Insights on the evolution and adaptation toward high-altitude and cold environments in the snow leopard lineage

Qigao Jiangzuo; Joan Madurell-Malapeira; Xinhai Li; Darío Estraviz-López; Octávio Mateus; Agnès Testu; Shijie Li; Shiqi Wang; Tao Deng

doi:10.1126/sciadv.adp5243

. 2025 Jan 15;11(3):eadp5243. doi: 10.1126/sciadv.adp5243

Insights on the evolution and adaptation toward high-altitude and cold environments in the snow leopard lineage

Qigao Jiangzuo ^1,^2,^*, Joan Madurell-Malapeira ^3,⁴, Xinhai Li ^5,⁶, Darío Estraviz-López ^7,⁸, Octávio Mateus ^7,⁸, Agnès Testu ^9,¹⁰, Shijie Li ^1,¹¹, Shiqi Wang ^1,^11,^*, Tao Deng ^1,^11,^*

^¹Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 10044, China.

^²Key Laboratory of Orogenic Belts and Crustal Evolution, School of Earth and Space Sciences, Peking University, 5 Yiheyuan Road, Beijing 100871, China.

^³Earth Sciences Department, Paleo[Fab]Lab, Università di Firenze, Via G. La Pira 4, 50121 Firenze, Italy.

^⁴Department of Geology, Faculty of Sciences, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain.

^⁵Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.

^⁶College of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, China.

^⁷GEOBIOTEC, Department of Earth Sciences, NOVA School of Science and Technology, Caparica, Portugal.

^⁸Museu da Lourinhã, Lourinhã, Portugal.

^⁹Université de Perpignan Via Domitia UMR 7194 ‘Histoire Naturelle de l'Homme Préhistorique, Perpignan, France.

^¹⁰EPCC–Centre Européen de Recherches Préhistoriques, Tautavel, France.

^¹¹College of Earth and Planetary Sciences, University of the Chinese Academy of Sciences, Beijing 100049, China.

Corresponding author. Email: jiangzuo@ivpp.ac.cn (Q.J.); wangshiqi@ivpp.ac.cn (S.W.); dengtao@ivpp.ac.cn (T.D.)

Roles

Qigao Jiangzuo: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing

Joan Madurell-Malapeira: Conceptualization, Data curation, Investigation, Methodology, Project administration, Resources, Validation, Visualization, Writing - original draft, Writing - review & editing

Xinhai Li: Formal analysis, Methodology, Software, Validation, Writing - review & editing

Darío Estraviz-López: Resources, Software, Validation

Octávio Mateus: Resources, Software, Validation

Agnès Testu: Resources, Software, Validation

Shijie Li: Conceptualization, Methodology, Software

Shiqi Wang: Formal analysis, Funding acquisition, Investigation, Methodology, Validation, Writing - review & editing

Tao Deng: Conceptualization, Funding acquisition, Investigation, Project administration, Resources, Software, Supervision, Validation, Writing - review & editing

PMCID: PMC11734717 PMID: 39813339

Abstract

How snow leopard gradually adapted to the extreme environments in Tibet remains unexplored due to the scanty fossil record in Tibet. Here, we recognize five valid outside-Tibet records of the snow leopard lineage. Our results suggest that the snow leopard dispersed out of the Tibetan Plateau multiple times during the Quaternary. The osteological anatomy of the modern snow leopard shows adaptation to the steep slope and, to a lesser extent, cold/high-altitude environment. Fossils and phylogeny suggest that the snow leopard experienced a gradual strengthening of such adaptation, especially since the Middle Pleistocene (~0.8 million years). Species distribution modeling suggests that the locations of the fossil sites are not within most suitable area, and we argue that local landscape features are more influential factors than temperature and altitude alone. Our study underscores the importance of integrating morphology, fossil records, and species distribution modeling, to comprehensively understand the evolution, ecology, and inform conservation strategies for endangered species.

Integrated morphology, fossil records, and SDM reveal the evolution and adaptation in the snow leopard lineage.

INTRODUCTION

The snow leopard (Panthera uncia) is one of the iconic animals of the Tibetan Plateau and distributes also in the ranged mountainous regions of central Asia as the Mongolian Plateau (1–6). It has distinctive morphological features, e.g., long and dense pelage, long tail, short face, steep and wide forehead, enlarged anterior chamber (ectotympanic) of the auditory bulla, high and steep mandibular symphysis, and relatively large cheek teeth (1, 7–10), that clearly distinguish it from the other members of genus Panthera. Although historically classified in its own genus, Uncia (1, 11, 12), modern phylogenetic analyses based on genetic and genomic data have conclusively placed it within the Panthera genus, particularly as the sister species of the tiger (Panthera tigris) (13–16).

The snow leopard typically inhabits within high alpine regions, above 3000 m, or above the tree line (17) but may also occur at much lower elevations below 1000 m in some areas of Russia (18). The status of the snow leopard in the International Union for Conservation of Nature Red List is vulnerable, with ~4000 individuals (17). However, under global warming, its distribution is expected to be substantially affected, as moving northward (19) or upward to a higher altitude (20) based on species distribution modeling (SDM) methods on current known distribution.

