The number of passenger pigeons went from billions to zero in mere decades, in contrast to conventional wisdom that enormous population size provides a buffer against extinction. Our understanding of the passenger pigeon’s extinction, however, has been limited by a lack of knowledge of its long-term population history. Here we use both genomic and ecological analyses to show that the passenger pigeon was not always super abundant, but experienced dramatic population fluctuations, which could increase its vulnerability to human exploitation. Our study demonstrates that high-throughput–based ancient DNA analyses combined with ecological niche modeling can provide evidence allowing us to assess factors that led to the surprisingly rapid demise of the passenger pigeon.
To assess the role of human disturbances in species’ extinction requires an understanding of the species population history before human impact. The passenger pigeon was once the most abundant bird in the world, with a population size estimated at 3–5 billion in the 1800s; its abrupt extinction in 1914 raises the question of how such an abundant bird could have been driven to extinction in mere decades. Although human exploitation is often blamed, the role of natural population dynamics in the passenger pigeon’s extinction remains unexplored. Applying high-throughput sequencing technologies to obtain sequences from most of the genome, we calculated that the passenger pigeon’s effective population size throughout the last million years was persistently about 1/10,000 of the 1800’s estimated number of individuals, a ratio 1,000-times lower than typically found. This result suggests that the passenger pigeon was not always super abundant but experienced dramatic population fluctuations, resembling those of an “outbreak” species. Ecological niche models supported inference of drastic changes in the extent of its breeding range over the last glacial–interglacial cycle. An estimate of acorn-based carrying capacity during the past 21,000 y showed great year-to-year variations. Based on our results, we hypothesize that ecological conditions that dramatically reduced population size under natural conditions could have interacted with human exploitation in causing the passenger pigeon’s rapid demise. Our study illustrates that even species as abundant as the passenger pigeon can be vulnerable to human threats if they are subject to dramatic population fluctuations, and provides a new perspective on the greatest human-caused extinction in recorded history.
This article contains supporting information online at http://www.pnas.org/content/suppl/2014/06/13/1401526111.DCSupplemental/pnas.1401526111.sapp.pdf
Chih-Ming Hung, Pei-Jen L. Shaner,Robert M. Zink, Wei-Chung Liu,Te-Chin Chu, Wen-San Huang,Shou-Hsien Li
Drastic population fluctuations explain the rapid extinction of the passenger pigeon PNAS 2014 ; published ahead of printJune 16, 2014,
Technical and ethical challenges abound after first hurdle of taking cells from millennia-old bodies is cleared
Even a well-preserved carcass like this baby woolly mammoth is unlikely to provide viable cells for cloning, as used to create Dolly. Photograph: Aaron Tam/Getty
By Ian Wilmut
It is unlikely that a mammoth could be cloned in the way we created Dolly the sheep, as has been proposed following the discovery of mammoth bones in northern Siberia. However, the idea prompts us to consider the feasibility of other avenues. Even if the Dolly method is not possible, there are other ways in which it would be biologically interesting to work with viable mammoth cells if they can be found.
In order for a Dolly-like clone to be born it is necessary to have females of a closely related species to provide unfertilised eggs, and, if cloned embryos are produced, to carry the pregnancies. Cloning depends on having two cells. One is an egg recovered from an animal around the time when usually she would be mated.
In reality there would be a need for not just one, but several hundred or even several thousand eggs to allow an opportunity to optimise the cloning techniques. The cloning procedure is very inefficient. After all, after several years of research with sheep eggs, Dolly was the only one to develop from 277 cloned embryos. In species in which research has continued, the typical success rate is still only around 5% at best.
Photo: Rubén Portas
In this case the suggestion is to use eggs from elephants. Because there is a danger of elephants becoming extinct it is clearly not appropriate to try to obtain 500 eggs from elephants. But there is an alternative.
There is a considerable similarity in the mechanisms that regulate function of the ovaries in different mammals. It has been shown that maturation of elephant eggs is stimulated if ovarian tissue from elephants is transplanted into mice.
In this way it might be possible to obtain a considerable number of elephant eggs over a period of time if ovarian tissue is obtained from elephants that die.
Cells from mammoths are required to provide the genetic information to control development. The suggestion is to recover cells from the marrow of bones emerging from the frozen north of Siberia. However, these cells will degenerate rapidly at the temperature of melting snow and ice. This means that cells in the bones may well become useless for this capacity as they thaw.
