Animal Design Through Functional Dietary Diversity for Future Productive Landscapes

Pastoral livestock production systems are facing considerable societal pressure to reduce environmental impact, enhance animal welfare, and promote product integrity, while maintaining or increasing system profitability. Design theory is the conscious tailoring of a system for a specific or set of purposes. Then, animals—as biological systems nested in grazing environments—can be designed in order to achieve multi-faceted goals. We argue that phytochemical rich diets through dietary taxonomical diversity can be used as a design tool for both current animal product integrity and to develop future multipurpose animals. Through conscious choice, animals offered a diverse array of plants tailor a diet, which better meets their individual requirements for nutrients, pharmaceuticals, and prophylactics. Phytochemical rich diets with diverse arrangements of plant secondary compounds also reduce environmental impacts of grazing animals by manipulating the use of C and N, thereby reducing methane production and excretion of N. Subsequently functional dietary diversity (FDD), as opposed to dietary monotony, offers better nourishment, health benefits and hedonic value (positive reward increasing “liking” of feed), as well as the opportunity for individualism; and thereby eudaimonic well-being. Moreover, phytochemical rich diets with diverse arrangements of plant secondary compounds may translate in animal products with similar richness, enhancing consumer human health and well-being. Functional dietary diversity also allows us to design future animals. Dietary exposure begins in utero, continues through mothers' milk, and carries on in early-life experiences, influencing dietary preferences later in life. More specifically, in utero exposure to specific flavors cause epigenetic changes that alter morphological and physiological mechanisms that influence future “wanting,” “liking” and learning of particular foods and foodscapes. In this context, we argue that in utero and early life exposure to designed flavors of future multifunctional foodscapes allow us to graze future ruminants with enhanced multiple ecosystem services. Collectively, the strategic use of FDD allows us to “create” animals and their products for immediate and future food, health, and wealth. Finally, implementing design theory provides a link between our thoughtscape (i.e., the use of FDD as design) to future landscapes, which provides a beneficial foodscape to the animals, an subsequently to us.

Strong selective pressure by parasitoids mitigates the costs of consuming chemically defended plants

Co-evolutionary interactions between plants and herbivores have led to a range of plant defenses that minimize insect damage and a suite of counter-adaptations that allow herbivores to feed on defended plants. Consumption of plant secondary compounds results in herbivore growth and developmental costs but can be beneficial if eating these secondary compounds results in deterrence or harm to natural enemies.To test the role of secondary compounds on herbivore fitness in the context of natural enemies, I combined field measurements of the prevalence of a parasitoid wasp (Cotesia congregata) with detailed measurements of the costs of plant secondary compounds on growth, immune, and fitness traits across developmental stages in the herbivore Manduca sexta. When M. sexta larvae consume defended plants, Cotesia congregata are known to have reduced success. However, this anti-enemy benefit to the M. sexta host must be considered in relationship to parasitoid abundance and the type and strength of the fitness costs M. sexta incurs feeding on plant secondary compounds.I found that Cotesia congregata parasitoids exert large negative selective pressures, killing 31-57% of M. sexta larvae in the field. Manduca sexta developed fastest during the instars most at risk for parasitoid oviposition but growth was slowed by consumption of plant secondary compounds (nicotine and rutin). These negative size effects at the larval stage carried over to influence adult traits associated with flight and mating but there were no immune, survival, or fecundity costs of consuming plant defensive compounds as larvae.Synthesis. These results suggest that the developmental costs experienced by M. sexta herbivores consuming defensive compounds may be outweighed by a survival benefit in the face of abundant enemy pressures.

Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System

ABSTRACT Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized fungus gardens that act as external digestive systems and which degrade the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus, the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria-dominant bacterial community present within fungus gardens. In this study, we investigated the ability of symbiotic bacteria present within fungus gardens of leaf-cutter ants to degrade PSCs. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome P450 enzymes and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we showed that some of these degradation genes are expressed in situ. Most of the bacterial isolates grew unhindered in the presence of PSCs and, using gas chromatography-mass spectrometry (GC-MS), we determined that isolates from the genera Bacillus, Burkholderia, Enterobacter, Klebsiella, and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that subcolonies of fungus gardens reduced α-pinene and linalool over a 36-h period, while L. gongylophorus strains alone reduced only linalool. Overall, our results reveal that the bacterial communities in fungus gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system. IMPORTANCE Leaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut, composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their roles in the detoxification of plant secondary compounds. In this study, we assessed if the bacterial communities associated with leaf-cutter ant fungus gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus. Our findings suggest that the fungus garden and its associated microbial community influence the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores.

Enterotypes of the Gut Microbial Community and Their Response to Plant Secondary Compounds in Plateau Pikas

Animal gut microbiomes can be clustered into “enterotypes” characterized by an abundance of signature genera. The characteristic determinants, stability, and resilience of these community clusters remain poorly understood. We used plateau pika (Ochotona curzoniae) as a model and identified three enterotypes by 16S rDNA sequencing. Among the top 15 genera, 13 showed significantly different levels of abundance between the enterotypes combined with different microbial functions and distinct fecal short-chain fatty acids. We monitored changes in the microbial community associated with the transfer of plateau pikas from field to laboratory and observed that feeding them a single diet reduced microbial diversity, resulting in a single enterotype with an altered composition of the dominant bacteria. However, microbial diversity, an abundance of some changed dominant genera, and enterotypes were partially restored after adding swainsonine (a plant secondary compound found in the natural diet of plateau pikas) to the feed. These results provide strong evidence that gut microbial diversity and enterotypes are directly related to specific diet, thereby indicating that the formation of different enterotypes can help animals adapt to complex food conditions. Additionally, natural plant secondary compounds can maintain dominant bacteria and inter-individual differences of gut microbiota and promote the resilience of enterotypes in small herbivorous mammals.

Bacteria contribute to plant secondary compound degradation in a generalist herbivore system

Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized fungus gardens that act as external digestive systems, degrading the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus, the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria-dominant bacterial community present within fungus gardens. Here, we investigate the ability of symbiotic bacteria present within fungus gardens of leaf-cutter ants to degrade PSCs. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome p450s and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we show that some of these degradation genes are expressed in situ. Most of the bacterial isolates grew unhindered in the presence of PSCs and, using GC-MS, we determined that isolates from the genera Bacillus, Burkholderia, Enterobacter, Klebsiella, and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that sub-colonies of fungus gardens reduced α-pinene and linalool over a 36-hour period, while L. gongylophorus strains alone only reduced linalool. Overall, our results reveal that the bacterial community in fungus gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system.ImportanceLeaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their role in the detoxification of plant secondary compounds. Here, we assess if the bacterial community associated with leaf-cutter ant fungus gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus. Our findings suggest the fungus garden and its associated microbial community influences the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores.