Abstract
The responses of anurans to paleogeology, climate variability and anthropogenic factors play a crucial role in understanding their diversity and population dynamics. Despite substantial phylogeographic studies existing for northeast Asia, a region-wide synthesis linking divergence timing with major evolutionary drivers is lacking. To address this gap, we synthesised published divergence-time estimates for northeast Asian anurans from 1998 to present, and linked basal, stem and crown ages to their associated drivers and regional contexts. We integrated the data with time-calibrated genomic species trees, diversification analyses, and three key trait data (body size, elevation and latitude range) to assess temporal patterns of lineage divergence and compare diversification dynamics among the major anuran families in northeast Asia. Our synthesis identifies four recurrent evolutionary drivers: (1) paleogeology and landscape barriers, (2) climate fluctuations and latitudinal gradients, (3) glaciations and past sea-level change, and (4) anthropogenic influences. Across families, we highlight unresolved species boundaries, detect the genetic imprint of human-mediated disturbance, synthesise phenotypic, ecological, and macroevolutionary patterns using openly available datasets, and identify cases where multiple drivers interact within species complexes. Bayesian Analysis of Macroevolutionary Mixtures (BAMM) trait reconstructions showed that across all three traits, Ranidae had the highest trait values through time, indicating broader ecological breadth and greater macroevolutionary expansion than Bufonidae and Microhylidae. Our synthesis integrates divergence timing, trait evolution, and environmental drivers, providing a general framework for understanding biodiversity responses to long-term environmental change.
This is a preview of subscription content, access via your institution
Access options
Access through your institution
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to the full article PDF.
USD 39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Impacts of an industrial deep-sea mining trial on macrofaunal biodiversity
Molecular phylogeny and species delimitation unravel climate-driven diversification and cryptic radiation in Iranian steppe Vipers (Vipera ursinii-renardi complex)
Mitochondrial genomes reveal mid-Pleistocene population divergence, and post-glacial expansion, in Australasian snapper (Chrysophrys auratus)
Data availability
All sequences used in this study were obtained from publicly available databases, including GenBank and the NCBI Sequence Read Archive (NCBI, https://www.ncbi.nlm.nih.gov/genbank), with accession details provided in Table S4. The methodology and supporting data for integrative dating information are available in the electronic supplementary material. Nexus alignments, BEAST input files (.xml), BAMM input files, and the R script used for speciation-extinction and macroevolutionary trait analyses can be accessed through the Mendeley Data (URL: https://data.mendeley.com/datasets/nbkhzc84df/1).
References
Andersen D, Jang Y, Borzée A (2023) Influence of landscape and connectivity on anuran conservation: population viability analyses to designate protected areas. Anim Conserv 26:381–397.
Google Scholar
Anderson SAS, Weir JT (2022) The role of divergent ecological adaptation during allopatric speciation in vertebrates. Science 378:1214–1218.
Google Scholar
Arrighi JM, Lencer ES, Jukar A, Park D, Phillips PC, Kaplan RH (2013) Daily temperature fluctuations unpredictably influence developmental rate and morphology at a critical early larval stage in a frog. BMC Ecol 13:18.
Google Scholar
Bae Y, Park J, Othman SN, Jang Y, Borzée A (2022) Record of invasive Rana huanrenensis Fei, Ye, and Huang, 1990 and Pelophylax nigromaculatus (Hallowell, 1861) on Ulleung Island, Republic of Korea. BioInvasions Rec 11:278–286.
Google Scholar
Birand A, Vose A, Gavrilets S (2012) Patterns of species ranges, speciation, and extinction. Am Nat 179:000–000.
Google Scholar
Van Bocxlaer I, Roelants K, Biju SD, Nagaraju J, Bossuyt F (2006) Late cretaceous vicariance in Gondwanan amphibians. PLoS One 1:e74.
Google Scholar
Van Bocxlaer I, Loader SP, Roelants K, Biju SD, Menegon M, Bossuyt F (2010) Gradual adaptation toward a range-expansion phenotype initiated the global radiation of toads. Science 327:679–682.
Google Scholar
Borzée A, Kwon S, Koo KS, Jang Y (2020a) Policy recommendation on the restriction on amphibian trade toward the Republic of Korea. Front Environ Sci 8:129.
