Deciphering the evolution of metabolic allometry in an ancient insect order (Odonata)

Abstract

As the “engine of life”, metabolic rate is one of the most well-studied physiological traits across the animal kingdom. Metabolic rates have been linked to key physiological and life-history traits as well as to large scale ecological processes. For decades, scientists have tried to understand and explain metabolic allometry – the relationship between metabolic rate MR and body mass M (MR = bMa). Two major theories are based on the body’s surface-area-to-volume ratio or its nutrient supply network and propose a metabolic scaling exponent a of 2/3 or 3/4 across animals, respectively. However, recent evidence has challenged these theories and metabolic allometries are likely less constrained by physical laws than previously thought. Here, I uncover the inter- and intraspecific metabolic allometries in one of the oldest insect orders, the dragonflies and damselflies (Odonata). I measured the standard metabolic rate (SMR) of 359 field-collected individuals from 36 species in South Sweden. These data were combined with SMR measurements of previously published studies (Sweden and the US), leading to a compiled set of 654 individuals of 56 species. Taking phylogenetic relatedness, within-species variation and sample sizes into account, I show that the interspecific scaling exponent does not fit the traditional 2/3 or 3/4 power laws in Odonata. Instead, the interspecific scaling relationship is significantly steeper, with an allometric slope close to one. The metabolic scaling relationship does not differ statistically between suborders (dragonflies and damselflies), flight behaviors (fliers and perchers), sexes, or mated and unmated individuals. By contrast, the mean intraspecific slope for the metabolic allometry after phylogenetic correction was consistent with the expected 2/3 or 3/4 slopes. However, at the intraspecific level, the slopes and intercepts of the SMR-body mass relationship vary substantially across species. Several species deviated significantly in slope and/or intercept from the common interspecific allometric relationship. Using phylogenetic comparative analyses, I further show that the intraspecific slopes and intercepts are relatively stable across the Odonata phylogeny and only rare shifts of single species or small clades deviating from this common allometric trend have happened. Next, I reveal evidence for constraining forces operating over long-term evolutionary periods and several optima shifts in mass-specific SMR over 237 million years of evolution. One such supported optimum shift is located at the branch leading towards the hawker family (Aeshnidae), which exhibits relatively high SMR. This family comprises agile and fast fliers and, therefore, their high activity level might have caused the evolution of high SMR. However, no support for separate SMR optima for fliers and perchers was found. Similarly, there was no statistical evidence for different evolutionary optima between the two suborders (dragonflies and damselflies). Furthermore, I found evidence for rapid evolution of both mass-specific nucleus size and cell size across the Odonata phylogeny, with closely-related species often having dramatically different nucleus and cell sizes. Both these cellular traits seem to evolve in close concordance with each other but in discordance with SMR. Lastly, I used phylogenetic path analysis to investigate the causal relationships between morphological and cellular traits that are supposed to influence metabolic allometry. My results confirm the well established direct effect of body mass on SMR and an indirect effect of body volume on SMR via body mass. By contrast, I neither found statistical support for the often-proposed relationship between genome size or cell size and SMR nor for a causal link between surface-area to SMR. Overall, these results question several well-established theories and mechanistic models and thus motivate a rethinking of metabolic allometries and their evolutionary drivers.

Popular Abstract

The evolution of metabolic rates in dragonflies and damselflies

Energy is a limited resource that each animal has to divide between self maintenance, growth, reproduction and survival. As the “engine of life”, metabolic rate (MR) is one of the most measured physiological traits across animals. The metabolic rate of animals can be measured by analyzing the amount of carbon dioxide they produce or the amount of oxygen they consume. Metabolic rates vary widely among animals and increase with increasing body mass, a relationship called metabolic allometry. Previous studies have found an exponential, positive relationship between MR and body mass M (MR = Mb). Specifically, Kleiber’s Law proposes a scaling exponent b of 3/4 across all animals (Fig. 2, bottom line). Accordingly, when accounting for their body weight, smaller animals, such as mice, are expected to have larger metabolic rates compared to larger animals, such as elephants.

Studying metabolic allometries gives valuable insights into the physiology and metabolism of animals and allows us to predict large-scale ecological processes. In particular, in the face of current climate change, it is crucial to understand how animals and their physiology respond to warmer temperatures. However, the metabolic allometric relationship for each animal group is equivocal, making it difficult to forecast future patterns. Furthermore, empirical studies have reported a large variation in the metabolic scaling exponents and it is still unclear what mechanisms drive this variation. Previous work has mostly assumed physical limits to cause metabolic allometries. For instance, one hypothesis is based on the rate of heat loss of an animal. Essentially, larger animals have a smaller surface-to-volume ratio compared to smaller animals. Hence, they are expected to lose less heat via their smaller relative surface and so, need to produce relatively less energy. In addition, the size of cells and the genome are potential factors that could influence metabolic allometries.

So far, metabolic allometries have been mostly investigated in birds and mammals, leaving “cold blooded” ectothermic animals such as insects unstudied. Here, I present the first insights into metabolic allometry and its evolution across the ancient dragon- and damselflies (Fig. 1).

I collected dragon- and damselflies of 43 species in South Sweden and estimated their metabolic rates by measuring carbon dioxide production. These data were then combined with previously-published measurements. To relate the surface-to-volume ratio to the metabolic allometry, I used 3D computer-tomography (CT) scans to estimate the body volume and surface of each species. In addition, I extracted body fluids from each species to analyze the size of their cells and nuclei. This enabled me to relate these factors with the scaling exponent and the variation in metabolic rates.

My results show that the metabolic scaling exponent for 56 dragonfly and damselfly species is drastically different from the expected 3/4 law reported from other animals (Fig. 2, top line). I also show that the within-species metabolic allometry varies considerably between all dragonfly or damselfly species. This demonstrates that Kleiber’s law does not apply to all animals. Metabolic allometries are rather more variable across and within species than previously assumed.

Next, I reconstructed the evolution of metabolic rate, nucleus size and cell size. My results suggest that the metabolic rate of dragonflies and damselflies stayed relatively stable across 237 million years. Only some small groups or single species have evolved towards higher or lower metabolic rates (Fig. 3, dark or light colors). By contrast, nucleus and cell size evolve rapidly across species. This indicates that cell and nucleus sizes change according to the specific environment and lifestyle of a species.

Finally, to disentangle the mechanisms driving this deviation in metabolic allometry, I used phylogenetic path analysis. This approach makes it possible to characterize the direct and indirect effects of genome and cell size, body mass, body volume and surface-area on metabolic rate. I found no evidence for an effect of genome and cell size on metabolic rate or body mass. Moreover, surface-area did not affect metabolic rate either. These results suggest that physical limits might be less important as the shaping factors for metabolic allometries than previously thought. Instead, it is more likely that these metabolic allometric patterns are an outcome of natural selection resulting in the “most-optimal” allometry according to the environment and lifestyle of each species.


Master’s Degree Project 2023 in Biology – 60 credits
Department of Biology, Lund University

Supervisor: Prof. Erik I. Svensson
Evolutionary Ecology Unit, Lund University

• author: Schönberger, Daniel
• supervisor: Erik Svensson
• organization: Degree Projects in Biology
• course: BION03 20222
• year: 2023
• type: H2 - Master's Degree (Two Years)
• subject: Biology and Life Sciences
• language: English
• id: 9135531
• date added to LUP: 2023-08-29 14:34:18
• date last changed: 2023-08-29 14:34:18