Environmental and biotic controls on the evolutionary history of insect body size

Abstract

Giant insects, with wingspans as large as 70 cm, ruled the Carboniferous and Permian skies. Gigantism has been linked to hyperoxic conditions because oxygen concentration is a key physiological control on body size, particularly in groups like flying insects that have high metabolic oxygen demands. Here we show, using a dataset of more than 10,500 fossil insect wing lengths, that size tracked atmospheric oxygen concentrations only for the first 150 Myr of insect evolution. The data are best explained by a model relating maximum size to atmospheric environmental oxygen concentration (pO 2 ) until the end of the Jurassic, and then at constant sizes, independent of oxygen fluctuations, during the Cretaceous and, at a smaller size, the Cenozoic. Maximum insect size decreased even as atmospheric pO 2 rose in the Early Cretaceous following the evolution and radiation of early birds, particularly as birds acquired adaptations that allowed more agile flight. A further decrease in maximum size during the Cenozoic may relate to the evolution of bats, the Cretaceous mass extinction, or further specialization of flying birds. The decoupling of insect size and atmospheric pO 2 coincident with the radiation of birds suggests that biotic interactions, such as predation and competition, superseded oxygen as the most important constraint on maximum body size of the largest insects.paleoecology | temperature | maximum likelihood estimation B ecause metabolic oxygen demand increases with increasing body size, environmental oxygen concentration (pO 2 ) is frequently invoked as an important constraint on the size of animals (1-6). Giant late Paleozoic insects, with wingspans as large as 70 cm, are the iconic example of the oxygen-body size link; hyperoxic conditions during the Carboniferous and Permian are thought to have permitted the spectacular sizes of the largest insects ever (2, 4). The physiological basis linking insect body size and pO 2 has been elucidated in numerous experimental tests (5,7,8). Body size and metabolic rate respond to pO 2 when insects are reared in hypoxic or hyperoxic atmospheres (7,8), although the effects are not uniform in all taxa (9). Flying insects should be particularly susceptible to variations in atmospheric pO 2 because their flight musculature has high energy demands (10), particularly during periods of active flight (11, 12). The volume occupied by tracheae, tubes that transport oxygen throughout the body, scales hypermetrically with body volume, imposing further surface area-to-volume constraints on maximum size (13,14).Although these responses underscore the physiological importance of oxygen, developmental plasticity exhibited by different insect groups may not be indicative of evolutionary changes (15), especially in natural settings where other abiotic influences, biotic interactions, and selective pressure from allometric scaling of life-history traits are also important (16)(17)(18)(19)(20). For example, temperature can also be an important influence on insect body size via physiologica...

The largest known odonate in China: Hsiufua chaoi Zhang et Wang, gen. et sp. nov. from the middle jurassic of inner mongolia

“…An analysis of changes in the wing length of the largest odonatopterans through their geological history demonstrates that the level of atmospheric oxygen is only one of the controlling factors limiting maximum body size of insects [41]. A recent study shows [42] that changes in wing length of the largest insects from the Middle Carboniferous to the Late Jurassic are consistent with changes in the level of atmospheric oxygen shown by the GEOCARBSULF model [37]. If the changes in atmospheric oxygen partial pressures in the Phanerozic are correctly predicted by the GEOCARBSULF model (Figure 3), then the fact that the maximum size (forewing length) of Odonata is smaller in the Permian than in the Mesozoic [41] probably results from earlier competition for food resources between Odonata and Protodonata.…”

Biotic interactions modify the effects of oxygen on insect gigantism

“…1) and a model of stasis, with additional changes in stasis at 90-60 Mya. The work by Clapham and Karr (9) argues that the first shift coincides with the diversification of birds and later, increases in their maneuverability. Aerially adept predators would have placed substantial pressure on large Fig.…”

“…They then apply statistical models to determine the contributions of oxygen partial pressure, temperature, and stasis during different time periods, to size variation among 10-Myr time intervals (9). They include temperature (using paleolatitude as a proxy) because of the known positive relationship between the maximum size of insects in an assemblage and ambient temperature (9,14). They find that, between the mid-Carboniferous (the start of their data series) and about 140 Mya, maximum size tracks atmospheric oxygen concentration.…”

“…Most promising among these mechanisms is hypermetry of the tracheal system, such that the larger tracheae required for adequate performance of larger insects, under a 21% oxygen concentration, could simply not be accommodated by peripheral structures of the insect body (8). As is discussed in the work by Clapham and Karr (9), much of this recent discussion has focused on plastic responses and shortterm evolution of size under laboratory conditions. These aspects do not reflect longer-term changes under more natural conditions, where organisms simultaneously experience changes in a variety of conditions, such as the presence of competitors and predators.…”

“…These aspects do not reflect longer-term changes under more natural conditions, where organisms simultaneously experience changes in a variety of conditions, such as the presence of competitors and predators. By contrast, investigations of changes in the size distributions and maximum body sizes of naturally occurring insect assemblages certainly do, and this approach is precisely the approach adopted in the work by Clapham and Karr (9).…”