Google Scholar
Borzée A, Ahn J, Kim S, Heo K, Jang Y (2015) Seoul, keep your paddies! Implications for the conservation of Hylid species. Anim Syst Evol Divers 31:176–181.
Google Scholar
Borzée A, Santos JL, Sánchez-RamÍrez S, Bae Y, Heo K, Jang Y et al. (2017) Phylogeographic and population insights of the Asian common toad (Bufo gargarizans) in Korea and China: population isolation and expansions as response to the ice ages. PeerJ 5:e4044.
Google Scholar
Borzée A, McNeely J, Magellan K, Miller JRB, Porter L, Dutta T et al. (2020b) COVID-19 highlights the need for more effective wildlife trade legislation. Trends Ecol Evol 35:5–8.
Google Scholar
Borzée, Messenger A, Chae KR, Andersen S, Groffen D, Kim YI J et al. (2020c) Yellow sea mediated segregation between North East Asian Dryophytes species. PLoS One 15:e0234299.
Google Scholar
Borzée A, Shin Y, Poyarkov NA, Jeon JY, Baek HJ, Lee CH et al. (2022) Dwindling in the mountains: Description of a critically endangered and microendemic Onychodactylus species (Amphibia, Hynobiidae) from the Korean Peninsula. Zool Res 43:750–755.
Google Scholar
Borzée A, Shin Y, Bae Y, Jeong D, Amin H, Min MS et al. (2024) From Korean to northeast Asian endemicity: on the occurrence of Pelophylax chosenicus along the Eastern Coastal Yellow Sea. Front Biogeogr 16:e62301.
Google Scholar
Borzée, Jang A, Othman Y, Groffen SN, Maslova J, I V, Purevdorj Z et al. (2025) Integrating phylogeographic and phenotypic evidence to delimit deep evolutionary lineages in the Dryophytes japonicus species complex, with an assessment of their conservation needs. Herpetozoa 42:25–42.
Google Scholar
Borzée A (2024) Continental Northeast Asian amphibians: Origins, behavioural ecology, and conservation, 1st edn. Academic Press Elsevier.
Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A et al. (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 15:e1006650.
Google Scholar
Brigham-Grette J, Melles M, Minyuk P, Andreev A, Tarasov P, DeConto R et al. (2013) Pliocene warmth, polar amplification, and stepped Pleistocene cooling recorded in NE Arctic Russia. Science 340:1421–1427.
Google Scholar
Byun J, Paik K (2021) The development process of the Korean coastal mountain range: Examination from spatial distribution of knickzones. Prog Phys Geogr 45:541–563.
Google Scholar
Caves JK, Sjostrom DJ, Mix HT, Winnick MJ, Chamberlain CP (2014) Aridification of Central Asia and uplift of the Altai and Hangay mountains, Mongolia: Stable isotope evidence. Am J Sci 314:1171–1201.
Google Scholar
Che J, Zhou WW, Hu JS, Yan F, Papenfuss TJ, Wake DB et al. (2010) Spiny frogs (Paini) illuminate the history of the Himalayan region and Southeast Asia. Proc Natl Acad Sci USA 107:13765–13770.
Google Scholar
Chen W, Lu X (2011) Age and body size of Rana amurensis from northeastern China. Curr Zool 57:781–784.
Google Scholar
Chen W, Qian W, Miao K, Qian R, Yuan S, Liu W et al. (2022) Comparative mitogenomics of true frogs (Ranidae, Anura), and its implications for the phylogeny and evolutionary history of Rana. Animals 12:1250.
Google Scholar
Chen Z, Li H, Zhu Y, Feng Q, He Y, Chen X (2017) Molecular phylogeny of the family Dicroglossidae (Amphibia: Anura) inferred from complete mitochondrial genomes. Biochem Syst Ecol 71:1–9.
Google Scholar
Daru BH, Farooq H, Antonelli A, Faurby S (2020) Endemism patterns are scale dependent. Nat Commun 11:2115.
Google Scholar
Do MS, Son SJ, Choi G, Yoo N, Nam HK (2022) Comparison of breeding area characteristics between two frog species breeding at rice fields of the Midwest region of South Korea. J Asia-Pac Biodivers 15:165–171.
