Domestication as a model system for niche construction theory

Niche Construction Theory (NCT) provides a powerful conceptual framework for understanding how and why humans and target species entered into domesticatory relationships that have transformed Earth’s biota, landforms, and atmosphere, and shaped the trajectory of human cultural development. NCT provides fresh perspective on how niche-constructing behaviors of humans and plants and animals promote co-evolutionary interactions that alter selection pressures and foster genetic responses in domesticates. It illuminates the role of niche-altering activities in bequeathing an ecological inheritance that perpetuates the co-evolutionary relationships leading to domestication, especially as it pertains to traditional ecological knowledge and the transmission of learned behaviors aimed at enhancing returns from local environments. NCT also provides insights into the contexts and mechanisms that promote cooperative interactions in both humans and target species needed to sustain niche-constructing activities, ensuring that these activities produce an ecological inheritance in which domesticates play an increasing role. A NCT perspective contributes to on-going debates in the social sciences over explanatory frameworks for domestication, in particular as they pertain to issues of reciprocal causation, co-evolution, and the role of human intentionality. Reciprocally, domestication provides a model system for evaluating on-going debates in evolutionary biology concerning the impact of niche construction, phenotypic plasticity, extra-genetic inheritance, and developmental bias in shaping the direction and tempo of evolutionary change.     

Common trends in mutualism revealed by model associations between invertebrates and bacteria

Mutually beneficial interactions between microorganisms and animals are a conserved and ubiquitous feature of biotic systems. In many instances animals, including humans, are dependent on their microbial associates for nutrition, defense, or development. To maintain these vital relationships, animals have evolved processes that ensure faithful transmission of specific microbial symbionts between generations. Elucidating mechanisms of transmission and symbiont specificity has been aided by the study of experimentally tractable invertebrate animals with diverse and highly evolved associations with microorganisms. Here, we review several invertebrate model systems that contribute to our current understanding of symbiont transmission, recognition, and specificity. Although the details of transmission and symbiont selection vary among associations, comparisons of diverse mutualistic associations are revealing a number of common themes, including restriction of symbiont diversity during transmission and glycan–lectin interactions during partner selection and recruitment.     

Reviewing the ecological evidence base for management of emerging tropical zoonoses: Kyasanur Forest Disease in India as a case study

Zoonoses disproportionately affect tropical communities and are associated with human modification and use of ecosystems. Effective management is hampered by poor ecological understanding of disease transmission and often focuses on human vaccination or treatment. Better ecological understanding of multi-vector and multi-host transmission, social and environmental factors altering human exposure, might enable a broader suite of management options. Options may include “ecological interventions” that target vectors or hosts and require good knowledge of underlying transmission processes, which may be more effective, economical, and long lasting than conventional approaches. New frameworks identify the hierarchical series of barriers that a pathogen needs to overcome before human spillover occurs and demonstrate how ecological interventions may strengthen these barriers and complement human-focused disease control. We extend these frameworks for vector-borne zoonoses, focusing on Kyasanur Forest Disease Virus (KFDV), a tick-borne, neglected zoonosis affecting poor forest communities in India, involving complex communities of tick and host species. We identify the hierarchical barriers to pathogen transmission targeted by existing management. We show that existing interventions mainly focus on human barriers (via personal protection and vaccination) or at barriers relating to Kyasanur Forest Disease (KFD) vectors (tick control on cattle and at the sites of host (monkey) deaths). We review the validity of existing management guidance for KFD through literature review and interviews with disease managers. Efficacy of interventions was difficult to quantify due to poor empirical understanding of KFDV–vector–host ecology, particularly the role of cattle and monkeys in the disease transmission cycle. Cattle are hypothesised to amplify tick populations. Monkeys may act as sentinels of human infection or are hypothesised to act as amplifying hosts for KFDV, but the spatial scale of risk arising from ticks infected via monkeys versus small mammal reservoirs is unclear. We identified 19 urgent research priorities for refinement of current management strategies or development of ecological interventions targeting vectors and host barriers to prevent disease spillover in the future.     

