QUARTERLY REVIEW OF BIOLOGY

THE EXPOSOME IN HUMAN EVOLUTION: FROM DUST TO DIESEL
Trumble BC and Finch CE
Global exposures to air pollution and cigarette smoke are novel in human evolutionary history and are associated with about 16 million premature deaths per year. We investigate the history of the human for relationships between novel environmental toxins and genetic changes during human evolution in six phases. Phase I: With increased walking on savannas, early human ancestors inhaled crustal dust, fecal aerosols, and spores; carrion scavenging introduced new infectious pathogens. Phase II: Domestic fire exposed early to novel toxins from smoke and cooking. Phases III and IV: Neolithic to preindustrial sapiens incurred infectious pathogens from domestic animals and dense communities with limited sanitation. Phase V: Industrialization introduced novel toxins from fossil fuels, industrial chemicals, and tobacco at the same time infectious pathogens were diminishing. Thereby, pathogen-driven causes of mortality were replaced by chronic diseases driven by sterile inflammogens, exogenous and endogenous. Phase VI: Considers future health during global warming with increased air pollution and infections. We hypothesize that adaptation to some ancient toxins persists in genetic variations associated with inflammation and longevity.
PRINCIPLES AND PATTERNS OF BAT MOVEMENTS: FROM AERODYNAMICS TO ECOLOGY
Voigt CC, Frick WF, Holderied MW, Holland R, Kerth G, Mello MAR, Plowright RK, Swartz S and Yovel Y
Movement ecology as an integrative discipline has advanced associated fields because it presents not only a conceptual framework for understanding movement principles but also helps formulate predictions about the consequences of movements for animals and their environments. Here, we synthesize recent studies on principles and patterns of bat movements in context of the movement ecology paradigm. The motion capacity of bats is defined by their highly articulated, flexible wings. Power production during flight follows a U-shaped curve in relation to speed in bats yet, in contrast to birds, bats use mostly exogenous nutrients for sustained flight. The navigation capacity of most bats is dominated by the echolocation system, yet other sensory modalities, including an iron-based magnetic sense, may contribute to navigation depending on a bat's familiarity with the terrain. Patterns derived from these capacities relate to antagonistic and mutualistic interactions with food items. The navigation capacity of bats may influence their sociality, in particular, the extent of group foraging based on eavesdropping on conspecifics' echolocation calls. We infer that understanding the movement ecology of bats within the framework of the movement ecology paradigm provides new insights into ecological processes mediated by bats, from ecosystem services to diseases.
New Weapons in the Toad Toolkit: A Review of Methods to Control and Mitigate the Biodiversity Impacts of Invasive Cane Toads (Rhinella Marina)
Tingley R, Ward-Fear G, Schwarzkopf L, Greenlees MJ, Phillips BL, Brown G, Clulow S, Webb J, Capon R, Sheppard A, Strive T, Tizard M and Shine R
Our best hope of developing innovative methods to combat invasive species is likely to come from the study of high-profile invaders that have attracted intensive research not only into control, but also basic biology. Here we illustrate that point by reviewing current thinking about novel ways to control one of the world’s most well-studied invasions: that of the cane toad in Australia. Recently developed methods for population suppression include more effective traps based on the toad’s acoustic and pheromonal biology. New tools for containing spread include surveillance technologies (e.g., eDNA sampling and automated call detectors), as well as landscape-level barriers that exploit the toad’s vulnerability to desiccation—a strategy that could be significantly enhanced through the introduction of sedentary, range-core genotypes ahead of the invasion front. New methods to reduce the ecological impacts of toads include conditioned taste aversion in free-ranging predators, gene banking, and targeted gene flow. Lastly, recent advances in gene editing and gene drive technology hold the promise of modifying toad phenotypes in ways that may facilitate control or buffer impact. Synergies between these approaches hold great promise for novel and more effective means to combat the toad invasion and its consequent impacts on biodiversity.
