) laying eggs latest, and females at the most southern latitude (CZ) laying eggs earliest. Such a trend was less evident or even absent in the other traits that differed among the three populations. CZ and DH females, although separated by a distance of approximately 1100 km as the crow flies, were similar to each other in most traits examined. LS females were distinguished from CZ and DH females by the fact that they laid a greater number of eggs, but these were smaller. The egg size–number trade‐off was evident in each of the three populations and, at a given level of relative fecundity, egg mass was significantly greater in the DH population than in the LS population. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 701–709.     

Sick plants in grassland communities: a growth‐defense trade‐off is the main driver of fungal pathogen abundance

Aboveground fungal pathogens can substantially reduce biomass production in grasslands. However, we lack a mechanistic understanding of the drivers of fungal pathogen infection and impact. Using a grassland global change and biodiversity experiment we show that the trade‐off between plant growth and defense is the main determinant of infection incidence. In contrast, nitrogen addition only indirectly increased incidence via shifting plant communities towards faster growing species. Plant diversity did not decrease incidence, likely because spillover of generalist pathogens or dominance of susceptible plants counteracted negative diversity effects. A fungicide treatment increased plant biomass production and high levels of infection incidence were associated with reduced biomass. However, pathogen impact was context dependent and infection incidence reduced biomass more strongly in diverse communities. Our results show that a growth‐defense trade‐off is the key driver of pathogen incidence, but pathogen impact is determined by several mechanisms and may depend on pathogen community composition.     

Discovery–dominance trade‐off among widespread invasive ant species

Ants are among the most problematic invasive species. They displace numerous native species, alter ecosystem processes, and can have negative impacts on agriculture and human health. In part, their success might stem from a departure from the discovery–dominance trade‐off that can promote co‐existence in native ant communities, that is, invasive ants are thought to be at the same time behaviorally dominant and faster discoverers of resources, compared to native species. However, it has not yet been tested whether similar asymmetries in behavioral dominance, exploration, and recruitment abilities also exist among invasive species. Here, we establish a dominance hierarchy among four of the most problematic invasive ants (Linepithema humile, Lasius neglectus, Wasmannia auropunctata, Pheidole megacephala) that may be able to arrive and establish in the same areas in the future. To assess behavioral dominance, we used confrontation experiments, testing the aggressiveness in individual and group interactions between all species pairs. In addition, to compare discovery efficiency, we tested the species' capacity to locate a food resource in a maze, and the capacity to recruit nestmates to exploit a food resource. The four species differed greatly in their capacity to discover resources and to recruit nestmates and to dominate the other species. Our results are consistent with a discovery–dominance trade‐off. The species that showed the highest level of interspecific aggressiveness and dominance during dyadic interactions.     

Density‐dependent survival varies with species life‐history strategy in a tropical forest

Species coexistence in diverse communities likely results from multiple interacting factors. Mechanisms such as conspecific negative density dependence (CNDD) and varying life‐history strategies related to resource partitioning are known to influence plant fitness, and thereby community composition and diversity. However, we have little understanding of how these mechanisms interact and how they vary across life stages. Here, we document the interaction between CNDD and life‐history strategy, based on growth‐mortality trade‐offs, from seedling to adult tree for 47 species in a tropical forest. Species’ life‐history strategies remained consistent across stages: fast‐growing species had higher mortality than slow‐growing species at all stages. In contrast, mean CNDD was strongest at early life stages (i.e. seedling, sapling). Fast‐growing species tended to suffer greater CNDD than slow‐growing species at several, but not all life stages. Overall, our results demonstrate that coexistence mechanisms interact across multiple life stages to shape diverse tree communities.     

Linking intra‐specific trait variation and plant function: seed size mediates performance tradeoffs within species

Substantial intra‐specific trait variation exists within plant communities, and in theory this variation could influence community dynamics. Although recent research has focused on intra‐specific variation in traits themselves, it is the influence of this variation on plant performance that makes intra‐specific trait variation relevant to ecological dynamics within or among species. Understanding the links between trait and performance variation, and the role of traits in mediating relationships among multiple components of performance, is critical for assessing the importance of intra‐specific trait variation for community dynamics. Seed size is thought to affect aspects of plant performance including fecundity, seedling growth, dispersal and tolerance of natural enemies. For two tropical tree species, we assessed how seed size was related to performance variation within each species and determined whether intra‐specific trait variation mediates intra‐specific performance tradeoffs. We used field seed rain collection to characterize size‐dependent outcomes of dispersal, sowed seeds of known size in soil collected near or far from conspecifics to characterize susceptibility to soil pathogens, and monitored growth of seedlings from seeds of known size. We found that intra‐specific seed size variation caused intra‐specific performance variation. The degree of trait‐based performance variation was consistently smaller than the degree of trait variation, and seed size influenced different components of performance for each species. One species exhibited a tradeoff in which small seeds had a fecundity advantage (more seedlings per unit reproductive mass) but produced smaller seedlings, whereas the other species exhibited a tradeoff in which small seeds dispersed to areas of low conspecific density but were less tolerant of density‐responsive natural enemies. Our results indicate that a single trait can influence multiple components of performance and can mediate different tradeoffs in co‐occurring species. Complex and heterogeneous effects of a single trait in multidimensional niche space may favour inter‐specific niche differentiation and coexistence.     

