Gutekunst and colleagues, 2021

Gutekunst J, Maiakovska O, Hanna K, Provataris P, Horn H, Wolf S, Skelton CE, Dorn NJ, Lyko F. 2021. Phylogeographic reconstruction of the marbled crayfish origin. Communications Biology 4(1): 1096. https://doi.org/10.1038/s42003-021-02609-w

 

Abstract

 

The marbled crayfish (Procambarus virginalis) is a triploid and parthenogenetic freshwater crayfish species that has colonized diverse habitats around the world. Previous studies suggested that the clonal marbled crayfish population descended as recently as 25 years ago from a single specimen of P. fallax, the sexually reproducing parent species. However, the genetic, phylogeographic, and mechanistic origins of the species have remained enigmatic. We have now constructed a new genome assembly for P. virginalis to support a detailed phylogeographic analysis of the diploid parent species, Procambarus fallax. Our results strongly suggest that both parental haplotypes of P. virginalis were inherited from the Everglades subpopulation of P. fallax. Comprehensive whole-genome sequencing also detected triploid specimens in the same subpopulation, which either represent evolutionarily important intermediate genotypes or independent parthenogenetic lineages arising among the sexual parent population. Our findings thus clarify the geographic origin of the marbled crayfish and identify potential mechanisms of parthenogenetic speciation.

 

Keywords: None provided.

Allo or auto? Betting on Marmorkrebs origins

In a new article in PNAS, James Mallet writes:

An extraordinary recent case is the marbled crayfish Procambarus virginalis, which seems to have originated via a hybrid between two North American Procambarus species and was likely spread via the pet trade. The marbled crayfish is a triploid hybrid, very likely created in captivity, and is entirely parthenogenetic. After escaping from captivity, it has since spread to become invasive in many European countries as well as in Madagascar.

Mallet cites Gutekunst and colleagues (2018) to support this. But they specifically said, “We do not think Marmorkrebs is a hybrid.”

Alternative hypotheses involving allopolyploid formation with P. alleni appear unlikely due to the lack of hybrid morphological features and the considerable genetic differences.

And it’s not just them. Vogt and colleagues (2016) wrote:

The morphological features and microsatellite patterns strongly suggest that marbled crayfish originated by autopolyploidisation and not by hybridisation with a closely related species, which is by far the most frequent cause of triploidy in animals.

There is some overlap in the author lists of Gutekunst et al. (2018) and Vogt et al. (2016). Having the some of the same authors makes it not surprising that the two papers reach the same conclusions. But they are not the only ones. Martin and colleagues (2016) reached the same conclusion:

Martin et al. (2010) suggested that the Marmorkrebs originated directly from sexual P. fallax without hybridization.

Our data tentatively support this conclusion. Based on the assumption of a hybridization between P. fallax and P. alleni, one would expect that the numerically different karyotypes of these two species would have led to a chromosome number higher than that counted in Marmorkrebs. Furthermore, a preliminary comparison of the nuclear protein coding histone H3 gene (H3) and the nuclear elongation factor 2 gene (EF-2) revealed at least seven polymorphic positions within the EF-2 intron that suggest a non-hybrid origin of the Marmorkrebs.

For a very long time, I would have bet money that Marmorkrebs was a hybrid, because so many cases of asexual reproduction trace back to hybridization events. All of the papers above go on to say that, strictly speaking, there is still a very slight possibility that Marmorkrebs is a hybrid. But hybridization isn’t the way to bet any more.

References

Gutekunst J, Andriantsoa R, Falckenhayn C, Hanna K, Stein W, Rasamy J, Lyko F. 2018. Clonal genome evolution and rapid invasive spread of the marbled crayfish. Nature Ecology & Evolution 2(3): 567–573. https://doi.org/10.1038/s41559-018-0467-9

Mallet J. 2018. Invasive insect hybridizes with local pests. Proceedings of the National Academy of Sciences: in press. https://doi.org/10.1073/pnas.1804081115

Martin P, Thonagel S, Scholtz G. 2016. The parthenogenetic Marmorkrebs (Malacostraca: Decapoda: Cambaridae) is a triploid organism. Journal of Zoological Systematics and Evolutionary Research 54(1): 13-21. http://dx.doi.org/10.1111/jzs.12114

Vogt G, Falckenhayn C, Schrimpf A, Schmid K, Hanna K, Panteleit J, Helm M, Schulz R, Lyko F. 2015. The marbled crayfish as a paradigm for saltational speciation by autopolyploidy and parthenogenesis in animals. Biology Open 4(11): 1583-1594. http://dx.doi.org/10.1242/bio.014241

