Guenon Monkeys Cross Species Boundary

“Jimmy” is a hybrid male monkey in Dr. Kate Detwiler’s study group in Gombe National Park. Photo credit: Manano Mpongo/ Gombe Hybrid Monkey Project

By Gisele Galoustian

Leakey Foundation grantee Kate Detweiler from Florida Atlantic University is the first to document that two genetically distinct species of guenon monkeys inhabiting Gombe National Park in Tanzania, Africa, have been successfully mating and producing hybrid offspring for hundreds maybe even thousands of years. Her secret weapon? Poop.

Prior studies and conventional wisdom have suggested that the physical characteristics of guenon monkeys with a variety of dazzling colors and very distinct facial features like bushy beards and huge nose spots are a function of keeping them from interbreeding. The idea is that their mate choices and the signals they use to select a mate are species specific and that they share common traits linked to their species.

So if their faces don’t match, they shouldn’t be mating, right? Wrong, according to evidence from a novel study published in the International Journal of Primatology.

For the study, Detwiler, who first studied these monkeys in Gombe National Park in 1994, examined the extent and pattern of genetic transfer or gene flow from “red-tailed” monkeys (Cercopithecus ascanius) to “blue” monkeys (Cercopithecus mitis) due to hybridization.

These two species are the only forest guenons that colonized the narrow riverine forests along Lake Tanganyika that characterize Gombe National Park. They co-exist in the same forests as Jane Goodall’s chimpanzees and baboons. Detwiler identifies hybrid monkeys by their combined markings from both parental species. She estimates that about 15 percent of this population is made up of hybrids, which is very unusual.

Kate Detwiler, Ph.D., lead author and an assistant professor in the Department of Anthropology in FAU’s Dorothy F. Schmidt College of Arts and Letters, who first studied these monkeys in 1994, collects fecal samples from monkeys in Gombe National Park. Photo credit: Amelia Villaseñor

Using mitochondrial DNA, extracted non-invasively from the feces of 144 red-tailed monkeys, blue monkeys, and hybrids, Detwiler is the first to show the movement of genetic material from one guenon species to another in an active hybrid zone. After examining the fecal samples, she found that all of the monkeys – hybrids, red-tails and blues have red-tailed mitochondrial DNA – all traced back to female red-tailed monkeys.

For this lineage of monkeys, it is the first time that science shows that not only is the DNA there, but so are the hybrids. Detwiler used mitochondrial DNA because it is more abundant than nuclear DNA in fecal samples, and only comes from the mother – indicating the maternal species in the hybridizing pair.

“There’s a lot of promiscuity taking place in Gombe National Park. Red-tails are mating with blues, blues are mating with red-tails, blues are mating with blues, red-tails are mating with red-tails, and hybrids are mating with everyone,” said Detwiler. “But we’re just not seeing any negative consequences from these two very different species repeatedly mating and producing offspring on an ongoing basis. If the differences in their facial features are so important and signal that they shouldn’t be mating, then why is this happening and why do I keep finding hybrid infants?”

A key finding from the study shows that the blue monkeys in Gombe National Park emerged out of the hybrid population, tracing their origins back to hybridization events between resident red-tails and blues most likely from outside the park. For her control groups, Detwiler collected and examined feces from blue monkeys from a park to the north and a park to the south where hybrids do not exist. These monkeys only had blue monkey mitochondrial DNA.

Detwiler speculates that red-tailed monkeys got to Gombe National Park first and thrived in the environment. Male blue monkeys outside the park had to find new homes after they were kicked out of their groups, which happens when they reach sexual maturity. Sex-driven, they ventured out into the landscape to find appropriate mates – female blue monkeys. Instead, they found the red-tailed females. Apparently, some female red-tailed monkeys were attracted to novel males with different faces and welcomed the sexual advances from these male blue monkeys.

“I keep coming back to the idea that if they are only supposed to mate with their own kind, then why did these red-tailed monkeys mate with the blue monkeys, especially if they had males of their own species around,” said Detwiler. “The female red-tailed monkeys present as willing partners and they are not coerced or forced into copulation with blue monkeys.”