The competition–dispersal trade‐off exists in forbs but not in graminoids: A case study from multispecies alpine grassland communities

Much theoretical evidence has demonstrated that a trade‐off between competitive and dispersal ability plays an important role in facilitating species coexistence. However, experimental evidence from natural communities is still rare. Here, we tested the competition–dispersal trade‐off hypothesis in an alpine grassland in the Tianshan Mountains, Xinjiang, China, by quantifying competitive and dispersal ability using a combination of 4 plant traits (seed mass, ramet mass, height, and dispersal mode). Our results show that the competition–dispersal trade‐off exists in the alpine grassland community and that this pattern was primarily demonstrated by forbs. The results suggest that most forb species are constrained to be either good competitors or good dispersers but not both, while there was no significant trade‐off between competitive and dispersal ability for most graminoids. This might occur because graminoids undergo clonal reproduction, which allows them to find more benign microenvironments, forage for nutrients across a large area and store resources in clonal structures, and they are thus not strictly limited by the particular resources at our study site. To the best of our knowledge, this is the first time the CD trade‐off has been tested for plants across the whole life cycle in a natural multispecies plant community, and more comprehensive studies are still needed to explore the underlying mechanisms and the linkage between the CD trade‐off and community composition.     

Dispersal and neutral sampling mediate contingent effects of disturbance on plant beta‐diversity: a meta‐analysis

A major challenge in ecology, conservation and global‐change biology is to understand why biodiversity responds differently to similar environmental changes. Contingent biodiversity responses may depend on how disturbance and dispersal interact to alter variation in community composition (β‐diversity) and assembly mechanisms. However, quantitative syntheses of these patterns and processes across studies are lacking. Using null‐models and meta‐analyses of 22 factorial experiments in herbaceous plant communities across Europe and North America, we show that disturbance diversifies communities when dispersal is limited, but homogenises communities when combined with increased immigration from the species pool. In contrast to the hypothesis that disturbance and dispersal mediate the strength of niche assembly, both processes altered β‐diversity through neutral‐sampling effects on numbers of individuals and species in communities. Our synthesis suggests that stochastic effects of disturbance and dispersal on community assembly play an important, but underappreciated, role in mediating biotic homogenisation and biodiversity responses to environmental change.     

Trade‐offs between carbon stocks and biodiversity in European temperate forests

Policies to mitigate climate change and biodiversity loss often assume that protecting carbon‐rich forests provides co‐benefits in terms of biodiversity, due to the spatial congruence of carbon stocks and biodiversity at biogeographic scales. However, it remains unclear whether this holds at the scales relevant for management, and particularly large knowledge gaps exist for temperate forests and for taxa other than trees. We built a comprehensive dataset of Central European temperate forest structure and multi‐taxonomic diversity (beetles, birds, bryophytes, fungi, lichens, and plants) across 352 plots. We used Boosted Regression Trees (BRTs) to assess the relationship between above‐ground live carbon stocks and (a) taxon‐specific richness, (b) a unified multidiversity index. We used Threshold Indicator Taxa ANalysis to explore individual species’ responses to changing above‐ground carbon stocks and to detect change‐points in species composition along the carbon‐stock gradient. Our results reveal an overall weak and highly variable relationship between richness and carbon stock at the stand scale, both for individual taxonomic groups and for multidiversity. Similarly, the proportion of win‐win and trade‐off species (i.e., species favored or disadvantaged by increasing carbon stock, respectively) varied substantially across taxa. Win‐win species gradually replaced trade‐off species with increasing carbon, without clear thresholds along the above‐ground carbon gradient, suggesting that community‐level surrogates (e.g., richness) might fail to detect critical changes in biodiversity. Collectively, our analyses highlight that leveraging co‐benefits between carbon and biodiversity in temperate forest may require stand‐scale management that prioritizes either biodiversity or carbon in order to maximize co‐benefits at broader scales. Importantly, this contrasts with tropical forests, where climate and biodiversity objectives can be integrated at the stand scale, thus highlighting the need for context‐specificity when managing for multiple objectives. Accounting for critical change‐points of target taxa can help to deal with this specificity, by defining a safe operating space to manipulate carbon while avoiding biodiversity losses.