The Ambystoma Complex
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If you took a biology class in middle or high school, you were probably introduced to something called the biological species concept. First proposed in the 1940s by Ernst Myer, the biological species concept defines a species as a group of organisms that are actually or potentially capable of breeding with each other, but not with organisms outside the group. In other words, if two organisms can breed with each other, then they are part of the same species; if they cannot, they are different species. Simple, right?
Well, not really. The biological species concept is often taught and used as a kind of default definition for what a species is because it's so simple and because it emphasizes the documented importance of reproductive isolation in the development of the diversity we see across the tree of life. The problem is that its only really applicable to organisms that reproduce sexually - an organism that reproduces asexually doesn't mate with any other organism, but instead produces clonal copies of itself, making species definitions based on mating largely irrelevant.
What's more, even when we apply the concept only to sexually reproducing organisms, it produces some rather unintuitive results. Grey wolves (Canis lupus), for example, can hybridize with coyotes (Canis latrans). Such events are rare so long as both have members of their own species to breed with instead, but they do happen and, in fact, hybridization seems to have played an important part in the story of canine evolution more generally (Gopalakrishnan et al. 2018). So, do wolves and coyotes belong to the same species? Most scientists would say no, since they clearly prefer not to mate with each other, but you can see how species boundaries can actually end up being quite blurry in taxa that are mostly, but not entirely reproductively isolated.
While checking some trail cameras at work the other day, I came across another critter that mounts a challenge to the biological species concept, but in a way that makes canid hybridization look positively straightforward. It may not look like much, but this little salamander is one of the most wonderfully bizarre vertebrates on the planet. It's so weird that it doesn't even really have a traditional name. Most scientists just refer to it (fittingly, I think) as the Ambystoma salamander complex.
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The origins of the Ambystoma complex can be traced back approximately 5 million years to a hybridization event between two species of mole salamanders in the genus Ambystoma (Bi and Bogart 2010). We aren't exactly sure which two species were involved for reasons that we'll get into later, but what we do know is that their hybridization eventually resulted in several lines of salamanders that are (1) all female and (2) capable of reproducing asexually through a process known as gynogenesis. Gynogens produce unreduced egg cells with two complete sets of maternal chromosomes each. In order to start developing, these unreduced eggs must first be "activated" by sperm, meaning that the all-female Ambystoma complex salamanders must seek out purebred males of a closely related species in the Ambystoma genus to "mate" with. Unlike mating in sexually reproducing organisms, in which sperm and egg cells with one set of chromosomes each fuse into a zygote with two sets, the sperm of the purebred male salamander is not incorporated into the genome of the Ambystoma complex salamander's eggs. Thus, when reproducing via gynogenesis, the offspring of an Ambystoma complex salamander are always clones of their mother.
This is pretty interesting stuff, but it actually isn't what makes Ambystoma complex salamanders so weird. Gynogenesis isn't exactly common, but there are plenty of other organisms out there that reproduce using this method (Schlupp 2005). Fish, amphibians, and insects all include gynogen taxa and most originated in a very similar way to the Ambystoma complex salamanders - via hybridization between two closely related species. Because they depend on sperm from closely related purebred males, some researchers argue that hybrid taxa that reproduce using gynogenesis are not truly reproductively isolated from their parent species and thus cannot be classified as separate from them under the biological species concept (Dubois and Gunter 1982; Schlupp 2005). Others argue that they can be because they reproduce asexually and therefore cannot "truly" mate with their sexually reproducing parent species.
For a long time, Ambystoma complex salamanders were classified as belonging to two species - the silvery salamander (Ambystoma platineum) and the Tremblay's salamander (Ambystoma tremblayi). Species status was justified by T. M. Uzzel (1964), the scientist who first proposed these distinctions, using the second argument I've described above - the two hybrid species were asexual and thus reproductively isolated from their sexually reproducing parent species. Aside from the controversial nature of this argument, the problem was that when these names were proposed and widely adopted, there was no definitive proof that Ambystoma complex salamanders were actually gynogens. The fact that they are all female, have a high egg mortality rate, and are all very similar genetically was good evidence pointing in that direction, but could also be explained by another reproductive system used by all female taxa known as hybridogenisis, in which genetic material from the purebred male partner is incorporated during mating (Lowcock et al. 1987).