Google Scholar
Dong B, Che J, Ding L, Huang S, Murphy RW, Zhao E et al. (2012) Testing hypotheses of Pleistocene population history using coalescent simulations: Refugial isolation and secondary contact in Pseudepidalea raddei (Amphibia: Bufonidae). Asian Herpetol Res 3:103–113.
Google Scholar
Dufresnes C, Berroneau M, Dubey S, Litvinchuk SN, Perrin N (2020) The effect of phylogeographic history on species boundaries: a comparative framework in Hyla tree frogs. Sci Rep 10:5502.
Google Scholar
Dufresnes C, Litvinchuk SN, Borzée A, Jang Y, Li JT, Miura I et al. (2016) Phylogeography reveals an ancient cryptic radiation in East-Asian tree frogs (Hyla japonica group) and complex relationships between continental and island lineages. BMC Evol Biol 16:253.
Google Scholar
Dufresnes C, Jablonski D, Ambu J, Prasad VK, Gautam KB, Kamei RG (2025) Speciation and historical invasions of the Asian black-spined toad (Duttaphrynus melanostictus). Nat Commun 16:298.
Google Scholar
Farnsworth A, Lunt DJ, Robinson SA, Valdes PJ, Roberts WHG, Clift PD et al. (2019) Past East Asian monsoon evolution controlled by paleogeography, not CO₂. Sci Adv 5: eaax1697.
Google Scholar
Feng YJ, Blackburn DC, Liang D, Hillis DM, Wake DB, Cannatella DC et al. (2017) Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous–Paleogene boundary. Proc Natl Acad Sci USA 114:E5864–E5870.
Google Scholar
Fierst JL (2011) A history of phenotypic plasticity accelerates adaptation to a new environment. J Evol Biol 24:1992–2001.
Google Scholar
Fitch WM, Ayala FJ (1994) Tempo and mode in evolution. Proc Natl Acad Sci USA 91:6717–6720.
Google Scholar
Flanders Marine Institute (2018) IHO Sea Areas. marineregions.org.
Fong JJ, Yang BT, Li PP, Waldman B, Min MS (2020) Phylogenetic systematics of the Water Toad (Bufo stejnegeri) elucidates the evolution of semi-aquatic toad ecology and Pleistocene glacial refugia. Front Ecol Evol 7:523.
Google Scholar
Fong JJ, Li PP, Yang BT, Zhou ZY, Leaché AD, Min MS et al. (2016) Influence of geology and human activity on the genetic structure and demography of the Oriental fire-bellied toad (Bombina orientalis). Mol Phylogenet Evol 97:69–75.
Google Scholar
Fu J, Wen L (2023) Impacts of Quaternary glaciation, geological history and geography on animal species history in continental East Asia: A phylogeographic review. Mol Ecol 32:4497–4514.
Google Scholar
Fu J, Weadick CJ, Zeng X, Wang Y, Liu Z, Zheng Y et al. (2005) Phylogeographic analysis of the Bufo gargarizans species complex: A revisit. Mol Phylogenet Evol 37:202–213.
Google Scholar
Fu M, Waldman B (2022) Novel chytrid pathogen variants and the global amphibian pet trade. Conserv Biol 36:e13938.
Google Scholar
Fu X, Zhu W, Geng J, Yang S, Zhong K, Huang X et al. (2021) The present-day Yangtze River was established in the late Miocene: Evidence from detrital zircon ages. J Asian Earth Sci 205:104600.
Google Scholar
Fukutani K, Matsui M, Van TranD, Nishikawa K (2022) Genetic diversity and demography of Bufo japonicus and B. torrenticola (Amphibia: Anura: Bufonidae) influenced by the Quaternary climate. PeerJ 10:e13452.
Google Scholar
Garcia-Porta J, Litvinchuk SN, Crochet PA, Romano A, Geniez PH, Lo-Valvo M et al. (2012) Molecular phylogenetics and historical biogeography of the west-palearctic common toads (Bufo bufo species complex). Mol Phylogenet Evol 63:113–130.
