Mangrove rivulus fish experiencing microgravity in a random positioning machine. Photo credit: Andy Turko.

Mangrove rivulus fish experiencing microgravity in a random positioning machine. Photo credit: Andy Turko.

There is a very good reason why the largest creatures reside in our oceans. ‘The buoyant support of water can explain why whales are so much larger than elephants’, says Andy Turko, from the University of Guelph, Canada. In contrast, the skeletons of terrestrial animals are moulded by the effects of gravity: they can detect and adjust to changes as they gain or lose weight. Which begs the question: can fish skeletons also detect and respond to gravity? ‘Some researchers have assumed that they would never have needed to evolve the ability to sense or respond to gravity’, says Turko; terrestrial animals – including the whale's ancestors – were believed to have evolved the sense only after they left their fish cousins in the water. However, Turko and his colleagues Patricia Wright and Doug Fudge wondered whether the ability to sense gravity is more ancient. Knowing that amphibious fish, such as the mangrove rivulus (Kryptolebias marmoratus), routinely experience the effects of gravity when they clamber onto land, Wright, Fudge and Turko wondered whether the tiny fish can stiffen their skeletons when their weight increases after leaving the water.

Fixing on the 1 mm long gill arch as the most suitable bone in the fish's body to test, Turko and Fudge kept some of the fish on dry land for 1 and 2 weeks, while another group of fish was allowed to remain in water, before comparing the stiffness of their gill arches. Impressively, the gill arch bones of the fish that were out of water were 60% stiffer than those of the submerged fish after 1 week and the effects of gravity persisted for more than 2 weeks after the fish's return to water. However, the team wasn't entirely convinced that they could attribute the bone's increased stiffness to the effect of gravity alone: were they becoming stiffer as a result of drying? Turko and Wright realised that they would have to simulate weightless conditions while the fish were out of water before they could be convinced that gravity was the culprit.

Recalling that Roger Croll, Frank Smith and Matthew Stoyek, from Dalhousie University, used a random positioning machine to simulate the effects of low gravity on developing zebrafish embryos, Wright sent Turko to Dalhousie to test whether the fish's bones became stiffer when they were effectively weightless while out of water. After a week of gyrating the air-exposed fish in microgravity – to simulate weightlessness out of water – and measuring the stiffness of their gill arches, the bones were as flexible as those of the fish that were swimming free. So the bones had not become stiffer because they were drying out. Fish that climb out of water onto land are able to sense the effects of gravity and increase the stiffness of their bones to bear the extra weight.

But how were the high-and-dry fish modifying their bones to increase their stiffness? Extracting proteins from the bones of fish that had spent 2 weeks out of water, Dietmar Kültz, from the University of California, Davis, USA, was impressed to see an extraordinary (ninefold) increase in one protein, type X collagen, which is known to be involved in bone growth. ‘To see such a dramatic increase was exciting evidence that gravity exposure causes bone growth’, says Turko.

Having found that fish are able to sense the effects of gravity, Turko suspects that this ability may help fish to adapt their skeletons to withstand the stresses and strains of swimming. He also suggests that our ancient fish ancestors may have been able to stiffen their skeletons in response to weight gains when they first pulled themselves out of the water. ‘This may mean that something considered a major challenge during the invasion of land by vertebrates (supporting their own body weight) may not actually have been that challenging of an evolutionary problem’, says Turko.

Turko
,
A. J.
,
Kültz
,
D.
,
Fudge
,
D.
,
Croll
,
R. P.
,
Smith
,
F. M.
,
Stoyek
,
M. R.
and
Wright
,
P. A.
(
2017
).
Skeletal stiffening in an amphibious fish out of water is a response to increased body weight
.
J. Exp. Biol.
220
,
3621-3631
.