Eventually, firm evidence of gynogenesis in Ambystoma complex salamanders was obtained, but it came on the heels of discovering that they seem to be capable of producing both reduced and unreduced egg cells - that is, egg cells with either one or two sets of chromosomes (Sessions 1982; Lowcock et al. 1987). So, what exactly was going here?
Well, as it turns out, Ambystoma complex salamanders are neither exclusively sexual, nor exclusively asexual organisms - they are both. For the most part, they reproduce asexually using gynogenesis - they produce unreduced eggs that are then "activated" by the sperm of purebred males belonging to a closely related species. Sometimes, however, an Ambystoma complex salamander will actually reduce her egg cells and incorporate the genetic material of the male during mating (Bogart et al. 2007; Bi et al. 2008). The resulting offspring will still be all female and will still be able to reproduce using gynogenesis, but they will not be clones of their mother. What causes an individual salamander to incorporate male genetic material or not isn't really clear, but there is some evidence that it may have something to do with whether or not males from a species' whose genes can be incorporated are present or with some intrinsic feature of the particular line that the individual came from (Beauregard and Angers 2018).
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This unique reproductive system is called kleptogenesis and it has some really interesting implications for our understanding of the Ambystoma complex. First, as I mentioned above, it means that it's really hard for us to figure out how the complex originated. There are lines in the Ambystoma complex containing genetic material from at least five different species of salamanders in the Ambystoma genus. All Ambystoma complex salamanders appear to have mitochondrial DNA from a Kentucky population of streamside salamanders (Ambystoma barbouri), suggesting a possible location and maternal parent in the hybrid event that kicked off the complex (Bogart et al. 2007). All known lines also include genetic material from the blue-spotted salamander (Ambystoma laterale), meaning that it may also have been involved; indeed, most Ambystoma complex salamanders look very similar to purebred blue-spotted salamanders and it can be very hard to tell the difference without genetic testing (Bogart et al. 2009). The presence of continued gene exchange between complex and purebred individuals of multiple species, however, makes it hard to say for sure.
Kleptogenesis may also explain why the Ambystoma complex has been around for such a long time. Most researchers agree that organisms that reproduce using gynogenesis probably don't last very long on evolutionary time scales. This is because gynogenesis seems to combine the two biggest disadvantages of sexual and asexual reproduction into one system, requiring two individuals in order to reproduce, but not boosting diversity in the way that sex does (Schlupp 2005). Because they are all clones (with only relatively small genetic differences resulting from mutations), gynogens may not have the population level diversity needed to adapt to rapid changes in their environment. A kleptogen, on the other hand, can introduce diversity into her line by sometimes producing reduced eggs and incorporating male genetic material. The results of this strategy speak for themselves - the Ambystoma complex is the oldest known population of all female vertebrates in the world (Bi and Bogart 2010).
Finally, there is the question of what kleptogenesis means for the biological species concept in general and the taxonomic status of the Ambystoma complex specifically. It seems clear enough that Uzzel's argument for species status isn't going to work for any line that reproduces using kleptogenesis, but there is actually some evidence that a few lines in the Ambystoma complex do reproduce exclusively by gynogenesis (Beauregard and Angers 2018). So, should we classify those lines as species or does their reliance on sperm for egg activation violate the biological species concept? And what about the other lines? If they aren't species, then what are they? Do we take the mitochondrial connection to streamside salamanders or the prevalence of blue-spotted salamander DNA across the whole complex as reason enough to classify them with one of these two species? What would that say about the other three salamander species that contribute sperm to the complex? If they can all mate with a complex salamander that is technically a member of another species, does that dissolve their species status?
Honestly, I think that the big take away from this story is that these kinds of questions don't always have to have solid answers. At the end of the day, the biological species concept is a model, a collection of facts, relationships, and interpretations that we do our best to make correspond with the natural world. In addition to their obvious role in organizing, presenting, and using our scientific understanding of nature, models are also crucial framing devices that inform the kinds of questions that scientists ask when investigating new phenomena. It's a bit like how somebody doing a puzzle will often put together the edge pieces first - having that frame makes it easier to figure out where a new piece goes. Problems can arise, however, if you don't put the frame together right and so have an incorrect picture of what your options are. That's what happened when Uzzel jumped the gun and proposed species status for Ambystoma complex salamanders without definite confirmation that they were actually gynogens.
