Acute or chronic? Within-host models with immune dynamics, infection outcome, and parasite evolution

There is ample theoretical and experimental evidence that virulence evolution depends on the immune response of the host. In this article, we review a number of recent studies that attempt to explicitly incorporate the dynamics of the immune system (instead of merely representing it by a single black box parameter) in models for the evolution of parasite virulence. A striking observation is that the type of infection (acute or chronic) is invariably considered to be a constraint that model assumptions have to satisfy rather than as a potential outcome of the interaction of the parasite with its host's immune system. We argue that avoiding making assumptions about the type of infection will lead to a better understanding of infectious diseases, even though a number of fundamental and technical problems remain. Dynamical modeling of the immune system opens a wide range of perspectives: for understanding how the immune system eradicates a parasite (which it does for most pathogens but not for all, HIV being a notorious example of a virus that is not completely eliminated), for studying multiple infections through concomitant immunity, for understanding the emergence and evolution of the immune system in animals, and for evolutionary epidemiology in general (e.g., predicting evolutionary consequences of new therapies and public health policies). We conclude by discussing new approaches based on embedded (or nested) models and identify future perspectives for the modeling of infectious diseases.     

The Inability of Primary School to Introduce Children to the Theory of Biological Evolution

A great number of research papers in the English literature of science education present difficulties pupils have in understanding natural selection. Studies show that children have essentialist and teleological intuitive ideas when dealing with organisms and that these biases hinder their ability to understand the theory of evolution by natural selection. Consequently, it is interesting to ascertain if and how the school education offered today deals with the problem, i.e., helps the children confront these biases. To that purpose, this study answered the two following research questions: (a) How is biological evolution presented—from the past to the present day—in the official documentation of primary school education, namely the science curricula and the textbooks of Greece? and (b) what are the conceptions held by Greek primary school teachers of the concepts of evolutionary theory and relevant issues that they have to teach? Our research found that not only are the intuitive ideas not “confronted” but they are also “affirmed” in Greek primary education. This phenomenon, as some other international studies have shown, must not be only a Greek one. A drastic change in the content and structure of primary school curricula and the training of educators is necessary in order to improve and facilitate the teaching of biological evolution.     

A Clinical Perspective in Evolutionary Medicine: What We Wish We Had Learned in Medical School

Medical students have much to gain by understanding how evolutionary principles affect human health and disease. Many theoretical and experimental studies have applied lessons from evolutionary biology to issues of critical importance to medical science. A firm grasp of evolution and natural selection is required to understand why the human body remains vulnerable to many diseases. Although we often integrate evolutionary concepts when we teach medical students and residents, the vast majority of medical students never receive any instruction on evolution. As a result, many trainees lack the tools to understand key advances and miss valuable opportunities for education and research. Here, we outline some of the evolutionary principles that we wished we had learned during our medical training.     

University Evolution Education: The Effect of Evolution Instruction on Biology Majors�� Content Knowledge, Attitude Toward Evolution, and Theistic Position

Issues regarding understanding of evolution and resistance to evolution education in the United States are of key importance to biology educators at all levels. While research has measured student views toward evolution at single points in time, few studies have been published investigating whether views of college seniors are any different than first-year students in the same degree program. Additionally, students choosing to major in biological sciences have largely been overlooked, as if their acceptance of evolution is assumed. This study investigated the understanding of evolution and attitude toward evolution held by students majoring in biological science during their first and fourth years in a public research university. Participants included students in a first-year introductory biology course intended for biological science majors and graduating seniors earning degrees in either biology or genetics. The portion of the survey reported here consisted of quantitative measures of students’ understanding of core concepts of evolution and their attitude toward evolution. The results indicate that students’ understanding of particular evolutionary concepts is significantly higher among seniors, but their attitude toward evolution is only slightly improved compared to their first-year student peers. When comparing first-year students and seniors, students’ theistic position was not significantly different.     

Using case-study based modules to promote a better understanding of evolution in an undergraduate anatomy and physiology course

ABSTRACT

The impact of evolutionary processes in understanding human health and disease is an important idea for future health professionals to understand. These students, however, typically receive little to no formal instruction in the role of evolution in not only understanding human health, but its impact on how to treat human diseases. To address this issue, we developed and implemented a case-study based learning module designed with a learning cycle implementation as part of a larger evolution across the curriculum program. The module focused on the evolution of skin color to illustrate that natural selection occurs in humans, and that the process of evolution involves tradeoffs (a balance of costs and benefits). Student understanding of the tradeoffs of natural selection was assessed through a pre- post- test design, with students answering a set of questions before instruction and again after. The modules helped improve student comprehension of natural selection, particularly for lower-performing students who were not biology majors, and for those whom reported less interest in evolution.     