Competition for vitamin B1 (thiamin) structures numerous ecological interactions
Kraft CE and Angert ER
Thiamin (vitamin B1) is a cofactor required for essential biochemical reactions in all living organisms, yet free thiamin is scarce in the environment. The diversity of biochemical pathways involved in the acquisition, degradation, and synthesis of thiamin indicates that organisms have evolved numerous ecological strategies for meeting this nutritional requirement. In this review we synthesize information from multiple disciplines to show how the complex biochemistry of thiamin influences ecological outcomes of interactions between organisms in environments ranging from the open ocean and the Australian outback to the gastrointestinal tract of animals. We highlight population and ecosystem responses to the availability or absence of thiamin. These include widespread mortality of fishes, birds, and mammals, as well as the thiamin-dependent regulation of ocean productivity. Overall, we portray thiamin biochemistry as the foundation for molecularly mediated ecological interactions that influence survival and abundance of a vast array of organisms.
Review of Methods in Enzymology Volumes 551 and 552 Circadian Rhythms and Biological Clocks, Part A and B Edited by Amita Sehgal
Crane BR
Polydactyly in Development, Inheritance, and Evolution
Lange A and Müller GB
The occurrence of supernumerary digits or toes in humans and other tetrapods has attracted general interest since antiquity and later influenced scientific theories of development, inheritance, and evolution. Seventeenth-century genealogical studies of polydactyly were at the beginning of an understanding of the rules of inheritance. Features of polydactyly were also part of the classical disputes on the nature of development, including the preformation-versus-epigenesis and the atavism-versus-malformation debates. In the evolutionary domain, polydactyly was used in the criticism of the gradualist account of variation underlying Darwin’s theory. Today, extra digit formation plays a role in the conceptualization of gene regulation and pattern formation in vertebrate limb evolution. Recent genetic, experimental, and modeling accounts of extra digit formation highlight the existence of nongradual transitions in phenotypic states, suggesting a distinction between continuous and discontinuous variation in evolution. Unless otherwise noted, all translations are our own.
The Role of Brood in Eusocial Hymenoptera
Schultner E, Oettler J and Helanterä H
Study of social traits in offspring traditionally reflects on interactions in simple family groups, with famous examples including parent-offspring conflict and sibling rivalry in birds and mammals. In contrast, studies of complex social groups such as the societies of ants, bees, and wasps focus mainly on adults and, in particular, on traits and interests of queens and workers. The social role of developing individuals in complex societies remains poorly understood. We attempt to fill this gap by illustrating that development in social Hymenoptera constitutes a crucial life stage with important consequences for the individual as well as the colony. We begin by describing the complex social regulatory network that modulates development in Hymenoptera societies. By highlighting the inclusive fitness interests of developing individuals, we show that they may differ from those of other colony members. We then demonstrate that offspring have evolved specialized traits that allow them to play a functional, cooperative role within colonies and give them the potential power to act toward increasing their inclusive fitness. We conclude by providing testable predictions for investigating the role of brood in colony interactions and giving a general outlook on what can be learned from studying offspring traits in hymenopteran societies.
Patterns and Processes in Nocturnal and Crepuscular Pollination Services
Borges RM, Somanathan H and Kelber A
Night, dawn, and dusk have abiotic features that differ from the day. Illumination, wind speeds, turbulence, and temperatures are lower while humidity may be higher at night. Nocturnal pollination occurred in 30% of angiosperm families across 68% of orders, 97% of families with C3, two-thirds of families with crassulacean acid metabolism (CAM), and 71% dicot families with C4 photosynthesis. Despite its widespread occurence, nocturnal pollination occurs in more families with xerophytic adaptations than helophytes or mesophytes, suggesting that nocturnal flowering is primarily an adaptation to water stress since flowering is a water-intensive process. We propose the arid or water stress hypothesis for nocturnal flowering suggesting that plants facing water stress in a habitat (e.g., deserts) or a habitat stratum (e.g., upper canopy for epiphytes) gain a selective advantage by nocturnal flowering by reducing water loss through evapotranspiration, leading to larger flowers that provide more nectar or other resources, to support pollinators with higher rewards. Contrary to the wide taxonomic occurrence of nocturnal flowering, few animal taxa serve as nocturnal pollinators. We discuss the sensory and physiological abilities that enable pollinator movement, navigation, and detection of flowers within the nocturnal temporal niche and present a unified framework for investigation of nocturnal flowering and pollination.