While the distinctive characteristics of the snow leopard have long been acknowledged, the correlation between these traits and its adaptation to the Tibetan Plateau environment, as well as their evolutionary history, remains largely unexplored. This gap in understanding is primarily due to the scarcity of snow leopard fossils in the Tibetan Plateau and its surrounding regions. Nevertheless, several potential records from northern China and Europe (8, 21–23) provided insight into the evolution and adaptation of this species. However, these records have yet to be rigorously tested using phylogenetic or statistical approaches, leaving their validation and phylogenetic positions uncertain.

In this study, we provide in-depth analyses of potential snow leopard records (Fig. 1, A to D; see a review in the Supplementary Materials), especially the best-preserved skull from Manga Larga (Portugal) and a mandible from Longdan (China) with the implementation of phylogenetic and geometric morphometric analyses. We explored the ecological adaptation of the modern and fossil snow leopards, focusing on the function of their unique traits using anatomical study, finite element analysis, and morphometric approaches, and investigated how these traits evolved through the Quaternary. Then, we used species distribution models to predict the past distribution under the last glacial maximum (LGM) condition, which represents the potential largest distribution of the snow leopard, and this predicted distribution was compared with the fossil records to see whether the past adaptation of the snow leopard lineage is equivalent to that of the modern one. These analyses were then combined to infer the evolution and ecological adaptation/requirements of the snow leopard.

RESULTS AND DISCUSSION

Systematics

Order Carnivora Bowdich, 1821

Family Felidae Batsch, 1788

Subfamily Felinae Batsch, 1788

Genus Panthera Oken, 1816

Panthera uncia (Schreber, 1775)

Panthera uncia lusitana subsp. nov.

Diagnosis—small-sized pantherine cat (extant snow leopard-sized). Cranium broad and high, with short rostrum. Forehead slightly concave (in lateral view) and wide; orbit large; bony choana not widened; bulla relatively flat, with enlarged ectotympanic. Deep corpus, with vertical symphysis and low coronoid process; ventral margin of masseteric fossa not laterally expanded. P4 with straight buccal border; m1 slender with antero-buccal corner. Cheek teeth enlarged relative to skull overall size (large ratio of m1 length/mandible length).

Differential diagnosis—differs from modern P. uncia by having slightly narrower frontal and less inflated auditory bulla, P4 with straight buccal border; differs from P. pyrenaica by having slightly smaller size, shorter c-p3 diastema, larger cheek teeth, lower coronoid process; differs from all other Panthera species by having smaller size, wider frontal, concave forehead in lateral view, more inflated auditory bulla, more enlarged ectotympanic chamber, shorter rostrum, lower coronoid process.

Etymology—referred to Lusitania, the ancient region of the western Iberian Peninsula which became a Roman province and corresponds to most of the present-day Portugal and Spanish provinces of Salamanca and Cáceres.

Holotype—MG1355.0001-9, mostly complete skull with broken zygomatic arches and missing both upper second premolars and a few associated postcranial bones.

Type locality and age—Manga Larga (39.51972°N, 8.83114°W), Porto de Mós Municipality, central Portugal, Late Pleistocene.

Description and comparisons—See the Supplementary Materials.

Panthera aff. pyrenaica

Diagnosis—small-sized pantherine cat (extant leopard-sized). Symphysis relatively vertical (relative to horizontal plane) in orientation; ventral margin of masseteric fossa not laterally expanded. m1 buccolingually robust.

Differential diagnosis—differs from P. pyrenaica by having less elevated symphysis, buccolingually wider m1; differs from modern P. uncia and P. u. lusitana by having less elevated symphysis, longer c-p3 diastema, higher coronoid process, smaller cheek teeth; differs from P. palaeosinensis by having smaller size, lower symphysis, less ventrally extended angular process and non-expanded ventral border of the masseteric fossa; differs from all other Panthera species by having smaller size, non-expanded ventral border of the masseteric fossa.

Material—Institute of Vertebrate Paleontology and Paleoanthropology (IVPP), Chinese Academy of Sciences, Beijing, China, V31895.

Locality and age—Longdan, Linxia Basin, China, Early Pleistocene, 2.5 to 2.2 Ma.

Description and comparison—See the Supplementary Materials.

Ecomorphological adaptation of fossil snow leopard

The peculiar cranial morphology of the modern snow leopard has been noticed by many previous works (8, 11, 12, 24, 25). In the present study, we mainly compared its cranial anatomy with other pantherine cats, especially the similar-sized leopard Panthera pardus to elucidate the function of these traits.