Today, Gombe is an isolated forest habitat. Because they are very social and have had to share close quarters for decades or even centuries, Detwiler believes that they have socially learned that if you grow up in a hybrid group it is okay to mate with everyone.

“The Gombe hybrid population is extremely valuable because it can be used as a model system to better understand what hybridization looks like and how genetic material moves between species,” said Detwiler. “We have this amazing laboratory in nature to help us answer many questions about hybridization and how species boundaries are maintained. This research is very timely because hybridization often occurs in response to environmental changes, as we are seeing with climate change and modified landscapes — it is nature’s way to respond.”

This work was funded by a faculty research seed grant from FAU’s Division of Research, FAU’s Department of Anthropology, and doctoral dissertation research grants from the NSF (0424444), The Leakey Foundation, and the Wenner-Gren Foundation.

Video credit: Maneno Mpongo and Elizabeth Tapanes/Gombe Hybrid Monkey Project

Mapping Trees Can Help Count Endangered Lemurs

By Robin Ann Smith, Duke University

Putting a figure on the number of endangered lemurs left in the wild isn’t easy, but researchers say one clue might help: the plants they rely on for food. Photo by David Haring, Duke Lemur Center

The vast majority of lemur species are on the edge of extinction, experts warn. But not every lemur species faces a grim future. A study funded in part by The Leakey Foundation has shown that there may be as many as 1.3 million white-fronted brown lemurs still in the wild, and mouse lemurs may number more than 2 million.

“For some lemurs, there may be healthy populations remaining and our conservation efforts are preserving them,” said lead author James Herrera of Duke University.

The findings come from statistical modeling techniques that estimate the total population sizes and geographic ranges for 19 of the roughly 100 recognized lemur species across Madagascar by using the plants they rely on for food as a proxy for counting animals.

These tree-dwelling primates eat mostly fruits, leaves and flowers, such as African star apples, mangosteens, tamarinds and figs across Madagascar, the only place in the world where lemurs live in the wild.

In a study published August 30 in the Journal of Biogeography, researchers show that lemurs are less abundant in areas that lack certain tree species — even when environmental conditions such as temperature, precipitation and elevation are otherwise suitable.

Using this relationship, the team was able to come up with the first estimates of total population size for some lesser-known species, such as Crossley’s dwarf lemur. These estimates can be critical baseline data for managing what’s left.

About 95 percent of all lemurs are at risk of extinction because of deforestation, hunting and other factors. Since the 1950s, lemurs have lost more than 40 percent of their habitat. Tens of thousands of acres of forests each year are logged, cleared to make way for farms and pastures, or burned and harvested as charcoal.

But getting reliable population numbers for these elusive animals in the remote and rugged terrain where they live isn’t easy. Counting every individual is impossible. One alternative approach, based on statistical modeling, uses the correlation between species densities at a subset of sites and environmental conditions at those locations to infer how many individuals are present over larger areas.

Lowland rainforest,Masoala National Park, Madagascar. Photo by Flickr user Frank Vassan, CC-BY-2.0

Between 2011 and 2016, teams of researchers walked across Ranomafana National Park, Makira Natural Park and Masoala National Park in Madagascar, searching for lemurs.

“We would wake up at 4:30 or 5:00 in the morning, hike for six to eight hours to look for lemurs, and then go back out at night with our headlamps on to search,” said Herrera, a postdoctoral associate in Duke professor Charlie Nunn’s lab.

“A lot of these species are small nocturnal animals that are only active at night,” so researchers rarely see them, Herrera said. “You can walk for hours and not see a single lemur.”

Overall, they compiled data from more than 2,000 lemur sightings, as well as more than 3,000 sightings of the trees they eat.

Using these records, along with climate data from each location, the researchers identified other suitable areas for each of 14 lemur food trees across the 225,000-square mile island.

Then they used the resulting tree maps, along with temperature, rainfall, elevation and other data, to estimate the potential population size of each lemur species across its range.

This technique — incorporating tree distributions in addition to climate — proved more accurate than methods that estimate lemur numbers and ranges using climate alone.