The chances of cells being viable would be increased if bones could be recovered from the lowest possible temperature rather than waiting until they emerge from snow. The cells can then be warmed rapidly. Alternatively, the nuclei could be transferred directly into eggs.
The very first stages of embryo development are controlled by proteins that are in the egg when it is shed by the ovary. One for example has a critical role in cell division. Together these proteins have an extraordinary ability to repair damaged nuclei so it may not be strictly necessary for the cells to be viable. It would be best if the mammoth nucleus could be introduced into an egg immediately, by injection of the contents of the damaged cell into the egg.
Research in 2008 found that when nuclei from freeze-dried sheep cells were transferred into eggs, some of the cloned embryos developed for a few days, but not to term. This was a very clear indication of the ability of the egg to repair damaged nuclei. However, freeze-dried cells are likely to be more stable than those that have been frozen with liquid still present. In the case of the mammoth, the cells would likely be killed by large ice crystals formed from the liquid.
Finally, if embryos that developed normally for a few days could be produced, they would have to be transferred to surrogate mothers to develop through pregnancy. Embryo transfer is only carried out routinely in fewer than a dozen species, and the elephant is not one of them. Success in embryo transfer depends upon introducing the embryo to a womb that is in a receptive state. The mechanisms that bring about this state in elephants are currently being defined by research in a number of zoos.
Taken together, it can be seen that there is biological uncertainty about the availability of viable cells, and that several complex techniques would have to be developed for cloning of mammoths to be successful. There is no guarantee that these techniques are even biologically possible. There may be unknown differences between species that would prevent the procedures that we developed in sheep being successful in mammoths.
Copyright: Royal BC Museum
Mammoth stem cells
An alternative ambition would be to try to use mammoth cells to produce stem cells. In several different species it is possible simply by the introduction of four selected proteins to give adult cells the characteristics of embryo stem cells. The four factors give embryo stem cells their unique characteristics and were found to be able to impose these characteristics on skin cells. This type of stem cell can be grown for very long periods in the laboratory while retaining the ability to form all of the tissues of the body.
They would provide extraordinary opportunities to compare mammoth cells with those of elephants. This knowledge would be of fundamental biological interest. It would enable us to begin to answer groundbreaking questions. What are the differences between the cells and tissues of these species? What are the similarities? The mammoth lived in a different climate, so was the metabolism of their cells different? Does this information cast any light on the cause of extinction of mammoths?
Stem cells of this type can also be induced to form gametes. If the cells were from a female, this might provide an alternative source of eggs for use in research, and perhaps in breeding, including the cloning of mammoths.
From a male, they would be sperm, and they might be able to fertilise eggs to produce a new mammoth embryo. It would be interesting to know if mammoth sperm could fertilise eggs of the elephant. If so, would the embryos develop to term to produce a hybrid animal?
Only a small proportion of mixed matings between species produces viable offspring, but the mule is one example and has been used by humans for centuries.
In all of these discussions it is necessary to consider the welfare of the animals. Mammoths lived in cold climates, whereas their current relatives including potential surrogate mothers live in warmer regions.
It would be essential to provide mother and clone with the appropriate environment of temperature, moisture and diet. It would almost certainly be necessary to keep the animals in captivity, so it would be essential to provide as interesting an environment as possible. Ideally this should include other elephants, mammoths or hybrids to provide social interaction for the animal.
So while unlikely at present, the development of some form of mammoth creature or hybrid might be possible in the longer term, the research of which could lead to major biological discoveries and advances.
This is another area of biology where studies of stem cells would be very rewarding. In stem cell research rather than cloning there would also be fewer concerns over animal welfare, or the effect of the animal on the environment. All in all, research to produce mammoth stem cells would be the appropriate choice, and extraordinarily scientifically rewarding, should it be possible to find viable mammoth cells.
STATHAM, M. J., B. N. SACKS, K. B. AUBRY, J. D. PERRINE, AND S. M. WISELY
Red foxes (Vulpes vulpes) are native to boreal and western montane portions of North America but their origins are unknown in many lowland areas of the United States. Red foxes were historically absent from much of the East Coast at the time of European settlement and did not become common until the mid-1800s. Some early naturalists described an apparent southward expansion of native foxes that coincided with anthropogenic habitat changes in the region.
Alternatively, red foxes introduced from Europe during Colonial times may have become established in the east and subsequently expanded their range westward. The red fox also was absent historically from most lowland areas of the western United States. Extant populations of red foxes in those areas are considered to have arisen from intentional introductions from the east (and by extension are putatively European), escapes or releases from fur farms, or range expansions by native populations.