Reverse Engineering the Febrile System
Shepard AM, Bharwani A, Durisko Z and Andrews PW
Fever, the elevation of core body temperature by behavioral or physiological means, is one of the most salient aspects of human sickness, yet there is debate regarding its functional role. In this paper, we demonstrate that the febrile system is an evolved adaptation shaped by natural selection to coordinate the immune system to fight pathogens. First, we show that previous arguments in favor of fever being an adaptation are epistemologically inadequate, and we describe how an adaptationist strategy addresses this issue more effectively. Second, we argue that the mechanisms producing fever provide clear indications of adaptation. Third, we demonstrate that there are many beneficial immune system responses activated during fever and that these responses are not mere byproducts of heat on chemical reactions. Rather, we show that natural selection appears to have modified several immune system effects to be coordinated by fever. Fourth, we argue that there are some adaptations that coordinate the febrile system with other important fitness components, particularly growth and reproduction. Finally, we discuss evidence that the febrile system may also have evolved an antitumor function, providing suggestions for future research into this area. This research informs the debate on the functional value of fever and antipyretic use.
Landscape Demography: Population Change and its Drivers Across Spatial Scales
Gurevitch J, Fox GA, Fowler NL and Graham CH
Demographic studies of plants and animals have a rich history and literature in ecology, and are important for both fundamental and applied ecology and conservation biology. Almost all demographic work has focused on intensive studies in which births, deaths, growth of individuals, and related measures are quantified in a single population or a few populations. This has been for practical reasons due to the high demands of labor required for this work, and because the questions addressed in these studies have been asked at the level of individual populations, with implicit assumptions about generalizing from the results. We introduce the concept of landscape demography, the study of the demographic properties of populations and their drivers at multiple spatial scales, and of how the relationships among populations and their drivers at any one scale influence demographic outcomes at other scales. We explore the ways in which considering the dynamics of ensembles of populations at different spatial scales can advance progress in thinking about ecological issues of high current interest such as biological invasions, range expansions and contractions due to climate change, and the decline of threatened species, as well as fundamental ecological and evolutionary questions.
Four Commentaries on the Pope’s Message on Climate Change and Income Inequality. II. Integrating Ecology and Justice: The Papal Encyclical
Tucker ME and Grim J
Four Commentaries on the Pope’s Message on Climate Change and Income Inequality. III. Earth Stewardship and Laudato Si’
DeWitt CB
Four Commentaries on the Pope’s Message on Climate Change and Income Inequality. IV. Pope Francis’ Encyclical Letter Laudato Si’, Global Environmental Risks, and the Future of Humanity
Ceballos G
Evolution of Sex-Biased Dispersal
Trochet A, Courtois EA, Stevens VM, Baguette M, Chaine A, Schmeller DS and Clobert J
Dispersal is central in ecology and evolution because it influences population regulation, adaptation, and speciation. In many species, dispersal is different between genders, leading to sex-biased dispersal. Several theoretical hypotheses have been proposed to explain the evolution of this bias: the resource competition hypothesis proposed by Greenwood, the local mate competition hypothesis, and the inbreeding avoidance hypothesis. Those hypotheses argued that the mating system should be the major factor explaining the direction of such bias. Sociality and the presence of handicap in genders (exaggerated sexual characters or parental care) have recently been proposed to be linked with the direction of this bias. We tested these expected coevolutions using a database of 257 species. Based on phylogenetic approaches, our findings marginally corroborated Greenwood’s hypothesis by showing relationships between the direction of sex-biased dispersal, mating systems, and territoriality. More importantly, our results highlighted that the evolution of this bias was more linked to parental care and sexual dimorphism. These traits were also found to be associated with mating systems, suggesting that sexual asymmetry in morphology and parental care might be the main determinant of the evolution of sex-biased dispersal across species and not mating systems per se, as proposed in Greenwood’s hypothesis.
