Goliath and Titan – running out of leg room

A long, long time ago in a land far away, lived giant beasts stomping, scurrying and soaring over the earth. No, not a fairy tale but an image of life on earth around 290 million years ago before the climate continued to change, oxygen levels decreased and animals shrunk in size and long before humans came along.

In the late Carboniferous and early Permian, fossil evidence shows that most insects were much bigger than they are today. For example, Meganeura, a carboniferous dragonfly, had a wingspan of 75 cm and Ramsdelepedion schusteri, a carboniferous silverfish, was 6 cm long! Today, the largest insects include the Goliath beetles (Goliathus), which measure 5–11 cm in length as adults, and can reach weights of up to 80-100 g in the larval stage, Titan beetles (Titanus giganteus), which grow up to 16.7 cm in length (or 21 cm including antennae), the Titan stick insect (Acrophylla titan) with a body length of up to 50 cm and some butterflies and moths which have wingspans up to 28 cm. But why did the insects shrink?

There are a few evolutionary hypotheses for the decrease in size of the insects:

1. climate change – as oxygen levels decreased, it became more difficult to get enough oxygen to all the tissues via spiracles and diffusion alone.
2. the weight of an insect’s body at moulting might be greater than the soft cuticle could bear, and, being vulnerable to predators, they would probably have to hide.
3. the appearance and rise of vertebrate predators, e.g. reptiles made it an evolutionary advantage to get smaller to avoid predation and radiate into all the available empty niches.

A recent paper published in PNAS by Kaiser et al. lends extra support to the climate change hypothesis…

The argument goes that high oxygen levels in the Paleozoic (543-251 million years ago) atmosphere enabled animal gigantism, and the subsequent reduction in oxygen levels from 35% then to 21% now drove a reduction in body size because, in the case of the insects, the diffusion distance from the spiracles to the tissues at the centre of the body was too big to get the required oxygen to the tissues fast enough at these lower oxygen concentrations. A smaller body with a larger surface area to volume ratio gives a smaller diffusion distance from the spiracles on the cuticle through the air sacs into large tracheae and then into finer tracheoles which connect with the tissues. So maybe we have climate change to thank for the small size of our insects today - thank goodness!

Kaiser et al. used synchrotron x-ray phase-contrast imaging to visualise the tracheal system and quantify its dimensions in four species of darkling beetles varying in mass by 3 orders of magnitude. They were surprised to find that, in contrast to vertebrates, “larger insects devote a greater fraction of their body to the respiratory system, as tracheal volume scaled with mass^1.29.” What’s more, they found that the legs may be the limiting factor – “the cross-sectional area of the trachea penetrating the leg orifice scaled with mass^1.02, whereas the cross-sectional area of the leg orifice scaled with mass^0.77.” With increasing body mass the insects were literally running out of leg room for the tracheal system. When oxygen supply was higher during the late Carboniferous and early Permian, the tracheae could be smaller, which may have allowed the evolution of giant insects as limbs could reach larger sizes before the tracheal system became limited by spatial constraints.

So, why didn’t the insects just evolve modifications such as sac-like air pumps to enable them to retain their large size? We already know that caterpillars possess quite a sophisticated gaseous exchange system equivalent to the vertebrate lung – it seems that some unusual tracheal tufts in the rear end of many caterpillars’ bodies function pretty much in the same way as lungs. Further studies may show that this system is common to the Lepidoptera and may even occur in other orders. In the words of Jon Harrison, one of the authors, “One thing comparative biology has taught us is that evolutionary innovation tends to allow life to overcome physical limitations.”

Sources:
- McGavin, G. C. (2001) Essential Entomology: an order-by-order introduction. Oxford University Press, Oxford, UK, vi + 318 pp.
- Kaiser, A.; Klok, C. J.; Socha, J. J.; Lee, W. K.; Quinlan, M. C.; Harrison, J. F. (2007) Increase in tracheal investment with beetle size supports hypothesis of oxygen limitation on insect gigantism. Proceedings of the National Academy of Sciences of the United States of America 104 (32), 13198-13203.

Comments

[Gottsch Cattle Company]

The theory of the legs being a limiting factor is interesting to ponder. Will there be follow up research posted?

[Katherine Cameron]

As far as I am aware there hasn’t yet been any further research published on legs being a limiting factor of insect size since Kaiser et al's article in PNAS last year - but please do correct me if I'm wrong. You may be interested in a few other articles on insect body size that have been added to CAB Abstracts since the blog item was written:

