Range size positively correlates with temperature and precipitation niche breadths but not with dietary niche breadth in triatomine insects, vectors of Chagas disease.

Ecological theory predicts that species that can utilise a greater diversity of resources and, therefore, have wider niche breadths should also occupy larger geographic areas (the 'niche breadth-range size hypothesis'). Here, we tested this hypothesis for a blood-sucking group of insects of medical significance: the Triatominae (aka 'kissing bugs') (Hemiptera: Reduviidae). Given that niches can be viewed from different perspectives, we tested this hypothesis based on both dietary and climatic niches. We assembled the most complete dataset of triatomine feeding patterns to date by reviewing 143 studies from the literature up to 2021 and tested whether the niche breadth-range size hypothesis held for this group for both dietary and climatic components of the niche. Temperature and precipitation niche breadths were estimated from macro-environmental variables, while diet breadth was calculated based on literature data that used PCR and/or ELISA to identify different types of hosts as blood sources per triatomine species. Our results showed that temperature and precipitation niche breadths, but not dietary breadth, were positively correlated with range sizes, independent of evolutionary history among species. These findings support the predictions from the range size-niche breadth hypothesis concerning climate but not diet, in Triatominae. It also shows that support for the niche breadth-range size hypothesis is dependent upon the niche axis under consideration, which can explain the mixed support for this hypothesis in the ecological literature.

Turmeric shortens lifespan in houseflies.

Climate change poses a significant threat to food security and global public health with the increasing likelihood of insect pest outbreaks. Alternative ways to control insect populations, preferably using environmental-friendly compounds, are needed. Turmeric has been suggested as a natural insecticide with toxicity properties in some insect groups. However, empirical evidence of the effects of turmeric - and their interaction with other ecological factors such as diet - on insect survival has been limited. Here, we tested the effects of turmeric and its interactions with diets differing in protein source in the common housefly, Musca domestica. We found that turmeric shortened lifespan independent of diet and sex. Females in turmeric diets were heavier at death, which was likely driven by a combination of relatively lower rates of body mass loss during their lifetime and a higher percentage of water content at death. Each sex responded differently to the protein source in the diet, and the magnitude of the difference in lifespan between sexes were greatest in diets in which protein source was hydrolysed yeast; individuals from both sexes lived longest in sucrose-milk diets and shortest in diets with hydrolysed yeast. There was no evidence of an interaction between turmeric and diet, suggesting that the toxicity effects are independent of protein source in the diet. Given the seemingly opposing effects of turmeric in insects and mammals being uncovered in the literature, our findings provide further evidence in support of turmeric as a potential natural insecticide.

Optimum ratio of dietary protein and carbohydrate that maximises lifespan is shared among related insect species.

Animals often regulate the intake and quantity of nutrients to maximise fitness through life-history traits such as lifespan, but we still lack a proper understanding of how specific nutrients influence these traits. Here, I developed an algorithm which allowed me to create a nutrient-specific database from literature data, and investigated how the requirements of protein (P) and carbohydrate (C) needed to maximise lifespan evolved across nine insect species. I found moderate evidence of a phylogenetic signal on the optimal ratio of protein to carbohydrate ratio (PC ratio) that maximised lifespan, suggesting that optimal PC ratio for lifespan could have evolved non-independently among related species. I also found evidence for weak-to-strong sex-specific optimal PC ratios for lifespan, suggesting that sex-specific nutritional needs to maximise lifespan can emerge and persist in some species. Although limited in the number of species, the approach adopted here is portable to experiments with n number of nutrients and, thus, can be used in complex comparative precision nutrition studies for insights into the evolution of animal nutrition.

Super food or super toxic? Turmeric and spirulina as culprits for the toxic effects of food dyes in Drosophila.