Several species had populations that were smaller than anticipated.

The researchers estimated there were still 15,000 to 20,000 red-fronted brown lemurs in Madagascar in 2014. That’s down as much as 85 percent from the approximately 100,000 estimated in 2000, by a separate study based on lemur surveys and satellite images of the remaining rainforests.

Bamboo lemur populations may have shrunk by half over the last two decades, a study has shown. Photo by David Haring, Duke Lemur Center

Another species, the gentle bamboo lemur, may have shrunk by half in less than two decades, from roughly 20,000 individuals to 9,000-10,000.

The steep declines are partly due to continued habitat loss, the researchers say. Madagascar lost more than 380 square miles of forest per year between 2010 and 2014.

But numbers for other lemur species weren’t as low as they feared.

This study estimated roughly 50,000 red-bellied lemurs remaining, almost twice the figure estimated 14 years earlier.

What’s more, the study found that 16 of the 19 species had potential population sizes greater than 10,000 individuals, the threshold considered by the IUCN to be at risk of extinction.

“It was actually pretty good news for some of these species,” Herrera said.

Many of these species may still be at risk because of bushmeat hunting or the pet trade, which their models don’t account for, the researchers say.

But they hope their approach, in combination with measures of hunting pressure and other threats, will lead to more refined estimates of species’ vulnerability to extinction in the future, for lemurs or other animals.

This research was supported by the National Science Foundation Graduate Research Fellowship Program and SBE35 IBSS Postdoctoral Research Fellowship Program, a Turner Fellowship, an AGEP-T-FRAME Scholarship, Primate Conservation, Inc., the American Society of Primatologists, the International Primatological Society, the Primate Action Fund, La Conservatoire pour la Protection des Primates, Seneca Park Zoo, the Explorer’s Club Eddie Bauer Youth Award, the Margot Marsh Biodiversity Foundation (39 023815), the Mohamed bin Zayed Species Conservation Fund (1025935), the Rufford Small Grants Foundation, the Leakey Foundation, the Oregon Zoo, the National Geographic Society Conservation Trust (C135-08), and the David and Lucille Packard Foundation.

CITATION: “Estimating the Population Size of Lemurs: Modeling Lemurs Based on Their Mutualistic Food Trees,” James P. Herrera, Cortni Borgerson, Tongasoa Lydia, Pascal Andriamahazoarivosoa, B. J. Rodolph Rasolofoniaina, Eli R. Rakotondrafarasata, J. L. Rado Ravoavy Randrianasolo, Steig E. Johnson, Patricia C. Wright, Christopher D. Golden. Journal of Biogeography, August 30, 2018. DOI: 10.1111/jbi.13409

Seeing the World Through a Tarsier’s Eyes

By Sam Gochman

Opportunities like demonstrating our Tarsier Goggles at The Leakey Foundation’s 50th anniversary gala do not come often. So when we were invited to attend, we happily accepted and made our way from Dartmouth College to the St. Regis. The event proved to be informative from both anthropological and design perspectives, not to mention a great celebration!

Sam Gochman (left) and Benjamin Cooper (right) demonstrate their work designed and developed at Dartmouth College.

Tarsiers are small (tennis ball-sized) nocturnal primates that have the largest eyes relative to body size of any known living or extinct vertebrate. Their enormous eyes are thought to enhance visually-guided predation by increasing visual sensitivity in dim light and contrasting an object of focus with a progressive depth of field. In addition, protanopia (red-green color blindness) reduces color noise.

Our project uses virtual reality to contrast visual properties of tarsiers and humans and move beyond current educational methods toward a more personal, visceral experience. As a tool for educational outreach and science communication in the classroom and museum settings, it helps experientially teach about the impacts of natural selection and alternative optical systems. As a tool for introspection, it encourages users to question the limited extent to which their perceptual understandings of their surroundings is shared with other organisms.

Bernard Wood, Professor of Human Origins at George Washington University, tries on the headset for the first time.