Testing for spatial autocorrelation in ecological studies

We describe a statistical method appropriate for the analysis of spatial autocorrelation in data varying in time as well as space. In particular, the technique was developed lo address the issue of geographic synchrony in ecological variables that may change markedly from year to year such as population density of animals or seed production of trees. The method yields 'modified correlograms" that test for significant autocorrelation between sites located within any given range of distances apart. This technique facilitates detecting and understanding spatial processes m a variety of ecological phenomena, including testing the plausibility of causational hypotheses using cross-correlational analyses. Several examples are discussed, including population densities of squirrels in Finland, winter densities of two hawk species in California, and acorn production and radial growth by individual blue oak Quercus douglasii trees in central coastal California.     

Plants intertwine fluvial landform dynamics with ecological succession and natural selection: a niche construction perspective for riparian systems

Aim   To contribute to the development of a macroevolutionary framework for riparian systems, reinforcing conceptual linkages between earth surface processes and biological and ecological processes.
Location   Riparian systems.
Methods   Literature review leading to an original proposition for perceiving the functioning of riparian systems in a new and different way.
Results   Riparian systems provide diverse landforms, habitats and resources for animals and plants. Certain organisms, defined as 'ecosystem engineers', significantly create and modify the physical components of riparian systems. Many studies have highlighted such engineering effects by animals on riparian systems, but the identification and understanding of the effects and responses of plants within fluvial corridors have emerged only recently. The modulation of matter, resources and energy flows by engineering plants helps establish characteristic sequences of fluvial landform creation and maintenance associated with synergetic ecological successions. We relate this process to the concept of niche construction, developed mainly by evolutionary biologists. Feedbacks between adaptive responses of riparian plants to flow regime and adjusting effects on biostabilization and bioconstruction are discussed in the context of niche construction at the scale of ecological succession and the evolution of organisms.
Main conclusions   Our conceptualization forges an integrated approach for understanding vegetated fluvial systems from a macroevolutionary perspective, for elucidating riparian ecosystem dynamics and potentially for establishing long-term stream conservation and restoration strategies.     

A framework for the study of zoonotic disease emergence and its drivers: spillover of bat pathogens as a case study

Many serious emerging zoonotic infections have recently arisen from bats, including Ebola, Marburg, SARS-coronavirus, Hendra, Nipah, and a number of rabies and rabies-related viruses, consistent with the overall observation that wildlife are an important source of emerging zoonoses for the human population. Mechanisms underlying the recognized association between ecosystem health and human health remain poorly understood and responding appropriately to the ecological, social and economic conditions that facilitate disease emergence and transmission represents a substantial societal challenge. In the context of disease emergence from wildlife, wildlife and habitat should be conserved, which in turn will preserve vital ecosystem structure and function, which has broader implications for human wellbeing and environmental sustainability, while simultaneously minimizing the spillover of pathogens from wild animals into human beings. In this review, we propose a novel framework for the holistic and interdisciplinary investigation of zoonotic disease emergence and its drivers, using the spillover of bat pathogens as a case study. This study has been developed to gain a detailed interdisciplinary understanding, and it combines cutting-edge perspectives from both natural and social sciences, linked to policy impacts on public health, land use and conservation.     

Identifying Transmission Cycles at the Human-Animal Interface: The Role of Animal Reservoirs in Maintaining Gambiense Human African Trypanosomiasis

Many infections can be transmitted between animals and humans. The epidemiological roles of different species can vary from important reservoirs to dead-end hosts. Here, we present a method to identify transmission cycles in different combinations of species from field data. We used this method to synthesise epidemiological and ecological data from Bipindi, Cameroon, a historical focus of gambiense Human African Trypanosomiasis (HAT, sleeping sickness), a disease that has often been considered to be maintained mainly by humans. We estimated the basic reproduction number of gambiense HAT in Bipindi and evaluated the potential for transmission in the absence of human cases. We found that under the assumption of random mixing between vectors and hosts, gambiense HAT could not be maintained in this focus without the contribution of animals. This result remains robust under extensive sensitivity analysis. When using the distributions of species among habitats to estimate the amount of mixing between those species, we found indications for an independent transmission cycle in wild animals. Stochastic simulation of the system confirmed that unless vectors moved between species very rarely, reintroduction would usually occur shortly after elimination of the infection from human populations. This suggests that elimination strategies may have to be reconsidered as targeting human cases alone would be insufficient for control, and reintroduction from animal reservoirs would remain a threat. Our approach is broadly applicable and could reveal animal reservoirs critical to the control of other infectious diseases.     

