Culturing Science – biology as relevant to us earthly beings

Invasive species corrupt DNA, not just ecosystems (Fitzpatrick et al., PNAS 2010)

ResearchBlogging.org

I rarely think about how invasive species affect genetics.  It’s always in terms of ecosystems or species: invasive brown tree snakes gobbling up birds and lizards in Guam, or zebra mussels overwhelming and altering the environment of the Great Lakes.  How one species outcompetes and replaces another, changing the natural system.  This is partly because many of the common examples are of predator-prey relationships, where the two species are very distantly related and could never breed, thus keeping genetics out of the picture.  But what about situations where the introduced animal and native animal are similar?

This gets us into the muddy waters of what defines a species.  For sexually reproducing organisms, a species is the group of animals with whom one can exchange genetic material via reproduction, or, in other words, can produce fertile offspring.  To distinguish one species from another under this definition, a scientist would need a pretty wide worldview.  How else could he know that a squirrel from England could not mate with a US squirrel if it tried?  And the honest answer is: he can’t.  (Unless he collected squirrels from around the world and tried to mate them all with one another… but that’s a lot of work.)  Thus, species are often also defined based on location or geography, despite the fact that maybe they could mate if they had access to one another.  But what are the chances that a squirrel will swim across the Atlantic for a new girlfriend?

And there’s where invasive species fit in.  In a paper published this week in PNAS out of Knoxville, TN, Lexington, KY, and UC Davis, scientists studied the Salinas Valley in central California, where salamanders from Texas and New Mexico had been introduced in the 1950s for use as bait by fisherman.  These salamanders, the Barred Tiger Salamanders (Ambystoma tigrinum mavortium) had been defined as a separate species from the threatened native California Tiger Salamanders (Ambystoma californiense), as their populations had been living apart for 3-10 million years, and thus it was unlikely that they were still genetically similar enough to mate.  But – alas – this assumption was wrong.  The invasive salamanders have been mating with the native species for the last 50 years, producing hybrids which are able to mate with either species and one another.  The question: is this hybridization significantly changing the DNA of the native species?

To investigate this question, the researchers identified an introduction site at a pond in central California, and took samples of over 200 salamanders (by clipping the end of their tail and immediately releasing them) at this site and others within a region 200 km north.  Using salamanders of each species from non-invaded ranges, they determined the baseline genetic makeup of each species.

They scanned the genomes of the sampled salamanders (say it 10 times fast) for 68 genetic markers to see if any of the invasive genes had “taken over” the native genes.  They saw no real difference in 65 of these species — that is, the salamanders retained their native genes.  However, they saw a drastic increase in 3 of the genes.  In the figure below, taken from their paper (click on image for larger size),  the little “thermometers” measure the DNA differences at different sites, native in white and invasive in black, with the introduction site indicated by the red arrow.  The upper left (A) shows the big picture: of the 68 gene markers studied total, invasive genes are only apparent at the introduction site.  The other 3 boxes (B, C, D) show the three genes that have spread — and as you can see, they have spread far and deep, despite their invisibility overall (A).  The authors were thorough: they tested whether this pattern was due to either sampling error or random genetic drift without natural selection, and neither of these biases accounted for the pattern of these 3 genes.

The function of these genes is unknown.  However, by studying the behavior of the animals, it seems they are related to reproduction.  The hybrids have larger larvae with greater survival and develop more quickly, ever hastening their dispersal.  This raises a few questions:

1.  If these invasive genes are helping survival, then who cares if they invaded?  It is easy to look at this as actually beneficial to the threatened native salamanders.  However, it has unknown impacts on the surrounding ecosystem.  These bigger larvae eat a lot more, impacting the populations of their prey species through indirect effects of the invasion.  A change in the abundance of one species affects all others – what seems to be an immediate benefit can be incredibly harmful in the long run.

2.  How do we define a species?  The native salamanders are a threatened species.  If they have received genes that increase their numbers through hybridization, is this a comeback?  Are they still A. californiense?  Do these 3 genes alone make them A. mavortium?  Are they an entirely new species?  Is it possible to stop the invasion of these genes throughout the state without killing off a threatened species?

I don’t have the answers to these questions.  We human beings are drawn to classification: we want to put all of the animals in neat little piles and call it fin.  But the truth is that species are eternally evolving — as Peter and Rosemary Grant have shown with their Galapagos finches, most recently in November 2009.  The monkeys that live on one side of a jungle can have a different genetic makeup than the ones on the other side even if they can still mate.

