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A Stickleback – Full of Worms

Posted July 13, 2018

Around 40 percent of all species on Earth are parasitic – apparently a highly successful way of life. Even a fish such as the three-spined stickleback is plagued by up to 25 different parasites. One of them particularly appealed to Martin Kalbe, Tina Henrich and Nina Hafer from the Max Planck Institute for Evolutionary Biology in Plön: the tapeworm Schistocephalus solidus. The scientists are researching the numerous tricks that host and parasite use to outdo each other.

The three-spined stickleback is a cosmopolitan. Its geographic range extends across the entire northern hemisphere. Originally an inhabitant of the oceans, it probably first migrated to fresh water following the last ice age and now lives in rivers and lakes. Just as in the oceans, parasites are omnipresent in freshwater, too: roundworms, nematodes and tapeworms live at the expense of this small fish; carp lice attach themselves to its skin or in its gills and feed on its blood. Almost every part of the stickleback’s body serves as a home for one parasite or another – even its eye lenses.

Sometimes several tapeworm larvae grow within a single stickleback – in some cases more than 20. Their final weight can be greater than that of the host. The parasites don’t kill the fish, but they deprive it of nutrients, so the stickleback remains smaller than an uninfected conspecific. Credit: MPI for Evolutionary Biology/ M. Schwarz

Schistocephalus, then, is just one of many pests that make life difficult for the fish. Together with Tina Henrich, Martin Kalbe has been collecting sticklebacks and their worms in different regions for many years and has discovered some astounding differences. In Norway, for example, the infection rate in some populations is almost 100 percent, while in others, not a single fish is infected. The fish in Plön come in more toward the bottom end of the scale: out of 4,000 animals, only one is infested with Schistocephalus.

One of the reasons for these differences is habitat. In rivers and streams, parasites are quickly washed away by the flow of water, so they are less common there than in calmer waters. Sticklebacks that live in small, scattered populations are also less afflicted by parasites. And finally, the fishes’ predators also play a key role when it comes to the abundance of Schistocephalus, because only when the worm ends up in the right host can it complete its life cycle and produce eggs.

Initially, once the eggs have spent the winter at the bottom of a body of water, microscopically small, actively swimming larvae hatch. If they become prey and are eaten by a copepod – also known as a Cyclops because of its single eye – they continue to develop to the second larval stage. How-ever, the tiny crustacean is only the first intermediate host. Next comes the stickleback. If the latter eats the Cyclops and the larva manages to pass through the fish’s stomach without harm, it bores through the intestinal wall of the fish. The timing is important: the chances of success are greatest if the larva can develop within the crustacean for 13 to 15 days and then enter the stickleback.

The larva reaches the third larval stage in the fish’s abdominal cavity and massively increases in size and weight. Then it must wait once again until the host is eaten. This is vitally important for the Schistocephalus larva. However, it is also crucially important that it land in the right stomach. In this case, that means the digestive tract of a warm-blooded animal. As a rule, these are fish-eating birds such as herons, kingfishers and cormorants. Only at an ambient temperature of at least 38 degrees can the larvae mature into fertile worms, find a partner and mate. “In Lake Plön, for example, most sticklebacks fall victim to cold-blooded species such as perch and pike. The parasite life cycle thus ends in a cul-de-sac, which is why so few sticklebacks are infected here,” explains Henrich.

Evolutionary Arms Race

The stickleback and its worm are in a permanent competition against each other. Every advantage one of them gains is immediately countered by the other. The result is an evolutionary arms race in which the opponents permanently aim to outdo each other – like two wrestlers who have the appropriate defensive grip ready for each new attack.

The degree to which host and parasite struggle with each other is indirectly revealed when three-spined sticklebacks and Schistocephalus solidus from different areas meet: the tapeworms have even adapted to the small regional differences between the fish. Henrich and Kalbe have caught sticklebacks and their parasites in Canada, Norway and Germany and brought them together in various combinations in their laboratory in Plön. The worms are similarly infectious and grow to the same size when they have infected fish from their respective home. “Schistocephalus from Norway, however, seems to be more aggressive than its German conspecifics, because it infects fish from Lake Plön more often and grows faster in them than a German worm does in Canadian or Norwegian fish,” says Henrich.

The researchers don’t yet know why some local forms of worms are more aggressive than others, but one thing is clear: parasite and host have adapted to each other in such a way that the aggressive worms can exploit the differences between the fish populations to their benefit. And Kalbe and Henrich have gained another surprising insight: if a Norwegian worm and a German worm both infect a fish from Lake Plön, the Norwegian worm remains smaller than if it infects the fish alone. This is only to be expected – after all, it must share the nutrients. But oddly, the German worm, in contrast, grows larger than normal. The Norwegian worm seems to somehow benefit its competitor’s growth – what remains unclear is how.

Differences in adaptation also explain why Schistocephalus solidus infects exclusively the three-spined stickleback: “It has simply become so specialized in this species that it can no longer overcome the defensive strategies of other fish,” says Henrich. Those of the closely related nine-spined stickleback, for instance, which lives in the same waters as its cousin and is parasitized by Schistocephalus pungitii. Although the two tapeworms evolve only in their “own” species of fish, they can interbreed in the laboratory and produce fertile offspring. The hybrid worms that emerge from this interbreeding infest both the three- and the nine-spined stickleback. “So far, however, we haven’t discovered such hybrids in any body of water. We still don’t know why the two species don’t mix in nature even though they could,” says Henrich.

The scientists in Plön aren’t the only ones researching the arms race between the three-spined stickleback and Schistocephalus solidus. The stickleback and its tapeworm have been investigated in the laboratory since the 1960s. Today, a number of research groups worldwide use this fish and its parasite as a model system. One reason for this is that both reproduce relatively easily in the laboratory. The sticklebacks are especially easy to keep; they aren’t too demanding, and they easily lay eggs in commercially available aquariums.

Laboratory Life Cycle

As for the worm eggs, Henrich can store them in the dark for extended periods at four degrees. The larvae hatch when exposed to light. The scientist places each larva, together with a Cyclops, in the well of a laboratory cell culture plate and waits until the little copepod has picked up the parasite larva. She then feeds the infected crustacean to a stickleback.

Only the last step of the cycle deviates from its natural model, as keeping waterfowl and multiplying tapeworms in them would be too time-consuming. Instead, Henrich and her colleagues use a replacement for the bird’s intestine: a small bag of nylon gauze surrounded by a special nutrient solution. Although the bags were originally intended to hold tissue samples in medicine, Henrich must boil them in water for several hours. Only then do they cease to emit substances that are harmful to the worms. In these bags, submerged in a suitable nutrient solution at a pleasant 38 degrees, a worm couple willingly reproduces and eventually releases thousands of eggs.

In this way, the researchers in Plön managed to outwit the parasite and fool it into believing it was in a bird’s intestine. “It’s easier to simulate a final host than to develop an artificial intermediate host. In a bird, Schistocephalus can no longer grow, but only mate and produce eggs. Because the bird isn’t harmed by this, it hasn’t developed any defensive measures to which the worm must adapt. With the stickleback, in contrast, it has such an intimate relationship that it would be extremely difficult to reproduce it in the laboratory,” says Henrich.

Source: MPG

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