Prolonged exposure to food dyes, even for those considered safe for consumption, are known to have toxic effects. However, we lack a proper understanding of the underlying compounds that are responsible for the observed toxicity. Here, we tested the toxic effects of three common commercially available natural food dyes (red, green, blue), and their main ingredients (turmeric and spirulina), on Drosophila melanogaster oviposition, larval development, and larval foraging behaviour. Larval development and egg-to-adult survival was significantly impacted by blue and green dyes. These effects were recapitulated when flies were fed with increasing concentrations of turmeric and spirulina, suggesting that turmeric is a toxic component of the food dye. Red dye, which contains neither turmeric or spirulina, had little impact on fly health and behaviour. Green and blue food dyes decreased egg laying, an effect similar to that observed in increasing concentrations of turmeric and, to a lesser extent, spirulina. When given a choice, larvae preferred to feed as follows: control > red > blue > green diet patches, a pattern inversely correlating with the previously observed toxicity. Our results show that, despite turmeric being often considered a super food, it can have toxic effects that the impact health of organisms.

Social group composition modulates the role of last male sperm precedence in post-copulatory sexual selection.

In many species, the order in which males mate with a female explains much of the variation in paternity arising from post-copulatory sexual selection. Research in Drosophila suggests that mating order may account for the majority of the variance in male reproductive success. However, the effects of mating order on paternity bias might not be static but could potentially vary with social or environmental factors. To test this idea, we used an existing dataset, collated from an experiment we previously published (Morimoto et al., PLoS One, 11, 2016, e0154468), with the addition of unpublished data from the same experiment. These previous experiments manipulated larval density in Drosophila melanogaster which generated variation in male and female body size, assembled groups of individuals of different sizes, and measured the mating success and paternity share of focal males. The data presented here provides information on each focal male's mating order and the frequency in which focal males remated with same females ('repetitive matings'). We combined this information with our previously reported focal male reproductive success to partition variance in paternity into male mating order and repetitive matings across groups that differed in the body size composition of males and females. We found, as expected, that male mating order explained a considerable portion of the variance in male paternity. However, we also found that the impact of male mating order on male paternity was influenced by the body size composition of groups. Specifically, males that tended to mate last had a greater paternity advantage, and displayed lower variance, in groups containing a heterogenous mixture male body sizes than in groups with a single male body size. Repetitive mating only had a minor contribution to the variance in male paternity share across all experiments. Overall, our findings contribute to the growing body of research showing that post-copulatory sexual selection is subject to socio-ecological influences.

Nutrigonometry IV: Thales' theorem to measure the rules of dietary compromise in animals.

Diet specialists and generalists face a common challenge: they must regulate the intake and balance of nutrients to achieve a target diet for optimum nutrition. When optimum nutrition is unattainable, organisms must cope with dietary imbalances and trade-off surplus and deficits of nutrients that ensue. Animals achieve this through compensatory rules that dictate how to cope with nutrient imbalances, known as 'rules of compromise'. Understanding the patterns of the rules of compromise can provide invaluable insights into animal physiology and behaviour, and shed light into the evolution of diet specialisation. However, we lack an analytical method for quantitative comparisons of the rules of compromise within and between species. Here, I present a new analytical method that uses Thales' theorem as foundation, and that enables fast comparisons of the rules of compromise within and between species. I then apply the method on three landmark datasets to show how the method enables us to gain insights into how animals with different diet specialisation cope with nutrient imbalances. The method opens new avenues of research to understand how animals cope with nutrient imbalances in comparative nutrition.

Nutrigonometry I: Using Right-Angle Triangles to Quantify Nutritional Trade-Offs in Performance Landscapes.

