Kleptogenesis?

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Lorraine Boissoneault, "Genetic Mystery: The all-female salamanders of the Great Lakes", Great Lakes Now 11/2/2021:

Looking at them, you wouldn’t guess that the unisexual Ambystoma salamanders are any different than the other members of what was once considered their group.

These interlopers were previously grouped with five other mole salamander species: the tiger salamanders with yellow stripes; the blue-spotted salamander, marked as its name suggests; the brownish smallmouth salamander and Jefferson salamander; and the pale streamside salamander. All five species have lithe, wet bodies, bulbous eyes, and cutely smiling faces.

What sets the mysterious unnamed Ambystoma species apart is something that can only be seen by looking at their genetics. They’re an all-female lineage—and they steal genetic material from all five other species of salamander in their region, a feat that would seem impossible if not for the fact that these lady salamanders have been around for more than 5 million years.

“We often get asked, ‘What is the species name for these organisms?’ And the answer is that we don’t have one because they don’t play by the rules of what we would typically call a species,” said Rob Denton, professor of biology at Marian University.

Scientists aren’t quite sure of how these salamanders manage to combine so much divergent genetic material without their offspring having any ill effects. The reproductive process is a little more straightforward. Male salamanders of all these species will leave packets of sperm around the wetlands in the spring. The unisexual females seek out the sperm, absorb it into their own genitals, and this stimulates reproduction. The females can continue seeking out sperm packets and incorporating all that genetic material into their offspring, or they can make simple clones.

As for the females who belong to one of the distinct species, whether it’s the blue-spotted salamanders or the Jefferson salamanders, they can’t mate with males of different species.

Because the process is thought to be totally unique to this line of unisexual salamanders, it was given its own name: kleptogenesis, in which females steal genetic material.

According to Barbara Mable, "Sex in the postgenomic era.Trends in ecology & evolution 2007:

In combining genomic in situ hybridization (GISH), microsatellite genotyping and mitochondrial DNA sequencing with >20 years of data on genomic composition, Bogart et al.  have coined the term ‘kleptogenesis’ to describe the reproductive mode used by these salamanders. They propose that the unisexuals arose through an ancient hybridization event between an A. laterale male and an A. barboui-like female. The most intriguing implication of these studies is that the A. barbouri nuclear genome has been completely replaced, while leaving its mitochondrial genome behind. The current genomic composition of the hybrids has resulted from genome swapping and whole-genome additions as the unisexuals moved into sympatry with other sexual species from which they were able to ‘steal’ sperm (kleptos = to steal).

The cited source for the coinage is Bogart, James P., Ke Bi, Jinzong Fu, Daniel WA Noble, and John Niedzwiecki. "Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes.Genome 2007:

To persist, unisexual and asexual eukaryotes must have reproductive modes that circumvent normal bisexual reproduction. Parthenogenesis, gynogenesis, and hybridogenesis are the modes that have generally been ascribed to various unisexuals. Unisexual Ambystoma are abundant around the Great Lakes region of North America, and have variously been described as having all 3 reproductive modes. Diploid and polyploid unisexuals have nuclear genomes that combine the haploid genomes of 2 to 4 distinct sexual species, but the mtDNA is unlike any of those 4 species and is similar to another species, Ambystoma barbouri. To obtain better resolution of the reproductive mode used by unisexual Ambystoma and to explore the relationship of A. barbouri to the unisexuals, we sequenced the mitochondrial control and highly variable intergenic spacer region of 48 ambystomatids, which included 28 unisexuals, representatives of the 4 sexual species and A. barbouri. The unisexuals have similar sequences over most of their range, and form a close sister group to A. barbouri, with an estimated time of divergence of 2.4-3.9 million years ago. Individuals from the Lake Erie Islands (Kelleys, Pelee, North Bass) have a haplotype that demonstrates an isolation event. We examined highly variable microsatellite loci, and found that the genetic makeup of the unisexuals is highly variable and that unisexual individuals share microsatellite alleles with sexual individuals within populations. Although many progeny from the same female had the same genotype for 5 microsatellite DNA loci, there was no indication that any particular genome is consistently inherited in a clonal fashion in a population. The reproductive mode used by unisexual Ambystoma appears to be unique; we suggest kleptogenesis as a new unisexual reproductive mode that is used by these salamanders.

