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Although passenger pigeons were the victims of human hunters, we still don’t understand precisely how a species can decline from billions to none within a period of fifty years. Can genetics give us any useful clues?
As extinctions go, the extinction of the passenger pigeon is truly a stupendous human achievement, unparalleled in recorded history: thanks to our penchant for relentless killing combined with large-scale habitat destruction, these iconic birds’ population crashed from billions to zero in just fifty years. But how could these birds decline so rapidly? Surely, people did not murder every last one of them, did they? Shouldn’t mind-bogglingly huge and wide-spread populations protect a species from extinction? Why didn’t some pigeons survive in remote areas?
The mystery deepens
In a study published in 2014, researchers sought to understand how such an abundant species could possibly be driven extinct, particularly since many scientists have estimated that passenger pigeons were, arguably, the most populous bird species on the planet, ever. Despite their huge population, the 2014 study indicated that passenger pigeons had much less genetic diversity than expected. The authors of that study suggested that passenger pigeons were not always super-abundant (ref; read more).
The researchers’ analysis suggested that passenger pigeons’ numbers had either exploded recently (similar to the current human population explosion), or their population fluctuated naturally by a thousand-fold or more within short time periods (this population pattern is seen in several outbreak species, such as Australian plague locusts, Chortoicetes terminifera, or lemmings, Lemmus lemmus.). Based on their findings, the authors of the 2014 study concluded that the passenger pigeon was an “outbreak species” and that their periodic population crashes created genetic bottlenecks that reduced genetic diversity from expected levels. They also proposed that the passenger pigeon’s population was already in a natural decline when European immigrants and colonists came along and pushed them over the edge into extinction.
But a new study (ref) challenges that conclusion: after sequencing and analyzing four passenger pigeon genomes and 41 mitochondrial genomes from individuals collected throughout this bird’s expansive range, the authors of this new study confirmed that yes, the passenger pigeon genome had surprisingly low diversity compared to the overall size of their population.
But when the researchers examined the entire genome closely, they found that genetic diversity varied: some regions of the genome had very low diversity, whilst others did not. This was unexpected. The researchers reasoned that, if the passenger pigeon’s population had been fluctuating by a thousand-fold for long periods of time, then genetic diversity in all regions of the genome should be affected equally.
Further, they discovered that the genetic diversity in the mitochondrial genome did not correspond with the genomic data. Instead, the passenger pigeon mitochondrial genome indicated that their population had been stable for the past 20,000 years -- a time period that included dramatic climatic changes, such as the end of the last ice age in North America, which is precisely when you’d expect to see population fluctuations.
Curiouser and curiouser
The passenger pigeon, Ectopistes migratorius, were handsome medium-sized birds who raised their families in huge, social colonies throughout the eastern United States. Sleek and slender, this species was built for speed, and they wandered freely over vast distances (Figure 1A).
The passenger pigeon’s peregrinating lifestyle was captured in its genome, which did not reveal any discernible geographic structure that is typically seen in more sedentary species (Figure 1B).
As I mentioned, it was fairly widely-accepted that the passenger pigeon’s population underwent huge periodic fluctuations that, in turn, reduced their overall genetic diversity from expected levels. But there is another possible explanation for their unusual level of genetic diversity: natural selection. It is conceivable that the process of natural selection acting on one particular gene resulted in a loss of diversity amongst other nearby genes, or amongst those genes that are somehow linked to the selected gene. This phenomenon -- where a selected gene affects the fate of other genes in its genomic neighborhood -- is known in the literature as the “hitch-hiking effect” (ref).
A team of researchers investigated the genetic diversity of the passenger pigeon and compared this to the genome from the band-tailed pigeon, Patagioenas fasciata.
Although these two species are each other’s closest relatives and they are ecologically similar, they do have one big difference that was especially important for this particular study: the band-tailed pigeon’s population is much smaller than the passenger pigeon’s, and always has been.
“The only difference between them is really this population size, so we can start to dig into what the evolutionary consequences of being a super-big population might be,” said molecular biologist and senior co-author of the study, Beth Shapiro, who is a professor in the Department of Ecology and Evolutionary Biology at the University of California, Santa Cruz.
To do this work, Professor Shapiro and her colleagues obtained tiny tissue samples from the toe pads of passenger pigeon specimens collected across the eastern United States (Figure 1A), that are held in a number of museum collections. Using those tissue samples, the research team extracted the nuclear or mitochondrial genomes from individual passenger pigeons. They compared the passenger pigeon’s genetic markers to those of the band-tailed pigeon.
Based on their analyses, Professor Shapiro and her colleagues saw that some portions of the passenger pigeon genome had high genetic diversity, indicating they had lived as a very large population for a very long time (Figure 2).
But other regions of the passenger pigeon’s genome had a lower-than-expected level of genetic diversity (Figure 2), despite being “neutral mutations”. Neutral mutations are neither beneficial nor detrimental but they could serve as essential raw material for natural selection to act upon in the future as the birds adapted to a changing landscape. Thus, the authors concluded that the passenger pigeon’s genome did show a “hitch-hiking effect” of strong natural selection.
