A “parthenogenetic” crayfish reproduces without sex: is it a new species?

There must have been more than a dozen readers who sent me links to the article below by Carl Zimmer in the New York Times (thanks, all!). I skimmed it but was more interested in the published scientific papers about the marbled crayfish. This “species”, if you can call it that (see more below), is parthenogenetic—that is, it reproduces without having sex. That means that all individuals are females, and males, who normally contribute sperm in the ancestor, are absent. The population of the marbled crayfish doesn’t need males, and a whole lake can be populated from a single individual. I think Zimmer’s going a bit overboard in saying that the new mutant is “taking over Europe”, but otherwise it’s a reasonable article.

But let’s look at the original papers (links and free access below) to see what’s going on.

It’s pretty simple to summarize, though a bit complex genetically. In 1995 a “marbled crayfish” appeared in the German aquarium trade, apparently originating from a single mutant individual that was a member of the species Procambarus fallax, the “slough crayfish”. Here’s what the marbled crayfish looks like, having a mottled appearance similar to that of its immediate ancestor P. fallax:

Photo: Huetter, C./picture alliance/Arco Images G/Newscom

It’s the only parthenogenetic species of decapod crustacean known (the group contains shrimp, crayfish, lobsters and crabs); and it reproduces by apomictic parthenogenesis—an egg is formed simply by normal cell division, or mitosis, and it’s fertile. No sperm required! This gives a single individual the capacity to invade a habitat and populate it, something that’s possible in sexually reproducing organisms only if the female is inseminated.

That parthenogenesis, combined with the marbled crayfish’s omnivorous diet, means that this thing is a threat, and it is spreading, especially, as the paper of Gutekunst et al. shows, in Madagascar.  Now the parthenogenetic habit doesn’t necessarily mean the species (it’s really a clone, as we’ll see in a second) will replace other crayfish. It may be ecologically different from not only other crayfish species, but also from its ancestor P. fallax, in which case it could persist alongside them. According to population-genetic theory, “mutants” like this are expected to replace sexual forms in the same species, but only if their ecology is the same.  But its ability to eat anything and to invade freshwater lakes with single individuals, makes it a worrisome threat.

How did this thing form? Its formation is in fact the key to its ability to reproduce asexually. It is a triploid: instead of having the normal complement of 184 chromosomes (two sets of 92) it has three sets: 276. (That’s a lot of chromosomes—humans have only 46.) What probably happened is that an ancestral P. fallax produced a diploid egg with 184 chromosomes instead of the normal 92-chromosome haploid egg. That egg then fused with the 92-chromosome sperm of another individual of the species, giving rise to a 276-chromosome triploid.

The triploid can’t make viable eggs by the normal process of meiosis, as that would involve three chromosomes of each type trying to pair and then separate, which would produce a mess. If an egg was even formed by that process, it wouldn’t have full sets of chromosomes, but might be missing some and have extras of others, which, when fertilized, would produce a zygote (incipient offspring) whose development would be screwed up. It could, however, reproduce through normal cell division (mitosis), as that doesn’t require chromosomes to pair. And that’s how this new clone reproduces: producing eggs by simple division of somatic cells.

Along with this there must be some feature of the marbled clone that allows this triploid cell to develop on its own, without the need for fertilization by a sperm. (These clones can mate with P. fallax males, but the transferred sperm doesn’t contribute anything to the offspring.) We don’t know whether the feature that allows this clone to reproduce without sex is a genetic mutation, or is simply a byproduct of a cell having three sets of chromosomes.

To look at the origins of this thing, Gutekunst et al. sequenced its genome: the first full-genome sequence of any decapod crustacean. And what they found was what you’d expect on the origin theory above: the individual had three sets of chromosomes, with two of them nearly identical and one more divergent, but still within the ambit of a P. fallax genome. That means that the species surely originated, as predicted, from an unreduced egg cell of a P. fallax female fertilized by the sperm of another P. fallax male. And comparing the DNA of the clone with those from other arthropods, the authors found this phylogeny, showing the species clustering closest to a crayfish relative, Parhyale hawaiensisan amphipod crustacean.

(from paper): Phylogenetic clustering of 138 orthologues from recently published arthropod genomes. Shimodaira–Hasegawa-like branch support <1 is indicated by numbers.

