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Article

Karyotypes of 10 Anuran Species from the Qinghai–Tibetan Plateau

by
Qiheng Chen
1,2,
Shengchao Shi
1,2,
Ningning Lu
1,
Cheng Shen
1 and
Jianping Jiang
1,2,3,*
1
Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China
2
Chengdu Institute of Biology, University of Chinese Academy of Sciences, Beijing 100049, China
3
Mangkang Biodiversity and Ecological Station, Tibet Ecological Safety Monitor Network, Changdu 854500, China
*
Author to whom correspondence should be addressed.
Diversity 2023, 15(9), 947; https://doi.org/10.3390/d15090947
Submission received: 27 June 2023 / Revised: 16 August 2023 / Accepted: 19 August 2023 / Published: 22 August 2023
(This article belongs to the Special Issue Herpetofauna of Eurasia)
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Abstract

:
The Qinghai–Tibet Plateau (QTP) is the highest and largest mountain plateau in the world, which has become a focus area of amphibian biodiversity research and conservation, depending on its large number of endemic and threatened species. Among the 58 families of Anura, only a few species of four families (Megophryidae, Bufonidae, Dicroglossidae, Ranidae) are distributed in QTP. Revealing the genetic diversity of these species is crucial for research on their environmental adaptability and biodiversity conservation. Chromosome rearrangements are a critical source of genetic variation, which is recognized as a driver of speciation, providing the genetic material for differentiation and environmental adaptation of amphibians. Here, we identified the karyotypes of 10 species of the above families from the QTP. The karyotypes of these species were obtained from new sites that were not previously reported. Among them, the karyotypes of D. himalayanus and tetraploid B. zamdaensis were reported for the first time. In particular, the ploidy of B. zamdaensis from Zanda, China, was found to be distinctly different from the ploidy from Spiti River, India. This indicates that they have presented species differentiation and supports the multiple and complicated polyploidization events in the Bufotes toads. Furthermore, the different locations of the secondary constriction between the Weixi and Zhongdian populations of O. xiangchengensis support that there is a karyotypic variation between the two subspecies (O. xiangchengensis xiangchengensis vs. O. xiangchengensis deqinicus). A series of chromosomal variations may have facilitated the rapid evolution of amphibians in the QTP, and our study will provide support for further research on amphibian genetic diversity and biodiversity conservation.

1. Introduction

The Qinghai–Tibet Plateau (QTP) is the highest and largest mountain plateau in the world, with a mean elevation of over 4500 m above sea level and a surface area of 2.3 million km2 [1]. It is known as ‘the roof of the world’ and has been classified as a biodiversity hotspot [2]. Its landscape of river gorges and steep mountains has led to dramatic ecological stratification and environmental heterogeneity in a relatively small area [3], resulting in one of the most diversified fauna and flora in the world [4,5].
QTP has become a focus area of amphibian biodiversity research and conservation, given its large number of endemic and threatened species [6]. Only a few species of four families (Megophryidae, Bufonidae, Dicroglossidae, Ranidae) among the 58 families of Anura are distributed in QTP [6,7], attracting growing scientific attention. To explore the influence of a high-elevation environment on amphibian species and how they adapt to it, numerous aspects of amphibians in QTP have been studied, including phylogeography [8,9], diversity [10], ecological niche [11], functional phenotype [12], and symbiotic microbiome [13]. Previous studies have suggested that high-elevation environment adaption of amphibians may benefit from their unique genetic diversity.
Systematic data on native taxa are critical to understanding environmental adaptation and biodiversity, which is crucial for biodiversity conservation in QTP. Cytogenetic data provide some of the most fundamental information about the genome [14] and have been used as clues to study phylogenies and geographical clines [15]. Karyotypic variations, including polyploidization, inversion, and translocation, have been found to drive speciation, adaptive divergence, and alternate reproductive strategies [16,17,18,19]. Research on amphibian cytotaxonomy has a history of more than 140 years [20]. To date, over 8600 amphibian species have been described [7], and about 1900 of them have been reported to possess karyotypes [14], indicating an urgent need for more cytogenetic data. Previous studies on genomes and karyotypes have suggested that amphibians exhibit high levels of diversity in chromosome numbers and genome sizes [14,21], which likely reflects their unique evolutionary history [22]. Therefore, the identification of karyotypes in amphibians from QTP is important for the diversity and conservation of amphibians in this region.
In this study, we investigated the karyotypes of 10 anuran species in the QTP and explored variations in chromosome number and structure. These data will contribute to revealing the genetic diversity of amphibians in the QTP. Furthermore, our karyotypic data will provide support for research on environmental adaptation and conservation of amphibians.

2. Materials and Methods

2.1. Specimens

We collected 25 individuals of 10 amphibian species from Yunnan, Xinjiang, and Xizang of China in 2019 and 2022 (Table 1). The taxonomic identity of each individual was confirmed by morphological and molecular data. After having taken samples for the karyotype test, specimens were fixed in 75% ethanol and deposited at the Chengdu Institute of Biology, Chinese Academy of Sciences (CIB, CAS), Chengdu, China.

