The demographic analyses showed the grouse population reached a peak ~ 40,000 years ago followed by sharp decrease with a bottleneck ~ 20,000 years ago. The population expansion can be explained by the warmer weather during the Greatest Lake Period (30,000 - 40,000 years ago) as the alpine conifer forests, the primary habitat for Chinese Grouse [1], reached their greatest extent at this time [10, 12]. The Palaeo-distribution of coniferous forests changes in the QTP and adjacent mountains inferred by pollen cores [35] support the demographic changes inferred of Chinese Grouse [35, 36]. The demographic results and palaeo coniferous forests data show that coniferous forests played a pivotal role in Chinese Grouse demographic history by providing permanent refugias in the eastern QTP during the Quaternary. The QTP with its special intricate geographical environment had a significant influence on biodiversity and changes in the geographic distribution of animals in east of Asia during the Pleistocene and may play a key role on potential responses and feedbacks to global change in the future [11, 37].
Our demographic analyses highlighted that a high Ne of Chinese grouse persisted from the Early Pleistocene (2.43 million years ago-0.73 million years ago) to the Mid Pleistocene (0.73 million years ago - 0.10 million years ago) and that a population expansion occurred after the retreat of the Penultimate Glaciation (0.30-0.13 million years ago). Three significant glaciations have occurred in QTP during this time, the Xixiabangma glaciation in Early Pleistocene, Nyanyaxungla glaciation in Middle Pleistocene and Guxiang glaciation in late Middle Pleistocene [14, 15]. Like previous work, our results suggest that the QTP had several Pleistocene refugia which have affected Ne in this grouse inhabiting coniferous forests [10]. During the Pleistocene, many avian species living in coniferous forest in the boreal taiga and the QTP have diverged and are classified as superspecies or different subspecies, as a result of allopatric divergence and local adaptation [8, 23, 38, 39]. A narrow high altitude boreal forests were preserved in the southeast edge of the QTP by the uplift which comprise one of the key high-altitude biodiversity hotspots in the world [40]. This region harbors one of the world’s richest fauna and floras, because it harbored large and complicated refugial areas in different mountain regions, lowland, rivers and basins [10, 41, 42].
A population bottleneck occurred during the last glacial maximum (~20,000 years ago), when substantial alpine glaciations (for example, Gongga glacial II) likely resulted in extensive loss of coniferous forests [15]. Population bottlenecks in the same region coinciding with the LGM have also been identified in other animals such as the giant panda [12] and snub-nosed monkeys (Rhinopithecus) [13], suggesting that the Last Glaciation and palaeo coniferous forests changes had strong impacts on the population sizes of arboreal species. The sharp decline in Ne for Chinese Grouse, as in the Giant panda, snub-nosed monkeys, is consistent with the extreme cooling of the climate during the LGM.
Many previous studies have suggested that the LIG was a favorable period for other avian species, such as black grouse (Tetrao tetrix) because of increased seasonality in temperatures [43, 44]. During this period, black grouse and Greenland rock ptarmigan (Lagopus muta) populations expanded to a high Ne and reached their peaks [43, 45]. It is suggested that the severe reduction in avian population sizes approximately coincide with the beginning of the last glacial period (LGP, 110-12 kya) or occurring during this period [44]. In contrast to previous work, the demographical results of Chinese Grouse show no fluctuations associated with historical climatic changes during Early Pleistocene and Middle Pleistocene [44]. Instead a peak followed by a sharp decrease and a bottleneck occurred during this period. This pattern observed in Chinese Grouse may be related to the special geographical position, climate change and the mass accumulation rate (MAR) of Chinese loess, an index indicating cold and dry or warm and wet climatic periods in China [46, 47].
The SDM results showed that climate change had an influence on the amount and distribution shifts of suitable habitat of Chinese grouse. The model also revealed that suitable habitat during the LGM was more widely available than both during the warmer LIG and mid Holocene. Climate events during the LGM period resulted in an expansion of suitable habitat to low altitude regions in eastward areas compared with the LIG period and a shrink from this low altitude region to a more westward distribution during the mid-Holocene period. The result parallels patterns of population size change in Chinese Grouse estimated from the PSMC model, which suggested an expansion in population size from LIG period and then a peak and a bottleneck occurring at the LGM. Significantly, the suitable habitat of Chinese Grouse expanded toward lower altitudes in eastern areas during the LGM. I in contrast, the population moved into high altitudes in the western areas during the mid-Holocene. It is of significance that the geographic distribution of Chinese Grouse populations shifted in an east-west direction from LIG to the LGM and the LGM to mid-Holocene. The reason is that the shift of coniferous forests was significantly affected by seasonal extremes in temperature. In addition, the formation of the loess plateau stopped the forest to spread to the north.
Alarmingly, our results suggest that although suitable areas for the Chinese Grouse in the present-day are larger than during the mid-Holocene, the LGM and the LIG, the Ne has been kept at a low size after the bottleneck during the LGM. Dense coniferous forests are of critical importance for the Chinese Grouse, which are affected by climate change and recent human actions [1]. Our GAP analysis between the present-day distribution of Chinese Grouse and extent of present day coniferous forest shows that the Chinese Grouse populations were severely affected by loss and fragmentation of suitable forests. Forest fragmentation has profound and lasting influences around the globe, not only on the Earth’s biological diversity, but on ecosystem function and numerous ecosystem services [48, 49]. Because of the increase in density of local people with the high demands for farmland, timber, firewood and roads, deforestation of Chinese grouse’s mountain habitats continued until 1998 when a disastrous flooding happened, which motivated greater conservation of forests [1, 6]. Previous work on Chinese Grouse, blood pheasant (Ithaginis cruentus) and Sichuan jay (Perisoreus internigrans) have found that their distributions would be decreased and fragmented severely in the future [5, 6, 50]. The Chinese Grouse distributions under climate change scenarios is similar to other montane species [51], which would shift northward and upward under realistic climate change scenarios [6]. This long term fragmentation of coniferous forests may have effect on gene flow, speciation and divergence of these endemic isolated populations.