So what we have here is a clone that reproduces without sex, similar to those viruses and bacteria that reproduce without true meiotic sex (these microbes do have a way of exchanging some genes, though).

But is it a new species? The paper of Frank Lyko (reference below) says it is, naming the triploid clone Procambarus virginalis. On what basis does he deem it a new species? Not morphology, for there are no traits that can absolutely distinguish the triploid clone from P. fallax.  But one can tell the clone genetically apart from the ancestral species because it has a diagnostic mitochondrial DNA. Yet that’s only because the first mutant individual had a unique sequence of DNA in the mitochondria (which all of us do!) that has been passed on to its clonal ancestors. To me, that’s just an arbitrary trait that enables one to tell the clone and ancestor apart, but has no biological significance.

Finally, Lyko notes that the clonal “species” is reproductively isolated from P. fallax: they can’t exchange genes. Reproductive isolation of one group from another is, of course, the biological hallmark of a species, so this deserves closer consideration.  But that alone doesn’t mean that P. virginialis adheres to the classical biological species definition for this reason: individuals within the clonal species are also reproductively isolated from each other! The Biological Species Concept (BSC) notes that a species is “a group of interbreeding individuals that is reproductively isolated from other such groups.” But individuals of P. virginialis aren’t interbreeding: they can’t mate with each other!

Thus, the isolates of the clonal species, left alone in different lakes, could diverge via evolution indefinitely, and one would never be able to test their reproductive compatibility through either observing them in aquaria or seeing what happens if they once again regain contact. In both cases no matings are possible, and thus “interbreeding” cannot be judged.

This means that, like bacteria or other asexual groups, we can’t use the BSC to see if this clone represents a new species. Species delineation in such groups becomes a more or less arbitrary exercise based on degrees of genetic or morphological difference, and there’s no way to tell whether each population of the clone, left in a different lake, will become a different species. Is a single nucleotide difference in the huge genome, diagnostic for a lake, sufficient to delineate a new species within P. virginialis? If not, how much difference is necessary? This is why the species concept is easier to apply in sexually reproducing organisms: if they meet in nature, they either interbreed or not (there may, of course be problematic cases of very limited interbreeding, but in many groups those aren’t a problem).

By deciding to call this a new species, Lyko is making a judgment call—one very different from deciding that Drosophila simulans is a species different from D. melanogaster, since they co-occur in nature but never exchange genes (hybrids are sterile and most are inviable).

Other species of parthenogenetic animals have also been named, like the famous fish Poeciliopsis monacha-occidentalis, which arose by hybridization between two different species but has been asexual for over 100,000 generations. This, too, is now a clone, and the species designation is more or less arbitrary when one takes into account that there is nothing promoting interbreeding or preventing genetic divergence between groups of clones.

So that’s my take on whether this thing is a new species: it’s problematic because the crayfish is an asexual clone. The biology, however, is fascinating, and it would be nice to find out what feature of the single original triploid individual enabled it to reproduce without sex.

____________

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

Lyko, F. 2017. The marbled crayfish (Decapoda: Cambaridae) represents an independent new species. Zootaxa 4363:544-552.

70 Comments

  1. Posted February 8, 2018 at 10:47 am | Permalink

    This is very interesting !

  2. ThyroidPlanet
    Posted February 8, 2018 at 10:52 am | Permalink

    Thank you PCC(E).

    … if I may:

    This is what I do not like about … about … well, you have the biology, the topic, the subject and all that good stuff…

    But then someone goes and writes a headline, and then we have two enormous, separate things to discuss, you see?… I’ll stop there.

    • Posted February 8, 2018 at 11:15 am | Permalink

      I’m not sure what you mean here, but if you’re talking about the NYT headline; well, Zimmer almost certainly didn’t write that, and it’s really not important. The biology is important.

      • ThyroidPlanet
        Posted February 8, 2018 at 11:40 am | Permalink

        The “its taking over Europe” part – put it this way : if I saw that in a news feed, I’d skip the entire thing.

