Across Asia and beyond: The evolutionary story of the Common Pheasant

Genetic study reconstructs the Asian diversification of the Common Pheasant.

When I visit my family in Belgium, we often go for walks with our dog Mira (a Hungarian vizsla). While strolling through the local nature reserves, we sometimes disturb a Common Pheasant (Phasianus colchicus) hiding in the tall grass. Females mostly fly off with a loud alarm call, whereas males tend to run away in a seemingly random direction. These colorful birds – the males anyway – are not native to this part of Europe, but were introduced for hunting purposes. Common Pheasants originated in Asia where they display an amazing diversity of male plumage, resulting in a proliferation of more than 30 subspecies.

A recent study in the Journal of Biogeography focused on the native range of the Common Pheasant and reconstructed its evolutionary history based on a handful of genetic markers. The researchers found that this species diversified into eight distinct lineages during the Late Pleistocene. Let’s explore the Asian expansion of the Common Pheasant.

Spreading across Asia

Simin Liu and colleages sampled more than 200 individuals across the range of the Common Pheasant, which extends from the Black Sea to Korea. Analyses of seven nuclear and two mitochondrial genes revealed that the diversification within this species started at the end of the Pleistocene, between 700,000 and 200,000 years ago. Our evolutionary story starts at the eastern edge of the Qinghai-Tibetan Plateau from where several lineages spread in different directions.

One population expanded to the Chinese mountain ranges in the south-east, giving rise to the elegans-lineage. Because the climate remained relatively stable in this region, this lineage shows a stable population size of time and did not diversify into more sub-lineages. A second expansion to the east brought pheasants into a more unstable area where periods of drought promoted diversification into multiple lineages. Here, we currently find the torquatus and strauchi–vlangallii lineages that were occasionally connected by gene flow. One population traveled further east and became isolated on the island of Taiwan (the formosanus-lineage). Finally, a third movement to the west resulted in the evolution of several Central Asian lineages: tarimensis,, mongolicus, principalis–chrysomelas and colchicus. The exact evolutionary relationships between these lineages remain to be disentangled.

The genetic analyses pointed to eight distinct lineages (see phylogeny on top) that spread across Asia from the Qinghai-Tibetan Plateau (map below). From: Liu et al. (2020) Journal of Biogeography.

Taxonomic Decisions

This study nicely shows how different environmental conditions affect the evolutionary trajectory of a population. The relatively stable climate of the Chinese mountains resulted in a stable population of Common Pheasants, making further diversification of this lineage (elegans) unlikely. Other populations ended up in regions with more pronounced climatic cycles that led to diversification into several separate lineages. Ultimately, the researchers could discriminate between eight distinct lineages.

Taxonomic-minded readers might be wondering if all these lineages should be elevated to species rank. At the moment, the researchers argue that the diversity within the Common Pheasant can be captured in three species: the Yunnan Pheasant (P. elegans), the Chinese Pheasant (P. vlangallii which includes the torquatus, strauchi–vlangallii and formosanus lineages) and the Turkestan Pheasant (P. colchicus which includes the tarimensis, principalis–chrysomelas, mongolicus and colchicus lineages). However, more research is needed to justify this classification.

References

Liu et al. (2020) Regional drivers of diversification in the late Quaternary in a widely distributed generalist species, the common pheasant Phasianus colchicus. Journal of Biogeography47(12), 2714-2727.

Featured image: Common Pheasant (Phasianus colchicus) © David Croad | Wikimedia Commons

You only need one genome to unravel the demographic history of the Chinese Grouse

Genomic analyses reveal population fluctuations during the Pleistocene.

A few weeks ago, scientists announced that they almost completed a sequence of the human genome. This might come as a surprise: did we not sequence the human genome in 2003 when the results from the Human Genome Project were published? That genome sequence was actually incomplete, about 15% was missing (especially stretches of repetitive DNA are difficult to assemble). Similarly, many avian genome assemblies contain significant gaps (see this blog post for more details). However, scientists can still extract a lot of information from incomplete genome assemblies. For instance, you can reconstruct the demographic history of a species from one genome using a pairwise sequentially Markovian coalescent (PSMC) analysis. This technique – developed by Heng Li and Richard Durbin – is nicely explained by David Reich in his book Who We Are and How We Got Here:

A 2011 paper by Heng Li and Richard Durbin showed that the idea that a single person’s genome contains information about a multitude of ancestors was not just a theoretical possibility, but a reality. To decipher the deep history of a population from a single person’s DNA, Li and Durbin leveraged the fact that any single person actually carries not one but two genomes: one from his or her father and one from his or her mother. Thus it is possible to count the number of mutations separating the genome a person receives from his or her mother and the genome the person receives from his or her father to determine when they shared a common ancestor at each location. By examining the range of dates when these ancestors lived—plotting the ages of one hundred thousand Adams and Eves—Li and Durbin established the size of the ancestral population at different times. In a small population, there is a substantial chance that two randomly chosen genome sequences derive from the same parent genome sequence, because the individuals who carry them share a parent. However, in a large population the chance is far lower. Thus, the times in the past when the population size was low can be identified based on the periods in the past when a disproportionate fraction of lineages have evidence of sharing common ancestors.

Population Fluctuations

A recent study in the journal BMC Genomics applied this PSMC analysis to the genome of a Chinese Grouse (Tetrastes sewerzowi). This forest-dwelling species can be found in the mountains east of the Qinghai-Tibet Plateau. It is currently considered “Near Threatened” because of population declines due to ongoing deforestation and fragmentation of its habitat.

