The ancestors of today's freshwater fishes came from the ocean. Although many fish stayed in the salty waters of the seas, those that moved into freshwater rivers and lakes faced some major challenges such as controlling their salt and water balance, a process termed osmoregulation. Over time, the formerly marine fish adapted to the strange fresh waters of their new home by doing the opposite of what their saltwater ancestors did: taking salt in and keeping water out. But what happens when the newly freshwater fish rediscover their oceanic roots? The prickly sculpin (Cottus asper), an ancestrally marine species with both freshwater and seawater populations, can be found in three types of habitats: inland lakes, coastal lakes and coastal rivers that flow into salty estuaries. Both lake habitats are freshwater, but the inland lakes have been isolated from the ocean longer than the coastal lakes and the sculpins that live in coastal rivers are barely removed from their salty origins. In a recently published study in Physiological Biochemical Zoology, Shaung Liu and colleagues from the University of British Columbia, Canada, investigated how moving into freshwater has changed the prickly sculpin's ability to control its salt balance.

Liu and colleagues suspected that lake sculpins would struggle with the high salt environment of seawater because of their freshwater specialization and that this would be most apparent in populations from inland lakes. After scouring southern British Columbia to collect sculpins from all three of the habitats, they transferred the fish to saltwater for several weeks and compared how well the different populations kept their salt and water levels in check. The freshwater sculpins struggled in seawater because the salt-managing machinery in their gills and intestine wasn't as good as that in their marine counterparts at getting rid of the extra salt.

The best thing that a marine fish can do for salt balance is take in as little salt as possible. When held in seawater, the coastal river sculpins kept sodium and chloride levels in their blood lower than in the sculpins from both lakes, indicating that they did a better job of limiting their salt intake compared with their freshwater relatives. The researchers turned their attention to two protein pumps that are essential for keeping salt balanced in the body, Na+/K+-ATPase and H+-ATPase. They discovered that these proteins from the lake sculpins weren't as good as the river sculpin proteins at keeping salt out of their cells.

Oceangoing fish remove calcium and magnesium salts from the seawater that they drink by producing carbonate pebbles in their intestines as part of the process that reduces the salt levels in their bodies. Knowing this, the team wondered if the sculpins from the saltiest environment – the coastal river – might carry more the pebbles in their intestines than the fish from the freshwater lakes. The researchers counted the number of pebbles in the intestines of the fish from the different habitats. They found that the sculpins from the coastal river had the most pebbles in their intestines and, therefore, were the best at getting rid of salt from the water they had drunk, ensuring that their bodies are well hydrated. In contrast, the sculpins from the inland lakes had very few pebbles in their intestines and have likely lost most of the ability to get rid of salt ions from the water they drink. The researchers also discovered that the number of carbonate pebbles in the sculpin intestines increased with the quantity of Na+/K+-ATPase pumps in the tissue, once again highlighting the importance of this protein for keeping the fish's salt levels balanced, enabling them to survive in freshwater.

Separated from the sea for over 10,000 years, freshwater prickly sculpins have lost some of their salt-regulating skills and struggle when returned to their ancestral habitat. This study emphasizes an underappreciated cost of adapting to a new environment: sometimes it requires losing something that gave you an advantage in the old one.

Liu
,
S.
,
Taylor
,
E. B.
and
Richards
,
J. G.
(
2023
).
Osmoregulatory performance among prickly sculpin (Cottus asper) living in contrasting osmotic habitats
.
Physiol. Biochem. Zool.
96
,
233
-
246
.