2.2. Chromosome Preparation and Measurement

Mitotic metaphase cells were obtained from bone marrow using the procedures described by Schmid [23], and each individual produced four slices. Chromosomes were stained with 10% Giemsa for 30 min and photographed using an Optec B302 microscope equipped with a Sony (Tokyo City, Japan) ICX285A CCD camera. Chromosomal measurements were conducted using ImageView (Chongqing Optec Instrument Co., Ltd., Chongqing City, China) software and analyzed based on Levan’s criterion [24]. Ten mitotic metaphase cells were randomly selected for measurement from each species. The character terminology and abbreviations used in this study are provided below:
p—short arm; q—long arm; SC—secondary constriction; cen—centrometric; inter—interstitial; per—peripherial; AR—arm ratio; CI—centrometric index (%); RL—relative length (%); LC—location of centromere; M—metacentric chromosome: 1.00 < AR <= 1.70, 37.50 < CI <= 50.00; SM, submetacentric chromosome: 1.70 < AR <= 3.00, 25.00 < CI <= 37.50; ST—subtelocentric chromosome: 3.00 < AR <= 7.00, 12.50 < CI <= 25.00; T—telocentric chromosome, 7.00 < AR, 0 < CI <= 12.50.

3. Results

3.1. Karyotype of Megophryidae

The karyotype of Oreolalax xiangchengensis consists of 26 chromosomes, including 6 pairs of large chromosomes and 7 pairs of small chromosomes (Figure 1A and Figure 2A). The SC is located on the 6qinter, and the AR ranges from 1.03~1.71. Among these chromosomes, all except chromosome No. 3 are metacentric, and chromosome No. 3 is submetacentric (2SM + 24M).
The karyotype of Scutiger boulengeri comprises 26 chromosomes, including 6 pairs of large chromosomes and 7 pairs of small chromosomes (Figure 1B and Figure 2B). Among these chromosomes, No. 5, 7, and 8 are submetacentric, while the others are metacentric (6SM + 20M). The secondary constriction (SC) is located on the 2pinter.

3.2. Karyotype of Bufonidae

The karyotype of Bufo gargarizans comprises 22 chromosomes, including 5 pairs of large chromosomes and 8 pairs of small chromosomes (Figure 1C and Figure 2C). All chromosomes are metacentric, and the AR ranges from 1.06 to 1.63. The SC is located on 6qter.
The karyotype of Duttaphrynus himalayanus consists of 22 chromosomes, including 6 pairs of large chromosomes and 5 pairs of small (Figure 1D and Figure 2D). All the chromosomes are metacentric (22M), and the AR ranges from 1.05 to 1.52. Chromosome No. 4 has the largest AR, and no obvious SC was observed.
Both Bufotes taxkorensi and Bufotes zamdaensis have a chromosome number of 44, and the SCs are located on the 11qter (Figure 1E,F and Figure 2E,F). The karyotype of B. zamdaensis includes one pair ST (No. 21) and two pairs of SM (No. 9, 13); the remaining chromosomes are metacentric (2ST + 4SM + 38M). While B. taxkorensis has four pairs of SM (No. 7, 8, 13, 14), and the remaining chromosomes are M (8SM + 36M).

3.3. Karyotype of Dicroglossidae

The karyotype of Maculopaa chayuensis consists of 26 chromosomes, consisting of 5 pairs of large chromosomes and 8 pairs of small (Figure 1H and Figure 2G). The AR of chromosomes ranges from 1.23 to 1.99, and five pairs of them are SM, while the other pairs are M (10SM + 16M). No obvious SC were observed.
The karyotype of Gynandropaa yunnanensis comprises 64 chromosomes, all of which are telocentric chromosome (64T) (Figure 1I and Figure 2H). The RL of 32 pairs of chromosomes ranges from 1.32~5.57. Since all chromosomes only have a long arm and no short arm, there are no AR or CI values in this karyotype (Table 2). No obvious SC was observed in this karyotype.
The karyotype of Nanorana parkeri consists of 26 chromosomes, including 5 pairs of large chromosomes and 8 pairs of small chromosomes (Figure 1G and Figure 2I). The SC is located on the 6qter. The AR ranges from 1.20 to 2.56, and 4 pairs of chromosomes are SM, while other pairs are M (8SM + 18M).

3.4. Karyotype of Ranidae

Rana chaochiaoensis has a chromosomes number of 2n = 26, including five large chromosomes and eight small chromosomes (Figure 1J and Figure 2J). The SC is on the 6qper. The AR of chromosomes changes from 1.16~3.33. One pair of chromosomes is T (No. 8), 4 pairs are SM (No. 2, 4, 11, 13), and the other pairs are all M (2T + 8SM + 16M).