Clearly the introduction of these salamanders, which was just an innocent attempt to raise some bait locally, has had unforeseen impacts on the ecosystem.  Humans’ ability to travel has meant that we are bringing animals together that have not evolved to live together, or have evolved apart millions of years ago.  In some ways it feels like what is done is done — and I am not enough of an expert on habitat restoration to tell you otherwise.  But try little things: wash the mud off of your boots before you go hiking in another state or country, don’t release your foreign pets locally (as my roommate Erinrose and I have been tempted to do with our pet turtle, Nicolas Cage), volunteer at your local wildlife refuge.  Biodiversity is important.

How can we save our planet?

Fitzpatrick, B., Johnson, J., Kump, D., Smith, J., Voss, S., & Shaffer, H. (2010). Rapid spread of invasive genes into a threatened native species Proceedings of the National Academy of Sciences, 107 (8), 3606-3610 DOI: 10.1073/pnas.0911802107

Written by Hanner

March 2, 2010 at 9:43 pm

13 Responses

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  1. Interesting work & cool post!
    What I really like is that this highlights the necessity of comprehensive approaches.. It makes me wonder how much more insight could have been gained if the salamanders were fully sequenced :).
    If ‘only’ 3 out of 68 genes have been replaced (or are in the process of being replaced), I think calling the DNA is ‘corrupted’ is a bit too strong. What it looks like to me is that the sudden influx of new genes into the gene pool simply shifted the balance of genes in favor of some and to the detriment of others. The hybrids have the luxury of receiving the best of both worlds (species) :). In this view, didn’t this invasion in a weird way increase biodiversity (because hybridization is occurring)?

    As you pointed out, it also highlights that our perception of species (on an organismal level) is muddy at best. All species that are alive today and ever lived really form a continuum. Because all the ancestors have gone, it’s tempting to view certain groups as ‘separate’. That this view is an oversimplification is underlined by this story (and supported by many other stories, like the Galapagos finches or the Victoria lake chiclids).
    Thanks for a cool post :).

    Lucas

    March 3, 2010 at 9:02 am

  2. Wow…really interesting post. And congrats on the researchblogging nomination – certainly well deserved :)

    @Lucas: I think that hybridization only increases biodiversity if the hybrid can manage to remain a separate species, rather than the only outcome of two species brought together by invasion. It’s been a while since I studied this though, so might be wrong…

    Lab Rat

    March 3, 2010 at 10:16 am

  3. @Lab Rat That’s certainly true on the level of species! On a gene / genomic level, I’m not so sure though.. In box B for example, now there are two different alleles in the population, where previously there was only the native one.

    Lucas

    March 4, 2010 at 2:59 am

  4. Talking about biodiversity is increasingly difficult since sometimes it can refer to genetic diversity and sometimes “species diversity.” (Whatever that means…) But while hybridization may seem like an increase of biodiversity because it forms an additional “species,” I think this story will not end up that way, with the native salamanders taking on life history traits of the non-native salamanders and, in the end, decreasing the number of phenotypes seen for that trait.

    @Lucas: I think we’ll have to wait and see what happens to these populations to see if genetic biodiversity increases. But if in every population that this gene enters it completely overtakes all loci, we actually lose biodiversity, since it’s the same allele that can be found in New Mexico and Texas. If the California gene can put up a fight, however, I guess it does increase biodiversity. But I’m pretty sure that this doesn’t make invasive species acceptable, since they have other effects besides diversity.

    Hannah

    March 4, 2010 at 7:52 pm

  5. Hannah – a few quick points
    First, nativeness is defined purely by the presumed absence of dispersal by humans (and has been since the 1840s). It’s a pre-Darwinian idea, based on the distinction between natural history and human history. It’s applicability to the modern world is questionable at best, and it certainly isn’t a biological concept. Second, invasiveness and invasibility are two ways of describing the relationship between particular systems and particular taxa. “Invasive” is not a valid type or category of bad species. Third, you’ll have to work much harder to make a case that salamanders mating with other salamanders and producing evidently ‘fit’ offspring damages their population in any way that matters to salamanders. How policing the mating choices or gene flow of salamanders contributes to “saving our planet” is very unclear, indeed.

    Matt

    March 8, 2010 at 3:44 pm

    • Hi Matt,

      Thanks for your comments. I struggle sometimes with the idea of “nonnative” species for the same reason you suggest — it’s hard for me to separate “natural history” and “human history.” Are we not part of nature? How is our movement of species different than other organisms’?