  3. Erik
    Posted February 8, 2018 at 10:55 am | Permalink

    I also had a chance the read the papers (and I summarized them in my Honors class about 2 hours ago). The most interesting aspect for me was the implication that their triploid genome contributed to them being a very successful invasive. There’s also a very informative website for this case:

    http://faculty.utrgv.edu/zen.faulkes/marmorkrebs/

  4. glen1davidson
    Posted February 8, 2018 at 10:59 am | Permalink

    I hope they’re tasty.

    Glen Davidson

    • Jon
      Posted February 8, 2018 at 12:10 pm | Permalink

      yah, my thought, too.

  5. boggy
    Posted February 8, 2018 at 11:04 am | Permalink

    In Europe and Japan and probably elsewhere the signal crayfish, Pacifastacus leniusculus in the 1960’s was imported as the native types were being decimated by the crayfish plague but it turned out that the signals were importing the disease.
    So, it would be interesting to know whether this new arrival is suceptible to the disease.
    Another thought: if it muliplies so teadily and can eat almost anything it could be the answer to the mass famine which threatens the human race.

  6. Eli Siegel
    Posted February 8, 2018 at 11:13 am | Permalink

    I heard that here in Massachusetts there is a species of salamander that exists in two forms – a diploid that reproduces sexually and a triploid that reproduces by parthenogenesis. I would guess that the triploid would be an evolutionary dead end.

    • Lars
      Posted February 8, 2018 at 2:13 pm | Permalink

      That’s the Ambystoma jeffersonianum complex – it’s actually more complex than just two species, and the geographic range extends up to Southern Ontario, but yes, the all-female triploid form is parthenogenic. However, as I recall, female triploids have to mate with male diploids – the male’s sperm contributes nothing to the zygote but apparently the stimulus of the sperm hitting the egg membrane is necessary to stimulate mitosis.

      • Mark Sturtevant
        Posted February 8, 2018 at 8:53 pm | Permalink

        But it could still be a dead end in the sense that it lacks genetic diversity.

  7. Liz
    Posted February 8, 2018 at 11:17 am | Permalink

    Is it possible, though, for these to become different species if left alone in different lakes? This was all very fascinating.

  8. Barry Lyons
    Posted February 8, 2018 at 11:17 am | Permalink

    Thanks for writing about this, Jerry. When I saw the NYT piece I was hoping you’d get around to it. I especially liked how you delineated the problem here, showing that we can’t be sure (yet) to call this a new species. Fascinating.

  9. robmunguia
    Posted February 8, 2018 at 11:25 am | Permalink

    Very interesting, thanks for the post.

    So, because of the lack of genetic exchange between the clones they could eventually form distinct lineages because their differential accumulated mutations along the time.

    • Posted February 8, 2018 at 1:20 pm | Permalink

      Yes, just like bacteria, which is why bacteria (and dandelions, which form asexual clones) are so hard to put into distinct “species”. They tend to spread out into a genetic and morphological continuum.

      The first chapter of my book with Allen Orr, “Speciation” discusses the issue of asexuality and species.

  10. Ken Kukec
    Posted February 8, 2018 at 11:29 am | Permalink

    Parthenogenetic reproduction without sex: Doesn’t sound like much fucking-fun, you ask me.

    Sorry. 🙂

    • Jonathan Wallace
      Posted February 8, 2018 at 12:53 pm | Permalink

      Yes, sex without reproduction is altogether more enjoyable.

  11. TJR
    Posted February 8, 2018 at 11:36 am | Permalink

    Can we do an experiment to change the environment that all the crayfish are in, and see if the sexually-reproducing species adapt to it better than the clone species?

  12. Darrin Carter
    Posted February 8, 2018 at 11:36 am | Permalink

    Supporting science posts

  13. Randall Schenck
    Posted February 8, 2018 at 11:37 am | Permalink

    Very interesting finding. What does the offspring call the parent – Mom and Dad?

    • jhs
      Posted February 8, 2018 at 12:50 pm | Permalink

      If I could clone myself, I would call her “Sista”. 🙂

      • Randall Schenck
        Posted February 8, 2018 at 1:19 pm | Permalink

        Good Grief…then no parents at all. So confusing…

    • Mark Sturtevant
      Posted February 8, 2018 at 8:54 pm | Permalink

      “Hello, older me”. “Hi, younger me”.