4. Discussion

4.1. Karyotype Comparison

4.1.1. Karyotype of Megophryidae

The karyotype of O. xiangchengensis population from Zhongdian County (ZD), Yunnan Province, has been reported by Li [25]. They have 26 chromosomes, including 3 pairs of SM (No. 3, 4, 5) and 10 pairs of M, with one pair of SC on the 6qper. On the other hand, the karyotype of the population from Weixi County (WX), Yunnan Province, only has one pair of SM (No. 3), and the SC is on the 6qinter. This suggests that there may be a chromosomal inversion or changes in the NORs (nucleolar organizing regions) locations occurring between different geographic populations of the O. xiangchengensis.
In a previous study, the karyotype of S. boulengeri from Kangding City, Sichuan Province, was reported as 2n = 26, with No. 7 chromosomes being SM, No. 5 being ST, and others being M, with the SC located on the 2pinter [26]. In this study, the chromosomal number and SC location of the population from Zanda County, Xizang Province, were found to be consistent with the Kangding population. However, the karyotype of the Zanda population, which includes 3 pairs of SM, 10 pairs of M and no ST, suggests that there are variations in AR and LC between these two populations of S. boulengeri.

4.1.2. Karyotype of Bufonidae

The karyotype of D. himalayanus population from Derung-Nu Autonomous County, Yunnan Province, has been identified in [22], while the specimens from this area have later been identified as D. cyphosus [6]. Therefore, in this study, the karyotype of D. himalayanus from Dingjie County, Xizang Province, is the first report of this species, which consisted of 22 metacentric chromosomes (22M).
B. gargarizans is widely distributed in China, and its karyotypes in several areas (Heilongjiang, Beijing, Shanghai, Sichuan, Fujian) have been reported [22]. In most previous studies, the karyotype of B. gargarizans had a chromosome number of 22, and the SC was located on the 6qter, which was consistent with our result.
The B. viridis complex comprises diploid (2n = 22), triploid (3n = 33) and tetraploid (4n = 44) bisexually reproducing taxa [27,28]. Among them, B. pewzowi is an allotetraploid with karyotype 4n = 44 [28,29]. The same chromosome number as B. taxkorensi and B. zamdaensis indicates that they are both allopolyploids. The B. pewzowi has four pairs of SM (No. 7, 8, 13, 14) that is identical to B. taxkorens, while different from B. zamdaensis (2ST + 4SM + 38M). The SCs in B. taxkorensi and B. zamdaensis are located on 11qter, while in B. pewzow, they are located on 12qter [29]. As they are all allopolyploids, it indicates that the SCs are located on only one pair of chromosomes in the No.6 tetrad, and therefore the positions of the SCs between these three tetraploid species are the same.

4.1.3. Karyotype of Dicroglossidae

The karyotype of M. chayuensis population in Lushui County, Yunnan Province, was previously reported to be 2n = 26, and it has 5 pairs of SM (No. 2, 3, 4, 6, 8) [30]. In this study, M. chayuensis from Derung-Nu Autonomous County, Yunnan, China, also has 26 chromosomes, including 5 pairs of SM (No. 2, 3, 4, 6, 13). However, among them, 4 pairs (No. 2, 3, 4, 6) are the same as the Lushui population, and 2 pairs (No. 8, 13) have different centromere positions.
All species in the genus Gynandropaa have 64 telocentric chromosomes (64T), and the SC location varies between different species or geographic populations [22]. In this study, no obvious SCs have been observed. Previous studies have reported that G. yunnanensis from Jingdong County, Jinping County, Tengchong City in Yunnan Province have SCs on 4qper, 2qinter and 15qinter, respectively [22,30,31]. Two different SC locations have been reported for G. phrynoides (Yimen County: 18qinter, Qujing City: 20qinter) [22,32]. G. sichuanensis from Zhaojue County, Sichuan Province, has an SC on 32qter [33]. Due to the similar chromosome morphology in G. sichuanensis, the differences in SC positions could be attributed to SC location polymorphism, or potential differences in measurement and ordering processes. Therefore, more cytogenetic techniques are needed to be conducted in different G. sichuanensis populations.
The karyotype of N. parkeri from Dingjie and Nanmulin Counties, Xizang Province, was found to be 2n = 26, with SC on the 6qter, which is consistent with the karyotype of the population from Lasa City, Xizang Province [26]. However, the locations of centromeres are different on some chromosomes. In this study, the karyotype of N. parkeri has 4 pairs of SM (No. 2, 3, 6, 9), while a previous study reported 6 pairs of SM (No. 2, 3, 4, 6, 8, 9) Sin Lasa population. It is difficult to determine whether these chromosomal differences arise from karyotypic variations or are simply caused by a problem in establishing chromosomal homologies. Therefore, further research is needed using more samples and additional techniques.

4.1.4. Karyotype of Ranidae

The karyotype of the R. chaochiaoensis populations from Kunming City, Zhongdian County, Yunnan Province, and Yanyuan City, Sichuan Province, have been reported previously [22,34,35]. All the results indicated that R. chaochiaoensis has a chromosome number of 26, and the SC is located at 6qper, which coincides with the findings of this study. Among different geographic populations, the No. 8 chromosomes are consistently ST, while the number of SM varies. The Yanyuan population has 5 pairs of SM (No. 2, 3, 7, 9, 13); the Kunming population has 3 pairs (No. 3, 9, 13); the Zhongdian population has 4 pairs; and the Weixi population has 4 pairs (No. 2, 4, 11, 13). These results suggest that the main characteristics of karyotypes among different populations of R. chaochiaoensis were constant, while the AR and SC positions show rich variations.

