Cryptic Diversity of the European Blind Mole Rat Nannospalax leucodon Species Complex: Implications for Conservation
Abstract
:Simple Summary
Abstract
1. Introduction
1.1. The Genus Nannospalax
1.2. The Role of Chromosomal Changes in Reproductive Isolation
1.3. Molecular Analysis of N. leucodon Genetic Differentiation
2. Materials and Methods
2.1. Sample Collection
2.2. DNA Extraction and Sequencing
2.3. Data Collection and Sequence Analysis
2.4. Genetic Diversity and Phylogenetic Analyses
3. Results
3.1. 16S rRNA Gene Nucleotide Sequence Comparison
3.2. MT-CYTB Gene Nucleotide Sequence Comparison
4. Discussion
4.1. Delineation of 11 N. leucodon CFs
4.2. Chromosomal Speciation, Reproductive Isolation, and the Biological Species Concept
4.3. Major Factors of Threat and Implications for Conservation
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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16S rRNA ID | MT-CYTB ID | Sample No | Sampling Locality b | Chromosomal Form | 2n/NF | Year of Capture | Tissue |
---|---|---|---|---|---|---|---|
MH979033 h 7 | OM714866 h 22 | 9RS a | Zlatibor Mt, RS | mse (a) | 56/82 | 1965 | Tooth |
MH979034 h 8 | OM714867 h 21 | 11RS a | Vlasina, RS | mse (a) | 56/82 | 1965 | Tooth |
/ | OM714872 h 11 | 23RS | Vlasina, RS | mse (a) | 56/82 | 2018 | Muscle |
OM691469 h 9 | OM714884 h 21 | 41RS | Vlasina, RS | mse (a) | 56/82 | 2020 | Liver |
OM691470 h 10 | OM714885 h 23 | 42RS | Jadovnik Mt, RS | mse (a) | 56/82 | 2020 | Liver |
OM691478 h 9 | OM714895 h 21 | 64RS | Vlasina, RS | mse (a) | 56/82 | 2021 | Liver |
OM691479 h 11 | OM714896 h 24 | 65RS | Mačvanski Pričinović, RS | mse (a) | 56/82 | 2017 | Liver |
OM691462 h 16 | OM714873 h 25 | 24RS a | Gvozd Mt, MN | her (b) | 54/90 | 1967 | Tooth |
MH979031 h 4 | OM714864 h 2 | 7RS a | Beograd, RS | syr (c) | 54/90 | 1962 | Tooth |
OL348372 h 5 | OM714881 h 1 | 38SL | Beograd, RS | syr (c) | 54/90 | 2019 | Liver |
OL348373 h 5 | OM714883 h 1 | 40RS | Beograd, RS | syr (c) | 54/90 | 2020 | Liver |
OL348374 h 5 | OM714887 h 1 | 44RS | Beograd, RS | syr (c) | 54/90 | 2021 | Liver |
MH979026 h 1 | OM714859 h 19 | 1RS | Šumarak, RS | hun (d) | 48/84 | 2016 | Liver |
MH979027 h 1 | OM714860 h 19 | 2RS | Šumarak, RS | hun (d) | 48/84 | 2016 | Liver |
MH979029 h 2 | OM714862 h 20 | 4RS | Pančevo, RS | hun (d) | 48/84 | 2017 | Liver |
MH979030 h 1 | OM714863 h 19 | 5RS | Kajtasovo, RS | hun (d) | 48/84 | 2018 | Liver |
OM691471 h 3 | OM714886 h 19 | 43RS | Vršački Breg, RS | hun (d) | 48/84 | 2020 | Liver |
MH979032 h 6 | OM714865 h 4 | 8RS a | Stražilovo, RS | msy (f) | 54/86 | 1965 | Tooth |
OL348375 h 6 | OM714893 h 3 | 62RS | Sremski Karlovci, RS | msy (f) | 54/86 | 2021 | Liver |
OL348376 h 6 | OM714894 h 3 | 63RS | Sremski Karlovci, RS | msy (f) | 54/86 | 2021 | Liver |
MK007078 h 15 | OM714869 h 15 | 15RS a | Šuica, BA | mon (g) | 54/84 | 1979 | Tooth |
