Here we have a case of selection by humans—killing elephants that have tusks because ivory is so valuable—increasing the frequency of tuskless African elephants in Mozambique over a 28-year period. (As we’ll see, only the proportion of tuskless females increased.) We have similar examples from other species, as in the reduction of horn size in bighorn sheep hunted for their horns as trophies, and the reduction in the size of some fish due to commercial fisherman going after the big ones.
Is this artificial or natural selection? Well, you could say it’s artificial selection because humans are doing the choosing, but after all human are part of nature. And this selection was not conducted to arrive at a given end. Dachshunds were selected to look like hot dogs to root out badgers in their burrows, but the reduction of tusk size in elephant, or horns in sheep, was not a deliberate target of selection, but a byproduct of greed. So I would hesitate to characterize this as artificial selection, since it’s not like breeders choosing a given characteristic to effect a desired change. In fact, the evolutionary change that occurred is the opposite of what the “selectors” wanted.
You can find the article in Science by clicking on the screenshot below, or get the pdf here. There’s a two page shorter take that’s an easier read, “Of war, tusks, and genes,” here.
The phenomenon: a civil war in Mozambique from 1977 to 1992, which increased the frequency of tuskless female elephants from 18.5% to 50.9%, nearly a threefold increase. Why? A model showed that such a change (which occurs among generations, so it’s not just selective killing within a generation) must have been due to natural selection rather than genetic drift. The killing was motivated by a desire to get money to fund the conflict. A female without tusks had five times the chance of surviving as a tusked female. That imposed strong selection in favor of tuskless females.
Usually, tuskless elephants are at a disadvantage, for tusks are multi-use features, employed for defense, digging holes for water, male-male competition, and stripping bark from trees to get food. But the natural selection to keep tusks in females was weaker than the “artificial selection” by humans against tusks.
Here’s a photo of a tuskless vs. a tusked female:
And the only kind of male that we see: ones with big tusks (tusk size varies, of course, as they continue to grow as the elephant lives). Tusks are homologous with our incisor teeth.
The authors first tried to determine the genetic basis of having versus lacking tusks. It turns out that, by and large, tusklessness behaves not as a complex trait caused by changes in many genes of small effect, but as a single dominant mutation on the X chromosome (like us, elephant males are XY and females are XX). Further, the dominant mutation causing tusklessness is lethal in males, killing them before birth. (This is probably not because the tuskless gene form is itself lethal, but is closely linked to a gene that is a recessive lethal.)
So here are the “genotypes” of the elephants. I’ve used “x” as the gene form on the X chromosome that produces tusks, and “X” as the alternative dominant allele that makes you tuskless.
Males: All have tusks and are thus xY. (Males have only one X chromosome and also a Y.) The XY genotype is lethal, so we never see males carrying the tuskless gene form (XY). Ergo, there are no tuskless males.
Females: We see two types:
Tuskless: Xx. These females will lose half their male offspring because when mated to an xy male (the only viable type), they produce half xY males, which are tuskers, and half XY males, which are lethal. Thus a population of tuskless females will produce a sex ratio in their offspring skewed towards females, which is what is observed.
We never see XX tuskless females because they’d have to inherit one “X” from from their fathers, but that XY genotype is lethal.
With tusks: xx.
There are a few complications, as other genes are involved (for example tusked mothers, who are xx, produce only 91% of tusked daughters when you’d expect the xx by xY cross to produce 100% xx (tusked) daughters. So things are not quite so simple, but in general a single gene seems largely responsible for the tuskless condition. (You might expect this, because if many genes were involved you simply wouldn’t get females lacking tusks: you’d get females with slightly smaller tusks, who would still be killed for their ivory. It would thus take many generations instead of a couple to raise the frequency of tuskless females.)
I won’t go into the gory genetic details, but the authors sequenced entire genomes from tusked and tuskless males and females and looked for signs of natural selection on some genes, comparing the tusked versus tuskless females. (One sign of rapid selection for tusklessness, for the cognoscenti, is the presence of DNA bases recurrent and common near the gene causing tusklessness.)
