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.