Denise Su, Curator and Head of Paleobotany & Paleoecology at the Cleveland Museum of Natural History, explores the world of the tarsier Photo by Sam Gochman.

At the Gala, we had the chance to socialize with prominent players in the field, learn about The Leakey Foundation’s history, and hear about research at the frontiers of anthropology. At the after-party, we brought Tarsier Goggles to anthropologists and entrepreneurs alike as a “Young Professionals” project alongside Lenovo. We had lots of fun sharing our project, and we also used that time to conduct user testing with our system. From the event, we learned about new ways to improve and streamline the user experience, and we hope to continue to make it more self-guided and polished in the future. This will be especially important as we move to collaborate with a local natural history museum.

Guests from diverse professional backgrounds experience tarsier vision Photo by Sam Gochman.

We thank The Leakey Foundation for giving us the opportunity to engage with such a prominent institution and share our work with the public.

Mother’s Milk Holds Key to Unlocking an Evolutionary Mystery From the Last Ice Age

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Sunrise at noon in the Arctic. Little exposure to sun was a piece of the genetic puzzle. Bering Land Bridge National Preserve, CC BY Leslea Hlusko, University of California, Berkeley

Leslea Hlusko, University of California, Berkeley

As biologists explore the variation across the genomes of living people, they’ve found evidence of evolution at work. Particular variants of genes increase or decrease in populations through time. Sometimes this happens by chance. Other times these changes in frequency result from the gene’s helping or hindering individuals’ survival, a phenomenon known as selection. If a gene conferred a survival advantage, people with the mutation would have more offspring and the mutation would become more common in subsequent generations.

Most of those past episodes of selection make sense, as they worked on genes involved with things like resisting disease, blood oxygen levels at high altitudes, and having paler skin at northern latitudes.

However, researchers have also identified an episode of strong selection that doesn’t have such an obvious logic. It’s a mutation on a gene involved with the development of a suite of traits that don’t seem very similar at first glance: hair, teeth, sweat glands and breasts. This one was a mystery — what could have been the adaptive value of this mutation that led to it being common in northeastern Asia but nowhere else?

My research usually focuses on teeth, specifically genetic influences on their development. I came to this particular evolution puzzle when my colleagues and I gathered in Boston at the AAAS meeting last year to discuss the latest evidence of how people first migrated into the Western Hemisphere. We put together the clues about this episode of selection on human genetic variation – and found an example of adaptation to life at high latitude during the last ice age.

Natural selection … of what?

We were trying to understand selection for a mutation in the gene called EDAR – it encodes the ectodysplasin A receptor that plays a role in how tightly cells adhere to each other during the development of hair, teeth, sweat glands and breasts. All of these anatomical structures form via a very similar developmental process that happens while you’re still in your mother’s womb. Slight changes to the developmental mechanism results in the final differences between hair and teeth and sweat and mammary glands. But there is a fundamental similarity that, among other things, includes the activity of EDAR.

This shared development is especially obvious when things go wrong. For example, 1 in 10,000 newborns have a disorder called ectodermal dysplasia, which causes disruption to the development of their hair, teeth, skin, sweat glands and breasts.

The V370A mutation that we focused on, the one that experienced strong selection, doesn’t disrupt development of these structures; rather, it augments them. People with V370A have thicker and straighter hair shafts, and their incisors have extra buttressing on the tongue side – a feature biologists call “shoveling.”

Human upper incisors with significant ‘shoveling’ on the tongue side. Christy G. Turner, II, courtesy G. Richard Scott, CC BY-ND

So why did this mutation provide such an advantage to people who carried it? Mice that have been experimentally induced to have the V370A mutation have thicker fur shafts and increased density of sweat glands. A previous study of modern human genomic variation interpreted the selection to have occurred in northern China during the last ice age and focused on the sweat glands. The researchers suggested that the selection was for improved sweating that could help with regulating body temperature. But to my colleagues and me, that just didn’t feel like a convincing adaptive scenario given that this took place during the (cold) ice age.

Instead of the sweat glands, our attention was drawn to another trait. Mice with the V370A mutation also have an increase in the branching of their mammary ducts – the tiny tubes that intertwine with breast tissue and extract nutrients to make milk. Maybe it was this change in the breast tissue that was so valuable to people with this mutation?

Christy G. Turner II, shown working in 1975, and his students assessed variation in incisor shoveling in over 30,000 people around the world. The current study relied on a subset of these data collected by co-author G. Richard Scott. Photo: G. Richard Scott and Joshua P. Carlson, CC BY-ND

Rather than trying to sample DNA from thousands of ancient people’s remains to see if they carried the mutation, we took advantage of the effect V370A has on human incisors. Relying on data collected over many years by my colleague G. Richard Scott from the University of Nevada, Reno, our group looked at the dental variation of over 5,000 skeletons from archaeological sites in Europe, Asia and the Americas to get a sense of how this mutation varied through time.

We found that all of the indigenous people living in the Western Hemisphere prior to European colonization had shovel-shaped incisors, which means they all likely had the V370A mutation. In contrast, only about 40 percent of the people in Asia had shovel-shaped incisors, and essentially no one in Europe did.

This pattern suggests that a population ancestral to Native Americans experienced the strong selection for V370A, an interpretation that differed from what my colleagues found when they only looked at genomic variation in living people. Using these ancient teeth, we were able to figure out when and where the selection happened. The next question we needed to address was why this selection occurred. What was going on to make this mutation so helpful and thus so much more prevalent?

An ice age advantage

Beringia outlined over today’s Siberia and Alaska.
U.S. National Park Service, CC BY

Previous genetic work found that Native Americans descend from a common ancestral population that lived in Beringia, the region that links Siberia and Alaska. During the dramatic climate change associated with the last ice age 28,000 to 18,000 years ago, plants and animals that had previously lived in Siberia took refuge in a circumscribed area called the Beringian Refugium. For about 5,000 years, they were genetically isolated from other populations because of a vast dry tundra to the west and a lot of ice to the east. The people who found haven there too are referred to as the Beringian Standstill population.

Modern-day mesic shrub tundra near the northwestern Alaskan town of Kotzebue is similar to what the environment would have been like in Beringia during the ice age. Scott Elias, CC BY-ND

It’s not easy to live that far north. Sure, it’s cold. But more importantly, at high latitudes, the sun is lower in the sky so sunlight must travel through more atmosphere to reach Earth’s surface. This journey through the atmosphere mostly filters out the Sun’s ultraviolet radiation. Most life forms need sun exposure to be healthy, in large part because UV exposure induces the body to make vitamin D.

Lighter skin tones let in more UV and have been selected for multiple times in human history. But once you get to the Arctic, skin depigmentation alone won’t suffice. In order to live with so little UV, people have culturally innovated, eating diets rich in vitamin D, such as oily fish. But nursing infants don’t eat these foods. Babies get their nutrients through their mother’s milk.

This is where our EDAR gene comes back into the picture. The V370A mutation in mice increases the branching density of the mammary ducts, and very likely does the same exact thing in human breasts. Scientists know that vitamin D deficient conditions induce more ductal branching during the breast development that happens with pregnancy. All of the evidence suggests that the increased ductal branching associated with V370A helped transfer nutrients from mother to infant through breast milk in a population that was extremely vitamin D deficient.

So the selection wasn’t for thicker hair or shovel-shaped incisors – instead, it was much more likely to have been on mammary ducts. The thicker hair and tooth variation just went along for the ride because they are created by the same basic developmental pathway. Selection on genetic variation in EDAR is probably related to health consequences for nursing infants rather than its effects on hair, teeth or sweat glands.

Excavation of a site occupied in Beringia 32,000 years ago. V. V. Pitul’ko & E. Yu. Pavlova, CC BY-ND

Still traceable genetic inheritance

Once the Earth started warming up at the end of the last ice age, those ice sheets started to melt, sea level rose and global climate became more humid. The people living in Beringia needed to move again. Some went east, populating the Western Hemisphere rapidly and extensively. Some went west, merging back into populations that were living in northern and eastern Asia. Scientists see traces of this migration today. The occurrence of incisor shoveling decreases as you move away from the Arctic, there is evidence of a long-lost language, and some of those Beringian Standstill mitochondrial DNA mutations can be found in Asian populations.