Evolution and medicine in undergraduate education: a prescription for all biology students

The interface between evolutionary biology and the biomedical sciences promises to advance understanding of the origins of genetic and infectious diseases in humans, potentially leading to improved medical diagnostics, therapies, and public health practices. The biomedical sciences also provide unparalleled examples for evolutionary biologists to explore. However, gaps persist between evolution and medicine, for historical reasons and because they are often perceived as having disparate goals. Evolutionary biologists have a role in building a bridge between the disciplines by presenting evolutionary biology in the context of human health and medical practice to undergraduates, including premedical and preprofessional students. We suggest that students will find medical examples of evolution engaging. By making the connections between evolution and medicine clear at the undergraduate level, the stage is set for future health providers and biomedical scientists to work productively in this synthetic area. Here, we frame key evolutionary concepts in terms of human health, so that biomedical examples may be more easily incorporated into evolution courses or more specialized courses on evolutionary medicine. Our goal is to aid in building the scientific foundation in evolutionary biology for all students, and to encourage evolutionary biologists to join in the integration of evolution and medicine.     

Students’ Mental Models of Evolutionary Causation: Natural Selection and Genetic Drift

In an effort to understand how to improve student learning about evolution, a focus of science education research has been to document and address students?? naive ideas. Less research has investigated how students reason about alternative scientific models that attempt to explain the same phenomenon (e.g., which causal model best accounts for evolutionary change?). Within evolutionary biology, research has yet to explore how non-adaptive factors are situated within students?? conceptual ecologies of evolutionary causation. Do students construct evolutionary explanations that include non-adaptive and adaptive factors? If so, how are non-adaptive factors structured within students?? evolutionary explanations? We used clinical interviews and two paper and pencil instruments (one open-response and one multiple-choice) to investigate the use of non-adaptive and adaptive factors in undergraduate students?? patterns of evolutionary reasoning. After instruction that included non-adaptive causal factors (e.g., genetic drift), we found them to be remarkably uncommon in students?? explanatory models of evolutionary change in both written assessments and clinical interviews. However, consistent with many evolutionary biologists?? explanations, when students used non-adaptive factors they were conceptualized as causal alternatives to selection. Interestingly, use of non-adaptive factors was not associated with greater understanding of natural selection in interviews or written assessments, or with fewer naive ideas of natural selection. Thus, reasoning using non-adaptive factors appears to be a distinct facet of evolutionary thinking. We propose a theoretical framework for an expert?Cnovice continuum of evolutionary reasoning that incorporates both adaptive and non-adaptive factors, and can be used to inform instructional efficacy in evolutionary biology.     

Education Is Life Itself: Biological Evolution as a Model for Human Learning

Schooling often rests uneasily on presumed dichotomies between coverage and inquiry, skill development, and creativity. By drawing on the often under-recognized parallels between biological evolution and human learning, this essay argues that formal education needs and ought not to forego the unconscious exploratory processes of informal learning. Rather than posit as natural the cultural story that formal schooling must prepare students to integrate with given cultures and foreknowable futures, the evolutionary perspective shows that education is better thought of as preparing students to create cultures and to change, and foster change, in relation to unknown futures. The properties that distinguish formal from informal learning—conscious reflection and a degree of collective consensus about what constitutes knowledge at any given time—are, we argue, useful not as ends in themselves, but as tools for maximizing, sharing, and extending unconscious, evolutionary learning. Working with them as such offers a way out of some of education’s persistent problems. Two autobiographical case studies provide examples of these evolutionary changes and indicate pathways of inquiry by which to pursue them.     

Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidae

Predicting the host range for herbivores has been a major aim of research into plant-herbivore interactions and an important model system for understanding the evolution of feeding specialization. Among many terrestrial insects, host range is strongly affected by herbivore phylogeny and long historical associations between particular herbivore and plant taxa. For small herbivores in marine environments, it is known that the evolution of host use is sculpted by several ecological factors (e.g., food quality, value as a refuge from predators, and abiotic forces), but the potential for phylogenetic constraints on host use remains largely unexplored. Here, we analyze reports of host use of herbivorous amphipods from the family Ampithoidae (102 amphipod species from 12 genera) to test the hypotheses that host breadth and composition vary among herbivore lineages, and to quantify the extent to which nonpolar secondary metabolites mediate these patterns. The family as a whole, and most individual species, are found on a wide variety of macroalgae and seagrasses. Despite this polyphagous host use, amphipod genera consistently differed in host range and composition. As an example, the genus Peramphithoe rarely use available macrophytes in the order Dictyotales (e.g., Dictyota) and as a consequence, display a more restricted host range than do other genera (e.g., Ampithoe, Cymadusa, or Exampithoe). The strong phylogenetic effect on host use was independent of the uneven distribution of host taxa among geographic regions. Algae that produced nonpolar secondary metabolites were colonized by higher numbers of amphipod species relative to chemically poor genera, consistent with the notion that secondary metabolites do not provide algae an escape from amphipod herbivory. In contrast to patterns described for some groups of phytophagous insects, marine amphipods that use chemically rich algae tended to have broader, not narrower, host ranges. This result suggests that an evolutionary advantage to metabolite tolerance in marine amphipods may be that it increases the availability of appropriate algal hosts (i.e., enlarges the resource base).     

Evolution of multihost parasites

Multihost parasites can infect different types of hosts or even different host species. Epidemiological models have shown the importance of the diversity of potential hosts for understanding the dynamics of infectious disease (e.g., the importance of reservoirs), but the consequences of this diversity for virulence and transmission evolution remain largely overlooked. Here, I present a general theoretical framework for the study of life-history evolution of multihost parasites. This analysis highlights the importance of epidemiology (the relative quality and quantity of different types of infected hosts) and between-trait constraints (both within and between different hosts) to parasite evolution. I illustrate these effects in different transmission scenarios under the simplifying assumption that parasites can infect only two types of hosts. These simple but contrasted evolutionary scenarios yield new insights into virulence evolution and the evolution of transmission routes among different hosts. Because many of the pathogens that have large public-health and agricultural impacts have complex life cycles, an understanding of their evolutionary dynamics could hold substantial benefits for management.     

Coevolutionary cycling of host sociality and pathogen virulence in contact networks

Infectious diseases may place strong selection on the social organization of animals. Conversely, the structure of social systems can influence the evolutionary trajectories of pathogens. While much attention has focused on the evolution of host sociality or pathogen virulence separately, few studies have looked at their coevolution. Here we use an agent-based simulation to explore host-pathogen coevolution in social contact networks. Our results indicate that under certain conditions, both host sociality and pathogen virulence exhibit continuous cycling. The way pathogens move through the network (e.g., their interhost transmission and probability of superinfection) and the structure of the network can influence the existence and form of cycling.     

Vector-Borne Pathogen and Host Evolution in a Structured Immuno-Epidemiological System

Vector-borne disease transmission is a common dissemination mode used by many pathogens to spread in a host population. Similar to directly transmitted diseases, the within-host interaction of a vector-borne pathogen and a host’s immune system influences the pathogen’s transmission potential between hosts via vectors. Yet there are few theoretical studies on virulence–transmission trade-offs and evolution in vector-borne pathogen–host systems. Here, we consider an immuno-epidemiological model that links the within-host dynamics to between-host circulation of a vector-borne disease. On the immunological scale, the model mimics antibody-pathogen dynamics for arbovirus diseases, such as Rift Valley fever and West Nile virus. The within-host dynamics govern transmission and host mortality and recovery in an age-since-infection structured host-vector-borne pathogen epidemic model. By considering multiple pathogen strains and multiple competing host populations differing in their within-host replication rate and immune response parameters, respectively, we derive evolutionary optimization principles for both pathogen and host. Invasion analysis shows that the \({\mathcal {R}}_0\) maximization principle holds for the vector-borne pathogen. For the host, we prove that evolution favors minimizing case fatality ratio (CFR). These results are utilized to compute host and pathogen evolutionary trajectories and to determine how model parameters affect evolution outcomes. We find that increasing the vector inoculum size increases the pathogen \({\mathcal {R}}_0\), but can either increase or decrease the pathogen virulence (the host CFR), suggesting that vector inoculum size can contribute to virulence of vector-borne diseases in distinct ways.     