4.2. Karyotypic Differences and Phylogenetic Differentiation

The chromosome number of Megophryidae species ranges from 22 to 30 [14]. Among them, all species belonging to the genus Oreolalax and Scutiger have the same chromosome number of 26 [14,22], but they can be easily distinguished by the disparate locations of SCs. The SCs of species in the genus Oreolalax are located entirely on the No. 6 chromosomes (6qper, 6qter or 6qinter), while those in the genus Scutiger are located entirely on the No. 2 chromosome (2pper) [22]. The difference in the location of SCs between Oreolalax and Scutiger species may cause by chromosomal structural variations, and it serves as an important characteristic for distinguishing the karyotypes of these two genera. These findings imply that the chromosomal rearrangement may be causally related to the divergence of Oreolalax and Scutiger.
In 1990, Yang described the O. xiangchengensis from Deqin County as a subspecies of O. xiangchengensis deqinicus [36] based on the differences in webbing morphology compared to O. xiangchengensis xiangchengensis [36,37]. Zhongdian County is close to Xiangcheng County, while Weixi County is close to Deqin County. There are significant differences in karyotype between these two populations (Table 3), specifically in the location of the SC, which is located in the 6qper (Zhongdian County) and 6qinter (Weixi County), respectively. This suggests the presence of an inversion or changes in the NOR location on the long arm of the No. 6 chromosome among different subspecies of O. xiangchengensis. Furthermore, despite the species’ high diversity and significant morphological differences in the genus Oreolalax, genetic distances based on mitochondrial DNA are relatively closer [38]. Therefore, the chromosomal variation may be one of the facilitating factors in the speciation within the genus Oreolalax.
In 1998, Fei et al. described B. zamdaensis as a valid species based on its morphological differences from B. taxkorensi and B. pewzowi [39]. Karyotypic data indicated that B. zamdaensis is not only diverse from B. taxkorensi and B. pewzowi in morphology but also in karyotype (Table 3). However, the karyotype of B. zamdaensis from Spiti River, India, has previously been reported as triploid (3n = 33) [33]. The different ploidy levels in the B. viridis complex are the result of multiple whole genome duplication (WGD) events, for which a relatively well-supported hypothesis for their formation has been proposed [28]. Prior to this report, tetraploid population of B. zamdaensis has not been identified in the karyotype. The individuals in this study were collected from the type locality of this species, and there is geographical isolation between these tetraploid populations and the previously reported triploid populations [40]. The discovery of tetraploid population in B. zamdaensis provides new evidence supporting the occurrence of multiple WGD events in the B. viridis complex.
Table 3. Comparison of the karyotypes of 10 Anuran species.
Table 3. Comparison of the karyotypes of 10 Anuran species.
SpeciesChr. NumberKaryotype CompositionSMSTTSCLocationRef.
Oreolalax xiangchengensis2624M + 2SM3 6qinterWeixi Lisu Autonomous County, Yunnan, China--
2620M + 6SM3, 4, 5 6qperZhongdian County, Yunnan Province, China[25]
Scutiger boulengeri2620M + 6SM5, 7, 8 2pinterDingjie County, Xizang, China--
2620M + 6SM5, 7, 8 2pinterDingqing, County, Xizang, China--
2620M + 6SM5, 7, 8 2pinterZhongba County, Xizang, China--
2622M + 2SM + 2ST75 2pinterKangding City, Sichuan Province, China[26]
Bufo gargarizans2222M 6qinterLijiang Naxi autonomous county, China--
2218M + 4SM4, 9 6qinterHeilongjiang Province, China[22]
2218M + 4SM4, 9 6qinterBeijing City, China[22]
2218M + 4SM4, 9 6qinterShanghai City, China[22]
2218M + 4SM4, 9 6qinterSichuan Province, China[22]
2218M + 4SM4, 9 6qinterFujian Province, China[22]
Duttaphrynus himalayanus2222M /Dingjie County, Xizang, China--
Bufotes taxkorensi4438M + 2ST + 4SM9, 1321 11qterTaxkorgan Tajik Autonomous County, Xinjiang, China--
Bufotes zamdaensis4436M + 8SM 7, 8, 13, 14 11qterZanda County, Xizang, China--
33/////Spiti River, India[40]
Bufotes pewzowi4436M + 8SM7, 8, 13, 14 12qterHotan Prefecture, Xizang Province, China[29]
Maculopaa chayuensi2616M + 10SM2–4, 6, 13 6pperDerung-Nu Autonomous County, Yunnan Province, China--
2616M + 10SM2–4, 6, 8 6pperLushui County, Yunnan Province, China[30]
Gynandropaa yunnanensis6464T 1–32/Binchuan County, Yunnan, China--
6464T 1–324qperJingdong County, Yunnan Province, China[31]
6464T 1–322qinterJinping County, Yunnan Province, China[22]
6464T 1–3215qinterTengchong City, Yunnan Province, China[30]
Gynandropaa phrynoides6464T 1–3218qinterYimen County, Yunnan Province, China[22]
6464T 1–3220qinterQujing County, Yunnan Province, China[32]
Gynandropaa sichuanensis6464T 32qterZhaojue County, Sichuan Province, China[33]
Nanorana parkeri2618M + 8SM2, 3, 6, 9 6qterDingjie and Nanmulin Counties, Xizang Province, China--
2616M + 10SM2–4, 6, 8, 9 6qterLasa City, Xizang Province, China[26]
Rana chaochiaoensis2616M + 8SM + 2ST2, 4, 11, 138 6qperWeixi Lisu Autonomous County, Yunnan, China--
2618M + 6SM + 2ST3, 9, 138 6qperKunming City, Yunnan Province, China[34]
2616M + 8SM + 2ST2, 3, 9, 138 6qperZhongdian County, Yunnan Province, China[22]
2614M + 10SM + 2ST2, 3, 7, 9, 138 6qperYanyuan City, Sichuan Province, China[35]

