In certain regions of Africa wracked by heavy poaching, people have observed an increased incidence of African elephants without their iconic white tusks, which are prized in the multibillion-dollar wildlife black market. But there has been no direct genetic evidence indicating how this was happening or why this trait was occurring exclusively in female elephants.
A team of scientists, led by researchers at Princeton University, have now implicated two genes associated with mammal tooth development to be at the center of the tuskless elephant phenomenon. And one of these genes is connected to the X-chromosome and is lethal to males, while humans who have that same gene mutation exhibit similar teeth defects.
The paper on theses findings, “Ivory poaching and the rapid evolution of tusklessness in African elephants,” was published in the latest issue of Science with Shane C. Campbell-Staton, assistant professor of ecology and evolutionary biology, and Brian J. Arnold, Schmidt DataX data scientist, listed as co-first authors.
“Elephants are such an iconic species that is so important for the savanna ecosystem and now we have a better understanding of how human activity is impacting them,” said Campbell-Staton.
Other researchers who have contributed to this paper are Robert Pringle, professor of ecology and evolutionary biology at Princeton; Dominique Gonçalves, Elephant Ecology Project Manager in Mozambique’s Gorongosa National Park; Petter Granli and Joyce Poole, co-founders and co-directors of ElephantVoices; and Ryan Long, associate professor of wildlife sciences at the University of Idaho. Campbell-Staton and Pringle are associated faculty with Princeton’s High Meadows Environmental Institute (HMEI), while Arnold, based in the computer science department, is supported by the DataX initiative, parts of which are overseen by the Center for Statistics and Machine Learning (CSML). Long and Poole are former Princeton postdocs.
A Response to a Population Bottleneck
Campbell-Staton, who conceived of the project while at the University of California, Los Angeles, had a hunch that the tuskless phenotype was passed down in the X chromosome, but collecting survey data and blood samples would be key to unraveling this mystery.
To collect these samples, Campbell-Staton and other research team members focused their efforts on the African bush elephants (Loxodonta africana) in the Gorongosa National Park in Mozambique. African bush elephants are considered to be Earth’s largest terrestrial land animal with a height reaching 13 feet at the shoulder, distinguishing it from its smaller cousins, the African forest and Asian elephants. Its tusks can measure up to six feet long and weigh in at 50 pounds each, with the tusks of some male elephants (called bulls) so large that they drag on the ground.
From 1977 to 1992, the Mozambican Civil War ravaged the park with opposing combatants poaching elephants for ivory and meat. The conflict saw a rapid decline in the elephant population, from over 2,500 to around 200 after the war. Along with this steep decline, there was an increase in tuskless female elephants, from 18.5% to 50.9%. Male tuskless elephants have not been seen in the park, but there have been rare anecdotal sightings of them elsewhere.
Arnold said they used simulated numerical models and statistical analysis to determine that a tuskless female elephant was five times more likely to survive versus one with tusks during the war, an example of a very strong natural selection created by poachers.
“Tusks suddenly became a liability, even though in natural circumstances, tusks are very useful organs for elephants,” said Arnold. “There was intense hunting pressure on tusked females. Specifically targeting tusked females gave tuskless females a huge competitive advantage.”
In another part of the study, researchers focused on analyzing the differences of whole genomes between tusked and tuskless elephants with tusked exhibiting fewer rare genetic variants, “which is consistent with a more severe population contraction of tusked individuals,” according to the paper. Crucially, the researchers also found that the condition of tusklessness among female offspring of the war survivors remained elevated at 33% of the population versus 50.9% immediately after the war.
Favorable Survival Trait, Less Fertility
Due to this increase of tusklessness exclusively among females, the researchers surmised that this favorable trait must be associated with the X chromosome. And because there were zero recordings of male tuskless elephants, this inherited trait may be lethal to males. Under this hypothesis, if a female tuskless elephant were to become pregnant with a male, she would spontaneously abort the fetus half of the time, Arnold said.
