Alistair M. Senior

A quantitative review of MHC-based mating preference: the role of diversity and dissimilarity

Sexual selection hypotheses stipulate that the major histocompatibility complex genes (MHC) constitute a key molecular underpinning for mate choice in vertebrates. The last four decades saw growing empirical literature on the role of MHC diversity and dissimilarity in mate choice for a wide range of vertebrate animals, but with mixed support for its significance in natural populations. Using formal phylogenetic meta‐analysis and meta‐regression techniques, we quantitatively review the existing literature on MHC‐dependent mating preferences in nonhuman vertebrates with a focus on the role of MHC diversity and dissimilarity. Overall, we found small, statistically nonsignificant, average effect sizes for both diversity‐ and dissimilarity‐based mate choice (r = 0.113 and 0.064, respectively). Importantly, however, meta‐regression models revealed statistically significant support regarding female choice for diversity, and choice for dissimilarity (regardless of choosy sex) only when dissimilarity is characterized across multiple loci. Little difference was found among vertebrate taxa; however, the lack of statistical power meant statistically significant effects were limited to some taxa. We found little sign of publication bias; thus, our results are likely to be robust. In light of our quantitative assessment, methodological improvements and fruitful future avenues of research are highlighted.

The impact of low-protein high-carbohydrate diets on aging and lifespan

AbstractMost research on nutritional effects on aging has focussed on the impact of manipulating single dietary factors such as total calorie intake or each of the macronutrients individually. More recent studies using a nutritional geometric approach called the Geometric Framework have facilitated an understanding of how aging is influenced across a landscape of diets that vary orthogonally in macronutrient and total energy content. Such studies have been performed using ad libitum feeding regimes, thus taking into account compensatory feeding responses that are inevitable in a non-constrained environment. Geometric Framework studies on insects and mice have revealed that diets low in protein and high in carbohydrates generate longest lifespans in ad libitum-fed animals while low total energy intake (caloric restriction by dietary dilution) has minimal effect. These conclusions are supported indirectly by observational studies in humans and a heterogeneous group of other types of interventional studies in insects and rodents. Due to compensatory feeding for protein dilution, low-protein, high-carbohydrate diets are often associated with increased food intake and body fat, a phenomenon called protein leverage. This could potentially be mitigated by supplementing these diets with interventions that influence body weight through physical activity and ambient temperature.

HETEROGENEITY IN INDIVIDUAL QUALITY AND REPRODUCTIVE TRADE‐OFFS WITHIN SPECIES

Interspecifically, a reasonable body of evidence supports a trade‐off between offspring size and number. However, at the intraspecific level, a whole manner of phenotypic correlations between offspring size and number are observed. These correlations may be predicted when heterogeneity in resource availability, or quality, is considered. Making the assumption that maternal size is a proxy for resource availability, we meta‐analytically quantified four phenotypic reproductive correlations within numerous species: (1) maternal size and offspring size, (2) maternal size and offspring number, (3) offspring number and offspring size, and (4) offspring number and offspring size after controlling for maternal size. Within species, maternal size showed a positive correlation with both offspring size and number. Despite this consistency, no correlation between offspring size and number was found. After controlling for maternal size, however, offspring size and number showed a significant negative correlation. A phylogenetic component of our analysis accounted for little heterogeneity in the data, suggesting that our findings show remarkable consistency across taxa. Overall, our results support an observable phenotypic trade‐off between offspring size and number. However, this analysis also highlights the importance of considering quality when examining trade‐offs, a task that is not always straightforward as quality is context dependant.