Evolutionary and population dynamics of host–parasitoid interactions

The role of evolutionary dynamics in understanding host–parasitoid interactions is interlinked with the population dynamics of these interactions. Here, we address the problems in coupling evolutionary and population dynamics of host–parasitoid interactions. We review previous theoretical and empirical studies and show that evolution can alter the ecological dynamics of a host–parasitoid interaction. Whether evolution stabilizes or destabilizes the interaction depends on the direction of evolutionary changes, which are affected by ecological, physiological, and genetic details of the insect biology. We examine the effect of life history correlations on population persistence and stability, embedding two types, one of which is competitively inferior but superior in encapsulation (for parasitoid, virulence), in a Nicholson–Bailey model with intraspecific resource competition for host. If a trade-off exists between intraspecific competitive ability and encapsulation (or virulence, as a countermeasure) in both the host and parasitoid, the trade-off or even positive correlation in the parasitoid is less influential to ecological stability than the trade-off in the host. We comment on the bearing this work has on the broader issues of understanding host–parasitoid interactions, including long-term biological control. Received: November 10, 1998 / Accepted: January 18, 1999     

Does the Segregation of Evolution in Biology Textbooks and Introductory Courses Reinforce Students’ Faulty Mental Models of Biology and Evolution?

The well-established finding that substantial confusion and misconceptions about evolution and natural selection persist after college instruction suggests that these courses neither foster accurate mental models of evolution’s mechanisms nor instill an appreciation of evolution’s centrality to an understanding of the living world. Our essay explores the roles that introductory biology courses and textbooks may play in reinforcing undergraduates’ pre-existing, faulty mental models of the place of evolution in the biological sciences. Our content analyses of the three best-selling introductory biology textbooks for majors revealed the conceptual segregation of evolutionary information. The vast majority of the evolutionary terms and concepts in each book were isolated in sections about evolution and diversity, while remarkably few were employed in other sections of the books. Standardizing the data by number of pages per unit did not alter this pattern. Students may fail to grasp that evolution is the unifying theme of biology because introductory courses and textbooks reinforce such isolation. Two goals are central to resolving this problem: the desegregation of evolution as separate “units” or chapters and the active integration of evolutionary concepts at all levels and across all domains of introductory biology.     

Perspective: Teaching evolution in higher education

Abstract.— In the past decade, the academic community has increased considerably its activity concerning the teaching and learning of evolution. Despite such beneficial activity, the state of public understanding of evolution is considered woefully lacking by most researchers and educators. This lack of understanding affects evolution/science literacy, research, and academia in general. Not only does the general public lack an understanding of evolution but so does a considerable proportion of college graduates. However, it is not just evolutionary concepts that students do not retain. In general, college students retain little of what they supposedly have learned. Worse yet, it is not just students who have avoided science and math who fail to retain fundamental science concepts. Students who have had extensive secondary-level and college courses in science have similar deficits. We examine these issues and explore what distinguishes effective pedagogy from ineffective pedagogy in higher education in general and evolution education in particular. The fundamental problem of students' prior conceptions is considered and why prior conceptions often underpin students' misunderstanding of the evolutionary concepts being taught. These conceptions can often be discovered and addressed. We also attend to concerns about coverage of course content and the influence of religious beliefs, and provide helpful strategies to improve college-level teaching of evolution.     

Valuing the Benefits of Weight Loss Programs: An Application of the Discrete Choice Experiment

Objective: Obesity is a leading health threat. Determination of optimal therapies for long‐term weight loss remains a challenge. Evidence suggests that successful weight loss depends on the compliance of weight loss program participants with their weight loss efforts. Despite this, little is known regarding the attributes influencing such compliance. The purpose of this study was to assess, using a discrete choice experiment (DCE), the relative importance of weight loss program attributes to its participants and to express these preferences in terms of their willingness to pay for them. Research Methods: A DCE survey explored the following weight loss program attributes in a sample of 165 overweight adults enrolled in community weight loss programs: cost, travel time required to attend, extent of physician involvement (e.g., none, monthly, every 2 weeks), components (e.g., diet, exercise, behavior change) emphasized, and focus (e.g., group, individual). The rate at which participants were willing to trade among attributes and the willingness to pay for different configurations of combined attributes were estimated using regression modeling. Results: All attributes investigated appeared to be statistically significant. The most important unit change was “program components emphasized” (e.g., moving from diet only to diet and exercise). Discussion: The majority of participants were willing to pay for weight loss programs that reflected their preferences. The DCE tool was useful in quantifying and understanding individual preferences in obesity management and provided information that could help to maximize the efficiency of existing weight loss programs or the design of new programs.     

Quantifying the Contribution of Hosts with Different Parasite Concentrations to the Transmission of Visceral Leishmaniasis in Ethiopia

Background

An important factor influencing the transmission dynamics of vector-borne diseases is the contribution of hosts with different parasitemia (no. of parasites per ml of blood) to the infected vector population. Today, estimation of this contribution is often impractical since it relies exclusively on limited-scale xenodiagnostic or artificial feeding experiments (i.e., measuring the proportion of vectors that become infected after feeding on infected blood/host).