OM691463 h 15 | OM714874 h 15 | 26RS a | Jakupica, MK | mak (h) | 52/86 | 1972 | Tooth |
OM691464 h 15 | OM714875 h 27 | 27RS a | Ohrid, MK | mak (h) | 52/86 | 1975 | Tooth |
/ | OM714879 h 10 | 35RS a | Strumica, MK | str (k) | 54/88 | 1975 | Tooth |
/ | OM714890 h 10 | 52RS a | Strumica, MK | str (k) | 54/88 | 1975 | Tooth |
OM691475 h 15 | OM714891 h 10 | 53RS a | Strumica, MK | str (k) | 54/88 | 1975 | Tooth |
OM691460 h 14 | OM714868 h 11 | 14RS a | Lefkothea, GR | epi (m) | 56/84 | 1975 | Tooth |
/ | OM714876 h 11 | 28RS a | Lefkothea, GR | epi (m) | 56/84 | 1975 | Tooth |
OM691465 h 14 | OM714877 h 11 | 29RS a | Lefkothea, GR | epi (m) | 56/84 | 1975 | Tooth |
OM691473 h 14 | OM714889 h 11 | 47RS a | Lefkothea, GR | epi (m) | 56/84 | 1975 | Tooth |
OM691477 h 18 | / | 59RS a | Lefkothea, GR | epi (m) | 56/84 | 1975 | Tooth |
OM691461 h 13 | OM714870 h 8 | 18RS a | Novo Selo, BG | thr (n) | 56/76–78 | 1976 | Tooth |
OM691466 h 19 | OM714878 h 13 | 30RS a | Levadia, GR | hel (o) | 58/88 | 1975 | Tooth |
OM691472 h 20 | OM714888 h 14 | 45RS a | Levadia, GR | hel (o) | 58/88 | 1975 | Tooth |
MH979028 h 12 | OM714861 h 6 | 3RS | Ristovac, RS | ser (p) | 54/98 | 2014 | Muscle |
MH979035 h 12 | OM714871 h 6 | 22RS | Klinovac, RS | ser (p) | 54/98 | 2018 | Muscle |
OM691468 h 12 | OM714882 h 6 | 39RS | Ristovac, RS | ser (p) | 54/98 | 2019 | Muscle |
OM691474 h 21 | / | 50RS a | Štip, MK | ovc (q) | 54/94 | 1986 | Tooth |
OM691467 h 22 | OM714880 h 8 | 37RS a | Çorlu, TR | tur (r) | 56/76–78 | 1976 | Tooth |
OM691476 h 17 | OM714892 h 12 | 56RS a | Popova Šapka, MK | unk (u) | 56/82 | 1972 | Tooth |
hun | syr | msy | mse | ser | her | mak | mon | unk | epi | str | hel | ovc | thr | tur | tra | sre | |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
hun | 0.006 | 0.009 | 0.009 | 0.007 | 0.006 | 0.007 | 0.009 | 0.006 | 0.007 | 0.007 | 0.006 | 0.009 | 0.011 | 0.012 | 0.004 | 0.008 | |
syr | 0.027 | 0.009 | 0.008 | 0.005 | 0.006 | 0.005 | 0.006 | 0.005 | 0.005 | 0.004 | 0.004 | 0.002 | 0.009 | 0.010 | 0.006 | 0.005 | |
msy | 0.045 | 0.040 | 0.006 | 0.010 | 0.010 | 0.010 | 0.012 | 0.008 | 0.009 | 0.009 | 0.009 | 0.012 | 0.010 | 0.011 | 0.009 | 0.009 | |
mse | 0.040 | 0.033 | 0.023 | 0.009 | 0.009 | 0.009 | 0.011 | 0.008 | 0.009 | 0.009 | 0.008 | 0.010 | 0.009 | 0.010 | 0.009 | 0.008 | |
ser | 0.025 | 0.014 | 0.044 | 0.039 | 0.007 | 0.003 | 0.005 | 0.005 | 0.006 | 0.003 | 0.004 | 0.004 | 0.010 | 0.010 | 0.006 | 0.006 | |
her | 0.022 | 0.023 | 0.044 | 0.037 | 0.027 | 0.008 | 0.010 | 0.006 | 0.007 | 0.007 | 0.006 | 0.009 | 0.011 | 0.012 | 0.006 | 0.006 | |
mak | 0.030 | 0.016 | 0.046 | 0.041 | 0.005 | 0.029 | 0.003 | 0.005 | 0.006 | 0.004 | 0.004 | 0.005 | 0.010 | 0.010 | 0.007 | 0.006 | |
mon | 0.038 | 0.020 | 0.059 | 0.048 | 0.010 | 0.038 | 0.004 | 0.007 | 0.008 | 0.005 | 0.006 | 0.005 | 0.009 | 0.012 | 0.009 | 0.008 | |