Meta-analysis of variation: ecological and evolutionary applications and beyond

Summary 1. Meta-analysis has become a standard way of summarizing empirical studies in many fields, including ecology and evolution. In ecology and evolution, meta-analyses comparing two groups (usually experimental and control groups) have almost exclusively focused on comparing the means, using standardized metrics such as Cohen’s / Hedges’d or the response ratio. 2. However, an experimental treatment may not only affect the mean but also the variance. Investigating differences in the variance between two groups may be informative, especially when a treatment influences the variance in addition to or instead of the mean. 3. In this paper, we propose the effect size statistic lnCVR (the natural logarithm of the ratio between the coefficients of variation, CV, from two groups), which enables us to meta-analytically compare differences between the variability of two groups. We illustrate the use of lnCVR with examples from ecology and evolution. 4. Further, as an alternative approach to the use of lnCVR, we propose the combined use of ln s (the log standard deviation) and ln � (the log mean) in a hierarchical (linear mixed) model. The use of ln s with ln � x overcomes potential limitations of lnCVR and it provides a more flexible, albeit more complex, way to examine variation beyond two-group comparisons. Relevantly, we also refer to the potential use of ln s and lnCV (the log CV) in the context of comparative analysis. 5. Our approaches to compare variability could be applied to already published meta-analytic data sets that compare two-group means to uncover potentially overlooked effects on the variance. Additionally, our approaches should be applied to future meta-analyses, especially when one suspects a treatment has an effect not only on the mean, but also on the variance. Notably, the application of the proposed methods extends beyond the fields of ecology and evolution.

Meta-evaluation of meta-analysis: ten appraisal questions for biologists

Meta-analysis is a statistical procedure for analyzing the combined data from different studies, and can be a major source of concise up-to-date information. The overall conclusions of a meta-analysis, however, depend heavily on the quality of the meta-analytic process, and an appropriate evaluation of the quality of meta-analysis (meta-evaluation) can be challenging. We outline ten questions biologists can ask to critically appraise a meta-analysis. These questions could also act as simple and accessible guidelines for the authors of meta-analyses. We focus on meta-analyses using non-human species, which we term ‘biological’ meta-analysis. Our ten questions are aimed at enabling a biologist to evaluate whether a biological meta-analysis embodies ‘mega-enlightenment’, a ‘mega-mistake’, or something in between.

The Multidimensional Nutritional Niche

The dietary generalist-specialist distinction plays a pivotal role in theoretical and applied ecology, conservation, invasion biology, and evolution and yet the concept remains poorly characterised. Diets, which are commonly used to define niche breadth, are almost exclusively considered in terms of foods, with little regard for the mixtures of nutrients and other compounds they contain. We use nutritional geometry (NG) to integrate nutrition with food-level approaches to the dietary niche and illustrate the application of our framework in the important context of invasion biology. We use an example that involves a model with four hypothetical nonexclusive scenarios. We additionally show how this approach can provide fresh theoretical insight into the ways nutrition and food choices impact trait evolution and trophic interactions.

Evolving Nutritional Strategies in the Presence of Competition: A Geometric Agent- Based Model

Access to nutrients is a key factor governing development, reproduction and ultimately fitness. Within social groups, contest-competition can fundamentally affect nutrient access, potentially leading to reproductive asymmetry among individuals. Previously, agent-based models have been combined with the Geometric Framework of nutrition to provide insight into how nutrition and social interactions affect one another. Here, we expand this modelling approach by incorporating evolutionary algorithms to explore how contest-competition over nutrient acquisition might affect the evolution of animal nutritional strategies. Specifically, we model tolerance of nutrient excesses and deficits when ingesting nutritionally imbalanced foods, which we term ‘nutritional latitude’; a higher degree of nutritional latitude constitutes a higher tolerance of nutritional excess and deficit. Our results indicate that a transition between two alternative strategies occurs at moderate to high levels of competition. When competition is low, individuals display a low level of nutritional latitude and regularly switch foods in search of an optimum. When food is scarce and contest-competition is intense, high nutritional latitude appears optimal, and individuals continue to consume an imbalanced food for longer periods before attempting to switch to an alternative. However, the relative balance of nutrients within available foods also strongly influences at what levels of competition, if any, transitions between these two strategies occur. Our models imply that competition combined with reproductive skew in social groups can play a role in the evolution of diet breadth. We discuss how the integration of agent-based, nutritional and evolutionary modelling may be applied in future studies to further understand the evolution of nutritional strategies across social and ecological contexts.