To test these hypotheses we compared mitochondrial DNA sequences (cytochrome band D-loop) from 110 individuals from 6 recently established populations to 327 native (primarily historical) individuals from Eurasia, Alaska, Canada, the northeastern United States, and montane areas in the western contiguous United States, and to 38 individuals from fur farms
We found no Eurasian haplotypes in North America, but found native haplotypes in recently established populations in the southeastern United States and in parts of the western United States. Red foxes from the southeastern United States were closely related to native populations in eastern Canada and the northeastern United States, suggesting that they originated from natural range expansions, not from translocation of European lineages, as was widely believed prior to this study.
Similarly, recently established populations in the Great Basin and in western Oregon originated primarily from native populations in western montane regions, but also contained a few nonnative North American haplotypes. In contrast, populations in western Washington and southern California contained nonnative, highly admixed stock that clearly resulted from intracontinental translocations. Several common haplotypes in these populations originated in regions where fur-farm stocks originated.
Although European red foxes translocated to the eastern United States during Colonial times may have contributed genetically to extant populations in that region, our findings suggest that most of the matrilineal ancestry of eastern red foxes originated in North America.
Statham, M. J., B. N. Sacks, K. B. Aubry, J. D. Perrine, and S. M. Wisely. 2012. The origin of recently established red fox populations in the United States: translocations or natural range expansions?. Journal of Mammalogy 93(1):52-65.
Access to the original paper in pdf: http://www.fs.fed.us/pnw/pubs/journals/pnw_2012_statham001.pdf
A new species of wild cat in central and north-eastern Brazil has been confirmed, according to a study published today in the journal Current Biology.
This recognition formally separates the two known tigrina species (Leopardus tigrinus and Leopardus guttulus) which, until now, were regarded as one.
According to the authors of the study, Eduardo Eizirik from the Pontifical Catholic University of Rio Grande do Sul and Tatiane Trigo from the University Federal of Rio Grande do Sul, the possibility that these two wild cat populations were two distinct species was considered in the 1960s, but the hypothesis was never tested.
For the first time, scientists are able to assess the two previously-recognised subspecies using molecular markers to analyse their genetic relationship.
The results showed that the housecat-sized tigrina populations are, in fact, completely separate species.
“Our analysis showed strong genetic differentiation between the tigrina populations, with no gene flow between them, indicating that these two populations are actually reproductively isolated and should be recognised as distinct species,” said Professor Eizirik and Dr Trigo.
Data on the two tigrina species also revealed a distinct geographical distribution of both populations.
L. tigrinus, found in central and north-eastern Brazil, live primarily in open and dry vegetation (shrublands and savannahs). The southern and south-eastern Brazilian areas, occupied by L. guttulus, are dominated by denser and wetter Atlantic forest-type habitats.
Such distinct habitat conditions provide clues to their different ecological requirements and the adaptive differences that may have been responsible for their evolutionary divergence.
The findings from this study also revealed the complexity of the relationships between the tigrinas and two other species of neotropical cats (commonly known as Geoffroy’s cats).
The evidence suggests that L. tigrinus’ evolutionary history includes hybridisation and movement of genes between them and the pampas cat, while extreme levels of interbreeding between L. guttulus and Geoffroy’s cats still occur along their contact zone.
Although there is no evidence that this interbreeding is expanding beyond the contact zone, it is clear that hybridisation can and does occur between distinct animal species.
Christopher Johnson, a professor of wildlife conservation from the University of Tasmania, said: “This study hints that hybridisation in the past has accelerated speciation. The acquisition of new genes by hybridisation can be a potent force in the evolution of species, and this could be a neat example where hybridisation in some parts of the range but not others has contributed to splitting of one species into two.
“We used to think that hybridisation between related species was not supposed to happen – by definition, species did not interbreed – but it’s clearly more significant than was realised.”
Professor Eizirik and Dr Trigo explained that hybridisation may occur quite frequently in the initial stages of species divergence, and the species involved may hybridise for some time and maintain a hybrid zone at their region of geographic overlap.
However, this may not necessarily lead to their complete admixture or the loss of the genetic and phenotypic integrity of each parental species.
“Currently, there is a strong genetic differentiation between these two cat species in areas farther from the contact zone. Selective pressure must be keeping the two species morphologically, ecologically, and even genetically distinct outside of this contact zone.