The overall cranium morphology of the snow leopard is characterized by the wide and high skull, with an expanded and domed forehead and frontal sinus (24). An enlarged frontal sinus (often posteriorly extended) is quite common in Carnivora, especially Ailuropoda and bone-cracking hyaenids, as well as other fossil groups (26–31) and is suggested to be related to resisting high stresses during biting on hard substances (32). This is unlikely to be the case for the snow leopard, whose frontal sinuses are not posteriorly expanded and the cheek teeth are not robust. The overall cranial morphology of the snow leopard is very similar to that of cheetah Acinonyx jubatus. A greatly laterally expanded frontal sinus was observed in both P. uncia and A. jubatus (24). Anatomical studies suggest that the frontal sinus is connected with nasal passages through small ostia and is normally in continual communication with the nasal air (33). An expanded frontal sinus in P. uncia and A. jubatus can serve as warming the cold air, or heat dissipation during running, and help in promoting the respiratory efficiency of the animals (31, 34–36). P. uncia lives at high altitudes with low-oxygen concentration, and A. jubatus has a chasing hunting behavior with vigorous locomotion (1, 10, 37, 38). Therefore, although the adaptations of P. uncia and A. jubatus are different, the enlarged frontal sinus can help in both cases in respiratory efficiency during hunting. We interpret this anatomical feature in the snow leopard, as an adaptation to high-altitude and cold environments. The enlarged cheek teeth are often correlated with slicing meat, and resisting forces of tendons and skin often seen in sabertoothed cats (39, 40). In the Tibetan Plateau, food sources and competitors are relatively rare, and snow leopards stay near its kills for longer periods than do other large cats to consume its prey (41–43). In high-altitude and cold environments, the kills will soon freeze, and the large cheek teeth of the snow leopard are also helpful in chewing hard frozen meat.

Other craniodental and postcranial traits are, however, not directly adapted to cold environments themselves. The short rostrum brings (Fig. 1) a high mechanical advantage to the anterior part of the jaw. The high and steep symphysis suggests a strong resistance to stresses induced by the canine bite (44). Our finite element analyses on the mandibular profile also show averaged low Von Mises stress (reflected by the stress contour diagram) at the symphysis part in modern P. uncia given by the same bite force (Fig. 2). These findings suggest that the anterior portion of the jaw has better mechanical performance, enabling the snow leopard to withstand high bite forces in this region more effectively. The relatively short braincase and absence of a posteriorly extended lambdoidal crest imply that the temporal muscle has a more vertical component and a small posterior component. Such muscle direction benefits a strong upward force during occlusion and a lower force to track the coronoid backward and resulted in low speed of occlusion. All these traits, as well as the rounded canine cross section (1, 45), support a strong canine bite of the snow leopard compared with P. pardus (Fig. 2). The short rostrum and low speed of occlusion lead to a relatively slow bite. This is in accordance with the fact that P. uncia predates mainly on Caprini bovids (3, 46–48), which have short metapodial bones. The short distal limbs in mammals are correlated with a low speed but higher strength (49, 50). Another important cranial trait of the snow leopard is the large and more anteriorly oriented orbit. The orbit diameter/condylobasal length ratio of P. uncia reaches 0.278 (0.264 to 0.296, n = 13), much larger than that of other species of Panthera (mean 0.226, 0.189 to 0.254, n = 48), suggesting a larger eye, and R square of lineal model (n = 90) of orbit diameter/condylobasal ratio and condylobasal of Panthera is very low at 0.24, suggesting that there is no significant allometry. The angle between the long axis of the orbit and the sagittal plane (in dorsal view) is significantly larger than other species of Panthera and Puma but comparable to A. jubatus (Fig. 3A2). A large angle suggests that the orbit is oriented more anteriorly, therefore with a large overlap of eyesight range of both eyes. This, together with the short rostrum, leads to a better stereo vision of P. uncia compared with the other species of Panthera, which is needed in prey discovery and focusing on the open mountainous region, as Caprini bovids generally have protective coloration in rock cover. Similar adaptation with a short rostrum and a more anteriorly oriented orbit can be seen in many open environment felid species, e.g., Otocolobus manul, Felis margarita, or Felis nigripes (fig. S12). The enlarged ectotympanic chamber (Fig. 3A3) is also similar to that of Acinonyx but unlike that of other Panthera being adapted to hearing ability in the open environment (51). These cranial traits of the snow leopard are adapted to hunting Caprini bovids in the open mountainous region.

Fig. 2. — (A) Cranial comparison of *P. uncia* AMNH M166952 and *P. pardus* AMNH M89009, highlighting functional traits related to high/cold adaptation (green) and (prey type related) mountain life (red). (B) Finite element analyses of mandibles of modern and fossil *P. uncia*, modern *P. pardus*, and several fossil snow leopards.

Fig. 3. — (A) Cranial angles of felids; (A1) Angle in the lion *P. leo*; (A2) angle in the snow leopard *P. uncia*; (A3) angle α and its impact on eyesight; (A4) comparison of angle α in modern and fossil felids; (A5) comparison of angle β in modern and fossil felids; (B) comparison of the ratio of ectotympanic and entotympanic area in modern and fossil felids; (C) comparison of angle γ in modern and fossil felids.