HIV Treatment as Prevention: The Utility and Limitations of Ecological Observation

Results from several observational studies of HIV-discordant couples and a randomized controlled trial (HIV Prevention Trials Network 052) show that antiretroviral therapy (ART) can greatly reduce heterosexual HIV transmission in stable HIV-discordant couples. However, such data do not prove that ART will reduce HIV incidence at the population level. Observational investigations using ecological measures have been used to support the implementation of HIV treatment for the specific purpose of preventing transmission at the population level. Many of these studies note ecological associations between measures of increased ART uptake and decreased HIV transmission. Given the urgency of implementing HIV prevention measures, ecological studies must de facto be used to inform current strategies. However, the hypothesis that widespread ART can eliminate HIV infection may have raised expectations beyond what we may be able to achieve. Here we review and discuss the construct of the exposure and outcome measures and analysis methods used in ecological studies. By examining the strengths and weaknesses of ecological analyses, we aim to aid understanding of the findings from these studies to inform future policy decisions regarding the use of ART for HIV prevention.     

Ecology and Feeding Habits Drive Infection of Water Bugs with <Emphasis Type="Italic">Mycobacterium ulcerans</Emphasis>

Mycobacterium ulcerans (MU), the causative agent of Buruli ulcer, is present in a wide spectrum of environments, including terrestrial and aquatic ecosystems in tropical regions. The most promising studies on the epidemiological risk of this disease suggest that some ecological settings may favor infection of animals with MU including human. A species’ needs and impacts on resources and the environment, i.e., its ecological niche, may influence its susceptibility to be infected by this microbial form. For example, some Naucoridae may dive in fresh waters to prey upon infected animals and thus may get infected with MU. However, these studies have rarely considered that inference on the ecological settings favoring infection and transmission may be confounded because host carrier sister species have similar ecological niches, and potentially the same host–microbe interactions. Hence, a relationship between the ecological niche of Naucoridae and its infection with MU may be due to a symbiotic relationship between the host and the pathogen, rather than its ecological niche. To account for this confounding effect, we investigated the relationships between surrogates of the ecological niche of water bug species and their susceptibility to MU, by performing phylogenetic comparative analyses on a large dataset of 11 families of water bugs collected in 10 different sites across Cameroon, central Africa. Our results indicate that MU circulates and infects a couple of host taxa, i.e., Belostomatidae, Naucoridae, living both in the aquatic vegetation and as predators inside the trophic network and sister species of water bugs have indeed similar host–microbe interactions with MU.     

Transmission as a predictor of ecological host specificity with a focus on vertical transmission of microsporidia

Consideration of vertical transmission is particularly important for understanding the life cycles of entomopathogens that are naturally occurring in invertebrate populations, are a problem in beneficial insect colonies, or are under consideration as classical biological control agents. Empirical studies generally corroborate the evolutionary hypothesis that virulence should be relatively low for pathogen species that utilize vertical transmission as one mechanism for maintenance in the host population. Nevertheless, many entomopathogens with significant effects on host populations are vertically as well as horizontally transmitted. In addition to gaining a better understanding of pathogen-host interactions and population dynamics, studies of the host range and specificity of putative biological control agents can benefit by using transmission studies to better predict ecological host specificity from physiological data. Horizontal transmission requires a tightly organized host-pathogen relationship to succeed, but still involves, albeit restricted by host behavior and pathogen dosage, the physiological susceptibility of the nontarget host. Vertical transmission studies can provide increased stringency for determining the ecological host specificity of a species and may be one very accurate predictor of the ability of a pathogen to successfully host-switch when introduced into a na?ve population.     