      The problem I eventually find with considering humans a part of nature is that there is no point to conservation. If we are simply organisms living on this earth, if we ignore our moral instincts and feel free to consume or move things around as we wish, there is no basis for trying to protect anything. And that is where I disagree with this argument. It’s true we are animals to a point, but we have evolved empathy. To ignore the fact that we have the ability to care for others besides ourselves and to simply plow through is to go against our very natures. Do you see conservation fitting into a world where we see ourselves as completely enmeshed in nature?

      Secondly, I do agree that it is problematic that this “invasive” gene increases the survival of the salamanders in terms of marking invasives as “bad.” The main problem that I see, however, is not with gene pool diversity or anything like that — but mainly how the increased numbers of salamanders, due to this invasive gene, will effect the rest of the ecosystem. I may not have a PhD, but I have studied trophic indirect effects in many different settings. A small increase in the salamander population may do nothing. But over time, more salamanders means increased predation which trickles on down through the trophic web. That is mainly where I am concerned — looking at it from a system-wide perspective instead of single-species.

      I was being melodramatic when I mentioned saving the planet. You may see me as a hippie conservationist, a nature-lover and not a real scientist. But all these little instances matter in terms of the disruption of ecosystems. And, yes, new systems will follow — but do we want to see systems like those in the overfished Mediterranean where they are dominated by trophic dumps like jellyfish? Some systems will be able to revive and evolve to react to change – but not all can. And I guess I don’t think it’s worth it to take that chance.

      Best,
      Hannah

      Hannah

      March 9, 2010 at 8:03 am

  6. Hannah-

    You seem to be approaching conservation as an all-or-nothing affair: preserve everything or give up on it all. That is, in the original hippie idiom, “a cop out”.

    Like exploitation, conservation means someone has preferences and is imposing them on the landscape. It entails the classic ethical dilemmas: what IS vs. what OUGHT to be; and what criteria apply if the IS appears undesirable. It requires negotiation between all kind of preferences.

    Furthermore, many, perhaps most conservation goals can only be met by continuously intervening in ongoing processes. That means, paradoxically for the all-or-nothing view, that you can only intentionally preserve wildness by artificial means, by fencing and gardening and regulating it, by cutting it off from the ‘real world’ and remaking it according to your own intersts.

    That said, even achieving total consensus about a ‘desired future condition’ is inadequate for making it happen if the system just doesn’t work that way. Everything that IS self evidently CAN BE. The OUGHT you desire may not be achievable for any of a million reasons.

    Left ‘alone’ even nature (personified or not) does not preserve everything. Much the opposite, in fact. What nature do you love? The one that IS, that preserves jellyfish in the Mediterranean and constantly remakes odds and ends into ecosystems, or the ‘past perfect’ one you’ve never seen, know only by rumour, and pine for nostalgically?

    I suggest that you read “Chance and Change: Ecology for Conservationists” (University of California Press, 1998) by William H. Drury, who was a seabird ornithologist and ecologist with Massachusetts Audubon for many years, and a professor at the College of the Atlantic. I will leave you with this quotation from the book:

    “To sum up: Chance and change are ubiquitous; habitats are heterogeneous; selection drives parents to produce great excess of young; death (disturbance) is necessary for life; and movements of individuals are pervasive … I think, in fact, that these, not order and integration, are what allow species to ride out the tribulations of this imperfect world.”

    Matt

    March 9, 2010 at 12:40 pm

  7. Matt-

    I think we’re just going to have to agree to disagree. In the end, I’m still an INFP – and I just don’t feel like it’s right to let systems degrade, even if I’m the organisms don’t care that it’s degrading.

    Best to you,
    Hannah

    Hannah

    March 12, 2010 at 7:43 am

  8. In the end? Are you saying you know everything you need to know? Or everything you want to know? Well, that’s one way to live. But if that isn’t what you mean, accept the challenge. Read Drury, and spend some time thinking about what ‘degradation’ means. It’s a metaphor we bring to studying ecology, not something we learn from it. A raft of subjective, mostly tacit desires underlie the interpretation of change to a system as degradation. Explaining the world in terms of decline and fall due to human failings is a far older habit than doing science, and is (I suspect) rooted in our ability and inclination to imagine a benign world that we’d rather live in than this puzzling, amoral one. It’s the ‘Golden Age’ myth of the Greeks, or the ‘fall of man’ and expulsion from the Garden of Eden in a shiny new wrapper. It’s no accident that many environmental advocacy books have the word ‘paradise’ in their titles.

    Matt

    March 12, 2010 at 4:32 pm

    • No no no, do not think that I am as simple as that. I was just trying to end this thread with a bit of a joke.