Google Scholar
Garg S, Biju SD (2019) New microhylid frog genus from Peninsular India with Southeast Asian affinity suggests multiple Cenozoic biotic exchanges between India and Eurasia. Sci Rep 9:1906.
Google Scholar
Gorin VA, Scherz MD, Korost DV, Poyarkov NA (2021) Consequences of parallel miniaturisation in Microhylinae (Anura, Microhylidae), with the description of a new genus of diminutive South East Asian frogs. Zoosyst Evol 97:21–54.
Google Scholar
Groffen J, Kong S, Jang Y, Borzée A (2019) The invasive American bullfrog (Lithobates catesbeianus) in the Republic of Korea: History and recommendations for population control. Manag Biol Invasions 10:517–535.
Google Scholar
Guo ZT, Ruddiman WF, Hao QZ, Wu HB, Qiao YS, Zhu RX et al. (2002) Onset of Asian desertification by 22Myr ago inferred from loess deposits in China. Nature 416:159–163.
Google Scholar
Harrison TM, Copeland P, Kidd WSF, Yin A (1992) Raising Tibet. Science 255:1663–1670.
Google Scholar
Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913.
Google Scholar
Hui Z, Zhou X, Chevalier M, Wei X, Pan Y, Chen Y (2021) Miocene East Asia summer monsoon precipitation variability and its possible driving forces. Palaeogeogr Palaeoclimatol Palaeoecol 581:110609.
Google Scholar
Igawa T, Kurabayashi A, Usuki C, Fujii T, Sumida M (2008) Complete mitochondrial genomes of three neobatrachian anurans: A case study of divergence time estimation using different data and calibration settings. Gene 407:116–129.
Google Scholar
IUCN (2024) The IUCN Red List of Threatened Species. Version 2024-1.
Jang Y, Hahm EH, Lee HJ, Park S, Won YJ, Choe JC (2011) Geographic variation in advertisement calls in a tree frog species: Gene flow and selection hypotheses. PLoS One 6:e23297.
Google Scholar
Jeon JY, Cho S, Suk HY, Lee CH, Borzée A, Song J et al. (2021) Resolving the taxonomic equivocacy and the population genetic structure of Rana uenoi – insights into dispersal and demographic history. Salamandra 4:529–540.
Jetz W, Pyron RA (2018) The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat Ecol Evol 2:850–858.
Google Scholar
Jin L, Yang SN, Liao WB, Lüpold S (2016) Altitude underlies variation in the mating system, somatic condition, and investment in reproductive traits in male Asian grass frogs (Fejervarya limnocharis). Behav Ecol Sociobiol 70:1197–1208.
Google Scholar
Jung JH, Choi S, Suh JH, Do MS (2024) Spatial distributional prediction of Korean Brown Frogs (Rana uenoi, R. huanrenensis and R. coreana) according to climate change. Curr Herpetol 43:135–147.
Google Scholar
Kamath PL, Sepulveda AJ, Layhee M (2016) Genetic reconstruction of a bullfrog invasion to elucidate vectors of introduction and secondary spread. Ecol Evol 6:5221–5233.
Google Scholar
Kasatani M, Takeuchi H (2023) Phylogeography of the Miyako Toad, Bufo gargarizans miyakonis (Anura: Bufonidae), inferred from mitochondrial sequence data. Curr Herpetol 42:144–161.
Google Scholar
Kim DE, Seong YB, Weber J, Yu BY (2020) Unsteady migration of Taebaek Mountain drainage divide, Cenozoic extensional basin margin, Korean Peninsula. Geomorphology 352:107012.
Google Scholar
Kim GU, Oh H, Kim YS, Son JH, Jeong JY (2023) Causes for an extreme cold condition over Northeast Asia during April 2020. Sci Rep 13:3315.
Google Scholar
Kim DY (2021) Phylogeography and taxonomic status of Korean Glandirana emeljanovi (Anura: Ranidae). Seoul National University.
Kim HW, Adhikari P, Chang MH, Seo C (2021). Potential distribution of amphibians with different habitat characteristics in response to climate change in South Korea. Animals 11.
Kishida O, Mizuta Y, Nishimura K (2006) Reciprocal phenotypic plasticity in a predator-prey. Ecology 87:1599–1604.
