Chapter One - Evolution of the Mechanisms Underlying Insect Respiratory Gas Exchange

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Abstract

Many factors influence gas exchange patterns in insects and are generally treated in isolation from one another. Here, we provide a review of the current state of knowledge on the physics of gas exchange, insect respiratory chemoreceptors, the diversity and the methods typically used in the characterisation of respiratory pattern types, briefly covering some of the new tools and techniques that are being incorporated into this field. We then discuss the functional significance of insect gas exchange pattern variation, and possible evolutionary explanations of discontinuous gas exchange as a derived control mechanism for effecting physiological change in the context of (a) adaptive hypotheses, (b) non-adaptive hypotheses and (c) mathematical modelling of gas exchange. The lack of consensus in the literature for all proposed adaptive or mechanistic hypotheses suggests that multiple factors influence which gas exchange pattern is displayed by any particular insect during a given experiment. Thus, while the primary function of a breathing pattern is to meet an animal's gas exchange requirements, it is an interacting hierarchy of constraints that most likely determines how this demand may be met. We conclude the review with a brief discussion of future directions for the field.

Introduction

Insects were among the very first terrestrial organisms on Earth, with current phylogenomic evidence indicating that they first arose in the early Ordovician period, over 479 million years ago (Misof et al., 2014). Their enormous success on land and subsequent colonisation and expansion into all terrestrial habitats, with the exception of the polar regions, were made possible by the evolution of a suite of adaptations to cope with the many challenges associated with life in air. Not least among these was the evolution of an air-filled respiratory system—the tracheal system (Fig. 1). The tracheal system is a network of air-filled tubes that develops from invaginations of the cuticular exoskeleton. These tubes subdivide and proliferate throughout the insect's body, providing a continuous air-filled lumen for the rapid movement of oxygen (O2) and carbon dioxide (CO2) between the insect's cells and the atmosphere. It is made up of collapsible air sacs, as well as tracheal tubes that range in size from the large tracheal trunks that run the length of the insect's body and communicate with the atmosphere through pores (spiracles) in the insect's cuticle, all the way down to the terminal branches of the blind-ending microscopic (> 1 μm diameter) tracheoles that pervade the insect's tissues. Stereological studies on locusts have shown that while trachea and air sacs comprise the majority of the intratracheal volume (> 50%), they are not the primary gas exchange surface. Rather, they are the conduits that carry respiratory gases from the atmosphere to the tracheoles. While the tracheoles comprise only 13% of the intratracheal volume, their high surface area-to-volume ratio allows them to provide more than 90% of the tracheal system's lateral diffusing capacity (Snelling et al., 2011).

Like most animal life, insects produce the majority of the ATP energy they require through the glycolytic pathway of aerobic respiration (Raven and Johnson, 2002). This process occurs primarily in the mitochondria, which require a constant supply of O2 to be delivered from the surrounding environment in order for electrons to be passed down the electron transport chain embedded in the mitochondrial inner membrane and ultimately for the phosphorylation of ADP to ATP to occur. Just as O2 must be delivered continuously to the respiring mitochondria, so too must the CO2 produced as a by-product of the Krebs cycle be removed continuously from the respiring tissues and released into the environment. The tracheal system fulfils both of these tasks by providing a bidirectional conduit for both O2 and CO2 to move between the atmosphere and the mitochondria located within the insect's cells.

The rate at which O2 must be supplied to, and CO2 removed from, respiring tissues is determined by their metabolic demand. This, in turn, varies with exogenous and endogenous factors, including activity (i.e. movement, growth, digestion, etc.) and body temperature.

Section snippets

The Physics of Gas Exchange

The tracheal system is a ‘direct-delivery’ respiratory system, allowing the movement of respiratory gases between the atmosphere and cells without requiring an intermediate circulatory system. Early work on insect gas exchange proposed that small insects may have sufficiently low metabolic rates (MRs) and have small diffusion pathways, such that diffusion alone may be sufficient to meet all gas flux needs (Harrison et al., 2012). While this may in fact be the case for some small insects (

Insect Respiratory Chemoreception Mechanisms

Respiratory chemoreceptors are a crucial element of the feedback loop required for regulating gas exchange, detecting changes and stimulating an appropriate corrective response if cellular respiration is to be maintained. To survive, insects must regulate their breathing to maintain physiologically acceptable levels of O2 and CO2 within their tissues. Respiratory chemoreceptors provide the sensor and effector by detecting when internal levels of these gases require adjustment and then

Diversity and Characterisation of Gas Exchange Patterns

Levels of both O2 and CO2 need to be regulated within certain limits to prevent asphyxiation, respiratory acidosis or alkalosis. While respiratory chemoreceptors provide the means of detecting excursions outside of the physiologically acceptable range, the nervous system must still stimulate the muscles and spiracles to produce a pattern of gas exchange that maintains an acceptable rate of O2 uptake and CO2 removal. Extensive measurements of insect gas exchange under a wide range of

Functional Significance and Evolution of Gas Exchange Patterns

Insect gas exchange patterns are commonly divided into (a) continuous or continuously erratic gas exchange, where O2 uptake and CO2 release occurs constantly; (b) cyclic patterns of alternating high and low gas exchange; and (c) discontinuous gas exchange cycles, commonly called DGCs or DGE cycles. This last discontinuous pattern has received by far the most attention in the literature due to its unusual temporal decoupling of O2 uptake and CO2 release during its repeating three-phase cycle (

Conclusions and Future Directions

The many factors that are known to influence gas exchange patterns in insects are generally treated in isolation from one another. However, the lack of consensus for all proposed adaptive or mechanistic hypotheses suggests that multiple factors influence which gas exchange pattern is displayed by any particular insect during a given experiment. Thus, while the primary function of a breathing pattern is to meet an animal's gas exchange requirements, it is an interacting hierarchy of constraints

Acknowledgement

This review was made possible by a CAREG award to P.G.D.M. and J.S.T. JST would like to dedicate this review to the loving memory of Charlene Herr who understood the value of academic pursuits.

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