Strategies of the home-team: symbioses exploited for vector-borne disease control

Symbioses between eukaryotes and unicellular organisms are quite common, with examples copiously disseminated throughout the earth's biota. Arthropods, in particular, owe much of their ecological success to their microbial flora, which often provide supplements either lacking in the limited host diet or which the hosts are unable to synthesize. In addition to harboring beneficial microbes, many arthropods (vectors) also transmit pathogens to the animals and plants upon which they prey. Vector-borne diseases exact a high public health burden and additionally have a devastating impact on livestock and agriculture. Recent scientific discoveries have resulted in the development of powerful technologies for studying the vector's biology, to discover the weak links in disease transmission. One of the more challenging applications of these developments is transgenesis, which allows for insertion of foreign DNA into the insect's genome to modify its phenotype. In this review, we discuss an approach in which the naturally occurring commensal flora of insects are manipulated to express products that render their host environment inhospitable for pathogen transmission. Replacing susceptible insect genotypes with modified counterparts with reduced pathogen transmission ability, might provide a new set of armaments in the battle for vector-borne disease reduction.     

The ecological relevance of sleep: the trade-off between sleep,memory and energy conservation

All animals in which sleep has been studied express signs of sleep-like behaviour, suggesting that sleep must have some fundamental functions that are sustained by natural selection. Those functions, however, are still not clear. Here, we examine the ecological relevance of sleep from the perspective of behavioural trade-offs that might affect fitness. Specifically, we highlight the advantage of using food-caching animals as a system in which a conflict might occur between engaging in sleep for memory/learning and hypothermia/torpor to conserve energy. We briefly review the evidence for the importance of sleep for memory, the importance of memory for food-caching animals and the conflicts that might occur between sleep and energy conservation in these animals. We suggest that the food-caching paradigm represents a naturalistic and experimentally practical system that provides the opportunity for a new direction in sleep research that will expand our understanding of sleep, especially within the context of ecological and evolutionary processes.     

The origin of human pathogens: evaluating the role of agriculture and domestic animals in the evolution of human disease

Many significant diseases of human civilization are thought to have arisen concurrently with the advent of agriculture in human society. It has been hypothesised that the food produced by farming increased population sizes to allow the maintenance of virulent pathogens, i.e. civilization pathogens, while domestic animals provided sources of disease to humans. To determine the relationship between pathogens in humans and domestic animals, I examined phylogenetic data for several human pathogens that are commonly evolutionarily linked to domestic animals: measles, pertussis, smallpox, tuberculosis, taenid worms, and falciparal malaria. The majority are civilization pathogens, although I have included others whose evolutionary origins have traditionally been ascribed to domestic animals. The strongest evidence for a domestic-animal origin exists for measles and pertussis, although the data do not exclude a non-domestic origin. As for the other pathogens, the evidence currently available makes it difficult to determine if the domestic-origin hypothesis is supported or refuted; in fact, intriguing data for tuberculosis and taenid worms suggests that transmission may occur as easily from humans to domestic animals. These findings do not abrogate the importance of agriculture in disease transmission; rather, if anything, they suggest an alternative, more complex series of effects than previously elucidated. Rather than domestication, the broader force for human pathogen evolution could be ecological change, namely anthropogenic modification of the environment. This is supported by evidence that many current emerging infectious diseases are associated with human modification of the environment. Agriculture may have changed the transmission ecology of pre-existing human pathogens, increased the success of pre-existing pathogen vectors, resulted in novel interactions between humans and wildlife, and, through the domestication of animals, provided a stable conduit for human infection by wildlife diseases.     

Integrating data mining and transmission theory in the ecology of infectious diseases

Our understanding of ecological processes is built on patterns inferred from data. Applying modern analytical tools such as machine learning to increasingly high dimensional data offers the potential to expand our perspectives on these processes, shedding new light on complex ecological phenomena such as pathogen transmission in wild populations. Here, we propose a novel approach that combines data mining with theoretical models of disease dynamics. Using rodents as an example, we incorporate statistical differences in the life history features of zoonotic reservoir hosts into pathogen transmission models, enabling us to bound the range of dynamical phenomena associated with hosts, based on their traits. We then test for associations between equilibrium prevalence, a key epidemiological metric and data on human outbreaks of rodent‐borne zoonoses, identifying matches between empirical evidence and theoretical predictions of transmission dynamics. We show how this framework can be generalized to other systems through a rubric of disease models and parameters that can be derived from empirical data. By linking life history components directly to their effects on disease dynamics, our mining‐modelling approach integrates machine learning and theoretical models to explore mechanisms in the macroecology of pathogen transmission and their consequences for spillover infection to humans.     