The researchers tested this hypothesis by undertaking a phenotype/population survey of female elephants and their offspring. Population patterns uncovered that tuskless mothers tended to have offspring that were 65.7% female, which again strongly suggested an X-linked trait with recessive lethality. This would also make these tuskless females less fertile overall, Arnold said.
To trace which genes were responsible for these unique traits, a deep dive into the whole genome was in order. The researchers sequenced genomes from the tusked and tuskless populations from the park and then used bioinformatics software programs to assemble all the data and perform custom analysis. They scanned the genomic data, trying to find genetic regions with strong links to selection by recent poaching and X-linked traits with recessive lethality, among other analysis. They then compared the genomes between tusked and tuskless to find “patterns of genetic divergence.”
“Under the hypothesized model of inheritance, we expected the genomes of tusked individuals to lack the specific mutation(s) causing tusklessness,” the paper read.
Through a series of winnowing down possible regions of the elephant genome that may contain the genes for tusklessness, the team narrowed their focus to the gene MEP1a, which codes for some aspects of teeth formation, and the X-linked gene amelogenin or AMELX, which is responsible for the biomineralization of teeth enamel and the formation of gums and cementum, a type of hard tissue that supports and anchors teeth.
In humans, deletions of AMELX and some nearby genes manifest in a condition called amelogenesis imperfecta, which feature missing or flawed enamel and cracked teeth. In addition, this disorder co-occurs with a syndrome in humans that is X-linked dominant and male lethal. What’s also interesting is that the affected women’s maxillary lateral incisors, a pair of teeth located in the upper row, are either smaller than normal or missing altogether. These incisors correspond to where tusks are located in an elephant’s mouth.
Other studies on mice have pinpointed that another gene, holocytochrome c-type synthetase (HCCS), was connected to recessive lethality and is located next to AMELX. Scientists found out that genetically engineered mice with deletions in this approximate region can have viable male offspring if they force the expression of the HCCS gene.
“It’s fascinating insight into the mystery of how the elephants lost their tusks — a phenomenon that biologists have long been aware of, but that nobody has ever explained,” said Pringle. "It’s a great example of how cross-disciplinary collaborations at the nexus of ecology, evolution and data science can enable us to unlock the answers to important environmental questions."
Besides the genes, there should be interesting implications to the rise of tuskless female elephants in terms of behavior and consequences to the larger environment, said Long.
“Tusks are a defining feature of elephants, and they use them for all sort of behaviors, including digging for water and stripping bark from trees. How individual elephants adapt behaviorally to being tuskless is still a mystery that we're hoping to unravel as we continue working on this project,” said Long. “Some of our preliminary data suggest, however, that tuskless elephants consume different diets than their tusked counterparts. Because elephants are a keystone species, changes in what they eat can affect the entire landscape, so a high rate of tusklessness in an elephant population could very well have ecosystem-wide consequences.”
Arnold said Pringle’s research has shown that tuskless elephants eat different plants than tusked ones, based on sequencing fecal DNA.
While this tuskless condition appears to be proof of humans driving rapid selection in a large herbivore, the research team cautions that further study needs to be undertaken on whether these genetic traits can be found in other populations in Africa.
Meanwhile, since the end of the war, the elephant population in Gorongosa has been steadily increasing, and the park has become a model for wildlife restoration and a vital, important place for research, scientific collaboration and adventure.
“Pursuing this study was probably the greatest adventure of my life so far. I feel incredibly lucky to have been able to team up with such brilliant people from such a wide range of disciplines to study a phenomenon that has been a somewhat of a mystery for quite some time,” said Campbell-Staton.
This research was supported by the University of California, Los Angeles; High Meadows Environmental Institute of Princeton University; National Geographic Society; Gorongosa Project; Crystal Springs Foundation; the Elephant Crisis Fund; Elephant Sanctuary in Tennessee; WildiZe Foundation; Oakland Zoo; Cameron Schrier Foundation; Greg Carr Foundation; and the US National Science Foundation (IOS-1656642 and IOS-1656527).