The genomic analyses revealed that the population size of the Chinese Grouse has fluctuated over time. Populations decreased during early to middle Pleistocene but showed an expansion during late Pleistocene (between 30,000 and 40,000 years ago), followed by a sharp decline during the last glacial maximum (about 20,000 years ago). Similar patterns have been found in other bird species, highlighting the influence of the climatic cycles during the Pleistocene (see for example this study by Krystyna Nadachowska-Brzyska and her colleagues).

The PSMC analysis showed population fluctuations of the Chinese Grouse during the Pleistocene. From: Song et al. (2020) BMC Biology.

Coniferous Forests

Next, the researchers focused on the underlying mechanisms of these population fluctuations. Why did the number of Chinese Grouse wax and wane during the Pleistocene? To answer this question, the researchers turned to Ecological Niche Modelling and reconstructed the distribution of the Chinese Grouse throughout the Pleistocene. This exercise showed that the population expansion during the late Pleistocene (30,000–40,000 years ago, also known as the Greatest Lake Period) can be explained by the warmer weather which allowed conifer forests, the primary habitat for Chinese Grouse, to reach their greatest extent. Later on, during colder periods, the coniferous habitat shrunk and the Chinese Grouse populations moved westwards into higher altitudes.

These findings indicate that the distribution of the Chinese Grouse is strongly dependent on the coniferous forest cover. It is thus essential to protect these fragmented forests and safeguard the future of this beautiful bird.

Ecological Niche Modelling showed how the suitable habitat for Chinese Grouse increased during the late Pleistocene (figure a), followed by extensive loss of habitat later on (figure b). The current distribution is depicted in figure c. From: Song et al. (2020) BMC Genomics.

References

Song, K., Gao, B., Halvarsson, P., Fang, Y., Jiang, Y. X., Sun, Y. H., & Höglund, J. (2020). Genomic analysis of demographic history and ecological niche modeling in the endangered Chinese Grouse Tetrastes sewerzowiBMC genomics21(1), 1-9.

Featured image: A drawing of Chinese Grouse (Tetrastes sewerzowi) © Ornithological Miscellany. Volume 2 | Wikimedia Commons

Bad news for the Brown Eared Pheasant?

Genomic study finds low genetic diversity and high levels of inbreeding in this vulnerable species.

Small populations are often at risk. They can get sucked in a negative feedback loop of genetic and demographic decline that culminates in their extinction (the so-called extinction vortex, which I covered in this blog post). In general, small populations are more vulnerable to genetic drift and inbreeding, leading to a loss of genetic diversity. This lower level of genetic diversity might prevent small populations from adapting to changing environments. However, it is not all misery and mayhem for small populations. One potential benefit of a small population size is genetic purging, the process in which deleterious variants appear more often due to inbreeding and get purged from the population because individuals carrying these variants fail to survive or reproduce. The result is a genetically healthier population, despite low levels of genetic diversity.

A recent study in the journal Molecular Biology and Evolution examined the situation of the brown eared pheasant (Crossoptilon mantchuricum), a vulnerable bird species that is declining across its range in China due to human activities, such as deforestation and hunting. Is this species heading for extinction or does it reap the benefits of genetic purging?

Genetic Purging?

Based on the genomes of 40 individuals, the researchers identified three distinct populations corresponding to locations in Shaanxi (Western), Shanxi (Central), and Hebei & Beijing (Eastern). The genetic diversity across these three populations was extremely low. In fact, it was the lowest genome-wide estimate for any bird species to date. But, as explained above, this low level of genetic diversity might result in genetic purging when deleterious alleles are filtered out by purifying selection.

The action of genetic purging can be tested with the population genetic statistic Tajima’s D. I have explained the rationale behind the statistic in another blog post, but for this story you only need to understand the main interpretation. In general, a negative Tajima’s D points to a selective sweep (and thus genetic purging), while a positive Tajima’s D suggests balancing selection. In the three brown eared pheasant populations, Tajima’s D was highly positive. There is thus no evidence for genetic purging. And that is bad news…

The brown eared pheasant shows very low levels of genetic diversity (left figure). The positive values of Tajima’s D suggest that there is little purifying selection across the genome of this species (right figure). Blue refers to the blue eared pheasant, Brown-W, Brown-C and Brown-E refer to three populations of the brown eared pheasant. Adapted from Wang et al. (2021) Molecular Biology and Evolution.

Genetic Load

Low genetic diversity is often the outcome of inbreeding. When related individuals mate, their offspring will mostly receive the same genetic variants from both parents. This results in large genomic regions with little genetic variation, also known as runs of homozygosity (ROHs). The brown eared pheasant did indeed show more ROHs compared to its sister species, the blue eared pheasant (C. auritum), that is of little conservation concern.

A closer look at these genomic regions revealed that some brown eared pheasant populations have accumulated missense and loss-of-function mutations. Missense mutations occur when a change in the DNA results in the wrong amino acid being incorporated into a protein. And loss-of-function mutations lead to functional problems in the activity of a protein. Clearly, the brown eared pheasant is suffering from inbreeding depression. Moreover, because natural selection seems unable to eliminate deleterious mutations, this species is accumulating a high genetic load. Unless conservation actions are implemented – such as a genetic rescue program – the brown eared pheasant might be heading for extinction.

The brown eared pheasant populations show more runs of homozygosity (ROHs) compared to the blue eared pheasant, suggesting high levels of inbreeding. From: Wang et al. (2021) Molecular Biology and Evolution.

References

Wang et al. (2021). Genomic Consequences of Long-Term Population Decline in Brown Eared Pheasant. Molecular Biology and Evolution38(1), 263-273.

Featured image: Brown eared pheasant (Crossoptilon mantchuricum) © Josh More | Flickr