AbstractAnimals regulate their food intake to maximize the expression of fitness traits but are forced to trade off the optimal expression of some fitness traits because of differences in the nutrient requirements of each trait ("nutritional trade-offs"). Nutritional trade-offs have been experimentally uncovered using the geometric framework for nutrition (GF). However, current analytical methods to measure such responses rely on either visual inspection or complex models of vector calculations applied to multidimensional performance landscapes, making these approaches subjective or conceptually difficult, computationally expensive, and, in some cases, inaccurate. Here, we present a simple trigonometric model to measure nutritional trade-offs in multidimensional landscapes (nutrigonometry) that relies on the trigonometric relationships of right-angle triangles and thus is both conceptually and computationally easier to understand and use than previous quantitative approaches. We applied nutrigonometry to a landmark GF data set for comparison of several standard statistical models to assess model performance in finding regions in the performance landscapes. This revealed that polynomial (Bayesian) regressions can be used for precise and accurate predictions of peaks and valleys in performance landscapes, irrespective of the underlying structure of the data (i.e., individual food intakes vs. fixed diet ratios). We then identified the known nutritional trade-off between life span and reproductive rate in terms of both nutrient balance and concentration for validation of the model. This showed that nutrigonometry enables a fast, reliable, and reproducible quantification of nutritional trade-offs in multidimensional performance landscapes, thereby broadening the potential for future developments in comparative research on the evolution of animal nutrition.

The Present and Future of Insect Biodiversity Conservation in the Neotropics: Policy Gaps and Recommendations.

Emerging evidence suggests that insect populations may be declining at local and global scales, threatening the sustainability of the ecosystem services that insects provide. Insect declines are of particular concern in the Neotropics, which holds several of the world's hotspots of insect endemism and diversity. Conservation policies are one way to prevent and mitigate insect declines, yet these policies are usually biased toward vertebrate species. Here, we outline some key policy instruments for biodiversity conservation in the Neotropics and discuss their potential contribution and shortcomings for insect biodiversity conservation. These include species-specific action policies, protected areas and Indigenous and Community Conserved Areas (ICCAs), sectoral policies, biodiversity offsetting, market-based mechanisms, and the international policy instruments that underpin these efforts. We highlight that although these policies can potentially benefit insect biodiversity indirectly, there are avenues in which we could better incorporate the specific needs of insects into policy to mitigate the declines mentioned above. We propose several areas of improvement. Firstly, evaluating the extinction risk of more Neotropical insects to better target at-risk species with species-specific policies and conserve their habitats within area-based interventions. Secondly, alternative pest control methods and enhanced monitoring of insects in a range of land-based production sectors. Thirdly, incorporating measurable and achievable insect conservation targets into international policies and conventions. Finally, we emphasise the important roles of community engagement and enhanced public awareness in achieving these improvements to insect conservation policies.

The transcriptomic signature of responses to larval crowding in Drosophila melanogaster.

Intraspecific competition at the larval stage is an important ecological factor affecting life-history, adaptation and evolutionary trajectory in holometabolous insects. However, the molecular pathways underpinning these ecological processes are poorly characterized. We reared Drosophila melanogaster at three egg densities (5, 60, and 300 eggs/mL) and sequenced the transcriptomes of pooled third-instar larvae. We also examined emergence time, egg-to-adult viability, adult mass, and adult sex-ratio at each density. Medium crowding had minor detrimental effects on adult phenotypes compared to low density and yielded 24 differentially expressed genes (DEGs), including several chitinase enzymes. In contrast, high crowding had substantial detrimental effects on adult phenotypes and yielded 2107 DEGs. Among these, upregulated gene sets were enriched in sugar, steroid and amino acid metabolism as well as DNA replication pathways, whereas downregulated gene sets were enriched in ABC transporters, taurine, Toll/Imd signaling, and P450 xenobiotics metabolism pathways. Overall, our findings show that larval crowding has a large consistent effect on several molecular pathways (i.e., core responses) with few pathways displaying density-specific regulation (i.e., idiosyncratic responses). This provides important insights into how holometabolous insects respond to intraspecific competition during development.

Intrauterine exposure to omeprazole increases the risk of teeth morphological anomalies in the offspring of a murine model.