Going through the motions: incorporating movement analyses into disease research

Though epidemiology dates back to the 1700s, most mathematical representations of epidemics still use transmission rates averaged at the population scale, especially for wildlife diseases. In simplifying the contact process, we ignore the heterogeneities in host movements that complicate the real world, and overlook their impact on spatiotemporal patterns of disease burden. Movement ecology offers a set of tools that help unpack the transmission process, letting researchers more accurately model how animals within a population interact and spread pathogens. Analytical techniques from this growing field can also help expose the reverse process: how infection impacts movement behaviours, and therefore other ecological processes like feeding, reproduction, and dispersal. Here, we synthesise the contributions of movement ecology in disease research, with a particular focus on studies that have successfully used movement‐based methods to quantify individual heterogeneity in exposure and transmission risk. Throughout, we highlight the rapid growth of both disease and movement ecology and comment on promising but unexplored avenues for research at their overlap. Ultimately, we suggest, including movement empowers ecologists to pose new questions, expanding our understanding of host–pathogen dynamics and improving our predictive capacity for wildlife and even human diseases.     

Epidemiological Risk Factors for Animal Influenza A Viruses Overcoming Species Barriers

Drivers and risk factors for Influenza A virus transmission across species barriers are poorly understood, despite the ever present threat to human and animal health potentially on a pandemic scale. Here we review the published evidence for epidemiological risk factors associated with influenza viruses transmitting between animal species and from animals to humans. A total of 39 papers were found with evidence of epidemiological risk factors for influenza virus transmission from animals to humans; 18 of which had some statistical measure associated with the transmission of a virus. Circumstantial or observational evidence of risk factors for transmission between animal species was found in 21 papers, including proximity to infected animals, ingestion of infected material and potential association with a species known to carry influenza virus. Only three publications were found which presented a statistical measure of an epidemiological risk factor for the transmission of influenza between animal species. This review has identified a significant gap in knowledge regarding epidemiological risk factors for the transmission of influenza viruses between animal species.     

Beyond ecological traps: perceptual errors and undervalued resources

Ecological traps arise when animals choose to settle in poor-quality habitats, leading to a reduction in their survival or productivity. Although this phenomenon has received comprehensive theoretical treatment in the recent literature, the corollary of the ecological trap (when animals choose to avoid good-quality habitats) is rarely discussed. Failure to recognize high-quality sites could influence the ability of a population to reach its threshold size. An exploration of this phenomenon brings new insights into existing cases of ecological traps. By considering the full range of pitfalls faced during settlement, the relationship between habitat quality and population size might become clearer. We argue here that an improved understanding of factors determining the colonization of high-quality sites could aid conservationists in mitigating the damaging effects of maladaptive habitat selection.     

DO TRADE‐OFFS HAVE EXPLANATORY POWER FOR THE EVOLUTION OF ORGANISMAL INTERACTIONS?

The concept of a trade-off has long played a prominent role in understanding the evolution of organismal interactions such as mutualism, parasitism, and competition. Given the complexity inherent to interactions between different evolutionary entities, ecological factors may especially limit the power of trade-off models to predict evolutionary change. Here, we use four case studies to examine the importance of ecological context for the study of trade-offs in organismal interactions: (1) resource-based mutualisms, (2) parasite transmission and virulence, (3) plant biological invasions, and (4) host range evolution in parasites and parasitoids. In the first two case studies, mechanistic trade-off models have long provided a strong theoretical framework but face the challenge of testing assumptions under ecologically realistic conditions. Work under the second two case studies often has a strong ecological grounding, but faces challenges in identifying or quantifying the underlying genetic mechanism of the trade-off. Attention is given to recent studies that have bridged the gap between evolutionary mechanism and ecological realism. Finally, we explore the distinction between ecological factors that mask the underlying evolutionary trade-offs, and factors that actually change the trade-off relationship between fitness-related traits important to organismal interactions.     