The biological species concept is a very useful model for understanding part of the story of diversification in sexually reproducing organisms, but as we have seen, has some series limitations when it comes to edge cases and asexuality. In response to these limitations, biologists have come up with a number of other species concepts that have their own strengths and weaknesses. We have yet to come up with a model that coherently incorporates all the empirical data and intuitions that we have about what a "species" is and I really don't think we ever will. What's important is that we learn to use the models we have to appropriately frame questions about biological diversity while always remembering that real nature won't always fit inside.
In their 1987 paper arguing against species status for the silvery and Tremblay's salamanders, Lowcock et al. conclude with an excellent quote from the famous theoretical physicist Werner Heisenberg. I think it sums up what I'm trying to say here much better than I ever could, so I am just going to steal their ending for my own Ambystoma essay:
"What we observe is not nature itself, but merely nature exposed to our method of questioning."
Author's Note: Having written this, I feel compelled to be very clear that I am not a geneticist and that researching this essay required me to read a lot of genetics papers. I am not really qualified to directly evaluate the methods and results of these papers, so I really focused a lot on the abstracts, introductions, and discussions. I did my best to compare my interpretations of what was said there to the interpretations of other authors citing these papers and to people writing about these salamanders in a popular context. I am pretty confident in my research, but it's still possible that I made some mistakes. If you know more about the Ambystoma complex or just genetics in general and think that I got something wrong, please comment or reach out and I will make any necessary corrections. Thanks!
Sources:
Beauregard, F., & Angers, B. (2018). Influence of genome and bio-ecology on the prevalence of genome exchange in unisexuals of the Ambystoma complex. BMC Evolutionary Biology, 18(1), 1-12.
Bi, K., & Bogart, J. P. (2010). Time and time again: unisexual salamanders (genus Ambystoma) are the oldest unisexual vertebrates. BMC evolutionary biology, 10(1), 1-14.
Bi, K., Bogart, J. P., & Fu, J. (2008). The prevalence of genome replacement in unisexual salamanders of the genus Ambystoma (Amphibia, Caudata) revealed by nuclear gene genealogy. BMC Evolutionary Biology, 8, 1-9.
Bogart, J. P., Bartoszek, J., Noble, D. W. A., & Bi, K. (2009). Sex in unisexual salamanders: discovery of a new sperm donor with ancient affinities. Heredity, 103(6), 483-493.
Bogart, J. P., Bi, K., Fu, J., Noble, D. W., & Niedzwiecki, J. (2007). Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes. Genome, 50(2), 119-136.
Dubois, A., & Gunter, R. (1982). Klepton and synklepton: two new evolutionary systematics categories in zoology. Zool. Jahrb. Syst., 109, 290-305.
Gopalakrishnan, Shyam, Mikkel-Holger S. Sinding, Jazmín Ramos-Madrigal, Jonas Niemann, Jose A. Samaniego Castruita, Filipe G. Vieira, Christian Carøe et al. "Interspecific gene flow shaped the evolution of the genus Canis." Current Biology 28, no. 21 (2018): 3441-3449.
Lowcock, L. A., Licht, L. E., & Bogart, J. P. (1987). Nomenclature in Hybrid Complexes of Ambystoma (Urodela: Ambystomatidae): No Case for the Erection of Hybrid" Species". Systematic Zoology, 36(3), 328-336.
Sessions, S. K. (1982). Cytogenetics of diploid and triploid salamanders of the Ambystoma jeffersonianum complex. Chromosoma, 84(5), 599-621.
Schlupp, I. (2005). The evolutionary ecology of gynogenesis. Annu. Rev. Ecol. Evol. Syst., 36, 399-417.
Uzzell Jr, T. M. (1964). Relations of the diploid and triploid species of the Ambystoma jeffersonianum complex (Amphibia, Caudata). Copeia, 257-300.
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