The great evolutionary biologist Leigh van Valen famously quipped: ‘Evolution is the control of development by ecology’. This aphorism neatly portrays how natural selection, over generations, sculpts organism development and results in the wonderful diversity of form exhibited in the animal kingdom. Nowhere is this more obvious than limb morphology – from wings to fins – in vertebrates. But van Valen never imagined the process of development being directly manipulated by an organism's environment. By and large, development is controlled by genetics, so the most obvious variations in limb anatomy between different species are encoded in the genome. However, limb morphology also exhibits substantial variation within individuals of the same species, especially when development takes place in different conditions. This suggests that, beyond the genome, an animal's environment may more directly control development.
To investigate the immediate impact that environment, particularly temperature, has on limb morphology, Andrea Pollard from the Royal Veterinary College, UK, and her colleagues studied the development of dwarf crocodiles. They observed that crocodiles incubated at 32°C had longer limbs than their siblings developing at 28°C (even relative to their larger total body size). More interesting still, the two groups had differently proportioned limbs: the warmer animals had longer tibiae (corresponding to the human shinbone) but short toes, whilst the cooler animals possessed ‘paddle-like’ limbs with elongated toes. The authors hypothesise that the differences may equip animals for better locomotor performance in their respective environments after hatching, as the fossil record intriguingly suggests that highly aquatic crocodilian ancestors – with more paddle-like limbs – inhabited cool temperate climates whereas extinct equatorial species – with longer legs but shorter toes – were terrestrial. But how could temperature have such a specific effect on limb development? The clue came from observing embryo activity; those incubated at higher temperature made more frequent spontaneous movements within the egg.
Pollard and her colleagues had identified a tantalising correlation between embryonic movement and limb development, but to provide an unequivocal link between the two they had to move to a more convenient organism to investigate: developing chicken embryos in eggs. The team was able to suppress the chick's limb movement with a drug that paralyses muscle contraction. Just like the less active crocodiles at low temperature, the immobilised chicks grew shorter and disproportioned limbs. The researchers also took snapshots of the birds’ development over time and they saw that different parts of the limb were more sensitive to muscle paralysis at different times.
In the final leg of their experiments, the team used molecular techniques to understand how movement is conveyed to the developing bones. They saw that cell division in specific growth zones – ‘growth plates’ – was slowed in the immobilised chicks. They also looked at gene expression in the nascent limbs, which was particularly rewarding during the critical periods when immobilisation had differing effects on growth in different parts of the limb. During one period, 58 genes were differentially expressed in the femur, in which immobilisation affected development, compared with the tibiotarsus (the avian equivalent of the tibia), which was not affected by muscle inhibition. They additionally saw that several genes associated with cell contraction were downregulated in the chicks that had been immobilised.
This intriguing new study demonstrates that embryonic development is not just a passive result of historical natural selection; development can be directly influenced by environment, and animals may be active architects of their own anatomy.