Impacts of human‐induced environmental change in wetlands on aquatic animals

Many wetlands harbour highly diverse biological communities and provide extensive ecosystem services; however, these important ecological features are being altered, degraded and destroyed around the world. Despite a wealth of research on how animals respond to anthropogenic changes to natural wetlands and how they use created wetlands, we lack a broad synthesis of these data. While some altered wetlands may provide vital habitat, others could pose a considerable risk to wildlife. This risk will be heightened if such wetlands are ecological traps – preferred habitats that confer lower fitness than another available habitat. Wetlands functioning as ecological traps could decrease both local and regional population persistence, and ultimately lead to extinctions. Most studies have examined how animals respond to changes in environmental conditions by measuring responses at the community and population levels, but studying ecological traps requires information on fitness and habitat preferences. Our current lack of knowledge of individual‐level responses may therefore limit our capacity to manage wetland ecosystems effectively since ecological traps require different management practices to mitigate potential consequences. We conducted a global meta‐analysis to characterise how animals respond to four key drivers of wetland alteration: agriculture, mining, restoration and urbanisation. Our overarching goal was to evaluate the ecological impacts of human alterations to wetland ecosystems, as well as identify current knowledge gaps that limit both the current understanding of these responses and effective wetland management. We extracted 1799 taxon‐specific response ratios from 271 studies across 29 countries. Community‐ (e.g. richness) and population‐level (e.g. density) measures within altered wetlands were largely comparable to those within reference wetlands. By contrast, individual fitness measures (e.g. survival) were often lower, highlighting the potential limitations of using only community‐ and population‐level measures to assess habitat quality. Only four studies provided habitat‐preference data, preventing investigation of the potential for altered wetlands to function as ecological traps. This is concerning because attempts to identify ecological traps may detect previously unidentified conservation risks. Although there was considerable variability amongst taxa, amphibians were typically the most sensitive taxon, and thus, may be a valuable bio‐indicator of wetland quality. Despite suffering reduced survival and reproduction, measures such as time to and mass at metamorphosis were similar between altered and reference wetlands, suggesting that quantifying metamorphosis‐related measures in isolation may not provide accurate information on habitat quality. Our review provides the most detailed evaluation to date of the ecological impacts of human alterations to wetland ecosystems. We emphasise that the role of wetlands in human‐altered ecosystems can be complex, as they may represent important habitat but also pose potential risks to animals. Reduced availability of natural wetlands is increasing the importance of altered wetlands for aquatic animals. Consequently, we need to define what represents habitat quality from the perspective of animals, and gain a greater understanding of the underlying mechanisms of habitat selection and how these factors could be manipulated. Furthermore, strategies to enhance the quality of these wetlands should be implemented to maximise their conservation potential.     

Weather Regulates Location,Timing, and Intensity of Dengue Virus Transmission between Humans and Mosquitoes

BackgroundDengue is one of the most aggressively expanding mosquito-transmitted viruses. The human burden approaches 400 million infections annually. Complex transmission dynamics pose challenges for predicting location, timing, and magnitude of risk; thus, models are needed to guide prevention strategies and policy development locally and globally. Weather regulates transmission-potential via its effects on vector dynamics. An important gap in understanding risk and roadblock in model development is an empirical perspective clarifying how weather impacts transmission in diverse ecological settings. We sought to determine if location, timing, and potential-intensity of transmission are systematically defined by weather.Conclusions/SignificanceLocal duration in limited areas of temperature-humidity weather-space identifies potential locations, timing, and magnitude of transmission. The weather-space profile of transmission-potential provides needed data that define a systematic and highly-sensitive weather-disease connection, demonstrating separate but coupled roles of temperature and humidity. New insights regarding natural regulation of human-mosquito transmission across diverse ecological settings advance our understanding of risk locally and globally for dengue and other mosquito-borne diseases and support advances in public health policy/operations, providing an evidence-base for modeling, predicting risk, and surveillance-prevention planning.