Gutekunst and colleagues, 2018

Gutekunst J, Andriantsoa R, Falckenhayn C, Hanna K, Stein W, Rasamy J, Lyko F. 2018. Clonal genome evolution and rapid invasive spread of the marbled crayfish. Nature Ecology and Evolution 2(3): 567–573. https://doi.org/10.1038/s41559-018-0467-9

Abstract

The marbled crayfish Procambarus virginalis is a unique freshwater crayfish characterized by very recent speciation and parthenogenetic reproduction. Marbled crayfish also represent an emerging invasive species and have formed wild populations in diverse freshwater habitats. However, our understanding of marbled crayfish biology, evolution and invasive spread has been hampered by the lack of freshwater crayfish genome sequences. We have now established a de novo draft assembly of the marbled crayfish genome. We determined the genome size at approximately 3.5 gigabase pairs and identified > 21,000 genes. Further analysis confirmed the close relationship to the genome of the slough crayfish, Procambarus fallax, and also established a triploid AA’B genotype with a high level of heterozygosity. Systematic fieldwork and genotyping demonstrated the rapid expansion of marbled crayfish on Madagascar and established the marbled crayfish as a potent invader of freshwater ecosystems. Furthermore, comparative whole-genome sequencing demonstrated the clonality of the population and their genetic identity with the oldest known stock from the German aquarium trade. Our study closes an important gap in the phylogenetic analysis of animal genomes and uncovers the unique evolutionary history of an emerging invasive species.

Keywords: comparative genomics • evolutionary genetics • invasive species

Martin and colleagues, 2010

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(3): 107-118. http://www.ctoz.nl/vol79/nr03/a03

Abstract

A mysterious parthenogenetic cambarid crayfish (the Marmorkrebs) has been spreading across the globe for the past decade. We compare this crayfish directly to two other cambarids, Procambarus fallax and P. alleni, that have been suggested to be related or even identical to the Marmorkrebs. Using external morphology and sequences of two mitochondrial genes we show clear correspondences between Marmorkrebs and P. fallax, a species found natively throughout peninsular Florida, USA. Based on these congruent results we suggest that the Marmorkrebs is the parthenogenetic form of P. fallax. This finding has potential evolutionary and ecological implications at several levels. The Marmorkrebs might be a type of geographical parthenogenesis, but a natural population in the wild is so far unknown. Furthermore, challenges arise in regard to the respective species status of the Marmorkrebs. Taxonomically we suggest that the Marmorkrebs is treated as “form” of P. fallax. Last but not least, the identity of this animal and its ecology has an impact for considering potential spread and effects of this species across the globe.

Keywords: 12S rRNA, annulus ventralis, COI, DNA barcoding, species concept, thelytoky

Edit, 29 December 2018: Link to article updated. Really wishing more journals used DOIs...

Hybridization

In vertebrates, nearly every case of parthenogenetic species can be traced back to a hybridization event. Does this mean it’s important to evolution generally? Jerry Coyne, whose main research is speciation, looks at this question.

An experiment gone wrong in Hong Kong?

I was re-reading the recent paper on the introduction of Marmorkrebs in Italy (Marzano et al., 2009), and noticed this:

In their publication on (sic) Nature, the authors even raised the hypothesis that Procambarus sp. is a transgenic species created by laboratories in Hong Kong.

The only Nature paper featuring Marmorkrebs to date is the first one (Scholtz et al., 2003). I freely admit that I miss things, and do not remember everything. But the paper is only one page, so a statement like that would be hard to miss. And I’d like to think I would have remembered a claim that Marmorkrebs were the result of a scientific experiment gone wrong.

I re-read the Nature paper. The words, “Hong Kong” do not appear in it. There is a brief mention of transgenics, but it is in a comment saying that Marmorkrebs would be good for transgenic experiments in the future, not that they were the result of transgenic experiments in the past. For a moment, I wondered in the reference cited (Nam et al., 2000) next to the comment about Marmorkrebs’ potential was from a Hong Kong lab, but the authors of that paper all gave South Korea as their country of origin.

The origin of this comment is almost as puzzling at the origins of Marmorkrebs itself.

Marmorkrebs already sound like they’ve stepped straight out from a science fiction potboiler. You cannot work with an invasive species of female clones (which Marmorkrebs is) without at least thinking of old monster movies or pulp magazines. If they were truly an escaped science experiment? And “made in Hong Kong” to boot? Forget my next grant proposal... I’m going to work on my screenplay.

