Reduced Mitochondrial Efficiency Explains Mismatched Growth and Metabolic Rate at Supraoptimal Temperatures

Martinez, Eloy; Menze, Michael A.; Agosta, Salvatore J.

doi:10.1086/689871

Cited by 16 publications

(18 citation statements)

References 24 publications

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“…Consequently, some fish on the low ration treatment were actually faster growing than others on the high ration treatment that were consuming three times as much food. While it has previously been shown that increased mitochondrial efficiency promotes fitness-related traits (physical performance [34], growth performance [9,[21][22][23]35], reproductive output [36] and ageing [9,14,36,37]), here we demonstrate that this relationship can even occur when animals are experiencing similar rates of food intake. As well as varying among Table 1.…”

Section: Discussioncontrasting

confidence: 40%

“…Thus, the higher this ratio, the more efficiently an animal converts its metabolic substrates into ATP, with the ATP then available for energy-demanding cellular processes such as protein synthesis and biomass production [18]. A number of studies have found positive links between mean growth rate and mean mitochondrial efficiency when comparing among treatment groups, populations or selection lines [9,[19][20][21][22][23], but until now there has, to our knowledge, been no assessment of whether mitochondrial efficiency could explain variation in growth rate among individual animals maintained with the same food intake.…”

Section: Introductionmentioning

confidence: 99%

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Differences in mitochondrial efficiency explain individual variation in growth performance

et al. 2019

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The physiological causes of intraspecific differences in fitness components such as growth rate are currently a source of debate. It has been suggested that differences in energy metabolism may drive variation in growth, but it remains unclear whether covariation between growth rates and energy metabolism is: (i) a result of certain individuals acquiring and consequently allocating more resources to growth, and/or is (ii) determined by variation in the efficiency with which those resources are transformed into growth. Studies of individually housed animals under standardized nutritional conditions can help shed light on this debate. Here we quantify individual variation in metabolic efficiency in terms of the amount of adenosine triphosphate (ATP) generated per molecule of oxygen consumed by liver and muscle mitochondria and examine its effects, both on the rate of protein synthesis within these tissues and on the rate of whole-body growth of individually fed juvenile brown trout ( Salmo trutta ) receiving either a high or low food ration. As expected, fish on the high ration on average gained more in body mass and protein content than those maintained on the low ration. Yet, growth performance varied more than 10-fold among individuals on the same ration, resulting in some fish on low rations growing faster than others on the high ration. This variation in growth for a given ration was related to individual differences in mitochondrial properties: a high whole-body growth performance was associated with high mitochondrial efficiency of ATP production in the liver. Our results show for the first time, to our knowledge, that among-individual variation in the efficiency with which substrates are converted into ATP can help explain marked variation in growth performance, independent of food intake. This study highlights the existence of inter-individual differences in mitochondrial efficiency and its potential importance in explaining intraspecific variation in whole-animal performance.

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Section: Discussioncontrasting

confidence: 40%

Section: Introductionmentioning

confidence: 99%

Differences in mitochondrial efficiency explain individual variation in growth performance

et al. 2019

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“…Manduca sexta serves as an important model organism for insect physiology and development (e.g. [ 36 , 37 ]) and, in interaction with Cotesia congregata , as a model system for host-parasite interactions and insect immunology (e.g. [ 38 , 39 ]) as well as tritrophic interactions (e.g.…”

Section: Methodsmentioning

confidence: 99%

Upper thermal limits differ among and within component species in a tritrophic host-parasitoid-hyperparasitoid system