Today, everyone with shovel-shaped incisors carries a little remnant of this ephemeral population with them and a reminder of the importance of the maternal-infant bond to human survival.

But they also have the other effects of the V370A mutation. The increase in mammary ductal branching seems likely to influence the transfer of nutrients from breast tissue into milk. It may also play a role in susceptibility to breast cancer, given that breast density differs between Asian and non-Asian women as does the occurrence of breast cancer, a relationship that matches the distribution of V370A around the world today.

These ideas present exciting hypotheses to test in future studies. For now, our research shows that the bones of our ancestors can provide evidence of human adaptation, evidence that shifts our understanding of how genes work.The Conversation

Leslea Hlusko, Associate Professor of Integrative Biology, University of California, Berkeley

Dr. Hlusko is a Leakey Foundation grantee.

This article was originally published on The Conversation. Read the original article.

Neanderthal Mother, Denisovan Father

This is a view of the valley from above the Denisova Cave archaeological site, Russia. Photo: Bence Viola, Max Planck Institute for Evolutionary Anthropology.

Together with their sister group the Neanderthals, Denisovans are the closest extinct relatives of currently living humans. “We knew from previous studies that Neanderthals and Denisovans must have occasionally had children together,” says Viviane Slon, a researcher at the Max Planck Institute for Evolutionary Anthropology (MPI-EVA) in Leipzig, Germany, and one of three first authors of a new study published in Nature on August 22. “But I never thought we would be so lucky as to find an actual offspring of the two groups.”

This bone fragment (‘Denisova 11’) was found in 2012 at Denisova Cave in Russia by Russian archaeologists and represents the daughter of a Neanderthal mother and a Denisovan father. Photo: T. Higham, University of Oxford.

The ancient individual is only represented by a single small bone fragment. “The fragment is part of a long bone, and we can estimate that this individual was at least 13 years old,” says Leakey Foundation grantee Bence Viola of the University of Toronto. The bone fragment was found in 2012 at Denisova Cave (Russia) by Russian archaeologists. It was brought to Leipzig for genetic analyses after it was identified as a hominin bone based on its protein composition.

“An interesting aspect of this genome is that it allows us to learn things about two populations – the Neanderthals from the mother’s side, and the Denisovans from the father’s side,” explains Fabrizio Mafessoni from the MPI-EVA who co-authored the study. The researchers determined that the mother was genetically closer to Neanderthals who lived in western Europe than to a Neanderthal individual that lived earlier in Denisova Cave. This shows that Neanderthals migrated between western and eastern Eurasia tens of thousands of years before their disappearance.

Analyses of the genome also revealed that the Denisovan father had at least one Neandertal ancestor further back in his family tree. “So from this single genome, we are able to detect multiple instances of interactions between Neanderthals and Denisovans,” says Benjamin Vernot from the MPI-EVA, the third co-author of the study.

“It is striking that we find this Neanderthal/Denisovan child among the handful of ancient individuals whose genomes have been sequenced,” adds Svante Pääbo, Director of the Department of Evolutionary Genetics at the MPI-EVA and lead author of the study. “Neanderthals and Denisovans may not have had many opportunities to meet. But when they did, they must have mated frequently – much more so than we previously thought.”

Original publication:

Viviane Slon, Fabrizio Mafessoni, Benjamin Vernot, Cesare de Filippo, Steffi Grote, Bence Viola, Mateja Hajdinjak, Stéphane Peyrégne, Sarah Nagel, Samantha Brown, Katerina Douka, Tom Higham, Maxim B. Kozlikin, Michael V. Shunkov, Anatoly P. Derevianko, Janet Kelso, Matthias Meyer, Kay Prüfer, Svante Pääbo

The genome of the offspring of a Neandertal mother and a Denisovan father, Nature, 22 August 2018

Story by Sandra Jacob, Max Planck Institute for Evolutionary Anthropology