The male salamanders of various Ambystoma species "leave packets of sperm around the wetlands in the spring", so why call the female/unisexual Ambystomas' actions "stealing" rather than "gathering" or "harvesting"? Maybe it's because there's a well-known Greek compound element klepto- for thief, used in English words like keptomania and kleptocrat, whereas English derivatives of e.g. ἀγείρω "of things, collect, gather" appear not to exist. Or maybe what these salamanders is doing is perceived as immoral as well as unusual?

The Great Lakes Now article is the most recent of several example where this word, and the concepts behind it, have appeared in the mass media:

Rachel Feltman, "How a female-only line of salamanders ‘steals’ genes from unsuspecting males", Popular Science 6/14/2017
Misti Crane, "Unisexual salamander evolution: A long, strange trip", OSU News 7/25/2018
Katie Garrett & Daniel Peterschmidt, "The Unisexuals: A Story of Salamanders and Sex", Science Friday 5/22/2019

[h/t Robert Shackleton]



23 Comments »

  1. J.W. Brewer said,

    November 20, 2021 @ 10:42 am

    "Kleptos" is, as its ending suggests, not the verb "to steal" or any obvious inflected form thereof. I had supposed it might be the related noun ("thief") but that's apparently κλέπτης. Wikipedia has an article on the related biological jargon-word https://en.wikipedia.org/wiki/Klepton. Not sure if that was coined simultaneously with "kleptogenesis" and, if not, which was first and then inspired the other.

  2. Philip Taylor said,

    November 20, 2021 @ 10:52 am

    The OED gives the etymology of 'kleptomania' as :

    Etymology: < Greek κλεπτο-, combining form of κλέπτης thief + mania n.

    Google Translate offers "stupidity" as the English translation of Greek κλέπτoς, but as κλέπτoς is otherwise unattested, this may just be stupidity on Google Translate's part …

  3. Philip Taylor said,

    November 20, 2021 @ 10:56 am

    Oops, my stupidity, not Google's — κλέπτoς may well be unattested, but κλέπτος most certainly is not. And yes, I know they look the same, but the former has penultimate Unicode Character “o” (U+006F) [lower case English 'o'] whilst the latter has penultimate Unicode Character “ο” (U+03BF) [lower case Greek omicron]

  4. Jason M said,

    November 20, 2021 @ 12:04 pm

    not just unique but “totally unique”…ugh.

  5. J.W. Brewer said,

    November 20, 2021 @ 12:15 pm

    The internet is telling me that κλέπτος means "gestohlen" or "verstohlen," which is consistent with it being a sufficiently rare lexeme that English dictionaries of ancient Greek might have omitted it but not so rare as to have escaped notice by the more Teutonically comprehensive Handwörterbuch der griechischen Sprache (1880).

  6. Batchman said,

    November 20, 2021 @ 1:57 pm

    What mystifies me is why the English combining term is spelled klepto- rather than clepto- … is it merely because the terminology did not arrive at us through Latin, unlike most medical terms (for example)?

  7. Jerry Friedman said,

    November 20, 2021 @ 3:01 pm

    Batchman: I suspect it's just the preference of whoever borrowed it. There's also "kinematic" (in physics) and "cinematic", and "leukemia" and "leucocyte".

  8. J.W. Brewer said,

    November 20, 2021 @ 3:03 pm

    @Batchman: You can certainly find the spellings "cleptomania" and "cleptomaniac" in 19th-century and early 20th-century English texts, but the google n-gram viewer suggests that the k-initial spellings became the dominant ones circa the 1850's and never relinquished that position. "Not via Latin" seems as plausible a hypothesis as any. Interestingly, while c-initial spellings are apparently standard in many other Romance languages, French has both "kleptomanie" and "cleptomanie," with (if the google n-gram French corpus is any good …) the k-initial option being the more common one although not by the same ratio as in English. Some sources suggest the word was first coined in French, by Charles Chrétien Henry Marc (1771-1840).