5. Conclusions

In conclusion, we identified the karyotypes of 10 amphibian species from the QTP. The karyotypes of these species were obtained from new sites that were not previously reported. Among them, the karyotypes of D. himalayanus and tetraploid B. zamdaensis were reported for the first time. The different ploidies of B. zamdaensis populations from Zanda, China (4n = 44) and the Spiti River, India (3n = 33) imply species differentiation and support the occurrence of multiple and complicated polyploidization events in the Bufotes toads. Furthermore, there are differences in the secondary constriction locations between the two subspecies of O. xiangchengensis (O. x. xiangchengensis and O. x. deqinicus). This study will provide further support for research on amphibian genetic diversity and biodiversity conservation.

Author Contributions

J.J. conceived the study. S.S. and C.S. performed the field sampling. Q.C. and N.L. conducted the laboratory experiments and analyzed the data. Q.C. and J.J. drafted the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Third Xinjiang Scientific Expedition (2022xjkk0205-1), and the Survey of Wildlife Resources in Key Areas of Tibet (ZL202203601), and China Biodiversity Observation Networks (Sino BON-Amphibian & Reptile).

Institutional Review Board Statement

The study was conducted according to the guidelines of the Declaration of Animal Care and Use Committee of Chengdu Institute of Biology and approved by the Institutional Ethics Committee of Chengdu Institute of Biology (permit No. CIBACUC20183110).

Data Availability Statement

No data were created.