Our analyses of postcranial skeletal proportions suggest that the snow leopard has relatively long distal limbs, a cursorial adaptation in congruence with previous results (52). In the principal components analyses (PCAs) of 16 proportions (see the Supplementary Materials for details of these proportions), the morphospace of P. uncia is remote from those of other felid species. The PC1 is positively correlated with humerus distal condyle height, femur medial side distal condyle height, scapular length, and pelvis length and negatively correlated with tibia length. The species with positive scores have large girdle bones allowing the powerful muscle attachment with high mechanic advantage. The PC2 is mainly positively correlated with radius length and, to a lesser extent, tibia length, and species having positive scores have cursorial adaptations. The postcranial morphology of P. uncia is therefore built for speed not strength. The long distal limb bones, especially the tibia, as well as the long lumbar vertebral column and the long tail (52), support a strong jumping ability and are adapted to mountain life on steeped slopes. On the other hand, the distal condyle heights of the humerus and femur (table S3), which directly correlated with a cross-sectional area that sustains the stress of joint, are related to sustaining the force from body mass and locomotion. In this aspect, the relatively low condyle of the snow leopard reflects its relatively small body size within Panthera. Alternatively, low condyle height of humerus can be balanced to retain high flexibility of foreleg for hunting.

In summary, the overall craniodental and postcranial morphology of the modern snow leopard shows the combination of adaptation to hunt in steeped slopes in open mountainous regions and adaptation to high altitude. The adaptations to mountainous regions exhibited in cranial and skeletal morphology (cranium mechanic design, skeleton proportions, and enlarged ectotympanic) seems to be more prominent than those to a high-altitude, cold, and low-oxygen environment (enlarged frontal sinuses and enlarged cheek teeth), suggesting that the local environment is probably more important concerning on the locomotion and hunting behavior than the climate for snow leopards. On the other hand, the white coat, long hair, and some physiological traits in the snow leopard represented adaption to the cold environment (10).

Multiple out-of-Tibet dispersal and the rapid evolution of the snow leopard during the Middle and Late Pleistocene

As our results show, the unique craniodental and postcranial traits of the snow leopard are adapted to mountainous regions, prey type, and climate. The fossil record could help to explore how these traits evolved during the Quaternary.

We identified and analyzed five potential records in Europe and northern China (including the specimen from Longdan, northern China) that putatively belonging to the snow leopard lineage (see the detailed morphological comparison in the Supplementary Materials). Unexpectedly, most of these records are located far away from the Tibetan Plateau. Four of these records are of relatively recent age [i.e., <0.6 million years (Ma)]. To better study their evolutionary position, we perform total evidence phylogenetic analyses of the Pantherini, including both modern and fossil species (the poorly preserved Plio-Pleistocene species are not included).

The total evidence phylogenetic analyses using combined morphological and genetic data were performed to investigate the position of these putative fossil snow leopards. Our phylogenetic tree (Fig. 4) supports the four potential records as a basal snow leopard and supports the oldest record P. aff. pyrenaica from Longdan as a very basal snow leopard (but with relatively low posterior probability at the latter, suggesting the presence of uncertainty). The phylogenetic tree using pure morphological data gives a similar result (fig. S13), with a different position of P. uncia lineage, but the same interspecies relationship within the P. uncia lineage. Both analyses support a successive sister group relationship of fossil records and modern species, which are fully consistent with their age (younger species are closer to living species). The topology supports a roughly rapid evolution of the snow leopard lineage since the Early Pleistocene.

Fig. 4. — (A) Plot on tibia/femur length ratio and radius/humerus ratio. (B) Plot on pelvis/femur length ratio and scapular/humerus ratio. (C) PCA plot of 16 postcranial skeleton ratios; see the explanation in the appendix and raw data in table S3. R, radius; H, humerus; T, tibia; DH, distal antero-posterior height (of long bone); DW, distal medio-lateral width (of long bone); Pe, pelvis; Sc, scapular; F, femur; L, length; MC, metacarpal; MT, metatarsal; P/p, upper/lower premolar.

Among these five records, only the latest Pleistocene Niuyan Cave one shows nearly the same traits as the modern snow leopard and should be assigned to the modern species P. uncia. The Late Pleistocene skull from Manga Larga shows partial discrepancy from the modern P. uncia, out of the range of modern species in some measurements, and is regarded as distinct subspecies. All other fossil records show significant differences from the modern species and should be regarded as distinct species. In general, the late Middle and Late Pleistocene (0.3 to 0.01 Ma) snow leopards already have basic adaptations similar to the modern species (wide forehead, short rostrum, elevated symphysis, enlarged cheek teeth, and enlarged ectotympanic) but still with certain differences. Specifically, P. u. lusitana from Manga Larga has a forehead (mainly frontal) with a less concave profile, and its bony choana is relatively narrower, whereas the mandibular corpus is much deeper than in modern P. uncia. Therefore, P. u. lusitana has less specialization of traits adapted to the cold environment compared with the modern species and also has a somewhat different feeding behavior from that of the modern species (deep mandibular corpus). The early Middle Pleistocene (0.6 to 0.5 Ma) snow leopard P. pyrenaica, however, does not have similar traits, as it has small cheek teeth similar to other pantherine cats, and the snout is also relatively longer, and these primitive traits are symplesiomorphic shared with P. pardus (23). The putative Early Pleistocene snow leopard P. aff. pyrenaica is basically similar to P. pyrenaica, although the symphysis is yet to be so verticalized, which is primitive in regard to modern P. uncia. The lack of large cheek teeth, short snout, and vertical symphysis (for P. aff. pyrenaica), as analyzed above, suggests less adaption to the cold environment and less reliance on Caprini prey type for P. pyrenaica and P. aff. pyrenaica. In the Longdan fauna, there is no Caprini recorded (53).

