Early warning signals: the charted and uncharted territories

The realization that complex systems such as ecological communities can collapse or shift regimes suddenly and without rapid external forcing poses a serious challenge to our understanding and management of the natural world. The potential to identify early warning signals that would allow researchers and managers to predict such events before they happen has therefore been an invaluable discovery that offers a way forward in spite of such seemingly unpredictable behavior. Research into early warning signals has demonstrated that it is possible to define and detect such early warning signals in advance of a transition in certain contexts. Here, we describe the pattern emerging as research continues to explore just how far we can generalize these results. A core of examples emerges that shares three properties: the phenomenon of rapid regime shifts, a pattern of “critical slowing down” that can be used to detect the approaching shift, and a mechanism of bifurcation driving the sudden change. As research has expanded beyond these core examples, it is becoming clear that not all systems that show regime shifts exhibit critical slowing down, or vice versa. Even when systems exhibit critical slowing down, statistical detection is a challenge. We review the literature that explores these edge cases and highlight the need for (a) new early warning behaviors that can be used in cases where rapid shifts do not exhibit critical slowing down; (b) the development of methods to identify which behavior might be an appropriate signal when encountering a novel system, bearing in mind that a positive indication for some systems is a negative indication in others; and (c) statistical methods that can distinguish between signatures of early warning behaviors and noise.     

Early warning signals and the prosecutor's fallacy

Early warning signals have been proposed to forecast the possibility of a critical transition, such as the eutrophication of a lake, the collapse of a coral reef or the end of a glacial period. Because such transitions often unfold on temporal and spatial scales that can be difficult to approach by experimental manipulation, research has often relied on historical observations as a source of natural experiments. Here, we examine a critical difference between selecting systems for study based on the fact that we have observed a critical transition and those systems for which we wish to forecast the approach of a transition. This difference arises by conditionally selecting systems known to experience a transition of some sort and failing to account for the bias this introduces—a statistical error often known as the prosecutor''s fallacy. By analysing simulated systems that have experienced transitions purely by chance, we reveal an elevated rate of false-positives in common warning signal statistics. We further demonstrate a model-based approach that is less subject to this bias than those more commonly used summary statistics. We note that experimental studies with replicates avoid this pitfall entirely.     

Plant defence signals and Batesian mimicry

In a game theory context, we investigated conditions for an evolutionarily stable equilibrium of defended, signalling plants, and plants mimicking these signals – that is, conditions for a stable mimicry complex. We modelled this in three steps. First, we analysed conditions for selection for defended, signalling plants, in a population of undefended plants. Second, we analysed conditions for when mimicking plants can invade a population of defended, signalling plants, leading to a stable equilibrium between the two strategies. Third, we analysed how sampling of signalling plants by herbivores affects the equilibrium between the strategies. The predictions show that mimicry of plant defence signals may be common, and even imperfect mimics could invade a population of defended, signalling plants. Whether the latter prediction holds or not depends on how herbivores generalize over signals, and on the length of their avoidance sequence'. The length of the avoidance sequence is the number of signalling plants that a herbivore avoids to attack, after attacking a defended plant. If herbivores always sample signalling plants, then mimicry cannot evolve, whereas if herbivores have a long avoidance sequence, this may allow selection even for imperfect mimics.     

Biodiversity loss through speciation collapse: Mechanisms,warning signals,and possible rescue*

Speciation is the process that generates biodiversity, but recent empirical findings show that it can also fail, leading to the collapse of two incipient species into one. Here, we elucidate the mechanisms behind speciation collapse using a stochastic individual‐based model with explicit genetics. We investigate the impact of two types of environmental disturbance: deteriorated visual conditions, which reduce foraging ability and impede mate choice, and environmental homogenization, which restructures ecological niches. We find that: (1) Species pairs can collapse into a variety of forms including new species pairs, monomorphic or polymorphic generalists, or single specialists. Notably, polymorphic generalist forms may be a transient stage to a monomorphic population; (2) Environmental restoration enables species pairs to reemerge from single generalist forms, but not from single specialist forms; (3) Speciation collapse is up to four orders of magnitude faster than speciation, while the reemergence of species pairs can be as slow as de novo speciation; (4) Although speciation collapse can be predicted from either demographic, phenotypic, or genetic signals, observations of phenotypic changes allow the most general and robust warning signal of speciation collapse. We conclude that factors altering ecological niches can reduce biodiversity by reshaping the ecosystem's evolutionary attractors.     