  9. Jerry Friedman said,

    November 20, 2021 @ 4:58 pm

    I see my examples have "k" before "e" or "i", where it affects the pronunciation, so here are some others courtesy of Wikipedia: eureka, kaleidoscope, Koine, krypton, kudos.

  10. Phil H said,

    November 20, 2021 @ 6:59 pm

    Rather than an implication of immortality, I would think the klepto-prefix is motivated by the sense that these salamanders are using sperm that doesn’t belong to them. It’s still an example of anthropomorphism, but not necessarily moralising.

  11. Gregory Kusnick said,

    November 21, 2021 @ 12:22 am

    If I may digress from the main point, I find this sentence curious:

    The unisexual females seek out the sperm, absorb it into their own genitals, and this stimulates reproduction.

    It seems clear that the intended structure is

    (A does X and Y) and (B does Z)

    But somehow the two unrelated conjunctions get collapsed into a single three-item list (X, Y, and (B does Z)). One sees plenty of examples of this in the wild, but it nevertheless seems wrong to me, so I'm wondering what motivates it or whether linguists have an explanation for it.

  12. ~flow said,

    November 21, 2021 @ 6:03 am

    People always want to now the 'why' but linguists often can only assure them they know the 'that' and can surmise 'how'. As such, language is a chaotic system where multitudes of seemingly random factors are competing and the outcomes are essentially unpredictable (although there may be different probabilities to different outcomes).

    One case I find interesting is 'cyber-' as in 'cybernetics', a word first coined to mean 'governance' (France, 1830s) but re-adopted by Norbert Wiener a hundred years later for the modern sense (roughly, 'automated control and regulation'). Maybe because of its French origin (if Wiener was indeed aware of it), maybe for some other reason (euphony?), Wiener chose to use 'cy-' not '*ky-' or '*ku-' for his coinage, otherwise one would talk about '*kybernetics' or '*kubernetics', '*kuberspace' and '*kuborgs' today. In German it's complicated, you have 'Kybernetik' but 'Cyberspace', 'Cyborg', as those latter terms are commonly used in their English forms. The spelling and pronunciation of that 'cy-' [sai-] prefix reiterates or absorbs two thousand years of sound changes in a word made up less than a hundred years ago (which arguably 'kinematics' does to a lesser degree—there are options).

    In another timeline one can imagine Wiener gravitating to 'governance' (because that's what Latin borrowing from Greek 'kyber-' gave us), so in that world we'd talk about '*governetics', '*goverspace' (?) and 'goverborgs' (??). For some reason that sounds less likely than either 'cyber-', 'kyber-' or 'kuber-', but that's maybe down to survivor bias.

  13. David Marjanović said,

    November 21, 2021 @ 7:27 am

    Wikipedia has an article on the related biological jargon-word https://en.wikipedia.org/wiki/Klepton. Not sure if that was coined simultaneously with "kleptogenesis" and, if not, which was first and then inspired the other.

    'Klepton' was coined decades ago.

  14. Jerry Friedman said,

    November 21, 2021 @ 12:26 pm

    Gregory Kusnick: The Fowler brothers called that "bastard enumeration" and said, "a quite unnecessary objection to the repetition of and no doubt supplies the motive."

    https://archive.org/stream/cu31924051009797/cu31924051009797_djvu.txt

    I don't know whether linguists have said anything about in, but the Fowlers' speculation would be mine. I'd add that "A, B, and C" is familiar pattern, and people often don't follow the prescription for parallel structure in many other contexts too.

  15. Philip Taylor said,

    November 21, 2021 @ 12:58 pm

    I don't have a problem with "The unisexual females seek out the sperm, absorb it into their own genitals, and this stimulates reproduction", and wonder whether those who do would find "The unisexual females seek out the sperm, absorb it into their own genitals, and this in turn stimulates reproduction." more acceptable. And would the Fowler brothers have also termed the amended version "bastard enumeration", I wonder.

