1 | INTRODUCTION
Climatic oscillations, especially during the
Quaternary,
have played a critical role in shaping the genetic diversity of animals
and plants by altering species distributions, periods of population
isolation, and influencing opportunities for secondary gene flow as
previously isolated species come into spatial contact (Hewitt, 2000;
Hoffmann & Sgro, 2011). Researchers commonly refer to climatic
oscillations such as glacial interglacial cycles as drivers of
biodiversity and evolutionary change (Oswald et al., 2016). During
climate oscillations, speciation events may increase as glacial barriers
cause large and previously continuous populations to split into several
smaller isolated populations (Wallis et al., 2016). Speciation may also
occur during interglacial periods in response to the expansion of
suitable habitat, leading to rapid population expansion followed by
subpopulation isolation due to factors such as changes in the size and
course of river systems, habitat fragmentation, or geological events
(Chen et al., 2015), as well as in response to changes in the direction,
intensity, and opportunities for gene flow within and between species
(Savolainen et al., 2013).
Several recent studies using genomic data and Pairwise Sequentially
Markovian Coalescent (PSMC) and Multiple Sequentially Markovian
Coalescent modeling (MSMC) (Schiffels & Durbin, 2014) have found that
climate-driven changes in species’ distributions are often associated
with major increases or decreases in effective population size (Liang et
al., 2018).
For
example, throughout the Quaternary, changes in the effective population
size of the giant panda (Ailuropoda melanoleuca ) closely tracked
climate change. Genetic data indicated that the population size of giant
pandas decreased significantly during both the longest Quaternary
glacial event (800,000-200,000 years ago) and the last glacial event
(20,000-10,000 years ago), but increased rapidly during interglacial
periods (Zheng et al., 2013). The effective population size of golden
snub-nosed monkey (Rhinopithecus roxellana ), with a sympatric
distribution with giant panda, showed a similar demographic pattern
(Zhou et al., 2014).
Over time, persistent barriers to gene flow in response to subpopulation
isolation, especially during periods of population contraction are
expected to result in the population extinction or adaptive evolution of
sister species (Abbott et al., 2013; Butlin et al., 2008; Crow et al.,
2010; Feder et al., 2012).
Subsequent environmental changes
or geologic events (e.g. volcanism) can result in secondary contact
between sister species, leading to periods of interspecific gene flow
and introgression (Hewitt, 2000; Hampe & Jump, 2011). Gene flow between
closely related species can act to retard speciation or result in
species’ extinction by merging gene pools or in response to competition
between hybrids and one or both parental species (Grant & Grant, 2014;
Moyle & Nakazato, 2010). Although methods based on genomic data have
been developed to detect gene flow during the differentiation of related
species (Han et al., 2017; Liu et al.,
2014),
lacking considering the species’ adaptation to their environment through
genetic changes might lead to be difficult to understand the mechanism
of species differentiation, particularly for closely related species,
only based on changes of distribution, effective population size and
gene flow.
François’
langur (Trachypithecus francoisi ) (Endangered) and White-headed
langur (T. leucocephalus ) (Critically Endangered) (IUCN, 2020,
https://www.iucn.org) represent two threatened species of nonhuman
primates that are endemic to the limestone forests and karst hills of
Southeast Asia. François’ langur distributes only in tropical and
subtropical regions of southwestern China (Guizhou, Chongqing, and
Guangxi Province) and northern Vietnam with a remaining wild population
of approximately 2,000 individuals, and White-headed langur is confined
to a narrow triangular area of karst hills totaling some 200
km2 in southern Guangxi province (107–108°E,
22°06′–22°42′N), China (Zhou & Huang, 2021). The population size of
White-headed langur is estimated at less than 1,000 individuals,
distributing in several small isolated subpopulations with being
surrounded by populations of François’ langur (Li et al., 2018).
Since White-headed langur were first described in 1955, there have
existed conflicting hypotheses concerning whether it represents an
independent species or a subspecies of François’ langur (Huang et al.,
2002). A recent study suggests that François’ langur and White-headed
langur diverged at the beginning of the Quaternary’s glacial maximum,
approximately 350,000 years ago (Liu et al., 2020).
Following
this initial divergence, both taxa
continuously experienced a second glacial event (at approximately
200,000 to 100,000 years ago) and a third glacial period (LGM
20,000-10,000 years ago) with a drop in temperatures, then followed by a
Holocene period of rising temperatures (Liu et al., 2020). Glacial
conditions during the period of 20,000-10,000 years ago appear to have
resulted in population bottlenecks among a diverse set of animal taxa,
such as the Nujiang catfish (Creteuchiloglanis macropterus ) (Kang
et al., 2017), Chinese alligators (Alligator sinensis ) (Wan et
al., 2013), Great tits (Parus major ) (Qu et al., 2015), Gray
wolves (Canis lupus ) (Fan et al., 2016), and snub-nosed monkeys
(Rhinopithecus spp.) (Zhou et al., 2016), suggesting that the
Guxiang glaciation (300,000 to 130,000 years ago) event should be a
primary driver of species diversification in the Tibetan Plateau and the
Hengduan Mountains of southeast China (Qu et al., 2015).
However, it remains unclear how changes in climatic suitability during
glacial and interglacial periods affected population
contraction/expansion and opportunities for gene flow between the these
two closely related langur species.
In addition, a clearer
understanding how the closely related and endangered species
historically respond to changes in habitat availability and climate is
beneficial for elucidating the process of speciation and developing
species conservation strategies, especially in the face of climate
change in the future. To examine these relationships, we used
climatic suitability, effective
population change, and gene flow to explain the diverse of the two
langur species and propose conservation strategies based on climate
change (Figure 1). We assumed that for the two species, the separation
of climatic suitability caused the changes of effective population size
and interspecific gene flow, which leaded to niche separation between
François’ langur and White-headed langur.