The Paradoxical Passenger Pigeon Genome

After years of intensive research, the analysis of specimens from four museum collections, and the combined efforts of more than a dozen scientists, the population genomics of the passenger pigeon have been published in Science, with some significant results for the field of genomics. The passenger pigeon’s genome proved to be a challenging analysis, owing to a paradox of population genomics.

The manuscript is an exploration of passenger pigeon natural history, based on its genome sequence. We found that passenger pigeons were highly genetically diverse, but not as diverse as would be expected given their census population size — an observation in population genetics known as “Lewontin’s paradox.” (See figure 1.)

Diversity does not track population size because of a phenomenon known as genetic linkage. On chromosomes, genes are linked together, except during reproduction. At that time, chromosomes shuffle through a process called recombination, which breaks the links between different versions of genes (called alleles). When recombination occurs frequently, the effects of selection on one gene are largely independent of those on other genes; however, when recombination happens rarely, selection on a gene effects its neighboring genes as well. In birds specifically, the recombination process creates long sections of the genome that are linked together via the near-absence of recombination.

Selection on genes decreases diversity, something that is very strong in large populations. Therefore, in areas of low recombination, the passenger pigeon has less diversity in these regions than its cousin, the band-tailed pigeon. (See the example in figure 1.) This linkage, in effect, weakens the process of natural selection for many genes in the population. However, in regions of the genome where recombination occurs frequently, we see very high levels of diversity and evidence for highly-efficient natural selection.

Half of the passenger pigeon’s genome has very low diversity, lower than that of a species with small numbers, while the other half of the genome has very high diversity. According to Lewontin’s paradox, this can only happen if the population was abundant for a long period of time.

Passenger pigeons were abundant for tens of thousands of years. While past studies have suggested that passenger pigeons experienced fluctuations in population size, that conclusion contradicts this new data if explained through Lewontin’s paradox. Because of the dual nature of passenger pigeon genomic diversity, the types of population models used to typically study genomes cannot be applied. Therefore, we have to rely on other population models, which we ascertained using the genetics of 41 passenger pigeons dating from 4,000 years ago to their extinction in the late 19^th century.

This is discovery has a big impact on genomics studies. It means that there is no universal method of calculating population trends from genomes. Many recent genomics studies have used the same tool to study population trends, without looking to see if the tool can be applied to the genome in question. In the future we need to be careful when trying to extract information from genomes.

Because passenger pigeon populations were large for a very long time, natural selection was a powerful evolutionary force that allowed them to become exquisitely adapted to life in a large population. The theory that natural selection is efficient when the population size is large is predicted by population genetics theory, but we were able to demonstrate this in a natural population at a genomic level for the first time.

The big takeaway is that the passenger pigeon was abundant during times of radical environmental change – climate swings, megafaunal extinctions, and complete changes in forest composition. In spite of all that change, the passenger pigeon was a constant success, and that was owed to their adaptation to a high-density lifestyle. Essentially, they can be considered a sort of “super species.”

But the effects of their lifestyle on their genome may have had consequences during catastrophic events, such as the over-harvest and deforestation begun by colonial Europeans and intensified by America’s industrial growth. It’s possible that selection for living in abundance incurred evolutionary tradeoffs making it difficult for passenger pigeons to live in low numbers for a prolonged period of time. In other words, they might have struggled to recover from a severe bottleneck.

But the nature of this is difficult to assess. It’s possible that the types of traits adapted to living in large numbers were plastic, and would not have been negatively affected by low numbers. A very recent study of the passenger pigeon reproduction rates shortly before their extinction failed to find any decreases in breeding success, so it appears that at least the breeding cycle of passenger pigeons didn’t experience an observable trade off historically. However, the extinction of the passenger pigeon was so rapid, negative effects may not have had time to show symptoms. Further research will help clarify some of the big questions scientists have always had about this devastating extinction: at what point was the passenger pigeon truly doomed? When could it have recovered on its own, had it been given the chance? When could modern conservation efforts have saved it had people tried?

The coolest part of this discovery is that it gives future generations a means to test if passenger pigeon de-extinction is a true success. Our goal is to give band-tailed pigeons the necessary mutations that will make them breed colonially, the same way that passenger pigeons did. This is the first step to enabling them to live in high-social densities, which is the key reason why passenger pigeons were hugely beneficial for the environment. We then need to give band-tailed pigeons the necessary adaptations to live in high social densities efficiently – traits that strengthen social cues, such as the red breast of the male passenger pigeon and their elegant tails. Other traits, like rapid juvenile growth, will be important for the new passenger pigeons to use food resources effectively without straining their parenting efforts at high numbers.

The band-tailed pigeon’s genome currently has lower diversity overall than a passenger pigeon’s genome, existing in a non-paradoxical state, as the species does not live in high abundance. If we do our job right, then a new generation of passenger pigeons will rise to abundance and over time their genomes will begin to look like what we have observed in the extinct passenger pigeon. We now have a long-term measure of whether or not our new passenger pigeons have truly taken to the passenger pigeon’s former lifestyle… though, it may take many generations to observe. This will be a long eco-evolutionary experiment indeed!