Acknowledgments

We sincerely thank Zujun Yang of the University of Electronic Science and Technology of China for his help with the method of these experiments.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Karyotype of ten amphibians. (A) Oreolalax xiangchengensis; (B) Scutiger boulengeri; (C) Bufo gargarizans; (D) Duttaphrynus himalayanus; (E) Bufotes taxkorensi; (F) Bufotes zamdaensis; (G) Nanorana parkeri; (H) Maculopaa chayuensis; (I) Gynandropaa yunnanensis; and (J) Rana chaochiaoensis.
Figure 1. Karyotype of ten amphibians. (A) Oreolalax xiangchengensis; (B) Scutiger boulengeri; (C) Bufo gargarizans; (D) Duttaphrynus himalayanus; (E) Bufotes taxkorensi; (F) Bufotes zamdaensis; (G) Nanorana parkeri; (H) Maculopaa chayuensis; (I) Gynandropaa yunnanensis; and (J) Rana chaochiaoensis.
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Figure 2. Paired chromosome of 10 amphibians. The pairs of chromosomes were arranged by relative length, and the secondary constrictions were marked by a black arrow.
Figure 2. Paired chromosome of 10 amphibians. The pairs of chromosomes were arranged by relative length, and the secondary constrictions were marked by a black arrow.
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Table 1. Information of samples used in karyotype identification.
Table 1. Information of samples used in karyotype identification.
SpeciesLocalityLongitude (°E)Latitude (°N)GenderVoucher Number
Oreolalax xiangchengensisWeixi Lisu Autonomous County, Yunnan, China98.9483758227.68311651♀CIB5334220116
Oreolalax xiangchengensisWeixi Lisu Autonomous County, Yunnan, China98.9483758227.68311651♀CIB5334220118
Scutiger boulengeriDingjie County, Xizang, China87.08145828.592544♀CIBXJ2021121
Scutiger boulengeriDingqing County, Xizang, China95.41696131.053237♂CIBXJ2021124
Scutiger boulengeriDingqing County, Xizang, China95.41696131.053237♂CIBXJ2021125
Scutiger boulengeriZhongba County, Xizang, China84.04785429.775521♂CIBXJ2021133
Scutiger boulengeriZhongba County, Xizang, China84.04785429.775521♀CIBXJ2021134
Bufo gargarizansLijiang Naxi autonomous county99.71270827.06504♂CIByN201909214
Duttaphrynus himalayanusDingjie County, Xizang, China87.08145828.592544♀CIBXJ2021130
Duttaphrynus himalayanusDingjie County, Xizang, China87.08145828.592544♂CIBXJ2021131
Duttaphrynus himalayanusDingjie County, Xizang, China87.08145828.592544♂CIBXJ2021132
Bufotes taxkorensiTaxkorgan Tajik Autonomous County, Xinjiang, China75.2149805637.83938056♂CIBXJ2021119
Bufotes taxkorensiTaxkorgan Tajik Autonomous County, Xinjiang, China75.2149805637.83938056♂CIBXJ2021126
Bufotes taxkorensiTaxkorgan Tajik Autonomous County, Xinjiang, China75.2149805637.83938056♂CIBXJ2021127
Bufotes zamdaensisZanda County, Xizang, China79.98440831.534458♂CIBXJ2021120
Bufotes zamdaensisZanda County, Xizang, China79.98440831.534458♂CIBXJ2021135
Bufotes zamdaensisZanda County, Xizang, China79.98440831.534458♂CIBXJ2021136
Maculopaa chayuensisDerung-Nu Autonomous County, Yunnan, China98.5966569227.76807508♂CIByN201909280
Maculopaa chayuensisDerung-Nu Autonomous County, Yunnan, China98.5966569227.76807508♀CIByN201909282
Gynandropaa yunnanensisBinchuan County, Yunnan, China100.33122525.91264♂CIB5334220131
Nanorana parkeriDingjie County, Xizang, China87.08145828.592544♀CIBXJ2021122
Nanorana parkeriDingjie County, Xizang, China87.08145828.592544♂CIBXJ2021123
Nanorana parkeriNanmulin County, Xizang, China89.105929.34904722♂CIBXJ2021128