unk | 0.025 | 0.014 | 0.036 | 0.028 | 0.014 | 0.021 | 0.016 | 0.023 | 0.005 | 0.005 | 0.005 | 0.005 | 0.010 | 0.011 | 0.006 | 0.005 | |
epi | 0.029 | 0.015 | 0.041 | 0.038 | 0.020 | 0.025 | 0.021 | 0.027 | 0.014 | 0.006 | 0.005 | 0.006 | 0.010 | 0.011 | 0.007 | 0.006 | |
str | 0.026 | 0.012 | 0.038 | 0.037 | 0.005 | 0.025 | 0.007 | 0.012 | 0.012 | 0.018 | 0.004 | 0.003 | 0.010 | 0.011 | 0.007 | 0.006 | |
hel | 0.029 | 0.018 | 0.044 | 0.039 | 0.017 | 0.026 | 0.017 | 0.024 | 0.020 | 0.020 | 0.015 | 0.004 | 0.009 | 0.010 | 0.006 | 0.005 | |
ovc | 0.032 | 0.003 | 0.050 | 0.038 | 0.007 | 0.027 | 0.010 | 0.010 | 0.009 | 0.015 | 0.005 | 0.016 | 0.010 | 0.010 | 0.008 | 0.007 | |
thr | 0.051 | 0.035 | 0.043 | 0.037 | 0.038 | 0.046 | 0.041 | 0.038 | 0.043 | 0.043 | 0.041 | 0.043 | 0.035 | 0.008 | 0.010 | 0.010 | |
tur | 0.065 | 0.052 | 0.056 | 0.050 | 0.052 | 0.064 | 0.050 | 0.054 | 0.056 | 0.057 | 0.054 | 0.055 | 0.037 | 0.031 | 0.011 | 0.010 | |
tra | 0.012 | 0.021 | 0.042 | 0.037 | 0.022 | 0.016 | 0.023 | 0.032 | 0.020 | 0.023 | 0.023 | 0.026 | 0.024 | 0.043 | 0.058 | 0.007 | |
sre | 0.032 | 0.016 | 0.036 | 0.029 | 0.020 | 0.020 | 0.021 | 0.029 | 0.016 | 0.021 | 0.018 | 0.021 | 0.017 | 0.039 | 0.050 | 0.025 |
N. l | N. x | N. e | S. g | S. m | S. a | R. s | |
---|---|---|---|---|---|---|---|
N. leucodon | 0.009 | 0.013 | 0.016 | 0.016 | 0.017 | 0.022 | |
N. xanthodon | 0.066 | 0.012 | 0.016 | 0.015 | 0.016 | 0.021 | |
N. ehrenbergi | 0.087 | 0.081 | 0.014 | 0.015 | 0.014 | 0.020 | |
S. graecus | 0.107 | 0.113 | 0.087 | 0.009 | 0.010 | 0.023 | |
S. microphthalmus | 0.110 | 0.112 | 0.099 | 0.041 | 0.010 | 0.022 | |
S. arenarius | 0.115 | 0.118 | 0.094 | 0.045 | 0.045 | 0.022 | |
R. sinensis | 0.173 | 0.172 | 0.153 | 0.172 | 0.164 | 0.167 |
mse | mak | tur | tra | hel | syr | her | msy | epi | unk | ser | hun | mon | str | leu | |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
mse | 0.015 | 0.015 | 0.014 | 0.017 | 0.016 | 0.014 | 0.013 | 0.018 | 0.017 | 0.015 | 0.013 | 0.013 | 0.018 | 0.015 | |
mak | 0.099 | 0.010 | 0.007 | 0.006 | 0.009 | 0.006 | 0.014 | 0.008 | 0.008 | 0.005 | 0.006 | 0.004 | 0.007 | 0.008 | |
tur | 0.090 | 0.050 | 0.011 | 0.011 | 0.013 | 0.011 | 0.016 | 0.011 | 0.013 | 0.010 | 0.011 | 0.010 | 0.013 | 0.012 | |
tra | 0.102 | 0.043 | 0.063 | 0.008 | 0.010 | 0.007 | 0.015 | 0.009 | 0.011 | 0.008 | 0.006 | 0.008 | 0.009 | 0.009 | |
hel | 0.100 | 0.027 | 0.052 | 0.035 | 0.011 | 0.007 | 0.018 | 0.007 | 0.008 | 0.006 | 0.009 | 0.007 | 0.009 | 0.010 | |
syr | 0.104 | 0.042 | 0.072 | 0.062 | 0.050 | 0.010 | 0.017 | 0.013 | 0.013 | 0.008 | 0.010 | 0.008 | 0.011 | 0.011 | |
her | 0.088 | 0.031 | 0.062 | 0.037 | 0.033 | 0.052 | 0.016 | 0.009 | 0.008 | 0.006 | 0.006 | 0.005 | 0.009 | 0.008 | |
msy | 0.071 | 0.093 | 0.094 | 0.103 | 0.100 | 0.108 | 0.102 | 0.018 | 0.018 | 0.016 | 0.014 | 0.014 | 0.019 | 0.017 | |
epi | 0.102 | 0.028 | 0.049 | 0.031 | 0.025 | 0.055 | 0.033 | 0.092 | 0.009 | 0.009 | 0.010 | 0.008 | 0.011 | 0.012 | |