      You write as if I am a newbie to these ideas that you’re putting forth and I need enlightening. Well, I hate to break it to you, but I am not. I have spent years performing and questioning conservation work, working for organizations that try to kill or otherwise control invasive species, or promote the reproduction of animals that simply have to habitat left. Over and over I have thought that it was a waste of time: due to the hopelessness of the tasks, the stability of these “degraded” systems, and the fact that if anything besides humans had caused the changes seen, we would be doing nothing about it.

      So I have thought about this before, but thanks for the book recommendation. (It is on my book list now.) I took a while to reply because I have spent several days reworking the arguments in my head. And I agree with you in a lot of respects. But mostly hypothetically, which is what I was trying to succinctly say in my last comment. Because while I am a rational human being, I am also an emotive, empathetic one. So I understand that maybe I strive to fix something that does not need to be fixed because it is not broken – but I treasure biodiversity and life and I will try and promote those the best I can. The worst that happens? I fail and a stable system continues that is not what I had hoped for, and I’ve wasted time and money.

      You may think that I am weak or ignorant for choosing this path – but I don’t think that the brain rules all, and that guts and intuition are worth listening to as well. We evolved them for a purpose, so I’m going to put them to one.

      I am still curious: in your opinion, is conservation worthwhile? And under what circumstances?

      Hannah

      March 12, 2010 at 5:28 pm

  9. This conversation began with the idea of corrupted DNA. But DNA that ‘codes’ for individual fitness under prevailing conditions is the DNA that will persist. That is the entire game of life. How those conditions were generated doesn’t matter to the DNA, or to the organism embodying it. Where the DNA came from doesn’t matter either, unless it fails to persist because we find its origin offensive and act to exterminate it. Let’s see what intuition can do for us, then.

    I suspect we both intuit that humans and human influences are really part of nature–although I may take that farther than you do, because I see technologies as extensions of human anatomy and physiology.

    By the early 1600s Francis Bacon intuited ‘we cannot command Nature except by obeying her’ (or as John Lennon put it later, ‘there’s nothing you can do that can’t be done’).

    In 1832 Charles Lyell intuited ‘the most insignificant and diminutive species, whether in the animal or vegetable kingdom, have each slaughtered their thousands, as they disseminated themselves over the globe.’

    Lyell also wrote ‘We may regard the involuntary agency of man as strictly analogous to that of the inferior animals. Like them we unconsciously contribute to extend or limit the geographical range and numbers of certain species, in obedience to general rules in the economy of nature, which are for the most part beyond our control’. It’s all a messy business that can’t be tidied without making further messes.

    I suspect we both intuit that ecologists can never cobble together anything but a limited inventory and a simplified model of any ecosystem at any given moment, and much less so an accurate, precise account of ecosystem development over time. With so much uncertainty about such complex stochasticity and contigency, conservation action can hardly be approached as a deterministic exercise, nor can its success be judged purely by predetermined criteria.

    That brings us to adaptive management, but (to be intuitively consistent) not of the kind that simply applies new methods to achieving old goals. Conservation action needs to be conceived with considerable tolerance for unforeseen outcomes and developments over time. Deploying ever more intensive, active interventions to make some ‘place’ what we thought it once was (or keep it like we think it is now), or to favor the persistence of any given species does indeed have the potential for making things ‘worse’ by creating dependency on management that may not be sustainable.

    If ‘wildness’ enters your value equation in some positive way, creating or maintaining systems only to meet pre-conceivable goals is actually anti-evolutionary. It denies that ‘nature’ has any adaptive capacity. It entails a very anthropocentric, naive view that evolution is powerless in the face of human agency, that some (again, imagined) past condition and roster of species represented the best of times, and that the future can only be ‘worse’.

    Is extinction worse than relegation to managed habitats? The choice collapses if we lack the capacity to maintain those habitats.

    In the simplest possible terms, I think the best we can do is to leave some room out there and tolerate what survives and what develops from it. Leaving that room is the core decision of conservation. (How to do that and what to leave requires ongoing local negotiation).

    With no apologies to Aldo Leopold fans, we aren’t very intelligent tinkerers, every cog and wheel is not equally important, and the ecological machine, while producing complex collective outcomes, has no particular associated purpose against which to judge any given outcome against any other. Beauty is in the eye of the beholder. Stability and integrity are scale-dependent at best, and imaginary at worst.

    Matt

    March 12, 2010 at 7:21 pm

  10. […] in Peril would like to plug the latest blog post by Hannah at Culturing Science. Hidden in a very well-researched scientific discussion of central […]

  11. […] all started with a blog post, obviously.  In March, I wrote about invasive salamanders and, with a traditional view of invasive […]


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