As a species showing clear adaptation to the environment of the Tibetan Plateau, the majority of its evolutionary history is likely to occur there. The records outside the Tibetan Plateau are rare and incomplete. Longdan in the Linxia basin is located at the northeastern border of Tibet, has a high altitude of ~2000 m (53, 54), and probably represents the general marginal distribution of the snow leopard at that time. The four other records are likely to represent the occasional spread of the snow leopard out of Tibet at (or shortly before) the age of the fossil records. These records can thus be used to trace the rapid specialization of the snow leopard during the Quaternary.

Although the overall shape [inferred from geometric morphometric (GM) analysis in Fig. 4] does not show a clear pattern, in regard to the most functional traits analyzed above and PCA plots (Fig. 5B), two periods can be distinguished. The first period is from the Early Pleistocene and early Middle Pleistocene. The snow leopard in this period gradually developed verticalized symphysis suitable to prey on Caprini, but the rostrum is relatively long, so its adaption is initial. Its cheek teeth are small, implying that its adaptation to the cold environment is less developed than that of the modern snow leopard. The second period is from the late Middle Pleistocene to the present day. The snow leopard in this period already has basically the same functional traits as in modern species, with a short rostrum and enlarged cheek teeth, enlarged frontal sinus, enlarged ectotympanic chamber, large orbit, and better adapted to prey on Caprini-type species and cold environments than the snow leopard from the first period. This is supported by morphological evolutionary rates inferred from Bayesian analyses using the approach of Zhang and Wang (55). The lineage leading to the modern P. uncia shows the highest morphological evolutionary rates among the branches in the tree (Fig. 4A). This is especially marked in the Middle-Late Pleistocene period. Such rapid evolution during the Early-Middle Pleistocene Transition is likely to be correlated with the onset of glaciation in the Tibetan Plateau in the Middle Pleistocene (56, 57), with the extensive period in marine isotope stages 18 to 16, 12, 6, and 4 to 2 (58). The climate and environmental change provided stronger selective pressure on the snow leopard adapted to living and catching unique prey in Tibet. The out-of-Tibet dispersal of the snow leopard is in accordance with its major prey, the Caprini bovids. The early evolution of Caprini is endemic to Tibet (59, 60). Since the Plio-Pleistocene, some species already began to spread out of Tibet (61–63), but the large wave of such dispersals only occurred since the Middle Pleistocene, with the appearance of Ovis and Hemitragus in Europe (64, 65) and Pseudois in lowland northern China (Beijing) (66, 67). The increased amplitude of glaciation since the Early-Middle Pleistocene Transition brought a long period of the colder environment in Eurasia during several glacial stages (68), providing both Caprini bovids and the snow leopard the opportunity to spread from Tibet to other mountainous regions in Eurasia. The functional trait PCA (Fig. 6) also supports a gradually shift of the snow leopard lineage from a leopard-like space to a more specialized space.

Fig. 5. — (A) Time-calibrated total evidence phylogenetic tree of pantherine cats and the morphological evolutionary rate. (B) Geometric morphometric analyses on lateral views of the cranium and mandible of the fossil snow leopard in comparison with modern species. (B1) Mandible lateral profile, (B2) cranial dorsal view, (B3) cranial lateral view, and (B4) cranial ventral view.

Fig. 6. — (A) The predicted probability of snow leopard presence under the LGM climate conditions. (B) Functional traits PCA morphospace, with reconstruction of fossil and modern snow leopards. Artwork by Jianhao Ye.

We find that during the late Middle and Late Pleistocene P. pardus also show certain adaptation toward Caprini prey (69–71), probably due to the harsh environment and abundance of Caprini during the different glacial stages (see the Supplementary Materials). Some characters of this leopard show some similarities to P. uncia (see details in the Supplementary Materials). However, our geometric morphometric analyses suggest that they are not much different from modern Asian P. pardus, and they lack some key traits seen in the snow leopard lineage (especially the auditory bulla). The lesser extent of cold/mountainous adaptations in P. pardus is likely due to the brief period during which leopards inhabited this environment and the unstable environmental conditions in Europe during the Middle and Late Pleistocene, which provided inconsistent selection pressures for cold/mountainous adaptations.