    • pck
      Posted February 9, 2018 at 8:18 am | Permalink

      Father, since they’re crawdaddies.

  14. Posted February 8, 2018 at 11:47 am | Permalink

    In the cases which don’t allow use of the BSC, what sort of characteristics should one look for? Or does it matter?

    I regard this as somewhat similar to the case over the use of “planet”. I wondered at the time whether it made sense to have a “comes in degrees” notion there; perhaps that can apply here too.

    • Mark Sturtevant
      Posted February 8, 2018 at 8:56 pm | Permalink

      There are other species concepts, and they can be used if appropriate. The evolutionary species concept might apply here as an argument for a new species. Certainly the BSC can’t.

  15. Posted February 8, 2018 at 11:52 am | Permalink

    I’m here mostly for the science articles like this. I’m not a scientist, but I refer to myself as a 78-yo science nerd. And I’m especially fascinated by evolution. Thanks for the great article.

  16. Hempenstein
    Posted February 8, 2018 at 11:55 am | Permalink

    Thanks very much for the due diligence! Also: Oy! 92 chromosomes!

  17. Paul S
    Posted February 8, 2018 at 11:57 am | Permalink

    Great post. I usually have to read the science posts a few times, but I think I got this one is a single go.

  18. Posted February 8, 2018 at 11:59 am | Permalink

    One might also point out that this case illustrates the still puzzling predominance of sexual reproduction among animals. Lines that can reproduce asexually have a clear advantage (as shown by the invasive spread of this crayfish), so there must be some other “costs” of giving up sex or we would see many more examples like this one.

    • Posted February 8, 2018 at 12:30 pm | Permalink

      They also have a clear DISadvantage- relative to sexually reproducing species they lack genetic diversity. Sexual reproduction provides a population with much more genetic tools that can act as a bulwark for the species’ survival chances in a changing environment. This doesn’t explain why some organisms reproduce sexually while others don’t, but there are advantages to it.

      • Jonathan Wallace
        Posted February 8, 2018 at 12:59 pm | Permalink

        Any potential benefit in terms of the SPECIES survival are unlikely to be the explanation. There has to be a fitness benefit accruing to the individual otherwise faster breeding asexual forms will invade and take over the population irrespective of any species or population level benefit.

        • Posted February 8, 2018 at 1:22 pm | Permalink

          Actually, species selection may be one explanation for the persistence of sexuality, though I don’t think that form of selection is very important. If asexual lineages tend to go extinct more often, and don’t arise very often, then perhaps selection on the species level could contribute to the prevalence of sexual forms. But I do think there must be some individual advantage of sexual reproduction. We just don’t know what it is yet.

          • Mark R.
            Posted February 8, 2018 at 6:18 pm | Permalink

            Do you buy any parts of the Red Queen arguments that meiosis creates an advantage for fighting parasites? (Paraphrasing here.)

          • Posted February 8, 2018 at 9:35 pm | Permalink

            In agree that this might be a situation where species selection is relevant. An asexual lineage is doomed to accumulate mildly deleterious mutations with no way to reconstruct mutation-free offspring. Eventually, that will push the lineage to extinction, a fate that sexual species can avoid by recombination. The disadvantage of asexuals is enhanced by if there are synergistic fitness interactions. (Dickinson, Genetics176:1571, 2008).

            • Posted February 8, 2018 at 9:37 pm | Permalink

              That should be Genetics 178.

            • Johnw
              Posted February 9, 2018 at 9:15 am | Permalink

              I recall Nick Lane observing that asexual eukaryotes usually go extinct in a few million years. Seems plenty of time too reak havoc.

        • Posted February 8, 2018 at 1:52 pm | Permalink

          Yes. I was referring to advantages for individuals. A clonal population has a single set of alleles to deal with contingency – my understanding is that these forms of life get around genetic diversity problems because there are multiple clonal populations. In that view, the different asexually reproducing populations are like individuals in sexually reproducing populations; the clones are subject to selection but there are enough clones for the species to accommodate contingency.

          As I said, I think these selection advantages/disadvantages don’t explain why a species sexually reproduces. I was only addressing your point “Lines that can reproduce asexually have a clear advantage…”. Sometimes they do (as the Crayfish show) but clearly not always as sexual reproduction is common.