2018

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Understanding how climate change affects host-parasite systems and predicting the consequences for ecosystems, economies, and human health has emerged as an important task for science and society. Some basic insight into this complex problem can be gained by comparing the thermal physiology of interacting host and parasite species. In this study, we compared upper thermal tolerance among three component species in a natural host-parasitoid-hyperparasitoid system from Virginia, USA. To assess the ecological relevance of our results, we also examined a record of maximum daily air temperatures collected near the study site in the last 124 years. We found that the caterpillar host Manduca sexta had a critical thermal maximum (CTmax) about 4°C higher than the parasitic wasp, Cotesia congregata, and the hyperparasitic wasp, Conura sp., had a CTmax about 6°C higher than its host, C. congregata. We also found significant differences in CTmax among instars and between parasitized and non-parasitized M. sexta. The highest maximum daily air temperature recorded near the study in the last 124 years was 42°C, which equals the average CTmax of one species (C. congregata) but is several degrees lower than the average CTmax of the other two species (M. sexta, Conura sp.) in this study. Our results combined with other studies suggest that significant differences in thermal performance within and among interacting host and parasite species are common in nature and that climate change may be largely disruptive to these systems with responses that are highly variable and complex.

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“…Similarly, it has also been shown in many studies that for insects, the cost of living is extremely high at stressful high temperatures (>35 • C). For example, the efficiency of the mitrochondria in converting carbohydrate substrates into energy has been shown to drop significantly at stressful high temperatures in Manduca sexta (Martinez et al, 2017). This reduction in mitochondrial capacity is linked with reduction in juvenile stages e.g., larval growth rates, whereby in the case of parasitoids, this may affect their phenology, abundance, and efficacy of host parasitisation.…”

Section: Temperature Effects On Parasitoid Physiology and Implicationmentioning

confidence: 99%

“…Prey (herbivore) diversity is another aspect that has been previously linked with plant nutritional quality (Marzetz et al, 2017). In the study, Martinez et al (2017) postulated three hypothetical scenarios of herbivore response to nutritional quality. First, the growth of the herbivore populations is promoted in diverse communities by co-occurrence of species with complementary nutritional traits.…”

Section: Impact Of Plant Nutritional Quality and Food Web Dynamicsmentioning

confidence: 99%

Global Climate Change as a Driver of Bottom-Up and Top-Down Factors in Agricultural Landscapes and the Fate of Host-Parasitoid Interactions

2019

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The global climate is rapidly changing and the evidence is increasingly manifesting across various biological systems. For arthropods, several studies have demonstrated how changing climates affect their distribution through phenological and physiological responses, largely focusing on various organismal fitness parameters. However, the net-effect of the changing climate among ecological communities may be mediated by the feedback pathways among interacting trophic groups under environmental change. For agroecosystems, the maintenance of the integrity of trophic interactions even under climate variability is a high priority. This is even more important in this era where there is advocacy for sustainable agriculture, with higher emphasis on environmentally benign methods. For this reason, pest management in food production systems using biological control (especially use of parasitoid antagonists) has come to the forefront. In this review, we give an overview of the diversity of physiological responses among host insect and parasitoid populations and how this may influence their interactions. We highlight how climate change may modify bottom-up and top-down factors among agroecosystems with a particular focus on plant-insect host-parasitoid tritrophic interactions. We also outline how habitat management may influence arthropod population dynamics and how it can be manipulated to improve on-farm climate resilience and parasitoid conservation. We wrap-up by highlighting how the application of knowledge of conservation biodiversity, designing of multifunctional resilient landscapes, and evolutionary physiology of arthropods under thermal stress may be used to improve the fitness of mass-reared parasitoids (in or ex situ) for the improvement in efficacy of parasitoids ecosystem services under thermally stressful environments

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Reduced Mitochondrial Efficiency Explains Mismatched Growth and Metabolic Rate at Supraoptimal Temperatures

Cited by 16 publications

References 24 publications

Differences in mitochondrial efficiency explain individual variation in growth performance

Differences in mitochondrial efficiency explain individual variation in growth performance

Upper thermal limits differ among and within component species in a tritrophic host-parasitoid-hyperparasitoid system

Global Climate Change as a Driver of Bottom-Up and Top-Down Factors in Agricultural Landscapes and the Fate of Host-Parasitoid Interactions

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