SDM analysis of potential LGM distribution and dispersal route of the snow leopard

To test whether the five fossil localities are within the area of suitable climate region of the snow leopard during the Pleistocene, we performed SDM to predict the probability of snow leopard presence under LGM climate conditions. Although none of the records can be precisely dated to LGM, the two Late Pleistocene ones are likely from this age. Nevertheless, during the LGM, the cold environment was predominant than at any other time of the Middle to Late Pleistocene (72, 73), and the snow leopard is likely to spread farthest from Tibet at the LGM. This condition, therefore, represents the largest potential distribution of the snow leopard. Note that the SDM cannot predict the presence or not of glaciation, which definitely present in the Tibetan Plateau during LGM, so the potential range of the snow leopard in the Tibetan Plateau must be much smaller during LGM.

The predicted suitable area (Fig. 6) is much larger than the current condition (see fig. S14 for the prediction under the current conditions for comparison). Except for the Longdan one, none of the other four putative records are located within the highly suitable area predicted by SDM, although they are all closer to the suitable area than they are found today. This makes sense considering the small number of snow leopard records discovered in these regions, and these records probably represent the occasional and marginal distribution of the Pleistocene snow leopard. All four Middle to Late Pleistocene localities are lower than 1000 m in altitude. This is especially true for the Loc. 3 of Zhoukoudian (74), which is not in a typical cold environment as in the LGM conditions.

The SDM results suggest that the fossil snow leopards probably have different climate adaptations as the modern snow leopards do. This is in accordance with our morphological analyses that most of these fossil snow leopards have less strong adaptation to cold and high altitudes. On the other hand, the snow leopard from Niuyan Cave, which we identified as modern snow leopard, is also located outside the predicted suitable area under the LGM conditions. Notably, the microenvironments are steeped slopes in mountainous regions in all four cases. We argue that for the snow leopard, climate and altitude only partially influence their distribution, but mountainous steeped slopes are necessary habitat. Most anatomical traits of the snow leopard analyzed above are adapted to preying focusing, catching, and killing in the mountainous region. In lowlands with heavy cover (warm and humid conditions), the advantage of the snow leopard (over the leopard) loses. This explains their rarity or absence in most of the faunae of the lowlands far away from Tibet. Overall, our analyses suggest that the mountainous region with steeped slopes and heavy rock cover are probably more important factors that influence the snow leopard distribution during its evolutionary history than the temperature and altitude themselves. This information would benefit further protection.

The predicted suitable area may also infer the dispersal routes of the snow leopard during glacial stages, as this provides potential connectivity. However, topography, prey type, etc., which is not included in the SDM analyses, are also important for real dispersal, so the exact dispersal routes are still waiting for more fossil records.

In summary, our analyses support five fossil records putatively corresponding to the Pleistocene snow leopard lineage. According to the obtained results, the former lineage suffered a rapid evolution during the Quaternary, especially since the Middle Pleistocene. The earliest putative record of the lineage is located at Longdan (Linxia Basin) near the border of Tibet with an estimated chronology of 2.2 to 2.5 Ma. The other four records are far from Tibet and not located in the suitable area predicted by SDM under the LGM conditions. In consequence, snow leopards could disperse out of Tibet to lowland eastern Asia and Europe through different routes. These later four fossil records are still out of the suitable area, representing the marginal distribution at that time. All three aspects (morphology, paleoenvironment of fossil occurrence, and SDM under the LGM conditions) support that the temperature and altitude are less important than the local microscale landscape, and steeped slope and heavy rock are more important factors for snow leopard survival.

Our study suggests climate, prey type, and especially landscape (mountainous region) are important for snow leopard, probably more than altitude itself. This information will be beneficial for the future protection of this iconic animal. We highlight the importance that the combination of morphology, fossil records, and ecological methods (SDM) can have for providing more comprehensive and testable data on the ecology and adaption of modern species and provide information that might be helpful to develop protection strategies for the animal.

MATERIALS AND METHODS

Phylogenetic analyses

To elucidate the evolutionary position of the analyzed specimens, a comprehensive phylogenetic analysis was performed, using a matrix modified from Salles (24), Werdelin and Flink (75), and Jiangzuo et al. (76). A total of 160 craniodental and postcranial characters are present in the matrix, which is initially designed for whole members of the family Felidae (including Machairodontinae), so the matrix has some characters not necessarily informative within the species included in this analysis. As we focus on the evolutionary history and trait evolutionary rates of the subfamily Pantherinae, most irrelevant taxa were not added, only leaving Catopuma temminckii as the outgroup. Genetic data were adopted from Johnson et al. (14), and four blocks (autosome DNA, X chromosome DNA, Y chromosome DNA, and Mitochondrial DNA) were set, together with the morphology block.

Bayes inferences with tip-dating under the fossilized birth-death model (77, 78), using the mkv model (79) for morphology block, and GTR + gamma for four DNA blocks were performed. MrBayes3.2.7 (80, 81) was used in inference. Two independent runs, each with four chains, were used in analyses. Ten million generations were performed in each run. See the detailed settings in the Supplementary Materials file.