Google Scholar
Ko MH, Kwan YS, Lee WK, Won YJ (2017) Impact of human activities on changes of ichthyofauna in Dongjin River of Korea in the past 30 years. Anim Cells Syst (Seoul) 21:207–216.
Google Scholar
Komaki S, Igawa T, Lin S, Tojo K, Min M, Sumida M (2015) Robust molecular phylogeny and palaeodistribution modelling resolve a complex evolutionary history: glacial cycling drove recurrent mtDNA introgression among Pelophylax frogs in East Asia. J Biogeogr 42:2159–2171.
Google Scholar
Komine H, Watari Y, Kaji K (2019) Ecological character displacement in non-congeneric frogs. Zool Sci 36:410–416.
Google Scholar
Kurabayashi A, Matsui M, Belabut DM, Yong H Sen, Ahmad N, Sudin A et al. (2011) From Antarctica or Asia? New colonization scenario for Australian-New Guinean narrow mouth toads suggested from the findings on a mysterious genus Gastrophrynoides. BMC Evol Biol 11:175.
Google Scholar
Lee C, Fong JJ, Jiang J-P, Li P-P, Waldman B, Chong JR et al. (2021) Phylogeographic study of the Bufo gargarizans species complex, with emphasis on Northeast Asia. Anim Cells Syst (Seoul) 25:434–444.
Google Scholar
Lee JE, Yang DE, Kim YR, Lee H, Lee HI, Yang S et al. (1999) Genetic relationships of Rana amurensis based on mitochondrial Cytochrome b gene sequences. Korean J Biol Sci 3:303–309.
Google Scholar
Lee KH, Shaner PJL, Lin YP, Lin SM (2016) Geographic variation in advertisement calls of a Microhylid frog – testing the role of drift and ecology. Ecol Evol 6:3289–3298.
Google Scholar
Leung KW, Yang S, Wang X, Tang K, Hu J (2021) Ecogeographical adaptation revisited: Morphological variations in the plateau brown frog along an elevation gradient on the Qinghai–Tibetan Plateau. Biology 10:1081.
Google Scholar
Li D, Jiang X, Gong W, Li C (2022) Tectonic uplift along the northeastern margin of the Qinghai–Tibetan Plateau: Constraints from the lithofacies sequence and deposition rate of the Qaidam Basin. Tectonophysics 827:229279.
Google Scholar
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760.
Google Scholar
Li JT, Wang JS, Nian HH, Litvinchuk SN, Wang J, Li Y et al. (2015) Amphibians crossing the Bering Land Bridge: Evidence from holarctic treefrogs (Hyla, Hylidae, Anura). Mol Phylogenet Evol 87:80–90.
Google Scholar
Li Z, Yu G, Rao D, Yang J (2012) Phylogeography and demographic history of Babina pleuraden (Anura, Ranidae) in Southwestern China. PLoS One 7:e34013.
Google Scholar
Liu K, Wang F, Chen W, Tu L, Min MS, Bi K et al. (2010b) Rampant historical mitochondrial genome introgression between two species of green pond frogs, Pelophylax nigromaculatus and P. plancyi. BMC Evol Biol 10:201.
Google Scholar
Liu K, Wang F, Chen W, Tu L, Min M-S, Bi K et al. (2010c) Rampant historical mitochondrial genome introgression between two species of green pond frogs, Pelophylax nigromaculatus and P. plancyi. BMC Evol Biol 10:201.
Google Scholar
Liu L, Field J, Fullagar R, Bestel S, Chen X, Ma X (2010a) What did grinding stones grind? New light on Early Neolithic subsistence economy in the Middle Yellow River Valley, China. Antiquity 84:816–833.
Google Scholar
Liu X, Guo Q, Guo Z, Yin ZY, Dong B, Smith R (2015) Where were the monsoon regions and arid zones in Asia prior to the Tibetan Plateau uplift? Natl Sci Rev 2:403–416.
Google Scholar
Luo T, Zhao ZF, Wang ZL, Lan CT, Xiao MY, Deng HQ et al. (2025) Diversification outbreaks and dynamics of Asian leaf-litter frogs, genus Leptobrachella (Anura, Megophryidae), with the description of a new species from Guizhou Province, China. Zoosyst Evol 101:223–243.