Virological factors that increase the transmissibility of emerging human viruses

Significance With changes in land use and increased urbanization, the frequency with which pathogens jump species barriers to emerge in new hosts is expected to rise. Knowing which viruses may be more likely to become transmissible among humans, as opposed to only generating dead-end spillover infections, would be of considerable benefit to pandemic planning. Using multivariate modeling and multimodel inference, we sought to both identify and quantify those biological features of viruses that best determine interhuman transmissibility. This analysis revealed that chronic, nonsegmented, non–vector-borne, nonenveloped viruses with low host mortality had the highest likelihood of being transmissible among humans whereas genomic features had little predictive power. Our analysis therefore reveals that multiple virological features determine the likelihood of successful emergence. The early detection of pathogens with epidemic potential is of major importance to public health. Most emerging infections result in dead-end “spillover” events in which a pathogen is transmitted from an animal reservoir to a human but is unable to achieve the sustained human-to-human transmission necessary for a full-blown epidemic. It is therefore critical to determine why only some virus infections are efficiently transmitted among humans whereas others are not. We sought to determine which biological features best characterized those viruses that have achieved sustained human transmission. Accordingly, we compiled a database of 203 RNA and DNA human viruses and used an information theoretic approach to assess which of a set of key biological variables were the best predictors of human-to-human transmission. The variables analyzed were as follows: taxonomic classification; genome length, type, and segmentation; the presence or absence of an outer envelope; recombination frequency; duration of infection; host mortality; and whether or not a virus exhibits vector-borne transmission. This comparative analysis revealed multiple strong associations. In particular, we determined that viruses with low host mortality, that establish long-term chronic infections, and that are nonsegmented, nonenveloped, and, most importantly, not transmitted by vectors were more likely to be transmissible among humans. In contrast, variables including genome length, genome type, and recombination frequency had little predictive power. In sum, we have identified multiple biological features that seemingly determine the likelihood of interhuman viral transmissibility, in turn enabling general predictions of whether viruses of a particular type will successfully emerge in human populations.

The fitness consequences of environmental sex reversal in fish: a quantitative review

Environmental sex reversal (ESR) occurs when environmental factors overpower genetic sex‐determining factors. The phenomenon of ESR is observed widely in teleost species, where it can be induced by exposing developing fish to endocrine disrupting chemicals (EDCs). EDC‐induced ESR has been exploited by the aquaculture industry, while ecological and evolutionary models are also beginning to elucidate the potential roles that sex‐reversed individuals play in influencing population dynamics. However, how EDC exposure affects individual fitness remains relatively unknown. To date, many experimental studies have induced sex reversal in fish and measured fitness—as indicated by related traits such as size, survival and gonadal somatic index (GSI), but the reported results vary. Here, we meta‐analytically combine the results of 78 studies of induced ESR to gain insight into the fitness of sex‐reversed individuals. Overall, our results suggest that the fitness of fish exposed to EDCs is reduced at the time of exposure, with exposed individuals having a smaller size and likely a smaller GSI. Given a period of non‐exposure, fish treated with EDCs can regain a size equal to those not exposed, although GSI remains compromised. Interestingly, survival does not appear to be affected by EDC treatment. The published reports that comprise our dataset are, however, based on captive fish and the general small size resulting from exposure is likely to lead to reduced survival in the wild. Additionally, reduced fitness‐related parameters are likely to be due to exposure to EDCs rather than ESR itself. We suggest that theoretical models of ESR should account for the fitness‐related effects that we report. Whilst we are able to shed light on the physical fitness of EDC‐exposed fish, the behaviour of such individuals remains largely untested and should be the focus of future experimental manipulation.

Gut Microbiota Modifies Olfactory-Guided Microbial Preferences and Foraging Decisions in Drosophila

The gut microbiota affects a wide spectrum of host physiological traits, including development [1-5], germline [6], immunity [7-9], nutrition [4, 10, 11], and longevity [12, 13]. Association with microbes also influences fitness-related behaviors such as mating [14] and social interactions [15, 16]. Although the gut microbiota is evidently important for host wellbeing, how hosts become associated with particular assemblages of microbes from the environment remains unclear. Here, we present evidence that the gut microbiota can modify microbial and nutritional preferences of Drosophila melanogaster. By experimentally manipulating the gut microbiota of flies subjected to behavioral and chemosensory assays, we found that fly-microbe attractions are shaped by the identity of the host microbiota. Conventional flies exhibit preference for their associated Lactobacillus, a behavior also present in axenic flies as adults and marginally as larvae. By contrast, fly preference for Acetobacter is primed by early-life exposure and can override the innate preference. These microbial preferences are largely olfactory guided and have profound impact on host foraging, as flies continuously trade off between acquiring beneficial microbes and balancing nutrients from food. Our study shows a role of animal microbiota in shaping host fitness-related behavior through their chemosensory responses, opening a research theme on the interrelationships between the microbiota, host sensory perception, and behavior.