(I’d cast Michael Praed to play me in the move.)

References

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(2): 401-404 http://dx.doi.org/10.3391/ai.2009.4.2

Nam YK, Cho, YS, Kim DS. 2000. Isogenic transgenic homozygous fish induced by artificial parthenogenesis. Transgenic Research 9(6): 463-469. http://dx.doi.org/10.1023/A:1026596422225

Scholtz G, Braband A, Tolley L, Reimann A, Mittmann B, Lukhaup C, Steuerwald F, & Vogt G. 2003. Parthenogenesis in an outsider crayfish. Nature 421(6925): 806-806. http://dx.doi.org/10.1038/421806a

Rare, threatened, or endangered?

I was listening to an interview with Sarah Pryke on The Science Show. She works with beautiful Gouldian finches (a gallery of them is here). It came up in the conversation that she has about 2,000 of these birds. She estimates that this may well be equal to the number of these birds left in the wild. Which is one of those astonishing thoughts. We forget how many species have most, if not all, of their populations essentially reliant on humans keeping them.

What do you call an animal with no known original wild population? “Extirpated”? No, that’s not quite right. “Extinct in the wild”? That assumes that there is an identified wild population. Regardless, an organism that had known no endemic territory left would be surely be worthy of a conservation effort, wouldn’t it?

Of course, Marmorkrebs fall into such category. We don’t know if they have a home besides our aquaria, or whether it’s under threat or how many Marmorkrebs there might be.

I’ve written a fair amount about Marmorkrebs’ potential to be an invasive species. And while they’ve been introduced into the wild, in Madagascar and elsewhere, but it is far too early to tell what the outcome there will be. If anything, there should probably be some efforts to try to control them in places like Madagascar, because they so obviously don’t belong there.

Nevertheless, it is worth considering the idea that Marmorkrebs might actually be rare, in the global sense. Unless we find a wild population – and there are some reasons to suspect that one might not exist – their future might depend on humans.

And being in that situation has rarely worked out well for the organisms concerned.

The closest relative of Marmorkrebs?

Digging back through the CRUST-L archive again, to bring forth this helpful post from Keith Crandall, dated 24 May 2006.

Scholtz called this crayfish Procambarus fallax in his wonderful paper in Nature describing the most interesting parthenogenesis phenomenon. I was skeptical with that definition (having worked on the Florida crayfish a bit and seeing a picture of the marbled crayfish - it looked much more like a Procambarus alleni to me) and therefore asked a few different folks in Europe to send me tissue samples from the marbled crayfish. I received samples from to different folks (Austria and Germany), sequenced these samples, and compared them to our extensive database of crayfish sequences. Our analyses clearly support the idea that the marble crayfish is indeed a Procambarus alleni - a species native to central and southern Florida in the US.

That said, in some follow-up emails to Keith, he recommended against calling the parthenogenetic marbled crayfish P. alleni and just calling it Marmorkrebs for now.

Early reports from pet owners

I was searching around on some of my old CD backups of data, and I found I had saved a copy of this post from the CRUST-L listserver. To this best of my knowledge, this may have been the first introduction of Marmorkrebs to the English-speaking scientific community. Jeff Shields' comment is wonderfully prescient, as was my recognizing that this post was interesting enough to save, something I don't have a habit of doing.

· · · · ·

Subject: [CRUST-L:629] Re: "Marmor"-Crayfish
Date: Fri, 07 Apr 2000 08:20:57 -0400
From: Jeffrey Shields
To: "Kai A. Quante"
CC: crust-l@VIMS.EDU

Here's an interesting one. Please respond to Kai Quante, and not to me.

Thanks, Jeff

At 11:26 AM 4/7/00 +0200, you wrote:

Hello,

I've a complicated question. Since more than two years it is possible to buy a crayfish in Germany which origin is unknown. The crayfish reaches a maximum sice of 12 cm and is usually brown. In hard alkaline water they become a little bit blue like older ones. In Germany it is called Marmor-Krebs without a scientific name :-(

The interesting thing is that there are reports that crayfishes which were kept alone for there whole life had eggs and childs. All reports say that every crayfish ever kept had eggs once or more in their life....

Please help! We are searching for the scientific name since two years.

THANKS in advance for any kind of help!

Kai

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The message above has been edited to remove potentially obsolete email addresses and web links. Kai Quante does still maintain an aquarium page, but I do not read German and have no idea if it is still up-to-date. And I see now that there's even links to a webpage on "Marmor-Krebs," with further links to notes on reproduction dating from 1997.