Google Scholar
Ma XC, Ding HQ, Shi JD, Hei L, Niu NK, Suo ZG et al. (2018) Cinobufacini from the skin of Bufo bufo gargarizans induces apoptosis, possibly via activation of the wnt/β-catenin pathway, in human osteosarcoma cells. Nat Prod Commun 13:201–204.
Macey JR, Schulte JA, Larson A, Fang Z, Wang Y, Tuniyev BS et al. (1998) Phylogenetic relationships of toads in the Bufo bufo species group from the eastern escarpment of the Tibetan Plateau: a case of vicariance and dispersal. Mol Phylogenet Evol 9:80–87.
Google Scholar
Malakhov DV (2004) Toads (Anura, Bufonidae) from the middle miocene in the Turgay depression (Central Kazakhstan). Biota 5:41–46.
Matsui M (2014) Description of a New Brown Frog from Tsushima Island, Japan (Anura: Ranidae: Rana). Zool Sci 31:613–620.
Google Scholar
Matsui M, Kawahara Y, Nishikawa K, Ikeda S, Eto K, Mizuno Y (2019) Molecular phylogeny and evolution of two Rhacophorus species endemic to mainland Japan. Asian Herpetol Res 10:86–104.
Matthews KJ, Maloney KT, Zahirovic S, Williams SE, Seton M, Müller RD (2016) Global plate boundary evolution and kinematics since the late Paleozoic. Glob Planet Change 146:226–250.
Google Scholar
McPeek MA, Brown JM (2007) Clade age and not diversification rate explains species richness among animal taxa. Am Nat 169:E97–E105.
Google Scholar
Mei X, Li R, Zhang X, Liu Q, Liu J, Wang Z et al. (2016) Evolution of the Yellow Sea Warm Current and the Yellow Sea Cold Water Mass since the Middle Pleistocene. Palaeogeogr Palaeoclimatol Palaeoecol 442:48–60.
Google Scholar
Mittan CS, Zamudio KR (2019) Rapid adaptation to cold in the invasive cane toad Rhinella marina. Conserv Physiol 7:coy075.
Google Scholar
Moore BR, Höhna S, May MR, Rannala B, Huelsenbeck JP (2016) Critically evaluating the theory and performance of Bayesian analysis of macroevolutionary mixtures. Proc Natl Acad Sci USA 113:9569–9574.
Google Scholar
Mori T, Yanagisawa Y, Kitani Y, Sugiyama M, Kishida O, Nishimura K (2015) Gene expression profiles in Rana pirica tadpoles following exposure to a predation threat. BMC Genomics 16:258.
Google Scholar
Nagai Y, Doi T, Ito K, Yuasa Y, Fujitani T, Naito J, ichi et al. (2018) The distributions and boundary of two distinct, local forms of Japanese pond frog, Pelophylax porosus brevipodus, inferred from sequences of mitochondrial DNA. Front Genet 9:5–10.
Google Scholar
Nomura F, Rossa-Feres DC, Langeani F (2009) Burrowing behavior of Dermatonotus muelleri (Anura, Microhylidae) with reference to the origin of the burrowing behavior of Anura. J Ethol 27:195–201.
Google Scholar
O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R et al. (2016) Reference sequence (RefSeq) database at NCBI: Current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 44:D733–D745.
Google Scholar
Oike A, Mochizuki M, Tojo K, Matsuo T, Nakamura Y, Yasumasu S et al. (2020) A phylogenetically distinct group of Glandirana rugosa found in Kyushu, Japan. Zool Sci 37:193–202.
Google Scholar
Othman SN, Chen Y-H, Chuang M-F, Andersen D, Jang Y, Borzée A (2020) Impact of the Mid-Pleistocene Revolution and anthropogenic factors on the dispersion of Asian Black-spined toads (Duttaphrynus melanostictus). Animals 10:1157.
Google Scholar
Othman SN, Putri ET, Messenger KR, Bae Y, Yang Y, Bova T et al. (2021) Impact of the Miocene orogenesis on Kaloula spp. radiation, and implication of local refugia on genetic diversification. Integr Zool 17:261–284.