  16. Jerry Friedman said,

    November 21, 2021 @ 5:40 pm

    Philip: The prescriptive objection to that sentence is that the conjuncts aren't parallel. "Seek out the sperm" and "absorb it into their genitals" are verbs with complements, whereas "this stimulates reproduction" is a complete sentence. Adding "in turn" doesn't change that.

    Of course people write and say things like that all the time, so you're among the many who don't have a problem with it.

    Such constructions can often be analyzed as asyndeton, and this one is an example. You can think of it as two sentences joined by "and":

    The unisexual females seek out the sperm, absorb it into their own genitals

    and

    this stimulates reproduction.

    Is the first sentence acceptable? It would certainly be strange in isolation—but a lot less strange to a lot of people when it's part of the actual sentence.

  17. Batchman said,

    November 21, 2021 @ 6:14 pm

    @Gregory Kusnick: I am pleased that someone else finds this elided "and" syntax annoying. It occurs all too often in professional writing; one can easily find examples in the day's news.

    Grammar texts warn against violating parallelism, but they usually have examples like "I like walking, running, and to swim," which, frankly, nobody ever speaks or writes like. More frequent is something like "He eats fruit, vegetables, and drinks water."

  18. Philip Taylor said,

    November 22, 2021 @ 6:24 am

    I understand the objections, and I thank you for explaining them to me, but nonetheless, from a purely personal perspective, I find the construct unexceptionable, as to me at least the meaning is clear. The females seek out the sperm, they absorb it into their own genitals, and the latter act stimulates reproduction. Could this not legitimately be deemed "elision" rather than "bastard enumeration" ?

  19. D-AW said,

    November 22, 2021 @ 9:26 am

    whereas English derivatives of e.g. ἀγείρω "of things, collect, gather" appear not to exist.

    agoragenesis/goragenesis?

    Cognates: gregarious, aggregate, f. L. grex, a flock; agoraphobia, category, allegory, f. Gk ageirein, to assemble

  20. Jerry Friedman said,

    November 22, 2021 @ 3:40 pm

    Philip: I agree that you could also analyze this one as eliding "they" before "absorb". The question then is whether that is standard, pleasing, or whatever. Again it's mostly the following "and" that licenses the elision. "The unisexual females seek out the sperm, absorb it into their own genitals" would be odd by itself, if that's the criterion.

  21. Kenny Easwaran said,

    November 22, 2021 @ 5:08 pm

    Biologists don't always take the Greek prefixes with precisely the standard Greek meaning. Most biological groups beginning with "eu-" are said to be the "true" versions of whatever follows, while the Greek word really means "good" or "well" or something.

  22. chris said,

    November 23, 2021 @ 7:20 pm

    Surely, you can't steal what is being freely donated? I'm no expert on salamander behavior but it seems to me that the male salamanders are leaving packets of sperm specifically in the hope (if that's not over-anthropomorphizing) that they might be picked up by some lady salamander and used to make salamander babies.

    "Absorb it into their own genitals" seems like odd phrasing to this mammal but presumably a salamander would find it exciting — I almost said "hot" but of course salamanders wouldn't use heat as a metaphor for emotional excitement.

    So if the males were capable of understanding what is going on, would anyone expect them to object?

  23. Kris said,

    November 24, 2021 @ 4:46 pm

    I think some are missing the point on the term kleptogenesis. This is certainly not moralizing on anything, it is giving a name a previously unknown method of reproduction within a species. Male salamanders of a certain species (say _Ambystoma laterale_) are leaving sperm packets around the wetlands. These sperm packets are intended for the reproduction of their own species, but animals from a different species (the all-female non-named species) are collecting them for their own reproduction. Because we call them both salamanders, we don't think of it as stealing for some reason, but in scientific terms I suppose it is. Perhaps better illustrated by a different example. If a species of robin went around stealing reproductive material of orioles, we would more readily consider it stealing even though both are birds. The robins may be threatening the viability or survival of the oriole population. Thus, stealing the genetic material of a different species for their own furtherance. Which is what the unnamed salamander species is doing to the other species of the area.

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