Conditions experienced in early life have long-lasting effects on offspring health. Despite this, little is known about how maternal exposure to drugs during pregnancy affects offspring teeth morphogenesis. In humans, omeprazole is a common drug used to mitigate Gastroesophageal Reflux Disease. Importantly, omeprazole is a non-specific proton-pump inhibitor, which may inhibit the proton pumps expressed in the developing tooth germ. To date, however, the effects of intrauterine life exposure to omeprazole on offspring tooth development remain unknown. In this study, we addressed this gap in a murine model. Pregnant female Swiss mice were exposed to daily doses of 40 mg/kg of omeprazole from the 5th to the 17th day of pregnancy and the effects of such exposure on offspring odontogenesis parameters such as morphological abnormalities, disruptions in the ameloblast and odontoblast layers and the presence of dentin matrix were measured. Omeprazole exposure significantly increased the prevalence (control: 21.6%; treatment: 60%; p = 0.001) and the risk (posterior mean and 95% credible interval; control: 0.230 [0.129; 0.347]; treatment: 0.593 [0.449; 0.730]) of offspring teeth morphological abnormalities, although there were no statistically significant effects of omeprazole exposure on other parameters of tooth development. These findings suggest that there are potential side-effects to offspring oral health of omeprazole use during pregnancy.

Uric acid metabolism modulates diet-dependent responses to intraspecific competition in Drosophila larvae.

Intraspecific competition drives ecological specialization, and niche expansion. In holometabolous insects, larval intraspecific competition ("crowding") has lasting fitness consequences for individuals and shapes adaptive responses. However, our understanding of the molecular profile of larval crowding responses remains allusive. Here, I used a genetic construct in Drosophila melanogaster with disrupted uric acid metabolism (uro -) to demonstrate the role of the uric acid metabolism-and its interactive effects with larval crowding, diet, and urea concentration-on female oviposition and larval development. Uro - larvae developed faster in sugar-rich diets. However, uro - larvae pupated at lower heights in protein- and sugar-rich diets in crowded larval conditions and showed slower development in protein-rich mixed-genotype environments. uro - did not affect female oviposition nor larval pupation success. Overall, this study provides the first step toward an integrated understanding of the molecular pathways underpinning the responses to intraspecific competition in holometabolous insects.

Nutrigonometry III: curvature, area and differences between performance landscapes.

Nutrition is one of the underlying factors necessary for the expression of life-histories and fitness across the tree of life. In recent decades, the geometric framework (GF) has become a powerful framework to obtain biological insights through the construction of multidimensional performance landscapes. However, to date, many properties of these multidimensional landscapes have remained inaccessible due to our lack of mathematical and statistical frameworks for GF analysis. This has limited our ability to understand, describe and estimate parameters which may contain useful biological information from GF multidimensional performance landscapes. Here, we propose a new model to investigate the curvature of GF multidimensional landscapes by calculating the parameters from differential geometry known as Gaussian and mean curvatures. We also estimate the surface area of multidimensional performance landscapes as a way to measure landscape deviations from flat. We applied the models to a landmark dataset in the field, where we also validate the assumptions required for the calculations of curvature. In particular, we showed that linear models perform as well as other models used in GF data, enabling landscapes to be approximated by quadratic polynomials. We then introduced the Hausdorff distance as a metric to compare the similarity of multidimensional landscapes.

Parental ecological history can differentially modulate parental age effects on offspring physiological traits in Drosophila.

Parents adjust their reproductive investment over their lifespan based on their condition, age, and social environment, creating the potential for inter-generational effects to differentially affect offspring physiology. To date, however, little is known about how social environments experienced by parents throughout development and adulthood influence the effect of parental age on the expression of life-history traits in the offspring. Here, I collected data on Drosophila melanogaster offspring traits (i.e., body weight, water content, and lipid reserves) from populations where either mothers, fathers both, or neither parents experienced different social environments during development (larval crowding) and adulthood. Parental treatment modulated parental age effects on offspring lipid reserves but did not influence parental age effects on offspring water content. Importantly, parents in social environments where all individuals were raised in uncrowded larval densities produced daughters and sons lighter than parental treatments which produced the heaviest offspring. The peak in offspring body weight was delayed relative to the peak in parental reproductive success, but more strongly so for daughters from parental treatments where some or all males in the parental social environments were raised in crowded larval densities (irrespective of their social context), suggesting a potential father-to-daughter effect. Overall, the findings of this study reveal that parental ecological history (here, developmental and adult social environments) can modulate the effects of parental age at reproduction on the expression of offspring traits.