Stillwell, R. C.; Fox, C. W. (2007) Environmental effects on sexual size dimorphism of a seed-feeding beetle. Oecologia 153 (2), 273-280.
Sexual size dimorphism is widespread in animals but varies considerably among species and among populations within species. Much of this variation is assumed to be due to variance in selection on males versus females. However, environmental variables could affect the development of females and males differently, generating variation in dimorphism. Here we use a factorial experimental design to simultaneously examine the effects of rearing host and temperature on sexual dimorphism of the seed beetle, Callosobruchus maculatus. We found that the sexes differed in phenotypic plasticity of body size in response to rearing temperature but not rearing host, creating substantial temperature-induced variation in sexual dimorphism; females were larger than males at all temperatures, but the degree of this dimorphism was smallest at the lowest temperature. This change in dimorphism was due to a gender difference in the effect of temperature on growth rate and not due to sexual differences in plasticity of development time. Furthermore, the sex ratio (proportion males) decreased with decreasing temperature and became female-biased at the lowest temperature. This suggests that the temperature-induced change in dimorphism is potentially due to a change in non-random larval mortality of males versus females. This most important implication of this study is that rearing temperature can generate considerable intraspecific variation in the degree of sexual size dimorphism, though most studies assume that dimorphism varies little within species. Future studies should focus on whether sexual differences in phenotypic plasticity of body size are a consequence of adaptive canalization of one sex against environmental variation in temperature or whether they simply reflect a consequence of non-adaptive developmental differences between males and females.

Vamosi, S. M.; Naydani, C. J.; Vamosi, U. C. (2007) Body size and species richness along geographical gradients in Albertan diving beetle (Coleoptera: Dytiscidae) communities. Canadian Journal of Zoology 85 (4), 443-449.
Species richness and body size often vary predictably along latitudinal and elevational gradients. Although these patterns have been well documented for a variety of taxa, the vast majority of studies have focused on terrestrial plants and animals. We used species lists of predaceous diving beetles (Coleoptera: Dytiscidae) collected from >400 lentic water bodies in southern Alberta to investigate the influences of latitude and elevation on species richness and body size. Because our data were based on species lists, we used proportion of, and probability of encountering at least one, large (i.e., mean body length >10 mm) diving beetle species as surrogates for the mean body size of diving beetles in a given water body. Species richness did not change with latitude and displayed a hump-shaped relationship with elevation, peaking at mid-elevations. High elevation (>2000 m) water bodies had markedly low species richness. Proportion of large species increased with latitude, although there was no effect on probability of occupancy by large species. Conversely, both measures tended to decrease with elevation, suggesting that large species are less prevalent at high elevations. We discuss potential factors contributing to the observed responses to latitude and elevation, with an emphasis on the potential impacts of oxygen limitation, productivity, and isolation at high elevation.

Yadav, J. P.; Singh, B. N. (2007) Evolutionary genetics of Drosophila ananassae: evidence for trade-offs among several fitness traits. Biological Journal of the Linnean Society 90 (4), 669-685.
Correlated responses to bi-directional selection on thorax length, examined on several life-history traits and chromosome inversion polymorphisms, have revealed apparent novel trade-offs in Drosophila ananassae. We provide evidence of trade-offs between hatching time and pupal period, pupal period and egg-pupa development time, and pupal period and larval development time (LDT). Body size shows positive correlations with ovariole number, LDT and DT (egg-fly). We provide evidence of sexual dimorphism for trade-offs between longevity and body size and starvation and longevity in females only. Trade-offs between wing/thorax (W/T) ratio and longevity, W/T ratio and starvation, and DT (egg- fly) and longevity are evident in males only. Sexual dimorphism is also evident for inversion polymorphism with body size and longevity. A longevity assay suggests that low line females outlived high line females whereas high line males outlived low line males. The mean longevity in males is negatively correlated with the 2L-ST and 3R-ST arrangement frequencies whereas the 3L-ST arrangement frequency is positively correlated with the mean longevity in males but opposite arrangements are found in females. Absolute starvation resistance is negatively correlated with 2L-ST and 3R-ST chromosome arrangements and results in a trade-off between longevity and absolute starvation resistance in females. Analyses of fecundity, hatchability, and viabilities based on age intervals in both G10 and G13 suggest that the early reproduction is favoured in D. ananassae. The productivity percentage is highest in the high line and there is no effect of late reproduction on it. Overall, we provide some unravelled trade-offs and striking sex differences, which may help in understanding the life-history evolution of the species.

Also see:

Pensel, S. M.; Remis, M. I. (2007) Variation in adult female body size related to chromosome polymorphism and female mating success in Sinipta dalmani (Orthoptera: Acrididae). Annals of the Entomological Society of America 100 (2), 283-288.

Tammaru, T.; Esperk, T. (2007) Growth allometry of immature insects: larvae do not grow exponentially. Functional Ecology 21 (6), 1099-1105.

Herren, J. K.; Gordon, I.; Holland, P. W. H.; Smith, D. (2007) The butterfly Danaus chrysippus (Lepidoptera: Nymphalidae) in Kenya is variably infected with respect to genotype and body size by a maternally transmitted male-killing endosymbiont (Spiroplasma). International Journal of Tropical Insect Science 27 (2), 62-69.

[contaminated soil]

Hey,
Its really very interesting post.I am aware there hasn’t yet been any further research published on legs being a limiting factor..

[Aajf 6]

I completely agree with the above comment, the internet is with a doubt growing into the most important medium of communication across the globe and its due to sites like this that ideas are spreading so quickly.