Four Commentaries on the Pope’s Message on Climate Change and Income Inequality. I. Our World and Pope Francis’ Encyclical, Laudato si’
Raven PH
From the Neutral Theory to a Comprehensive and Multiscale Theory of Ecological Equivalence
Munoz F and Huneman P
The neutral theory of biodiversity assumes that coexisting organisms are equally able to survive, reproduce, and disperse (ecological equivalence), but predicts that stochastic fluctuations of these abilities drive diversity dynamics. It predicts remarkably well many biodiversity patterns, although substantial evidence for the role of niche variation across organisms seems contradictory. Here, we discuss this apparent paradox by exploring the meaning and implications of ecological equivalence. We address the question whether neutral theory provides an explanation for biodiversity patterns and acknowledges causal processes. We underline that ecological equivalence, although central to neutral theory, can emerge at local and regional scales from niche-based processes through equalizing and stabilizing mechanisms. Such emerging equivalence corresponds to a weak conception of neutral theory, as opposed to the assumption of strict equivalence at the individual level in strong conception. We show that this duality is related to diverging views on hypothesis testing and modeling in ecology. In addition, the stochastic dynamics exposed in neutral theory are pervasive in ecological systems and, rather than a null hypothesis, ecological equivalence is best understood as a parsimonious baseline to address biodiversity dynamics at multiple scales.
RESILIENCE TO DROUGHTS IN MAMMALS: A CONCEPTUAL FRAMEWORK FOR ESTIMATING VULNERABILITY OF A SINGLE SPECIES
Rymer TL, Pillay N and Schradin C
ABSTRACT The frequency and severity of droughts in certain areas is increasing as a consequence of climate change. The associated environmental challenges, including high temperatures, low food, and water availability, have affected, and will affect, many populations. Our aims are to review the behavioral, physiological, and morphological adaptations of mammals to arid environments, and to aid research- ers and nature conservationists about which traits they should study to assess whether or not their study species will be able to cope with droughts. We provide a suite of traits that should be considered when making predictions about species resilience to drought. We define and differentiate between general adaptations, specialized adaptations, and exaptations, and argue that specialized adaptations are of little interest in establishing how nondesert specialists will cope with droughts. Attention should be placed on general adaptations of semidesert species and assess whether these exist as exaptations in nondesert species. We conclude that phenotypic flexibility is the most important general adaptation that may promote species resilience. Thus, to assess whether a species will be able to cope with increasing aridity, it is important to establish the degree offlexibility of traits identified in semidesert species that confer afitness advantage under drying conditions.
Yes! There are resilient generalizations (or "laws") in ecology
Linquist S, Gregory TR, Elliott TA, Saylor B, Kremer SC and Cottenie K
ABSTRACT It is often argued that ecological communities admit of no useful generalizations or "laws" because these systems are especially prone to contingent historical events. Detractors respond that this argument assumes an overly stringent definition of laws of nature. Under a more relaxed conception, it is argued that ecological laws emerge at the level of communities and elsewhere. A brief review of this debate reveals an issue with deep philosophical roots that is unlikely to be resolved by a better understanding of generalizations in ecology. We therefore propose a strategy for transforming the conceptual question about the nature of ecological laws into a set of empirically tractable hypotheses about the relative re- silience of ecological generalizations across three dimensions: taxonomy, habitat type, and scale. These hypotheses are tested using a survey of 240 meta-analyses in ecology. Our central finding is that generalizations in community ecology are just as prevalent and as resilient as those in population or ecosystem ecology. These findings should help to establish community ecology as a generality-seeking science as opposed to a science of case studies. It also supports the capacity for ecologists, working at any of the three levels, to inform matters of public policy.
