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The decade the clones came: Beware the mighty Marmokrebs!

The views expressed are those of the author and are not necessarily those of Scientific American.


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At the start of the decade, I had no idea that the invaders were among us. No scientist did.

Invasions are like that sometimes.

We expect invasions to be like H.G. Wells’ War of the Worlds: a large force arrives suddenly, announcing its presence with a voice that cannot be ignored. But sometimes they’re more like Invasion of the Body Snatchers: by the time someone notices, it might too late.

Early in 2000, I got an e-mail from a crustacean discussion list. A pet owner was asking for help identifying a crayfish that had been circulating in the European aquarium community for the last few years. The twist was that pet owners were reporting that single crayfish, kept alone in a tank for their whole life, were giving eggs that reproduced. The list moderator called the message an "interesting one," because of all the crabs, the crayfish, the lobsters, not one other species had the ability to reproduce alone.

I saved the e-mail but mostly forgot about it for years.

Fast forward to 2003, when a paper in Nature [1] confirmed what the German pet owners had been saying since the mid 1990s. These crayfish, which they called "Marmorkrebs," (German for "marbled crayfish") were all female and reproduced without any help from males, thank you very much — a kind of reproduction known as parthenogenesis. But confirming those facts unleashed a raft of other questions.

Where did Marmorkrebs come from? Nobody knew [2]. They weren’t related to European crayfish at all, but looked like species from the southern United States. It wasn’t until this year that it seems we’ve worked out the closest relative: the slough crayfish (Procambarus fallax), found throughout Florida and southern Georgia [3].

How did they get to be parthenogenetic? Even after a decade, this still isn’t clear. One paper reported an almost surreal rumor that these were "test tube" animals created in a Hong Kong laboratory [4]. (This isn’t supported by any other source I’ve been able to find.) Parthenogenetic vertebrates all seem to trace their origins back to a hybridization event [5], but there’s no evidence of this in Marmorkrebs yet.

Another possibility is that parthenogenesis has always been there. A parthenogenetic Marmorkrebs looks the same as a female slough crayfish. Crayfish can store sperm, too, so an adult that has been kept alone for a while can still have babies from a previous mating, which makes it tricky to tell if a male is needed. Indeed, there has been one report of clones in another crayfish [6], but this hasn’t yet been confirmed by another lab.

We’ve certainly been surprised more than once by species that we thought reproduced sexually who we then discovered could reproduce asexually, too. And these were not obscure species, either, but charismatic animals like boa constrictors [7] and the world’s largest lizard, the Komodo dragon [8].

Boas and Komodo dragons birth offspring without fathers, but the offspring are not identical to each other. There are many ways that females can reproduce without males. Which one did Marmorkrebs use? It turned out that they reproduced in a way that made the daughters effectively identical to their mothers [9]. In short, they were clones.

That genetic similarity makes Marmorkrebs a valuable animal for research. Crayfish have been studied in the lab by notables like Thomas Henry Huxley (famed as "Darwin’s bulldog") [10] and Sigmund Freud (who did neurobiology before psychology), and other researchers since. But despite the advantages of being common as dirt and tough as nails, crayfish have never been as popular in the lab as rats.

The classic lab rats are typically white because they are highly inbred to be as genetically similar to each other as possible. This helps reduce variation in experiments, so that effects caused by the experimenters’ manipulations are easier to detect. That Marmorkrebs are more similar than the most inbred white rat might offer new possibilities for studying development [11], aging [12], cancer [13] and more.

While it was clear that all these unanswered questions would make for some great science, the first Marmorkrebs paper came with a warning.

The eight scientists who wrote the paper said that Marmorkrebs "could be a menace."

A menace? Little crayfish?

Oh, yes.

"Crayfish eat everything, and everything eats crayfish," is how one researcher put it. Crayfish are right at the center of the food web, so a lake with crayfish looks utterly different than one without crayfish [14]. In North America, lake after lake has been invaded by rusty crayfish (Orconectes rusticus). The rusty crays eat down the plants until they can’t bounce back, even if you could get rid of all the crayfish [15].

The situation in Europe has been even worse [16]. American crayfish were introduced into Europe for fishing and farming decades ago. But what people didn’t know was that, like the Spanish conquistadors bringing smallpox to the New World, the North American crayfish carried an obscure microscopic organism, a water mold.

