Luke McNally

On the dimensionality of ecological stability

Ecological stability is touted as a complex and multifaceted concept, including components such as variability, resistance, resilience, persistence and robustness. Even though a complete appreciation of the effects of perturbations on ecosystems requires the simultaneous measurement of these multiple components of stability, most ecological research has focused on one or a few of those components analysed in isolation. Here, we present a new view of ecological stability that recognises explicitly the non-independence of components of stability. This provides an approach for simplifying the concept of stability. We illustrate the concept and approach using results from a field experiment, and show that the effective dimensionality of ecological stability is considerably lower than if the various components of stability were unrelated. However, strong perturbations can modify, and even decouple, relationships among individual components of stability. Thus, perturbations not only increase the dimensionality of stability but they can also alter the relationships among components of stability in different ways. Studies that focus on single forms of stability in isolation therefore risk underestimating significantly the potential of perturbations to destabilise ecosystems. In contrast, application of the multidimensional stability framework that we propose gives a far richer understanding of how communities respond to perturbations.

Combinatorial quorum sensing allows bacteria to resolve their social and physical environment

Significance Many bacterial species engage in a form of cell–cell communication known as quorum sensing (QS). Despite great progress in unravelling the molecular mechanisms of QS, controversy remains over its functional role. There is disagreement over whether QS surveys bacterial cell density or rather environmental properties like diffusion or flow, and moreover there is no consensus on why many bacteria use multiple signal molecules. We develop and test a new conceptual framework for bacterial cell–cell communication, demonstrating that bacteria can simultaneously infer both their social (density) and physical (mass-transfer) environment, given combinatorial (nonadditive) responses to multiple signals with distinct half-lives. Our results also show that combinatorial communication is not restricted solely to primates and is computationally achievable in single-celled organisms. Quorum sensing (QS) is a cell–cell communication system that controls gene expression in many bacterial species, mediated by diffusible signal molecules. Although the intracellular regulatory mechanisms of QS are often well-understood, the functional roles of QS remain controversial. In particular, the use of multiple signals by many bacterial species poses a serious challenge to current functional theories. Here, we address this challenge by showing that bacteria can use multiple QS signals to infer both their social (density) and physical (mass-transfer) environment. Analytical and evolutionary simulation models show that the detection of, and response to, complex social/physical contrasts requires multiple signals with distinct half-lives and combinatorial (nonadditive) responses to signal concentrations. We test these predictions using the opportunistic pathogen Pseudomonas aeruginosa and demonstrate significant differences in signal decay between its two primary signal molecules, as well as diverse combinatorial responses to dual-signal inputs. QS is associated with the control of secreted factors, and we show that secretome genes are preferentially controlled by synergistic “AND-gate” responses to multiple signal inputs, ensuring the effective expression of secreted factors in high-density and low mass-transfer environments. Our results support a new functional hypothesis for the use of multiple signals and, more generally, show that bacteria are capable of combinatorial communication.

Colour patterns do not diagnose species: quantitative evaluation of a DNA barcoded cryptic bumblebee complex

Cryptic diversity within bumblebees (Bombus) has the potential to undermine crucial conservation efforts designed to reverse the observed decline in many bumblebee species worldwide. Central to such efforts is the ability to correctly recognise and diagnose species. The B. lucorum complex (Bombus lucorum, B. cryptarum and B. magnus) comprises one of the most abundant and important group of wild plant and crop pollinators in northern Europe. Although the workers of these species are notoriously difficult to diagnose morphologically, it has been claimed that queens are readily diagnosable from morphological characters. Here we assess the value of colour-pattern characters in species identification of DNA-barcoded queens from the B. lucorum complex. Three distinct molecular operational taxonomic units were identified each representing one species. However, no uniquely diagnostic colour-pattern character state was found for any of these three molecular units and most colour-pattern characters showed continuous variation among the units. All characters previously deemed to be unique and diagnostic for one species were displayed by specimens molecularly identified as a different species. These results presented here raise questions on the reliability of species determinations in previous studies and highlights the benefits of implementing DNA barcoding prior to ecological, taxonomic and conservation studies of these important key pollinators.

The biogeography of polymicrobial infection

Microbial communities are spatially organized in both the environment and the human body. Although patterns exhibited by these communities are described by microbial biogeography, this discipline has previously only considered large-scale, global patterns. By contrast, the fine-scale positioning of a pathogen within an infection site can greatly alter its virulence potential. In this Review, we highlight the importance of considering spatial positioning in the study of polymicrobial infections and discuss targeting biogeography as a therapeutic strategy.