Larval crowding effects during early development in the Chinese oak silkmoth Antheraea pernyi (Lepidoptera: Saturniidae).

Chinese sericulture relies in part on the rearing of the Chinese oak silkmoth Antheraea pernyi, an insect with key cultural and ecological roles. While feeding primarily on oak, Antheraea species are known to accept alternative hosts such as birch Betula sp with little to no apparent negative fitness consequences. This opens up the range of hostplants that could be used for large-scale rearing of A. pernyi for silk production and food, or used by this species in possible invasions. To date, however, the natural history and ecology of A. pernyi remain subject of investigation. For instance, we still do not know how individuals respond to crowding developmental environments, which is an important factor to consider for the ecology of the species as well as for commercial rearing. Here, I describe the implications of larval crowding to the survival and growth of A. pernyi larvae during early development. I show that higher crowding is associated with stronger negative effects on growth and survival, corroborating findings from other holometabolous insects. I then discuss the implications of this findings for our understanding of optimum larval crowding. Overall, the findings reveal important ecological information for an insect species key for provisioning and cultural ecosystem services.

Nutrigonometry II: Experimental strategies to maximize nutritional information in multidimensional performance landscapes.

Animals regulate their nutrient consumption to maximize the expression of fitness traits with competing nutritional needs ("nutritional trade-offs"). Nutritional trade-offs have been studied using a response surface modeling approach known as the Geometric Framework for nutrition (GF). Current experimental design in GF studies does not explore the entire area of the nutritional space resulting in performance landscapes that may be incomplete. This hampers our ability to understand the properties of the performance landscape (e.g., peak shape) from which meaningful biological insights can be obtained. Here, I tested alternative experimental designs to explore the full range of the performance landscape in GF studies. I compared the performance of the standard GF design strategy with three alternatives: hexagonal, square, and random points grid strategies with respect to their accuracy in reconstructing baseline performance landscapes from a landmark GF dataset. I showed that standard GF design did not reconstruct the properties of baseline performance landscape appropriately particularly for traits that respond strongly to the interaction between nutrients. Moreover, the peak estimates in the reconstructed performance landscape using standard GF design were accurate in terms of the nutrient ratio but incomplete in terms of peak shape. All other grid designs provided more accurate reconstructions of the baseline performance landscape while also providing accurate estimates of nutrient ratio and peak shape. Thus, alternative experimental designs can maximize information from performance landscapes in GF studies, enabling reliable biological insights into nutritional trade-offs and physiological limits within and across species.

Assessing Anatomical Changes in Male Reproductive Organs in Response to Larval Crowding Using Micro-computed Tomography Imaging.

Ecological conditions shape (adaptive) responses at the molecular, anatomical, and behavioral levels. Understanding these responses is key to predict the outcomes of intra- and inter-specific competitions and the evolutionary trajectory of populations. Recent technological advances have enabled large-scale molecular (e.g., RNAseq) and behavioral (e.g., computer vision) studies, but the study of anatomical responses to ecological conditions has lagged behind. Here, we highlight the role of X-ray micro-computed tomography (micro-CT) in generating in vivo and ex vivo 3D imaging of anatomical structures, which can enable insights into adaptive anatomical responses to ecological environments. To demonstrate the application of this method, we manipulated the larval density of Drosophila melanogaster Meigen flies and applied micro-CT to investigate the anatomical responses of the male reproductive organs to varying intraspecific competition levels during development. Our data is suggestive of two classes of anatomical responses which broadly agree with sexual selection theory: increasing larval density led to testes and ejaculatory duct to be overall larger (in volume), while the volume of accessory glands and, to a lesser extent, ejaculatory duct decreased. These two distinct classes of anatomical responses might reflect shared developmental regulation of the structures of the male reproductive system. Overall, we show that micro-CT can be an important tool to advance the study of anatomical (adaptive) responses to ecological environments.

Sugar-rich larval diet promotes lower adult pathogen load and higher survival after infection in a polyphagous fly.