The water mold became known as the crayfish plague. The name is no exaggeration. European crayfish species were defenseless against it, and entire lakes have been emptied of native crayfish because of it. If released from the tanks of the pet owners who had discovered them in the 1990s, Marmorkrebs, being a North American lineage, might carry crayfish plague.

And it would only take one to start a population.

But stern warnings don’t stop invaders.

Individual Marmorkrebs popped up here and there in European streams. Only one year after Marmorkrebs were introduced to the scientific community, they were being sold as pets in North America [17]. For all we know, they may have crossed the pond earlier than that.

But the genuine first shock of invasion was on neither continent.

The clone army opened up on a third front in an unlikely place: Madagascar. Crayfish provide an example of the rich biodiversity that the island is known for: The Madagascar crayfish are the only ones in Africa. Some Madagascar communities rely heavily on crayfishing for food and trade.

Marmorkrebs were noticed in the markets in Antananarivo, the capital, around 2005 [18]. The only way Marmorkrebs could have gotten to the island is by being introduced by people. There’s no way to know whether it was accidental or deliberate. Since then, the clonal crays have been spreading rapidly throughout the island, and officials are worried [19]. Besides threatening to oust native crayfish, Marmorkrebs damage rice paddies. "Crayfish eat everything," remember?

Scientists like to think of themselves as being ahead of the curve. In the case of Marmorkrebs, we’ve consistently been about a few years behind events on the ground. Pet owners in Germany report the crayfish to scientists — paper comes out three years later. Marmorkrebs show up in market in Madagascar — paper comes out four years later. This isn’t anyone’s fault; it’s an indication both of how long careful science takes and how rapidly events are unfolding.

The most recent example of this lag was in Germany, where it all started. Another Marmorkrebs had been found there — but after a decade, it was starting to look like northern Europe might dodge a bullet. All the reports of Marmorkrebs in the streams of Europe were just scattered individuals, never any populations [20].

Less than four months later, so many Marmorkrebs were coming out of another pond in Germany that it made the newspapers [21]. Only two weeks later, another research paper [22] confirmed a Marmorkrebs population in another small German lake. In fact, the first paper suggesting Marmorkrebs may have no European populations and the one proving that there is a European population were published back-to-back in the same issue of the same journal.

We started the decade with no idea that these remarkable animals existed. We’ll end the decade with Marmorkrebs as a bona fide invader in Madagascar, established in Germany, released in three more countries (did I mentioned the one in Japan?), and circulating in the pet trade’s gray market in who-knows-how-many places.

But scientific research has helped stop invasions before; radar and cracking the Enigma code helped the Allies defeat the Nazis in World War II. There’s much more research on Marmorkrebs to come in the next decade, both in the lab and the field.

I just hope we can do it fast enough.

References:

1. Scholtz G, Braband A, Tolley L, Reimann A, Mittmann B, Lukhaup C, Steuerwald F, Vogt G (2003) Parthenogenesis in an outsider crayfish. Nature 421: 806-806.

2. Vogt G, Tolley L, Scholtz G (2004) Life stages and reproductive components of the Marmorkrebs (marbled crayfish), the first parthenogenetic decapod crustacean. Journal of Morphology 261: 286-311.

3. Martin P, Dorn NJ, Kawai T, van der Heiden C, Scholtz G (2010) The enigmatic Marmorkrebs (marbled crayfish) is the parthenogenetic form of Procambarus fallax (Hagen, 1870). Contributions to Zoology 79: 107-118.

4. Marzano FN, Scalici M, Chiesa S, Gherardi F, Piccinini A, Gibertini G (2009) The first record of the marbled crayfish adds further threats to fresh waters in Italy. Aquatic Invasions 4: 401-404.

5. Avise J (2008) Clonality: The Genetics, Ecology, and Evolution of Sexual Abstinence in Vertebrate Animals. New York: Oxford University Press.

6. Yue GH, Wang GL, Zhu BQ, Wang CM, Zhu ZY, Lo LC (2008) Discovery of four natural clones in a crayfish species Procambarus clarkii. International Journal of Biological Sciences 4: 279-282.

7. Booth W, Johnson DH, Moore S, Schal C, Vargo EL. Evidence for viable, non-clonal but fatherless Boa constrictors. Biology Letters: in press. DOI 10.1098/rsbl.2010.0793.