The researchers found one X-linked gene form with strong signs of selection called AMELX, which in other mammals codes for a protein that leads to the mineralization of enamel and regulates other tooth-associated genes. Another gene not on the sex chromosome, MEP1a, also is associated with tusklessness, but not as strongly. This gene, too, is known to be associated with tooth formation in other mammals. Here’s the diagram from the paper of which parts of the tusk are controlled by which gene. You can see that AMELX is expressed only in the “tusky” part of the tusk:
The upshot: Human-imposed (“anthropogenic”) selection that causes evolution in the wild has been demonstrated before, so this phenomenon is not new. What is new is that the genes involved in an anthropogenic evolutionary change—the increase in frequency of the tuskless allele, which is evolution—have been identified for the first time, and we know the kind of selection that’s caused the evolution. What is also unusual (I know of no other case) is that selection for tusklessness is in opposite directions (“antagonistic selection”) in the two sexes so long as tuskless females survive better. As the authors note:
Physical linkage between AMELX and proximate male-lethal loci on the X chromosome, such as HCCS, may underpin the proposed X-linked dominant, male-lethal inheritance of tusklessness in the Gorongosa population. If our interpretation is correct, this study represents a rare example of human-mediated selection favoring a female-specific trait despite its previously unknown deleterious effect in males (sexually antagonistic selection). Given the timeframe of selection, speed of evolutionary response, and known presence of the selected phenotype before the selective event, the selection of standing genetic variation at these loci is the most plausible explanation for the rapid rise of tusklessness during this 15-year period of conflict.
What of the future? Even though the conflict is over, poachers continue to kill tuskers for their ivory in much of Africa. What will happen? We expect the frequency of the dominant tuskless allele to increase. That itself will not lead to extinction of the population because tuskless males are simply not produced: all tuskless females will remain Xx and produce half the normal number of males. Tusked females will still be produced as Xx females crossed to xY males will produce both Xx (tuskless) and xx (tusked) females. But the reduction in the number of males produced by anthropogenic selection, coupled with continual poaching of both males and females with tusks may drive the population size so low, with an unequal sex ratio, that it could become severely endangered.
Since tusks are good for elephants, the solution is not only to ban the trade in ivory, which has been done in part, but some countries continue to trade in elephant ivory. Further, we must stop the poachers cold, as there’s still a market for both legal and illegal ivory, and prices are high. That’s easier said than done given the area that must be monitored. Note, though, that in 2017, Donald Trump lifted the ban on ivory imports from Zimbabwe, which had been put in place by his predecessor. And the elephant is the Republican symbol!
h/t: Pat, Matt, and several other readers.
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S. C. Campbell-Staton et al.. 2021. Ivory poaching and the rapid evolution of tusklessness in elephants. Science 374, 483-487.
A very good post. Why does it make me so mad. The idea that the human race allows the murder of these great animals is beyond understanding.
I would argue that it is natural selection. Any predator that only went for tusked victims would have the same effect. I don’t think it’s right to call it artificial selection just because one of the animals involved is human.
I think this is the important distinction. If the poachers were deliberately selecting elephants, they’d be breeding for more tusked animals, not fewer.
Nicely put. And thanks as always to our host for an informative and educational post.
Thanks for posting on this.
. A very interesting post. Unfortunately, WEIT risks the charges of transphobia and microaggression because of this phrase: “(like us, elephant males are XY and females are XX)”. Readers should be aware of this danger if they recommend WEIT to anyone else, particularly students. The approved terminology would presumably be “elephant males are assigned at birth XY and females are assigned etc. etc.”.
LOL. I of course was writing this as a biologist, not thinking about gender issues and the like. So I’d reply to those critics: “I was referring to the biological sexes.”
Wow what a cool paper. I read it but didn’t find an explanation why the dominant tusk mutant X is lethal in XY males (with one copy of the mutant) but not lethal in Xx females (who also have one copy of the mutant)? I see that the data are consistent with that model, but I don’t understand how it happened.
Is the explanation that the dominant tusk mutant X just happened to arise first on a sex chromosome that happened to also have a recessive lethal mutation at another gene nearby? And the lethal mutant (at the second gene) is so closely linked to the new dominant tusk mutant X that they only ever occur together?