Nutrition is a central factor influencing immunity and resistance to infection, but the extent to which nutrition during development affects adult responses to infections is poorly understood. Our study investigated how the nutritional composition of the larval diet affects the survival, pathogen load and food intake of adult fruit flies, Bactrocera tryoni, after septic bacterial infection. We found a sex-specific effect of larval diet composition on survival post-infection: survival rate was higher and bacterial load was lower for infected females raised on a sugar-rich larval diet than for females raised on a protein-rich larval diet, an effect that was absent in males. Both males and females were heavier when fed a balanced larval diet compared with a protein- or sugar-rich diet, while body lipid reserves were higher for those that had consumed the sugar-rich larval diet compared with other diets. Body protein reserves were lower for flies that had been raised on the sugar-rich larval diet compared with other diets in males, but not females. Both females and males shifted their nutrient intake to ingest a sugar-rich diet when infected compared with sham-infected flies without any effect of the larval diet, suggesting that sugar-rich diets can be beneficial to fight off bacterial infection as shown in previous literature. Overall, our findings show that nutrition during early life can shape individual fitness in adulthood.

'Holey' niche! finding holes in niche hypervolumes using persistence homology.

Living organisms are limited in the range of values of ecological factors they can explore. This defines where animals exist (or could exist) and forms an ecological fingerprint that explains species' distribution at global scales. Species' ecological fingerprints can be represented as a n-dimensional hypervolume - known as Hutchinson's niche hypervolume. This concept has enabled significant progress in our understanding of species' ecological needs and distributions across environmental gradients. Nevertheless, the properties of Hutchinson's n-dimensional hypervolumes can be challenging to calculate and several methods have been proposed to extract meaningful measurements of hypervolumes' properties. One key property of hypervolumes are holes, which provide important information about the ecological occupancy of species. However, to date, current methods rely on volume estimates and set operations to identify holes in hypervolumes. Yet, this approach can be problematic because in high-dimensions, the volume of region enclosing a hole tends to zero. We propose the use of persistence homology (PH) to identify holes in hypervolumes and in ecological datasets more generally. PH allows for the estimates of topological properties in n-dimensional niche hypervolumes independent of the volume estimates of the hypervolume. We demonstrate the application of PH to canonical datasets and to the identification of holes in the hypervolumes of five vertebrate species with diverse niches, highlighting the potential benefits of this approach to gain further insights into animal ecology. Overall, our approach enables the study of a yet unexplored property of Hutchinson's hypervolumes, and thus, have important implications to our understanding of animal ecology.

Density-by-Diet Interactions during Larval Development Shape Adult Life History Trait Expression and Fitness in a Polyphagous Fly.

AbstractHabitat quality early in life determines individual fitness, with possible long-term evolutionary effects on groups and populations. In holometabolous insects, larval ecology plays a major role in determining the expression of traits in adulthood, but how ecological conditions during the larval stage interact to shape adult life history and fitness, particularly in nonmodel organisms, remains subject to scrutiny. Consequently, our knowledge of the interactive effects of ecological factors on insect development is limited. Here, using the polyphagous fly Bactrocera tryoni, we conducted a fully factorial design where we manipulated larval density and larval diet (protein rich, standard, and sugar rich) to gain insights into how these ecological factors interact to modulate adult fitness. As expected, a protein-rich diet resulted in faster larval development and heavier and leaner adults that were more fecund compared with the standard and sugar-rich diets, irrespective of larval density. Females from the protein-rich larval diet had overall higher reproductive rate (i.e., eggs per day) than females from other diets, and reproductive rate decreased linearly with density for females from the protein-rich diet but nonlinearly for females from the standard and sugar-rich diets over time. Surprisingly, adult lipid reserve increased with larval density for adults from the sugar-rich diet (as opposed to decreasing as in other diets), possibly because of a stress response to an extremely adverse condition during development (i.e., high intraspecific competition and poor nutrition). Together, our results provide insights into how ecological factors early in life interact and shape the fate of individuals through life stages in holometabolous insects.