Methodology

We developed a novel mechanistic model that facilitates the quantification of the contribution of hosts with different parasitemias to the infection of the vectors from data on the distribution of these parasitemias within the host population. We applied the model to an ample data set of Leishmania donovani carriers, the causative agent of visceral leishmaniasis in Ethiopia.

Results

Calculations facilitated by the model quantified the host parasitemias that are mostly responsible for the infection of vector, the sand fly Phlebotomus orientalis. Our findings indicate that a 3.2% of the most infected people were responsible for the infection of between 53% and 79% (mean – 62%) of the infected sand fly vector population.

Significance

Our modeling framework can easily be extended to facilitate the calculation of the contribution of other host groups (such as different host species, hosts with different ages) to the infected vector population. Identifying the hosts that contribute most towards infection of the vectors is crucial for understanding the transmission dynamics, and planning targeted intervention policy of visceral leishmaniasis as well as other vector borne infectious diseases (e.g., West Nile Fever).     

Improving How Evolution Is Taught: Facilitating a Shift from Memorization to Evolutionary Thinking

In North America, public understanding and acceptance of evolution is alarmingly low. Moreover, acceptance rates are declining, and studies suggest that even students who have taken courses in evolution have the same misunderstandings as the general public. These data signal deficiencies in our educational system and provide a “call to arms” to improve how evolution is taught. Many studies show that student education can be improved by replacing lecture-based pedagogy with active learning approaches—where the role of students changes from passive note taking to active problem solving. Here, we describe changes made to a second-year undergraduate evolution course to facilitate a shift to active learning and improve student understanding of evolution. First, lectures were used only sparingly and were largely replaced by problem-solving activities. Second, standard textbooks were replaced by “popular” books applying evolutionary thinking to topics students encounter on a daily basis. Lastly, predefined laboratory exercises were replaced by student-designed and implemented research projects. These changes led to increased student engagement and enjoyment, improved understanding of evolution and ability to apply evolutionary thinking to biological problems, and increased student recognition that evolutionary thinking is important not only in the classroom but also in their daily lives.     

The Importance of Understanding the Nature of Science for Accepting Evolution

Many students reject evolutionary theory, whether or not they adequately understand basic evolutionary concepts. We explore the hypothesis that accepting evolution is related to understanding the nature of science. In particular, students may be more likely to accept evolution if they understand that a scientific theory is provisional but reliable, that scientists employ diverse methods for testing scientific claims, and that relating data to theory can require inference and interpretation. In a study with university undergraduates, we find that accepting evolution is significantly correlated with understanding the nature of science, even when controlling for the effects of general interest in science and past science education. These results highlight the importance of understanding the nature of science for accepting evolution. We conclude with a discussion of key characteristics of science that challenge a simple portrayal of the scientific method and that we believe should be emphasized in classrooms.     

Interwoven Biology of the Tsetse Holobiont

Microbial symbionts can be instrumental to the evolutionary success of their hosts. Here, we discuss medically significant tsetse flies (Diptera: Glossinidae), a group comprised of over 30 species, and their use as a valuable model system to study the evolution of the holobiont (i.e., the host and associated microbes). We first describe the tsetse microbiota, which, despite its simplicity, harbors a diverse range of associations. The maternally transmitted microbes consistently include two Gammaproteobacteria, the obligate mutualists Wigglesworthia spp. and the commensal Sodalis glossinidius, along with the parasitic Alphaproteobacteria Wolbachia. These associations differ in their establishment times, making them unique and distinct from previously characterized symbioses, where multiple microbial partners have associated with their host for a significant portion of its evolution. We then expand into discussing the functional roles and intracommunity dynamics within this holobiont, which enhances our understanding of tsetse biology to encompass the vital functions and interactions of the microbial community. Potential disturbances influencing the tsetse microbiome, including salivary gland hypertrophy virus and trypanosome infections, are highlighted. While previous studies have described evolutionary consequences of host association for symbionts, the initial steps facilitating their incorporation into a holobiont and integration of partner biology have only begun to be explored. Research on the tsetse holobiont will contribute to the understanding of how microbial metabolic integration and interdependency initially may develop within hosts, elucidating mechanisms driving adaptations leading to cooperation and coresidence within the microbial community. Lastly, increased knowledge of the tsetse holobiont may also contribute to generating novel African trypanosomiasis disease control strategies.