DO SYMPTOMS OF ILLNESS SERVE SIGNALING FUNCTIONS? (HINT: YES)
Tiokhin L
Symptoms of illness provide information about an organism's underlying state. This notion has inspired a burgeoning body of research on organisms' adaptations for detecting and changing behavior toward ill individuals. However, little attention has been paid to a likely outcome of these dynamics. Once an organism's fitness is affected by others' responses to symptoms of illness, natural selection can favor individuals who alter symptom expression to influence the behavior of others. That is, many symptoms may originate as cues, but will evolve into signals. In this paper, I develop the hypothesis that symptoms of illness serve signaling functions, and provide a comprehensive review of relevant evidence from diverse disciplines. I also develop novel empirical predictions generated by this hypothesis and discuss its implications for public health. Signaling provides an ultimate explanation for otherwise opaque aspects of symptom expression, such as why symptoms fluctuate in social contexts, and can exist without underlying pathology, and why individuals deliberately generate symptoms of illness. This analysis suggests that signaling theory is a major organizing framework for understanding symptom etiology.
INSURMOUNTABLE HEAT: THE EVOLUTION AND PERSISTENCE OF DEFENSIVE HYPERTHERMIA
Clint E and Fessler DM
Fever, the rise in body temperature set point in response to infection or injury, is a highly conserved trait among vertebrates, and documented in many arthropods. Fever is known to reduce illness duration and mortality. These observations present an evolutionary puzzle: why has fever continued to be an effective response to fast-evolving pathogenic microbes across diverse phyla, and probably over countless millions of years? Framing fever as part of a more general thermal manipulation strategy that we term defensive hyperthermia, we hypothesize that the solution lies in the independent contributions to pathogen fitness played by virulence and infectivity. A host organism deploying defensive hyperthermia alters the ecological environment of an invading pathogen. To the extent that the pathogen evolves to be able to function effectively at elevated temperatures, it disadvantages itself at infecting the next (thermonormative) host, becoming more likely to be thwarted by that host's immune system and outcompeted by wild ecotype conspecifics (a genetically distinct strain adapted to specific environmental conditions) that, although more vulnerable to elevated temperatures, operate more effectively at the host's normal temperature. We evaluate this hypothesis in light of existing evidence concerning pathogen thermal specialization, and discuss theoretical and translational implications of this model.
HOW MATE AVAILABILITY INFLUENCES FILIAL CANNIBALISM
Deal ND and Wong BB
Parents sometimes eat their young to reduce the consequences of brood overcrowding, for nutritional gain, and/or to redirect investment toward future reproduction. It has been predicted that filial cannibalism should be more prevalent when mate availability is high as parents can more easily replace consumed young. Reviewing the available evidence--which comes almost exclusively from studies of paternal caring fish--we find support in some species, but not others. To explain this, we hypothesize that sexual selection against filial cannibalism and/or the tendency to acquire larger broods under conditions of high mate availability discourages filial cannibalism. Additionally, filial cannibalism might occur when mate availability is low to facilitate survival until access to mates improves. Since attractiveness can also influence remating opportunities, we review its effect on filial cannibalism, finding that attractive parents engage in less filial cannibalism. More research is needed to determine if this relationship is a result of individuals showing adaptive plasticity in filial cannibalism based on self-perceived attractiveness, or if the attractiveness of individuals is reduced by their propensity to commit filial cannibalism. More generally, to advance our understanding of how mate availability influences filial cannibalism, future studies should also focus on a wider range of taxa.