unk | 0.080 | 0.020 | 0.051 | 0.035 | 0.030 | 0.048 | 0.027 | 0.081 | 0.024 | 0.009 | 0.010 | 0.007 | 0.011 | 0.012 | |
ser | 0.097 | 0.022 | 0.050 | 0.044 | 0.024 | 0.038 | 0.033 | 0.099 | 0.031 | 0.025 | 0.007 | 0.005 | 0.006 | 0.007 | |
hun | 0.093 | 0.033 | 0.062 | 0.029 | 0.040 | 0.053 | 0.032 | 0.092 | 0.038 | 0.033 | 0.038 | 0.006 | 0.010 | 0.008 | |
mon | 0.091 | 0.017 | 0.049 | 0.041 | 0.026 | 0.041 | 0.026 | 0.097 | 0.027 | 0.018 | 0.019 | 0.029 | 0.008 | 0.007 | |
str | 0.108 | 0.029 | 0.063 | 0.045 | 0.036 | 0.053 | 0.040 | 0.111 | 0.045 | 0.033 | 0.018 | 0.047 | 0.028 | 0.009 | |
leu | 0.108 | 0.043 | 0.071 | 0.056 | 0.046 | 0.061 | 0.044 | 0.118 | 0.046 | 0.043 | 0.037 | 0.049 | 0.037 | 0.041 |
N. e | N. l | S. z | N. x | S. a | R. s | S. ar | S. m | S. g | |
---|---|---|---|---|---|---|---|---|---|
N. ehrenbergi | 0.012 | 0.017 | 0.015 | 0.016 | 0.021 | 0.017 | 0.018 | 0.017 | |
N. leucodon | 0.129 | 0.017 | 0.012 | 0.018 | 0.023 | 0.018 | 0.018 | 0.018 | |
S. zemni | 0.201 | 0.194 | 0.021 | 0.014 | 0.022 | 0.009 | 0.012 | 0.013 | |
N. xanthodon | 0.123 | 0.100 | 0.188 | 0.022 | 0.029 | 0.022 | 0.022 | 0.021 | |
S. antiqus | 0.187 | 0.199 | 0.120 | 0.196 | 0.022 | 0.013 | 0.014 | 0.010 | |
R. synensis | 0.266 | 0.287 | 0.286 | 0.292 | 0.274 | 0.022 | 0.023 | 0.022 | |
S. arenarius | 0.200 | 0.205 | 0.055 | 0.193 | 0.110 | 0.282 | 0.011 | 0.012 | |
S. microphthalmus | 0.218 | 0.211 | 0.101 | 0.192 | 0.131 | 0.306 | 0.084 | 0.014 | |
S. graecus | 0.196 | 0.205 | 0.112 | 0.185 | 0.067 | 0.290 | 0.094 | 0.126 |
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Bugarski-Stanojević, V.; Stamenković, G.; Jojić, V.; Ćosić, N.; Ćirović, D.; Stojković, O.; Veličković, J.; Savić, I. Cryptic Diversity of the European Blind Mole Rat Nannospalax leucodon Species Complex: Implications for Conservation. Animals 2022, 12, 1097. https://doi.org/10.3390/ani12091097
Bugarski-Stanojević V, Stamenković G, Jojić V, Ćosić N, Ćirović D, Stojković O, Veličković J, Savić I. Cryptic Diversity of the European Blind Mole Rat Nannospalax leucodon Species Complex: Implications for Conservation. Animals. 2022; 12(9):1097. https://doi.org/10.3390/ani12091097
Chicago/Turabian StyleBugarski-Stanojević, Vanja, Gorana Stamenković, Vida Jojić, Nada Ćosić, Duško Ćirović, Oliver Stojković, Jelena Veličković, and Ivo Savić. 2022. "Cryptic Diversity of the European Blind Mole Rat Nannospalax leucodon Species Complex: Implications for Conservation" Animals 12, no. 9: 1097. https://doi.org/10.3390/ani12091097
APA StyleBugarski-Stanojević, V., Stamenković, G., Jojić, V., Ćosić, N., Ćirović, D., Stojković, O., Veličković, J., & Savić, I. (2022). Cryptic Diversity of the European Blind Mole Rat Nannospalax leucodon Species Complex: Implications for Conservation. Animals, 12(9), 1097. https://doi.org/10.3390/ani12091097