Metric and geometric morphometric analyses

To clarify the morphology and the taxonomical position of the studied specimens, we performed biometric, as well as, geometric morphometric analyses. Only species that has the potential to be misidentified as P. uncia was included in metric and geometric morphometric analyses to clarify their differences, i.e., extant P. uncia, extant P. pardus from Africa and Asia, Panthera onca, and Puma concolor. Dentognathic specimens from mammalian collection of American Museum of Natural History (AMNH M), New York, USA; Smithsonian National Museum of Natural History (USNM), Washington DC, USA; Museum of Comparative Zoology (MCZ), Boston, USA; Institute of Zoology, Chinese Academy of Sciences, Beijing, China (IOZ); and Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China (KIZ), Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining (NWIPB) were used in analyses. The landmarks and semilandmarks were obtained using software tpsDig2.32. The measurements of lower dentition and mandible follow the study of Jiangzuo and Liu (9). Geometric morphometric analyses were performed using Geomorph 4.0.1 package (82) of R 4.0.5 (83), and plots were made using the package ggplot2 (84). PCA analyses were performed in software past 4.0.3 (85).

Anatomical study and fossil records

We reviewed the literature and the available fossil collections in Eurasian Museums and Research Centers to find potential snow leopard fossil records, which are tested and analyzed in this study. The details on the comments on fossil records are provided in the Supplementary Materials. Two of them, Niuyan Cave and Loc. 3 of Zhoukoudian, are both from Fangshan, Beijing, China (67, 74), one from Arago cave, Tautavel, France (8, 23), and one from Manga Larga Cave, Santo António Plateau, Portugal (21). None of these four records were identified as the snow leopard when they were first published but as P. pardus or Panthera sp. (or Felis sp.), but the similarity with the snow leopard was mostly recognized. The anatomic, morphometric, and geometric morphometric analyses of the mandible and lower dentition were carried out to study the phylogenetic and taxonomic features of these four records. The faunal composition of the four records was analyzed to infer the paleoenvironment.

Finite element analyses

Finite element analyses were performed in the Abaqus computer-aided engineering (CAE) (v. 6.14) software. For simplicity, two-dimensional (2D) finite element modeling for hemimandibles was used (86, 87). First, photos of the mandibles of P. uncia AMNH M166952 and P. pardus AMNH M89009 were taken in the right lateral view. The outlines were plotted in the AutoCAD 2018 software, scaled to the same size, and exported .dxf files. The exported outline files were loaded into Abaqus CAE and generated 3D planar shell models with a uniform thickness of 2 mm. The models were assigned the homogeneous material property approximating mammalian cortical bone, with a Young’s modulus of 15 GPa and a Poisson’s ratio of 0.28, following the study of Drake et al. (88). As our goal is to compare the mandibular mechanical behavior, we set the same bite force of temporal and masseteric muscles as 3000 and 1000 N, respectively, for all taxa used. The direction of muscle (temporal and masseteric) of the modern species is measured in the case seen in Fig. 1, and the exact angle and bite force are given in table S1. The fossil species related to modern P. uncia were set as the same angle. The following boundary conditions were set: 1, one point at the posterior border of the condyle, only allowing vertical movement; 2, one point at the dorsal border of the condyle, only allowing horizontal movement; and 3, the tip point of the canine, all the six movements were constrained.

Species distribution modeling

Data

The snow leopard occurrence data used in this study were from field surveys, literature, and the Global Biodiversity Information Facility database (table S4). Most of the occurrences were derived from camera trap records, and others were from feces or footprints marked during line transect surveys (20, 89, 90). All occurrences used for SDMs were from recent surveys conducted after 2010, and more than 60% of the records were based on the surveys in the past 5 years. The minimum distance between occurrences is 5 km. All occurrences were recorded using GPS handsets.

We used the 19 bioclimate variables (30 arc sec) from the WorldClim 2.0 dataset (https://worldclim.org/) for current (1960–1990) climate conditions; and we used the WorldClim 1.4 downscaled data for climate conditions at the LGM (about 22,000 years ago) (91). For the LGM data, we selected the global climate model CCSM4, because it is a moderate model with temperature and precipitation neither too high nor too low (92).

Models

We used environmental variables to explain the presence or absence of the snow leopard using the model logit(p) = f(x1, x2, … xk), where p is the probability of the presence of snow leopard at a location, and x are environmental variables.

We applied random forest (93) for SDMs. Random forest is a machine learning algorithm and is one of the frequently used SDM approaches (94–97). It is especially good for handling high-dimensional data (multiple correlated explanatory variables) and complex relationships such as interaction and high-order effects (98–100). We used the R package randomForest (101) for the analysis. We set the argument ntree (number of trees) to be 1000 and left others undefined (default settings, including no weights, were used).

For the current distribution of snow leopards, we used the occurrences and evenly distributed 50 × 50 = 2500 pseudo absence points as the dependent variables, with the 19 climate variables in the WorldClim dataset as explanatory variables, and build a model to quantify the association between snow leopard occurrences and climate variables. Then, we projected the historical distribution of the snow leopard using the model and the climate data at the LGM. The partial effects of the 12 most important elements and the basic evaluation parameter of the SDM model are provided in the Supplementary Materials.