Rana chaochiaoensisWeixi Lisu Autonomous County, Yunnan, China99.4270154727.58048148♂CIB5334220132
Rana chaochiaoensisWeixi Lisu Autonomous County, Yunnan, China99.4270154727.58048148♀CIB5334220104
Table 2. The measuring data of karyotype to 10 amphibians.
Table 2. The measuring data of karyotype to 10 amphibians.
Chr.Index (Mean ± SD)Oreolalax xiangchengensisScutiger boulengerBufo gargarizansDuttaphrynus himalayanusBufotes taxkorensiBufotes zamdaensisMaculopaa chayuensiGynandropaa yunnanensisNanorana parkeriRana chaochiaoensis
1AR1.15 ± 0.041.23 ± 0.061.22 ± 0.061.29 ± 0.071.18 ± 0.071.19 ± 0.051.45 ± 0.05--1.20 ± 0.051.16 ± 0.06
CI46.48 ± 0.8444.79 ± 0.9045.08 ± 0.8743.58 ± 0.8745.79 ± 1.0245.57 ± 0.9540.88 ± 0.85--45.47 ± 0.8446.34 ± 1.02
RL15.00 ± 0.5915.92 ± 0.6216.06 ± 0.5717.44 ± 0.768.23 ± 0.348.77 ± 0.3314.09 ± 0.545.57 ± 0.2315.27 ± 0.5713.55 ± 0.53
LCMMMMMMMTMM
2AR1.49 ± 0.071.36 ± 0.061.26 ± 0.051.06 ± 0.051.16 ± 0.051.26 ± 0.051.99 ± 0.09--2.32 ± 0.101.95 ± 0.09
CI40.21 ± 0.7842.45 ± 0.8444.23 ± 0.8248.55 ± 0.9746.31 ± 1.0144.21 ± 0.8833.44 ± 0.67--30.09 ± 0.5933.95 ± 0.70
RL12.28 ± 0.4811.92 ± 0.4715.86 ± 0.6814.47 ± 0.557.84 ± 0.308.61 ± 0.3312.86 ± 0.504.99 ± 0.2112.21 ± 0.4711.72 ± 0.47
LCMMMMMMSMTSMSM
3AR1.71 ± 0.061.38 ± 0.051.52 ± 0.061.48 ± 0.071.11 ± 0.061.20 ± 0.061.81 ± 0.07--2.35 ± 0.111.36 ± 0.05
CI36.85 ± 0.7042.10 ± 0.8339.75 ± 0.7440.32 ± 0.7947.29 ± 1.0045.55 ± 0.9235.59 ± 0.68--29.83 ± 0.5542.37 ± 0.85
RL10.71 ± 0.4010.39 ± 0.3814.04 ± 0.5713.59 ± 0.547.77 ± 0.317.41 ± 0.2910.91 ± 0.444.98 ± 0.1911.37 ± 0.4710.93 ± 0.42
LCSMMMMMMSMTSMM
4AR1.61 ± 0.081.29 ± 0.071.63 ± 0.101.52 ± 0.071.16 ± 0.071.07 ± 0.041.97 ± 0.09--1.50 ± 0.101.73 ± 0.07
CI38.35 ± 0.7043.68 ± 0.8337.98 ± 0.7839.71 ± 0.7746.32 ± 0.8548.20 ± 0.9433.65 ± 0.69--40.03 ± 0.8136.63 ± 0.69
RL10.59 ± 0.429.76 ± 0.3711.98 ± 0.4811.92 ± 0.487.21 ± 0.297.15 ± 0.2810.31 ± 0.404.40 ± 0.1710.32 ± 0.4010.73 ± 0.46
LCMMMMMMSMTMSM
5AR1.59 ± 0.082.37 ± 0.131.07 ± 0.061.28 ± 0.071.49 ± 0.081.30 ± 0.071.33 ± 0.06--1.35 ± 0.071.53 ± 0.09
CI38.56 ± 0.7829.70 ± 0.6048.39 ± 0.9743.88 ± 0.8640.14 ± 0.9043.41 ± 0.8742.85 ± 0.87--42.56 ± 0.8339.52 ± 0.80
RL8.84 ± 0.348.08 ± 0.3410.18 ± 0.4211.15 ± 0.467.21 ± 0.306.85 ± 0.279.39 ± 0.374.14 ± 0.179.69 ± 0.3810.12 ± 0.39
LCMSMMMMMMTMM
6AR1.30 ± 0.061.29 ± 0.071.54 ± 0.061.43 ± 0.081.56 ± 0.051.33 ± 0.071.91 ± 0.10--1.76 ± 0.091.21 ± 0.05
CI43.54 ± 0.8943.76 ± 0.7539.39 ± 0.8241.23 ± 0.8039.11 ± 0.7542.84 ± 0.8534.38 ± 0.69--36.25 ± 0.7545.22 ± 0.98
RL8.60 ± 0.357.98 ± 0.3010.10 ± 0.438.04 ± 0.316.76 ± 0.256.73 ± 0.266.11 ± 0.243.93 ± 0.166.47 ± 0.287.66 ± 0.32
LCMMMMMMSMTSMM
7AR1.17 ± 0.051.76 ± 0.081.34 ± 0.071.27 ± 0.051.76 ± 0.081.10 ± 0.071.58 ± 0.09--1.57 ± 0.081.42 ± 0.06
CI46.19 ± 0.8536.19 ± 0.7242.66 ± 0.8744.09 ± 0.9736.24 ± 0.7547.67 ± 0.9038.75 ± 0.80--38.85 ± 0.8141.40 ± 0.78
RL5.73 ± 0.235.94 ± 0.255.15 ± 0.205.42 ± 0.196.10 ± 0.255.59 ± 0.236.31 ± 0.274.30 ± 0.176.20 ± 0.265.63 ± 0.23
LCMSMMMSMMMTMM
8AR1.33 ± 0.061.84 ± 0.091.11 ± 0.051.23 ± 0.051.89 ± 0.121.89 ± 0.081.52 ± 0.07--1.23 ± 0.063.33 ± 0.16
CI42.88 ± 0.8135.22 ± 0.6947.41 ± 1.0144.84 ± 0.8334.63 ± 0.7134.66 ± 0.6439.63 ± 0.72--44.81 ± 0.9723.09 ± 0.46
RL5.14 ± 0.195.76 ± 0.254.62 ± 0.185.07 ± 0.195.97 ± 0.255.49 ± 0.225.83 ± 0.233.92 ± 0.155.24 ± 0.225.59 ± 0.25
LCMSMMMSMSMMTMST
9AR1.40 ± 0.061.39 ± 0.061.50 ± 0.081.16 ± 0.051.50 ± 0.071.48 ± 0.041.42 ± 0.06--2.56 ± 0.161.55 ± 0.06
CI41.61 ± 0.8041.75 ± 0.9140.01 ± 0.8046.40 ± 0.9340.00 ± 0.7840.40 ± 0.8941.35 ± 0.79--28.07 ± 0.5539.15 ± 0.75