“Therefore, at this point, it seems adequate to keep them as separate species and continue to investigate the extent and biological consequences of their hybridisation.”
Implications on conservation
Gerry Ryan, from the University of Melbourne, warned that the evidence for a recent or continuing hybrid zone between the southern tigrinas and Geoffroy’s cats will need closer investigation to determine if any conservation management actions are needed.
“The two tigrina species are listed as one on the IUCN’s Red List of Threatened Species. Now that they are considered to be separate species, they both need to be re-assessed. Each one will be at a higher risk of extinction, than when considered as one species, because smaller numbers automatically increase the risks.
“If the hybridisation is spurred by human-induced habitat alteration, then conservation management actions must be considered. But, given the already extensive gene flow, this may be too late.”
Hamish Campbell, from the University of Queensland, believes that the use of modern genetic techniques is crucial in determining when one species or sub-species should be declared distinct from another, particularly when it comes to managing rare and threatened species.
He explained: “This study is similar to that of the Scottish wildcat (Felis silvestris) which, using molecular techniques, was found to be breeding with feral domestic cats (Felis felis).
“Feral domestic cats are an environmental disaster, devastating native wildlife, while the Scottish wildcat is a rare and ancient species that needs to be conserved. But where do you draw the eradication line? What level of hybridisation is acceptable to declare the species a threat rather than a pest?
“Molecular techniques are helping us to map the evolutionary history of species, but how those findings are applied to the successful management of rare and threatened species is still in its infancy.”
According to Gerry Ryan, this case study shows us how modern genetic techniques can help clarify cryptic patterns of species diversity.
“As genetics and genomics continue to advance and be cheaper and faster, we can better understand the complex and dynamic nature of species boundary. We will then need to develop parallel conservation strategies to protect the diversity of life beyond linear concepts, and allow for adaptation and evolution in the face of global climactic change.”
Professor Eizirik and Dr Trigo agreed, saying: “Our study has opened new avenues for research, focusing on more in-depth evolutionary, genomic, morphological and ecological questions.
“We intend to further investigate Brazilian northeastern tigrinas which are virtually unknown with respect to most aspects of their biology. Some initial studies on its ecology (diet, feeding habits and habitat requirements) have been done, but information on its population density, habitat use and population trends remain unknown.
“There is also very little information on the ecological segregation between the two species. Thus, we consider studying L. tigrinus a priority for research and conservation actions.”
Wolves likely were domesticated by European hunter–gatherers more than 18,000 years ago and gradually evolved into dogs that became household pets, UCLA life scientists report.
“We found that instead of recent wolves being closest to domestic dogs, ancient European wolves were directly related to them,” said Robert Wayne, a professor of ecology and evolutionary biology in UCLA’s College of Letters and Science and senior author of the research. “This brings the genetic record into agreement with the archaeological record. Europe is where the oldest dogs are found.”
Ancient dog fossil A fossil of a dog that lived approximately 8,500 years ago, from the Koster archaeological site in Illinois. (Credit: Del Baston)
The UCLA researchers’ genetic analysis is published Nov. 15 in the journal Science and featured on the journal’s cover.
In related research last May, Wayne and his colleagues reported at the Biology of Genomes meeting in New York the results of their comparison of the complete nuclear genomes of three recent wolf breeds (from the Middle East, East Asia and Europe), two ancient dog breeds and the boxer dog breed.
“We analyzed those six genomes with cutting-edge approaches and found that none of those wolf populations seemed to be closest to domestic dogs,” Wayne said. “We thought one of them would be, because they represent wolves from the three possible centers of dog domestication, but none was. All the wolves formed their own group, and all the dogs formed another group.”
The UCLA biologists also hypothesized at that conference that a now-extinct population of wolves was more directly related to dogs.
For the current study in Science, the researchers studied 10 ancient “wolf-like” animals and eight “dog-like” animals, mostly from Europe. These animals were all more than 1,000 years old, most were thousands of years old, and two were more than 30,000 years old.
The biologists studied the mitochondrial DNA of the animals, which is abundant in ancient remains. (Mitochondria are tiny sub-cellular structures with their own small genome.) By comparing this ancient mitochondrial DNA with the modern mitochondrial genomes of 77 domestic dogs, 49 wolves and four coyotes, the researchers determined that the domestic dogs were genetically grouped with ancient wolves or dogs from Europe — not with wolves found anywhere else in the world or even with modern European wolves. Dogs, they concluded, derived from ancient wolves that inhabited Europe and are now extinct.