This, the authors argue, is because of the passenger pigeon’s abundance and tremendous mobility; this allowed beneficial mutations spread extremely quickly throughout the entire population whilst detrimental mutations disappeared just as quickly. Thanks to strong natural selection on a few beneficial genes, the diversity of other, nearby genes, that were neither beneficial nor detrimental was also affected -- consistent with the “hitch-hiking effect” model.
It’s impossible to adapt to mass murder
In retrospect, it’s obvious that the passenger pigeon could not tolerate much hunting -- and certainly not the sort of intense, consistent massacre that they were subjected to by European immigrants and colonists.
“Our mass murder of them over the course of decades was just too fast for evolution to keep up,” Professor Shapiro said.
“Our study shows that passenger pigeons were strikingly well adapted to living in large populations,” Professor Shapiro elaborated in email. “In large populations, natural selection is highly efficient. This suggests that if the environment had changed slowly (as it may have after the end of the last ice age) they would be able to adapt to these changes (as they did at the end of the last ice age).”
However, in the 1800s, the passenger pigeon environment changed suddenly due to hunting.
“We killed millions of passenger pigeons over the course of only a few passenger pigeon generations,” Professor Shapiro said in email. “There was no time at all for passenger pigeons to adapt to this new environment. They did not die because they had very little diversity ... but because they suddenly found themselves living in an environment that was very different from the one to which they were adapted, still being overexploited by a highly skilled predator, and now lacking an efficient means to evolve in response to this environmental change.”
Can we learn any practical lessons from this tragic extinction event? Neither this study nor the 2014 study, provide any genetic insights into the mystery of how the passenger pigeon went extinct so quickly. For example, none of the research published so far has figured out how to predict how many passenger pigeons could be killed before the entire population would collapse into nothingness, forever. When was that line crossed?
Conservation is tricky work. Generally, conservation biologists assume that a large population corresponds to a high genetic diversity, and this, presumably, acts as a buffer against extinction. But the passenger pigeon serves as a powerful cautionary example that this assumption is not necessarily true.
“There’s more that we should consider when we think about a population being endangered than just population size,” Professor Shapiro agreed. She pointed out that successful conservation efforts may require decisive action long before a given species’s population falls below what we think is a critically low level.
“We think now of restoring [endangered species] by creating patches of protected habitat,” Professor Shapiro said. “But we don’t know if the way they’ve evolved through their entire history means that they’re not fit for living in small populations.”
The passenger pigeon probably was unable to survive in small relict populations. Their vast numbers were probably one of their most effective survival strategies: no predator could possibly kill them all. This strategy is seen in some insects and other animals, and even in some vertebrate species. For example, the Atlantic cod, Gadus morhua, suffered a remarkably similar fate to that of the passenger pigeon. Historically, these fish lived in extremely large populations along Newfoundland’s Grand Banks until the 1990s, when its numbers crashed due to exuberant overfishing. Although all fishing of the Grand Banks population of the north Atlantic cod stopped more than 15 years ago, that fishery is still decreasing and is predicted to go extinct within 20 years (ref).
Genetics is only part of the story. Based on historic reports, we are fairly certain that passenger pigeons were behaviorally adapted to living in large communities.
“It’s known that they collaborated in finding food, and they also collaborated in rearing young,” said lead author Gemma Murray, an evolutionary biologist at UCSC. “[T]hese sorts of behaviors are the sorts of things which might work really well when your population size is large and dense. But when hunting had a big impact on their population, and their numbers went down hugely in the 19th century, maybe those things didn’t work anymore.”
Professor Shapiro and her colleagues’ data suggest that the passenger pigeon lacked the genetic resources necessary to adapt their physiology and behavior quickly enough to living in small communities, and that stemmed, at least partially, from a reduction in the genetic diversity that was necessary to make that happen. This resulted from a pattern of widespread, systemic abuse by people.
“The passenger pigeon extinction was avoidable,” Professor Shapiro remarked. “It was entirely our fault. We over-hunted and over-exploited this amazing animal, and we should try to be careful about what we're doing today.”
Source:
Gemma G. R. Murray, André E. R. Soares, Ben J. Novak, Nathan K. Schaefer, James A. Cahill, Allan J. Baker, John R. Demboski, Andrew Doll, Rute R. Da Fonseca, Tara L. Fulton, M. Thomas P. Gilbert, Peter D. Heintzman, Brandon Letts, George McIntosh, Brendan L. O’Connell, Mark Peck, Marie-Lorraine Pipes, Edward S. Rice, Kathryn M. Santos, A. Gregory Sohrweide, Samuel H. Vohr, Russell B. Corbett-Detig, Richard E. Green, and Beth Shapiro (2017). Natural selection shaped the rise and fall of passenger pigeon genomic diversity, Science, 358:951–954 | doi:10.1126/science.aao0960
Also cited:
Chih-Ming Hung, Pei-Jen L. Shanera, Robert M. Zink, Wei-Chung Liu, Te-Chin Chu, Wen-San Huang, and Shou-Hsien Li (2014). Drastic population fluctuations explain the rapid extinction of the passenger pigeon, Proceedings of the National Academy of Sciences, 111(29):10636–10641 | doi:10.1073/pnas.1401526111
Passenger pigeon extinction: it’s complicated
John Maynard Smith and John Haigh (1974). The hitch-hiking effect of a favourable gene, Genetic Research, 23(1):23-35 | doi:10.1017/S0016672300014634