Collective sensing and collective responses in quorum-sensing bacteria

Bacteria often face fluctuating environments, and in response many species have evolved complex decision-making mechanisms to match their behaviour to the prevailing conditions. Some environmental cues provide direct and reliable information (such as nutrient concentrations) and can be responded to individually. Other environmental parameters are harder to infer and require a collective mechanism of sensing. In addition, some environmental challenges are best faced by a group of cells rather than an individual. In this review, we discuss how bacteria sense and overcome environmental challenges as a group using collective mechanisms of sensing, known as ‘quorum sensing’ (QS). QS is characterized by the release and detection of small molecules, potentially allowing individuals to infer environmental parameters such as density and mass transfer. While a great deal of the molecular mechanisms of QS have been described, there is still controversy over its functional role. We discuss what QS senses and how, what it controls and why, and how social dilemmas shape its evolution. Finally, there is a growing focus on the use of QS inhibitors as antibacterial chemotherapy. We discuss the claim that such a strategy could overcome the evolution of resistance. By linking existing theoretical approaches to data, we hope this review will spur greater collaboration between experimental and theoretical researchers.

Cooperation and the evolution of intelligence

The high levels of intelligence seen in humans, other primates, certain cetaceans and birds remain a major puzzle for evolutionary biologists, anthropologists and psychologists. It has long been held that social interactions provide the selection pressures necessary for the evolution of advanced cognitive abilities (the ‘social intelligence hypothesis’), and in recent years decision-making in the context of cooperative social interactions has been conjectured to be of particular importance. Here we use an artificial neural network model to show that selection for efficient decision-making in cooperative dilemmas can give rise to selection pressures for greater cognitive abilities, and that intelligent strategies can themselves select for greater intelligence, leading to a Machiavellian arms race. Our results provide mechanistic support for the social intelligence hypothesis, highlight the potential importance of cooperative behaviour in the evolution of intelligence and may help us to explain the distribution of cooperation with intelligence across taxa.

Building the microbiome in health and disease: niche construction and social conflict in bacteria.

Microbes collectively shape their environment in remarkable ways via the products of their metabolism. The diverse environmental impacts of macro-organisms have been collated and reviewed under the banner of ‘niche construction’. Here, we identify and review a series of broad and overlapping classes of bacterial niche construction, ranging from biofilm production to detoxification or release of toxins, enzymes, metabolites and viruses, and review their role in shaping microbiome composition, human health and disease. Some bacterial niche-constructing traits can be seen as extended phenotypes, where individuals actively tailor their environment to their benefit (and potentially to the benefit of others, generating social dilemmas). Other modifications can be viewed as non-adaptive by-products from a producer perspective, yet they may lead to remarkable within-host environmental changes. We illustrate how social evolution and niche construction perspectives offer complementary insights into the dynamics and consequences of these traits across distinct timescales. This review highlights that by understanding the coupled bacterial and biochemical dynamics in human health and disease we can better manage host health.

Cooperative secretions facilitate host range expansion in bacteria

The majority of emergent human pathogens are zoonotic in origin, that is, they can transmit to humans from other animals. Understanding the factors underlying the evolution of pathogen host range is therefore of critical importance in protecting human health. There are two main evolutionary routes to generalism: organisms can tolerate multiple environments or they can modify their environments to forms to which they are adapted. Here we use a combination of theory and a phylogenetic comparative analysis of 191 pathogenic bacterial species to show that bacteria use cooperative secretions that modify their environment to extend their host range and infect multiple host species. Our results suggest that cooperative secretions are key determinants of host range in bacteria, and that monitoring for the acquisition of secreted proteins by horizontal gene transfer can help predict emerging zoonoses.

Beyond killing: Can we find new ways to manage infection?

The antibiotic pipeline is running dry and infectious disease remains a major threat to public health. An efficient strategy to stay ahead of rapidly adapting pathogens should include approaches that replace, complement or enhance the effect of both current and novel antimicrobial compounds. In recent years, a number of innovative approaches to manage disease without the aid of traditional antibiotics and without eliminating the pathogens directly have emerged. These include disabling pathogen virulence-factors, increasing host tissue damage control or altering the microbiota to provide colonization resistance, immune resistance or disease tolerance against pathogens. We discuss the therapeutic potential of these approaches and examine their possible consequences for pathogen evolution. To guarantee a longer half-life of these alternatives to directly killing pathogens, and to gain a full understanding of their population-level consequences, we encourage future work to incorporate evolutionary perspectives into the development of these treatments.

Vultures acquire information on carcass location from scavenging eagles

Vultures are recognized as the scroungers of the natural world, owing to their ecological role as obligate scavengers. While it is well known that vultures use intraspecific social information as they forage, the possibility of inter-guild social information transfer and the resulting multi-species social dilemmas has not been explored. Here, we use data on arrival times at carcasses to show that such social information transfer occurs, with raptors acting as producers of information and vultures acting as scroungers of information. We develop a game-theoretic model to show that competitive asymmetry, whereby vultures dominate raptors at carcasses, predicts this evolutionary outcome. We support this theoretical prediction using empirical data from competitive interactions at carcasses. Finally, we use an individual-based model to show that these producer–scrounger dynamics lead to vultures being vulnerable to declines in raptor populations. Our results show that social information transfer can lead to important non-trophic interactions among species and highlight important potential links among social evolution, community ecology and conservation biology. With vulture populations suffering global declines, our study underscores the importance of ecosystem-based management for these endangered keystone species.