Wayne said that that the domestication of predatory wolves likely occurred among ancient hunter–gatherer groups rather than as part of humans’ development of sedentary, agricultural-based communities.
“The wolf is the first domesticated species and the only large carnivore humans ever domesticated,” Wayne said. “This always seemed odd to me. Other wild species were domesticated in association with the development of agriculture and then needed to exist in close proximity to humans. This would be a difficult position for a large, aggressive predator. But if domestication occurred in association with hunter–gatherers, one can imagine wolves first taking advantage of the carcasses that humans left behind — a natural role for any large carnivore — and then over time moving more closely into the human niche through a co-evolutionary process.”
The idea of wolves following hunter–gatherers also helps to explain the eventual genetic divergence that led to the appearance of dogs, he said. Wolves following the migratory patterns of these early human groups would have given up their territoriality and would have been less likely to reproduce with resident territorial wolves. Wayne noted that a group of modern wolves illustrates this process.
“We have an analog of this process today, in the only migratory population of wolves known existing in the tundra and boreal forest of North America,” he said. “This population follows the barren-ground caribou during their thousand-kilometer migration. When these wolves return from the tundra to the boreal forest during the winter, they do not reproduce with resident wolves there that never migrate. We feel this is a model for domestication and the reproductive divergence of the earliest dogs from wild wolves.
“We know also that there were distinct wolf populations existing ten of thousands of years ago,” Wayne added. “One such wolf, which we call the megafaunal wolf, preyed on large game such as horses, bison and perhaps very young mammoths. Isotope data show that they ate these species, and the dog may have been derived from a wolf similar to these ancient wolves in the late Pleistocene of Europe.”
In research published in the journal nature in 2010, Wayne and colleagues reported that dogs seem to share more genetic similarity with living Middle Eastern gray wolves than with any other wolf population, which suggested a Middle East origin for modern dogs. The new genetic data have convinced him otherwise.
“When we previously found some similarity between Middle Eastern wolves and domestic dogs, that similarity, we are now able to show, likely was the result of interbreeding between dog and wolves during dog history. It does not necessarily suggest an origin in the Middle East,” Wayne said. “This alternative hypothesis, in retrospect, is one that we should have considered more closely. As hunter–gatherers moved around the globe, their dogs trailing behind probably interbred with wolves.”
Wayne considers the new genetic data “persuasive” but said they need to be confirmed with an analysis of genetic sequences from the nucleus of the cell (roughly 2 billion base pairs) — a significantly larger sample than that found in mitochondrial DNA (approximately 20,000 base pairs). This is challenging because the nuclear DNA of ancient remains tends to become degraded.
While Wayne plans to pursue this follow-up research, he said he does not expect a nuclear genome analysis to change the central finding. However, he said, it will fill in more of the details.
“This is not the end-story in the debate about dog domestication, but I think it is a powerful argument opposing other hypotheses of origin,” he said.
There is a scientific debate over when dogs were domesticated and whether it was linked with the development of agriculture fewer than 10,000 years ago, or whether it occurred much earlier. In the new Science research, Wayne and his colleagues estimate that dogs were domesticated between 18,000 and 32,000 years ago.
The research was federally funded by the National Science Foundation.
Co-authors on the Science paper include Olaf Thalmann, a former postdoctoral scholar in Wayne’s laboratory who is currently the Marie Curie Postdoctoral Fellow at Finland’s University of Turku; Daniel Greenfield, a former technician in Wayne’s laboratory; Francesc López-Giráldez, a former graduate student in Wayne’s laboratory who is currently a postdoctoral scholar at Yale University; Adam Freedman, a former postdoctoral scholar in Wayne’s laboratory; Rena Schweizer, a current UCLA graduate student in Wayne’s laboratory; Klaus Koepfli, a former postdoctoral scholar in Wayne’s laboratory; and Jennifer Leonard, who earned her doctorate from UCLA.
Approximately 80 percent of dog breeds are modern breeds that evolved in the last few hundred years, Wayne said. But some dog breeds have ancient histories that go back thousands of years.
Wolves have been in the Old World for hundreds of thousands of years. The oldest dogs from the archaeological record come from Europe and Western Russia. A dog from Belgium dates back approximately 36,000 years, and a group of dogs from Western Russia is approximately 15,000 years old, Wayne said.
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