Acknowledgments

We thank Second Comprehensive Scientific Expedition on the Tibetan Plateau for supporting financial and logistical support in the fieldwork. We would like to thank the staff from the Geological Museum of Lisbon (R. Dias, J. Moita, and J. Sequeira) and J. L. Cardoso for permission to study the snow leopard of Algar da Manga Larga. We thank Y. Sun for discussion on the topic. For help in accessing collections, we thank M. Surovy, E. Hoeger, S. Ketelsen, N. Duncan, and N. Simmons (AMNH modern mammal collections); D. Lunde and J. J. Ososky (USNM modern mammal collections); M. Omura (MCZ modern mammal collections), X. Zhu and Y. Yang (IOZ modern mammal collections); W. Li (NWIPB modern mammal collections); and Z. Qiu, J. Chen, W. He, S. Chen, and L. Zhang (fossil collections of the IVPP and HMV).

Funding: This work was supported by National Key Research and Development Program of China 2023YFF0804501 to S.W.; National Natural Science Foundation of China 42102001 to Q.J.; National Natural Science Foundation of China 42430207 to T.D.; China Scholarship Council and the Frick Fund, Department of Vertebrate Paleontology, Division of Paleontology, AMNH to Q.J.; Agència de Gestió d’Ajuts Universitaris i de Recerca: 2021 SGR 00620 to J.M.-M.; Agencia Estatal de Investigación-European Regional Development Fund of the European Union: PID2020-116908GB-I00 to J.M.-M.; Portuguese Foundation for Science and Technology PhD grant 2020.05395.BD. to D.E.-L.; and GeoBioTec FCT grant UIDB/04035/2020 of the Fundação para a Ciência e Tecnologia to O.M.

Author contributions: Q.J.: Writing—original draft, conceptualization, investigation, writing—review and editing, methodology, resources, funding acquisition, data curation, validation, supervision, formal analysis, software, project administration, and visualization. J.M.-M.: Writing—original draft, conceptualization, investigation, writing—review and editing, methodology, resources, data curation, validation, project administration, and visualization. X.L.: Writing—review and editing, methodology, validation, formal analysis, and software. D.E.-L.: Resources, validation, and software. O.M.: Resources, validation, and software. A.T.: Resources, validation, and software. S.L.: Conceptualization, methodology, and software. S.W.: Investigation, writing—review and editing, methodology, funding acquisition, validation, and formal analysis. T.D.: Conceptualization, investigation, writing—review and editing, resources, funding acquisition, validation, supervision, software, and project administration.

Competing interests: The authors declare that they have no competing interests.

Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials.

Supplementary Materials

The PDF file includes:

Figs. S1 to S16

Tables S1 to S7

Legends for data S1 to S3

References

sciadv.adp5243_sm.pdf^{(2.9MB, pdf)}

Other Supplementary Material for this manuscript includes the following:

Data S1 to S3

sciadv.adp5243_data_s1_to_s3.zip^{(68.7KB, zip)}

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Figs. S1 to S16

Tables S1 to S7

Legends for data S1 to S3

References

sciadv.adp5243_sm.pdf^{(2.9MB, pdf)}

Data S1 to S3

sciadv.adp5243_data_s1_to_s3.zip^{(68.7KB, zip)}

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PERMALINK

Insights on the evolution and adaptation toward high-altitude and cold environments in the snow leopard lineage

Qigao Jiangzuo

Joan Madurell-Malapeira

Xinhai Li

Darío Estraviz-López

Octávio Mateus

Agnès Testu

Shijie Li

Shiqi Wang

Tao Deng

Roles

Abstract

INTRODUCTION

Fig. 1. Fossil snow leopards from Eurasia.

RESULTS AND DISCUSSION

Systematics

Ecomorphological adaptation of fossil snow leopard

Fig. 2. Craniodental ecomorphology of the snow leopard and related taxa.

Fig. 3. Functional statistical traits of Panthera uncia and its fossil relatives in comparison with other felids.

Multiple out-of-Tibet dispersal and the rapid evolution of the snow leopard during the Middle and Late Pleistocene

Fig. 4. Functional statistical postcranial traits of Panthera uncia in comparison with other felids.

Fig. 5. Phylogenetic position and morphospace of modern and fossil snow leopards.

Fig. 6. SDM predicted suitable distribution and morphospace of the modern and fossil snow leopards.

SDM analysis of potential LGM distribution and dispersal route of the snow leopard

MATERIALS AND METHODS

Phylogenetic analyses

Metric and geometric morphometric analyses

Anatomical study and fossil records

Finite element analyses

Species distribution modeling

Data

Models

Acknowledgments

Supplementary Materials

The PDF file includes:

Other Supplementary Material for this manuscript includes the following:

REFERENCES AND NOTES

Associated Data

Supplementary Materials

ACTIONS

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