RL4.94 ± 0.215.48 ± 0.224.52 ± 0.184.79 ± 0.195.55 ± 0.235.33 ± 0.215.08 ± 0.224.19 ± 0.185.16 ± 0.205.46 ± 0.22
LCMMMMMMMTSMM
10AR1.03 ± 0.041.30 ± 0.081.13 ± 0.061.05 ± 0.061.14 ± 0.051.67 ± 0.081.27 ± 0.07--1.38 ± 0.071.38 ± 0.07
CI49.23 ± 1.0543.52 ± 0.8746.99 ± 0.9548.78 ± 0.9746.66 ± 0.8837.48 ± 0.8143.99 ± 0.92--42.05 ± 0.8442.09 ± 0.79
RL4.79 ± 0.165.37 ± 0.243.86 ± 0.164.60 ± 0.215.20 ± 0.215.27 ± 0.205.08 ± 0.193.61 ± 0.144.93 ± 0.204.93 ± 0.21
LCMMMMMMMTMM
11AR1.04 ± 0.041.31 ± 0.081.06 ± 0.061.07 ± 0.061.06 ± 0.041.28 ± 0.041.50 ± 0.08--1.45 ± 0.052.23 ± 0.11
CI49.13 ± 0.9643.24 ± 0.8748.64 ± 0.8948.35 ± 1.0148.43 ± 1.0043.78 ± 0.8840.05 ± 0.76--40.82 ± 0.8131.00 ± 0.66
RL4.64 ± 0.184.68 ± 0.193.62 ± 0.133.50 ± 0.125.06 ± 0.204.43 ± 0.174.74 ± 0.193.45 ± 0.144.89 ± 0.214.87 ± 0.20
LCMMMMMMMTMSM
12AR1.18 ± 0.071.15 ± 0.05 1.27 ± 0.061.42 ± 0.081.23 ± 0.05--1.33 ± 0.061.30 ± 0.06
CI45.86 ± 0.8646.44 ± 0.99 44.14 ± 1.0141.32 ± 0.7944.92 ± 0.89--42.85 ± 0.8243.40 ± 0.90
RL4.49 ± 0.174.49 ± 0.17 4.61 ± 0.184.11 ± 0.184.69 ± 0.183.55 ± 0.154.33 ± 0.174.35 ± 0.18
LCMM MMMTMM
13AR1.23 ± 0.051.09 ± 0.06 1.74 ± 0.071.90 ± 0.111.96 ± 0.12--1.37 ± 0.071.96 ± 0.10
CI44.84 ± 1.0347.75 ± 0.99 36.54 ± 0.7534.48 ± 0.7033.80 ± 0.63--42.15 ± 0.8333.78 ± 0.73
RL4.26 ± 0.174.23 ± 0.18 2.89 ± 0.133.27 ± 0.134.60 ± 0.193.66 ± 0.143.92 ± 0.174.47 ± 0.17
LCMM SMSMSMTMSM
14AR 1.80 ± 0.071.37 ± 0.08 --
CI 35.73 ± 0.7142.26 ± 0.79 --
RL 2.92 ± 0.112.89 ± 0.11 3.02 ± 0.13
LC SMM T
15AR 1.14 ± 0.051.30 ± 0.06 --
CI 46.72 ± 0.8743.45 ± 0.89 --
RL 2.52 ± 0.112.73 ± 0.11 3.02 ± 0.12
LC MM T
16AR 1.20 ± 0.061.03 ± 0.04 --
CI 45.54 ± 0.9149.22 ± 10.00 --
RL 2.46 ± 0.112.63 ± 0.10 2.70 ± 0.10
LC MM T
17AR 1.17 ± 0.061.18 ± 0.07 --
CI 46.04 ± 0.9345.79 ± 1.03 --
RL 2.36 ± 0.102.45 ± 0.09 3.08 ± 0.13
LC MM T
18AR 1.61 ± 0.091.22 ± 0.06 --
CI 38.30 ± 0.7945.02 ± 0.93 --
RL 2.22 ± 0.092.39 ± 0.10 2.70 ± 0.10
LC MM T
19AR 1.10 ± 0.061.27 ± 0.07 --
CI 47.67 ± 1.0244.08 ± 0.82 --
RL 2.00 ± 0.082.18 ± 0.08 2.76 ± 0.11
LC MM T
20AR 1.04 ± 0.051.16 ± 0.06 --
CI 49.09 ± 0.9946.30 ± 0.90 --
RL 1.86 ± 0.082.00 ± 0.08 2.60 ± 0.10
LC MM T
21AR 1.43 ± 0.063.76 ± 0.18 --
CI 41.13 ± 0.8320.99 ± 0.42 --
RL 1.67 ± 0.071.94 ± 0.08 2.44 ± 0.10
LC MST T
22AR 1.23 ± 0.051.51 ± 0.06 --
CI 44.92 ± 0.9639.86 ± 0.78 --
RL 1.60 ± 0.061.79 ± 0.07 2.81 ± 0.10
LC MM T
23AR --
CI --
RL 2.60 ± 0.11
LC T
24AR --
CI --
RL 2.60 ± 0.10
LC T
25AR --
CI --
RL 2.54 ± 0.09
LC T
26AR --
CI --
RL 2.23 ± 0.09
LC T
27AR --
CI --
RL 1.91 ± 0.08
LC T
28AR --
CI --
RL 1.91 ± 0.07
LC T
29AR --
CI --
RL 1.91 ± 0.08
LC T
30AR --
CI --
RL 1.75 ± 0.07
LC T
31AR --
CI --
RL 1.43 ± 0.06
LC T
32AR --
CI --
RL 1.32 ± 0.05
LC T
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Chen, Q.; Shi, S.; Lu, N.; Shen, C.; Jiang, J. Karyotypes of 10 Anuran Species from the Qinghai–Tibetan Plateau. Diversity 2023, 15, 947. https://doi.org/10.3390/d15090947

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Chen Q, Shi S, Lu N, Shen C, Jiang J. Karyotypes of 10 Anuran Species from the Qinghai–Tibetan Plateau. Diversity. 2023; 15(9):947. https://doi.org/10.3390/d15090947

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Chen, Qiheng, Shengchao Shi, Ningning Lu, Cheng Shen, and Jianping Jiang. 2023. "Karyotypes of 10 Anuran Species from the Qinghai–Tibetan Plateau" Diversity 15, no. 9: 947. https://doi.org/10.3390/d15090947

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