          I welcome correction.

  19. Nell Whiteside
    Posted February 8, 2018 at 12:01 pm | Permalink

    Fascinating. Thanks.

  20. nicky
    Posted February 8, 2018 at 12:27 pm | Permalink

    IIRC these asexually reproducing ‘species’, at least those who lost the ability to reproduce sexually, are short lived (ie in biological, paleontological, geological terms) 10’s or 100’s of thousands of years.
    The only exception would be the bdelloid rotifers, of course, and we do not really know how they do it.

  21. davidintoronto
    Posted February 8, 2018 at 12:47 pm | Permalink

    Science post read.

  22. jhs
    Posted February 8, 2018 at 12:53 pm | Permalink

    Thanks. I just learned something new today.

  23. Posted February 8, 2018 at 12:55 pm | Permalink

    If all these parthenogenetic crayfish are essentially clones, does that not make their entire “species” vulnerable to disease and parasites in particular? On the other hand, that parthenogenetic fish species has been around for a long time. Is that just one lucky fish?

    • Posted February 8, 2018 at 1:23 pm | Permalink

      Yes, it could, which is why such groups may go extinct more often than sexually reproducing species. Do remember, though, that mutations will happen even in the clones, which if they’re big enough and have been around long enough, can help them adapt to environmental change (including disease).

      • Posted February 8, 2018 at 1:56 pm | Permalink

        I seem to recall parthenogenetic species also revert to sexual reproduction in response to overcrowding. Do I remember that correctly? Are there other reasons they can switch?

      • Posted February 8, 2018 at 3:11 pm | Permalink

        The advantage, I think, that sex confers is the ability to deliver change to both alleles of an affected gene. In other words, asexual reproduction can result in a helpful mutation to one allele of a diploid organism, which may or may not fully confer a phenotypic advantage. To arrive at mutated alleles in both chromosomes, you need sex. (or wait for the mutation to occur twice in asexual reproducers)

        • Posted February 8, 2018 at 4:38 pm | Permalink

          “or wait for the mutation to occur twice in asexual reproducers”

          Wouldn’t half the asexual creature’s offspring have the mutation in both alleles? So that wait would be very short.

          • Posted February 8, 2018 at 5:08 pm | Permalink

            Asexual reproduction results in exact copies or clones of the parent. In order to derive a homozygous mutant asexually, both alleles would have to mutate spontaneously; obviously a very rare event. Both can produce heterozygous mutants, but only through sex are homozygous mutants readily available (in the next generation).
            Sex, then, is the R&D lab of a lineage. It allows unfavorable mutations to be hidden (as heterozygotes) and favorable mutations to be readily available. It allows you to tinker with an allele with little penalty for malfeasance, and rewards you if the tinkering is favorable. The monkeys banging on the typewriter can write War and Peace in no time if they can hide the garbled words and preserve the the intelligible ones.

  24. Posted February 8, 2018 at 1:50 pm | Permalink

    As a plant taxonomist, I’d say, “Of course those parthenogenic crawfish can be treated as a species.” We botanists like the Biological Species Concept. It’s our first choice. However, in many cases, like this one, it can’t be applied. It sounds to me like the parthenogenic form has a different ecology, being much more invasive. We have reasons to want to talk about this crawfish. We can call it a species.

    (Classification is a human activity, hopefully reflecting biology but not equal to biology.)

    For asexual species, most of us agree that we have to accept a higher level of intraspecific variation than in a typical sexual species because, as you say, we get lots of mutant clones out there that look a little different.

    The worst to classify, actually, are plants that combine mostly asexual reproduction with occasional sexual reproduction. You get clones distinct enough to name, plus “hybrids” of those clones, each “hybrid” forming another clone, ad infinitum. Examples include blackberries and crabapples.

    • HBB
      Posted February 8, 2018 at 2:45 pm | Permalink

      I’m not a botanist, so I didn’t want to “speak for the trees,” but IMO this seems like a good way to think about these cases of animal parthenogenesis. I have not read the papers closely, but this crayfish seems like a good place to apply the Phylogenetic Species Concept in the sense that it appears to be monophyletic with respect to mtDNA anyway.

