4 | DISCUSSION
Our results support the hypothesis that two endangered primate species, François’ langur and White-headed langur, diverged during the beginning of the Guxiang glacial period (300,000 to 130,000 years ago) (Zheng et al., 2002). Changes of climatic suitability of François’ langur and White-headed langur between LIG and LGM resulted in decrease of effective population size and interrupted interspecific gene flow. Given specific differences in behavior, ecology, morphology, and distribution (Table 3) (Huang et al., 2002; Groves, 2001; Li & Rogers, 2004, 2006; Liu et al., 2020; Zhou et al., 2021), we suggest that climatic niche differentiation should explain their divergence.
From LIG to the LGM period, the habitat average elevation for François’ langur (728 m) is higher than that for White-headed langur (188 m), which raised that climate shelter of White-headed langur has been isolated by François’ langur (Figure 5). We assume that glacial barriers and spatial isolation in refugia led to their evolutionary divergence (Figure 5), which is consistent with the assumption that, for most primate species, historical periods characterized by decreased temperature and rainfall result in a decrease in climatic suitability (Cavender-Bares et al., 2016; Liang et al., 2018). During the same periods, both the areas of climatic suitability for two langurs contracted and shifted their climatic suitability in response to major environmental changes (Figure 5), which was similar to others mammal, such as the Asian elephant (Elephas maximus ), the rhinoceros (Dicerorhinus sumatrensis , Rhinoceros unicornis , R. sondaicus ) and the giant panda (Li et al., 2015). In a previous study, we found that François’ langur and White-headed langur differ in the several features of their behavior, morphology, and physiology (Table 3) (Liu et al., 2020; Zhou et al., 2021). Accordingly, we suggest that climatic oscillations experienced by each species might result in these species-specific differences over the past 300,000 years.
From LIG to the LGM, the effective population size of François’ langur decreased at a considerably slower rate than that of White-headed langur (Figure 6). Changes in increases and decreases of their effective population size correlated with climatic suitability for François’ langur and White-headed langur (Figure 5-6). In addition, gene flow was primarily directed from François’ langur to White-headed langur from the LIG to the LGM (Figure 4). During this period, the temperature belt in China moved 2-6 degrees southward (Huang & Zhang, 2000), and climatic suitability for François’ langur surround White-headed langur (Figure 6). Asymmetric gene flow between these two species corresponded with François’ langur expanding its climatic suitability into previously isolated areas that White-headed langur populations inhabited (Figure 5). There is also considerable evidence that during the LGM, climate conditions led many temperate species to shift southward with decreasing temperatures (Davis & Shaw, 2001). For example, fossils of Equus hemionus were unearthed in Fusui County, Guangxi Zhuang Autonomous Region (the present distribution of White-headed langur), suggesting a cooler climate than today in south China (Wang & Mo, 2004).
During LGM period, both langurs survive in the climate shelter (Figure 5). During periods of severe range contraction, it is possible only for those subpopulations inhabiting forest refugia to survive (Bennett et al., 1991). Our results revealed that the climatic suitability of White-headed langur contracted in the LGM, indicating this species has been unable to expand into new ecological zones, although there was an increasing temperature over the past 10,000 years. And, although refugia can provide geographical and ecological opportunities to retreat, persist, and then begin a recolonization process under favorable environmental conditions (Morales-Barbero et al., 2018), it is obvious event that the refugia inhabited by White-headed langur, which were bordered by the Zuojiang River to the north and northwest and the Mingjiang River to the south and southwest, can only provide limited opportunities for this species to recolonize regenerating suitable habitat and be regarded as an effective barriers to gene exchange between the two langur species (Ayres & Clutton-Brock, 1992; Harcourt & Wood, 2012; Huang et al., 2002). Although the effective populations and climatic suitability of both species have been increasing over the last 10,000 years, the impact of human activities severely restricts the actual population recovery. For example, the farming culture in the south China from the Qin Dynasty (221-207 BC) seriously threatened to the survival of some large animals, such as Asiatic elephant, rhinoceroses, tiger, Asiatic black bear, and brown bear over the past 2000 years (Teng et al., 2019).
Temperature is a main driver of habitat change affecting the population size, distribution, and vegetative composition of expanding and contracting ecological zones, as well as the establishment of new suitable habitat (Parmesan, 2006). Our results indicated that from the LIG to the present, temperature and precipitation affected the climatic suitability of François’ langur (Table 1). During the LGM, warm mixed forests (WAMF) and temperate deciduous forests shifted southwards to ∼10° N and tropical seasonal rain forest (TSFO) was almost absent (Li et al., 2019). In contrast, during the mid-Holocene to the current period (6, 000 kyr ago), the TSFO, WAMF, and the temperate deciduous forest (TEDE) shifted northward 2°~5° (Li et al., 2019). These shifts in climate and habitat conditions, and the availability and distribution of suitable forest types are likely to have affected species-specific differences in behavior, ecology, and niche divergence between these closely related langur species (Li et al., 2016; Xiong et al., 2009; Zhou et al., 2009; Zhou & Huang, 2020), which might make François’ langur be easier to adapt to or tolerate wider range of temperatures and habitat types than did White-headed langur (Zhou et al., 2021). Accordingly, we suggest that climate oscillation, population isolation, and in situ evolution in refugia appears to have played a critical role in divergence and speciation for these two langurs.
By the year 2100, global temperature may reach 5-12 standard deviation units above the Holocene mean (Marcott et al., 2013). Lian et al. (2015) also found that temperature increase in southwest China’s karst region are not consistent with precipitation increases resulting in more frequent droughts and floods over the past 30 years. For those two species, the areas under the dual threat of human activity and climate change should be prioritized for protection, especially in Guangxi and Guizhou provinces (Figure 5; Supporting Information Figure S4). Also, our results indicated that White-headed langur would lose 33.8 percent of their climate suitability with climate change in 2050 (Supporting Information Figure S4). Thus, both François’ langur and White-headed langur will face more severe survival condition in the future.Other factors such as the expansion of industrial agriculture and pasture land will result in even further declines in suitable habitat for langurs in China (Supporting Information Figure S4). Moreover, the current habitat of these critically endangered and endangered primates is severely fragmented, which imposes severe limits on their ability to expand into new areas or exchange genes across subpopulations. The effective population size for these two species greatly exceeds their current population size, and both species are distributed in small and isolated subpopulations (Huang & Pan, 2010). Although the two langurs are listed the highest protect level, White-headed langur is facing an even more dire conservation situation than François’ langur. Given the existing small population size of each species, these populations are likely to go extinct before the end of the century without national priority for conservation, because the ability of species to adapt to climate change cannot keep pace with the rate at which humans are modifying, fragmenting, and converting natural habitats making them unsuitable for wild animal populations (IPBES, 2019; Wiens, 2016). Therefore, in the absence of an extensive and immediate management plans and conservation actions to expand suitable habitat and create corridors to connect isolated subpopulations, there remains little hope for the survivorship of these two primate species. The analysis not only allow better understand of species differentiation between two related species but also for multiple related species or for different geographical patterns of the same species. And understanding historical distribution changes can provide better recommendations for current and future species conservation, especially for endangered species.