8. Watts PC, Buley KR, Sanderson S, Boardman W, Ciofi C, Gibson R (2006) Parthenogenesis in Komodo dragons. Nature 444: 1021-1022.

9. Martin P, Kohlmann K, Scholtz G (2007) The parthenogenetic Marmorkrebs (marbled crayfish) produces genetically uniform offspring. Naturwissenschaften 94: 843-846.

10. Huxley TH (1880) The Crayfish: An Introduction to the Study of Zoology. New York: D. Appleton and Company. 371 p.

11. Vogt G (2008) The marbled crayfish: a new model organism for research on development, epigenetics and evolutionary biology. Journal of Zoology 276: 1-13.

12. Vogt G (2010) Suitability of the clonal marbled crayfish for biogerontological research: A review and perspective, with remarks on some further crustaceans. Biogerontology: In press. DOI 10.1007/s10522-010-9291-6.

13. Vogt G (2008) How to minimize formation and growth of tumours: Potential benefits of decapod crustaceans for cancer research. International Journal of Cancer 123: 2727-2734.

14. Smart AC, Harper DM, Malaisse F, Schmitz S, Coley S, Gouder de Beauregard A-C (2002) Feeding of the exotic Louisiana red swamp crayfish, Procambarus clarkii (Crustacea, Decapoda), in an African tropical lake: Lake Naivasha, Kenya. Hydrobiologia 488: 129-142.

15. Rosenthal SK, Stevens SS, Lodge DM (2006) Whole-lake effects of invasive crayfish (Orconectes spp.) and the potential for restoration. Canadian Journal of Fisheries and Aquatic Sciences 63: 1276-1285.

16. Holdich DM, Reynolds JD, Souty-Grosset C, Sibley PJ (2009) A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowledge and Management of Aquatic Ecosystems 394-395: 11.

17. Faulkes Z (2010) The spread of the parthenogenetic marbled crayfish, Marmorkrebs (Procambarus sp.), in the North American pet trade. Aquatic Invasions 5: 447-450.

18. Jones JPG, Rasamy JR, Harvey A, Toon A, Oidtmann B, Randrianarison MH, Raminosoa N, Ravoahangimalala OR (2009) The perfect invader: a parthenogenic crayfish poses a new threat to Madagascar’s freshwater biodiversity. Biological Invasions 11: 1475-1482.

19. Heimer K (2010) Invasion of self-cloning crayfish alarms Madagascar. Deutsche Presse-Agentur.

20. Martin P, Shen H, Füllner G, Scholtz G (2010) The first record of the parthenogenetic Marmorkrebs (Decapoda, Astacida, Cambaridae) in the wild in Saxony (Germany) raises the question of its actual threat to European freshwater ecosystems. Aquatic Invasions 5: 397–403.

21. Privenau K (2010) Marmorkrebs bringt Pest. Mitteldeutsche Zeitung.

22. Chucholl C, Pfeiffer M (2010) First evidence for an established Marmorkrebs (Decapoda, Astacida, Cambaridae) population in Southwestern Germany, in syntopic occurrence with Orconectes limosus (Rafinesque, 1817). Aquatic Invasions 5: 405-412.

Further reading:

Parthenogensis: Avise, J. 2008. Clonality: The Genetics, Ecology, and Evolution of Sexual Abstinence in Vertebrate Animals. Oxford University Press, New York.

Photo Credits: Amazing Stories cover from http://spec.lib.vt.edu/lifemars/amazing5.htm; Marmorkrebs with eggs from [22]; other photos by Zen Faulkes.

About the Author: Zen Faulkes is an Associate Professor of the Department of Biology at The University of Texas-Pan American. Some of the things that make him geek out are Doctor Who, kaiju, The Human League, Legend of the Five Rings, and film soundtracks. He is @DoctorZen on Twitter, blogs at http://neurodojo.blogspot.com, and is the webmaster for Marmorkrebs.org.

 

The views expressed are those of the author and are not necessarily those of Scientific American.

 






Comments 1 Comment

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  1. 1. shrmnnkfr 10:19 am 12/12/2010

    yeah.. scientists should study these animals…if that happens and its likely that:we can apply that to us humans especially on females..then whats the use of male species? lol

    Link to this

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