    • Posted February 8, 2018 at 3:04 pm | Permalink

      One way to think of it is that the evolutionary future of the triploid, parthenogenic crawfish is irredeemably separated from the future of its diploid, sexual ancestor. Therefore, it is a different species.

      • Posted February 8, 2018 at 5:29 pm | Permalink

        I sort of agree; you have to use a different species concept in organisms that are asexual. We discuss this in chapter 1 of speciation. The problem is that every lineage within a clone that has a new mutation is “irredemably separated from the future” of all other individuals in that clone. Would that lineage then be a new species within the clone? How much genetic differentiation would it take? With these crawfish, you could have a gazillion different “species” within the descendants of that first mutant crayfish.

        • Posted February 8, 2018 at 8:31 pm | Permalink

          Very true. Which is why we prefer to accept more variation with in an asexual variation in a asexual than a sexual variation. The urge to be split can’t always be resisted, but it should be controlled!

  25. Lars
    Posted February 8, 2018 at 2:16 pm | Permalink

    apomictic pathenogenesis

    …spelling error, I believe.

  26. Posted February 8, 2018 at 2:41 pm | Permalink

    Thank you, great post and very interesting commentary. I’ve learned quite a bit.

  27. Steve Pollard
    Posted February 8, 2018 at 3:05 pm | Permalink

    A very interesting article; many thanks for putting it up, and for explaining the science issues so clearly.

    There has been a bit of a problem in the UK with the invader signal crayfish (Pacifastacus leniusculus) outcompeting the native Austropotanobius pallupes (Hope to heck I’ve got those names right). Last thing we need is a predatory clone joining in.

  28. eric
    Posted February 8, 2018 at 3:56 pm | Permalink

    Very cool science.

    As for the species question, I expect the issue of clones are going to come up more often as science creates more viable ones. I have no problem broadening the definition of species to include groups of clones that are biologically incapable of ‘back-mating’ with the originator species. I agree with PCC that that’s nothing but a judgement call, but it makes more sense to me than claiming each individual in that group of clones is it’s own species – which seems what PCC’s logic taken to its natural end would imply.

  29. GBJames
    Posted February 8, 2018 at 4:48 pm | Permalink

    Thanks for a great post!

  30. cruzrad
    Posted February 8, 2018 at 5:17 pm | Permalink

    Great post, thanks!

  31. Posted February 8, 2018 at 5:40 pm | Permalink

    I think that for non-sexual reproducers, the species concept has little sense anyway.

  32. Hemidactylus
    Posted February 8, 2018 at 5:54 pm | Permalink

    There are invasive species of gecko rampant in Florida, one of which Hemidactylus garnotii is parthenogenic. I used to catch them and keep as pets. They would just lay eggs. Very cool critters. Cute, cuddly, with a beautiful chirp when agitated. Although “invasive” I give them a pass. Love seeing them stick to the walls. They seem to cold stun easily. Have scooped apparently dead ones up in buildings and my skin warmth brings them back. Bring them outside to sunlit area. Guess I am facilitating the invasion of my peeps.

    http://myfwc.com/wildlifehabitats/nonnatives/reptiles/indo-pacific-gecko/

    https://srelherp.uga.edu/lizards/hemgar.htm

  33. Posted February 8, 2018 at 10:01 pm | Permalink

    Fascinating!

  34. rickflick
    Posted February 8, 2018 at 11:15 pm | Permalink

    So I wonder why such a creature would not be genetically vulnerable. They lack the ability to introduce new gen combinations through sex which would allow it to adjust to changes in the environment. More generally, why do most species have sex? Is the advantage great enough so we can predict the crayfish has no long-term future?

  35. Darren Garrison
    Posted February 9, 2018 at 2:16 pm | Permalink

    In SF, I believe that this is a “cray goo” situation.

  36. David Fuqua
    Posted February 11, 2018 at 7:38 pm | Permalink

    Great explanation of the genetics.

  37. David Fuqua
    Posted February 11, 2018 at 7:39 pm | Permalink

    Great explanation.

  38. Posted February 16, 2018 at 10:38 am | Permalink

    Helpful synopsis. The BSC has always been a brute instrument for delimiting related groups, and the asexual marbled crayfish is a perfect example of the subjective calls we often have to make.


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