Then if the dominant tusk mutant X had happened to arise first on a normal sex chromosome without that recessive lethal mutation at another gene, then the mutant X would have swept the population under selection for lack of tusks, and would have eliminated tusks in males as well as females (and without the biased sex ratio among offspring of Xx females).
IDK if I understand this, but it seems to imply a big role for luck (the sex-linked recessive lethal mutant evolving first) in how this system arose before it experienced selection by poachers. Can others help me understand this better? Thanks!
The tuskless mutation is dominant, and is linked to a recessive lethal gene. We don’t get females homozygous for the tuskless mutation as they’d have to get the dominant gene from males, who are lethal. Thus you don’t get lethal females, which would be XX. The original tuskless mutation probably arose on a chromosome that had a lethal very close to new mutation, and that’s why the system behaves as it does. (It had to arise in a female, of course.) Yes, there is luck in the system. Populations are FULL of recessive lethal genes; each human is supposed to carry one or two, but of course we don’t see them because they are recessive. There are also recessive lethals on the X chromosome, but they aren’t expected to hang around long because they are lethal in males, so a third of them are eliminated each generation. The only reason they’re around in this population is because they’re linked to a gene that causes no tusks in females, and originated in a female. Half her offspring would be lethal males, but the other half wouldn’t. Luck is always involved in these cases of a gene linked to a lethal.
Great thank you!
I really like this piece. Thanks for the clear explanation. I wonder if the lethal, linked allele will decouple in time, allowing male tuskless elephants to survive? In the past, such males (if any) would have been gored to death in mating squabbles. Now, however, it could lead to their survival and reproductive success. Of course, poachers will still chase elephants as each animal can make four umbrella stands.
Crossover events at “hot spots” during meiosis can separate the two linked alleles and, for that mating event, yield gametes that have only one of the alleles. Lucky male offspring getting only the tuskless gene would survive — but would they be successful in competing for females as you wonder? An uphill battle deserving a leg-up from us.
The extent to which delinking occurs — linkage disequilibrium— depends classically on the number of base pairs that separate the two alleles and is an all or nothing event. However, if one of the alleles was on a transposable element, a so-called jumping gene, then in principle the two alleles could become widely separated, increasing the chance for independent inheritance. Tusk-less viable males would appear suddenly (for elephants) in that lineage, and such lineages would arise more often than if transposition were not allowed.
Sometimes even a large segment of a chromosome can translocate to another chromosome. These were detected early on because you can see them with low-tech microscopy. They are often deleterious because they don’t preserve the proper “in-line” cis relationship between regulator, promoter, and functional-protein genes. (On the other hand, healthy people don’t have their karyotypes done other than for research, so beware of ascertainment bias.). But if the translocation so disrupted the control of the lethal gene, it might thus cure the genetically lethal condition. Without knowing what the lethal gene does in elephants we can only speculate.
There is obviously more to it than I, a retired non-expert, — is there anything worse?—am just scratching the surface of.
Thank you! This makes sense.
You’re welcome. I was just pleased to be able to use “cis” in a context other than the culture wars. There are “trans” relationships in genetics, too.
Fascinating stuff, Jerry. I suppose similar rapid genetic changes have always occurred when farmers artificially select the animals they like to breed cows etc that don’t much resemble the auroch any more. There’ll be a world of genetic studies yet to be done if we ever overcome our collective squeamishness about GMO farm animals.
They really need to change it to the hippo. Since Nixon’s Southern strategy and even more so since tRump, they’ve gone completely hippo-critical.
The decrease in the size of tusks ( not the same thing as tusklessness) is a longstanding decline. I read (cant remember the source, but I remember it was a reputable one), that the size of tusks had decreased by half between the late ninteenth century and the 70’s of the 20th century . It can hardly just have been that older animals were thinned out. Although that must certainly have played a role, since tusks keep growing throughout life, and the older the faster, it cannot be the sole reason . If selection pressure is so strong that it can select for ‘tuskless’, some more subtle genetic influences must have caused those smaller tusks. We do not see the 2-3 m, 50 -100kg tusks of the 19th century anymore. See eg. the ‘Kilimanjaro tusks’ or the tusks in the museum of Central Africa in Tervuren near Brussels
May I suggest ‘Artificial Natural selection’ for these phenomena?