Future directions in the ontogeny of plant defence: understanding the evolutionary causes and consequences

Plant defence often varies by orders of magnitude as plants develop from the seedling to juvenile to mature and senescent stages. Ontogenetic trajectories can involve switches among defence traits, leading to complex shifting phenotypes across plant lifetimes. While considerable research has characterised ontogenetic trajectories for now hundreds of plant species, we still lack a clear understanding of the molecular, ecological and evolutionary factors driving these patterns. In this study, we identify several non‐mutually exclusive factors that may have led to the evolution of ontogenetic trajectories in plant defence, including developmental constraints, resource allocation costs, multi‐functionality of defence traits, and herbivore selection pressure. Evidence from recent physiological studies is highlighted to shed light on the underlying molecular mechanisms involved in the regulation and activation of these developmental changes. Overall, our goal is to promote new research avenues that would provide evidence for the factors that have promoted the evolution of this complex lifetime phenotype. Future research focusing on the questions and approaches identified here will advance the field and shed light on why defence traits shift so dramatically across plant ontogeny, a widespread but poorly understood ecological pattern.     

Predator exaptations and defensive adaptations in evolutionary balance: No defence is perfect

Summary The lubber grasshopper,Romalea guttata, is large, aposematic, and extremely toxic. In feeding trials with 21 bird and lizard species, none were able to consume this chemically defended prey. Predators that attempted to eat lubbers, often gagged, regurgitated, and sometimes died. Loggerhead shrikes,Lanius ludovicianus, regularly impale this toxic prey in peninsular Florida. They, like other bird species, are unable to consume fresh lubbers. However, our tests show that they are able to consume lubbers if the prey are allowed to age for 1–2 days. This suggests that lubber toxins degrade following death and that shrike impaling behaviour serves as a preadaptation for overcoming the toxic defences of this large and abundant prey. These results also imply that counter adaptations against chemical defences need not involve major morphological or metabolic specializations, but that simple behavioural traits can enable a predator to utilize toxic prey.     

Anti-predator defence and the complexity-stability relationship of food webs

The mechanism for maintaining complex food webs has been a central issue in ecology because theory often predicts that complexity (higher the species richness, more the interactions) destabilizes food webs. Although it has been proposed that prey anti-predator defence may affect the stability of prey-predator dynamics, such studies assumed a limited and relatively simpler variation in the food-web structure. Here, using mathematical models, I report that food-web flexibility arising from prey anti-predator defence enhances community-level stability (community persistence and robustness) in more complex systems and even changes the complexity-stability relationship. The model analysis shows that adaptive predator-specific defence enhances community-level stability under a wide range of food-web complexity levels and topologies, while generalized defence does not. Furthermore, while increasing food-web complexity has minor or negative effects on community-level stability in the absence of defence adaptation, or in the presence of generalized defence, in the presence of predator-specific defence, the connectance-stability relationship may become unimodal. Increasing species richness, in contrast, always lowers community-level stability. The emergence of a positive connectance-stability relationship however necessitates food-web compartmentalization, high defence efficiency and low defence cost, suggesting that it only occurs under a restricted condition.     

Upstream and downstream signals of nitric oxide in pathogen defence

Nitric oxide (NO) is now recognised as a crucial player in plant defence against pathogens. Considerable progress has been made in defining upstream and downstream signals of NO. Recently, MAP kinases, cyclic nucleotide phosphates, calcium and phosphatidic acid were demonstrated to be involved in pathogen-induced NO-production. However, the search for inducers of NO synthesis is difficult because of the still ambiguous enzymatic source of NO. Accumulation of NO triggers signal transduction by other second messengers. Here we depict NON-EXPRESSOR OF PATHOGENESIS-RELATED 1 and glyceraldehyde-3-phosphate dehydrogenase as central redox switches translating NO redox signalling into cellular responses. Although the exact position of NO in defence signal networks is unresolved at last some NO-related signal cascades are emerging.     

Early warning signals for critical transitions: a generalized modeling approach

Critical transitions are sudden, often irreversible, changes that can occur in a large variety of complex systems; signals that warn of critical transitions are therefore highly desirable. We propose a new method for early warning signals that integrates multiple sources of information and data about the system through the framework of a generalized model. We demonstrate our proposed approach through several examples, including a previously published fisheries model. We regard our method as complementary to existing early warning signals, taking an approach of intermediate complexity between model-free approaches and fully parameterized simulations. One potential advantage of our approach is that, under appropriate conditions, it may reduce the amount of time series data required for a robust early warning signal.     

Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies

Conclusions Contrasting effects of generalist and specialist herbivores can explain why all plants have not evolved high levels of defence. Maintenance of variation in concentration of defence substances can be explained by a shifting balance between natural selection for defence against herbivory by specialists and generalists. Generalist natural enemies will shift the optimal defence curve to lower concentrations of defences. Physiological costs of production of defence substances and selection by specialist herbivores of plant phenotypes with higher levels of defence compounds for sequestration are no essential elements of this model. They may, however, adjust the predicted optimum defence function and contribute to maintenance of variation of concentrations of defence substances.     

Neutral theory, phylogenies, and the relationship between phenotypic change and evolutionary rates

The neutral theory of molecular evolution predicts that rates of phenotypic change are largely independent from genotypic change. A recent study by Bromham et al. (2002) confirmed this expectation, finding no evidence for correlated phenotypic and molecular evolutionary rates in animals. We reevaluate this hypothesis, sampling at different taxonomic levels in plants and animals, using Bayesian inference to reconstruct phylogenetic trees and estimate rates of molecular evolution. We use independent contrasts in branch lengths to maximize the information extracted from each of the trees and nodal posterior probabilities to assess the influence of phylogenetic error. Our results indicate that in vascular plants between 2% and 11% of the variation in phenotypic rates of change can be explained by the rate of genotypic change. These results may be explained by the idea that processes that affect general evolutionary rates, such as body size, may also be expected to influence rates of morphological change.     

Oligosaccharide recognition signals and defence reactions in marine plant-microbe interactions.

Recent findings on the involvement of oligosaccharide signals in pathogen recognition and defence reactions in marine algae shine a new light on the ecology of their interactions with associated microorganisms. Since the marine environment encompasses lineages that have diverged a long time ago from the terrestrial phyla, these results suggest that cell-cell recognition pathways typical of terrestrial plants appeared very early in the evolution of eukaryotes. Production of oligosaccharides from marine algae using microbial recombinant polysaccharidases is also of industrial interest as plants can be protected from infections by preincubation in the presence of appropriate signals that mimic the attacks by pathogens.     

Homology versus analogy: possible evolutionary relationship of immunoglobulins, cupredoxins, and Cu,Zn-superoxide dismutase

The 'immunoglobulin-like' fold is one of most common structural motifs observed in proteins. This topology is found in more than 80 superfamilies of proteins, including Cu,Zn-superoxide dismutase (SOD) and cupredoxin. Evolutionary relationships have not been identified, but may exist. The challenge remains, therefore, of resolving the issue of whether the diverse distribution of the fold is accounted for by divergent evolution of function or convergent evolution of structure following multiple independent origins of function. Since the early studies that revealed conformational similarity of immunoglobulins and other proteins, the number of primary structures available for comparison has dramatically increased and new computational approaches for analysis of sequences have been developed. It now appears that a hypothesis of a common evolutionary origin for cupredoxins, Cu,Zn-SOD, and immunoglobulins may be credible. The distinction between protein homology and protein analogy is fundamental. The immunoglobulin-like fold may represent a robust system within which to examine again the issue of protein homology versus analogy.     

Evolving détente: the origin of warning signals via concurrent reciprocal selection

Casualties and impediments inflicted on consumers by defended prey, and vice versa, may be averted by vocalizations, postures, coloration, scents, and other warning, or so‐called aposematic, displays. The existence of aposematic signals has challenged biologists who have sought plausible mechanisms for their evolution. Here, we elaborate on the rationale for the hypothesis that aposematic signals arise via concurrent reciprocal selection (CRS) enacted between inimical signal receivers and signal emitters, where signal emitters, e.g., defended prey, select against non‐discriminating signal receivers, e.g., predators, and signal receivers select against unrecognized signal emitters. It is postulated that this mutual selective interaction culminates in the survival of discriminating signal receivers that avoid signal emitters, and recognized (distinctive) signal emitters that are avoided by signal receivers. A CRS hypothesis for the evolution of aposematism, therefore, maintains that distinctive features of prey arise in response to selection imposed by consumers, and that avoidances of those features by consumers arise in response to selection imposed by defended prey. We discuss the plausible inception of aposematism via CRS in light of related hypotheses, and describe points of concordance with previous observations and suggestions on the origin of aposematism. Aposematism arising via CRS is not contingent upon the relatedness of signallers, aversions acquired by learning, or other conditions postulated for some other evolutionary hypotheses. CRS is a credible alternative hypothesis for the evolution of warning signals in diverse consumer‐prey interactions.