Google Scholar
Othman SN, Choe M, Chuang M-F, Purevdorj Z, Maslova I, Schepina NA et al. (2022a) Across the Gobi Desert: impact of landscape features on the biogeography and phylogeographically-structured release calls of the Mongolian Toad, Strauchbufo raddei in East Asia. Evol Ecol 36:1007–1043.
Google Scholar
Othman SN, Litvinchuk SN, Maslova I, Dahn H, Messenger KR, Andersen D et al. (2022b) From Gondwana to the Yellow Sea, evolutionary diversifications of true toads Bufo sp. in the Eastern Palearctic and a revisit of species boundaries for Asian lineages. Elife 11:e70494.
Google Scholar
Othman SN, Shin Y, Kim HT, Chuang MF, Bae Y, Hoti J et al. (2022c) Evaluating the efficiency of popular species identification analytical methods, and integrative workflow using morphometry and barcoding bioinformatics for taxonomy and origin of traded cryptic brown frogs. Glob Ecol Conserv 38:e02253.
Othman SN, Wang Z, Qiu Z, Borzée A (2024). Overtrading of widespread generalist amphibians is a global biodiversity time-bomb. Biodiversity: 208–214.
Park HR, Rahman MM, Park SM, Choi JH, Kang HJ, Sung HC (2022) Risk assessment for the native anurans from an alien invasive species, American bullfrogs (Lithobates catesbeianus), in South Korea. Sci Rep 12:13143.
Google Scholar
Portik DM, Streicher JW, Wiens JJ (2023) Frog phylogeny: A time-calibrated, species-level tree based on hundreds of loci and 5,242 species. Mol Phylogenet Evol 188:107907.
Google Scholar
Pyron RA, Wiens JJ (2013) Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity. Proc R Soc B Biol Sci 280:20131622.
Google Scholar
Qi P, Huang X, Xu YJ, Li F, Wu Y, Chang Z et al. (2021) Divergent trends of water bodies and their driving factors in a high-latitude water tower, Changbai Mountain. J Hydrol 603:127094.
Google Scholar
Qi Y, Felix Z, Wang Y, Gu H, Wang Y (2019) Postbreeding movement and habitat use of the Plateau Brown Frog, Rana kukunoris, in a high-elevation wetland. Soc Study Amphib Reptil Stable 45:421–427.
R Core Team (2024) R: A language and environment for statistical computing. URL https://www.R-project.org/. R Found Stat Comput.
Rabosky DL (2014) Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS One 9:e89543.
Google Scholar
Rabosky DL, Slater GJ, Alfaro ME (2012) Clade age and species richness are decoupled across the Eukaryotic tree of life. PLoS Biol 10:e1001381.
Google Scholar
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904.
Google Scholar
Ratnikov VY (2016) Dynamics of East European modern amphibian and reptile species distribution areas and their potential use in Quaternary stratigraphy. Comptes Rendus Palevol 15:721–730.
Google Scholar
Ray N, Adams JM, Ray N (2001) A GIS-based vegetation map of the world at the Last Glacial Maximum (25,000-15,000 BP). Internet Archaeol 11:1–44.
Rochette NC, Rivera-Colón AG, Catchen JM (2019) Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol Ecol 28:4737–4754.
Google Scholar
San Mauro D, Vences M, Alcobendas M, Zardoya R, Meyer A (2005) Initial diversification of living amphibians predated the breakup of Pangaea. Am Nat 165:590–599.
Google Scholar
Sanchiz B (1997) Factores causales de biodiversidad: especiación, extinción y migración en la formación de la batracofauna europea. In: Aguirre E, Morales J, Soria D (eds) Registros fósiles e historia de la Tierra, Madrid, Ed. Complutense., pp 185–206.
Shen H, Xu M, Yang X, Chen Z, Xiao N, Chen X (2022) A new brown frog of the Genus Rana (Anura, Ranidae) from North China, with a taxonomic revision of the R. chensinensis species group. Asian Herpetol Res 13:145–158.
Shi JJ, Rabosky DL (2015) Speciation dynamics during the global radiation of extant bats. Evolution 69:1528–1545.
Google Scholar
Shi Y (2002) Characteristics of late Quaternary monsoonal glaciation on the Tibetan Plateau and in East Asia. Quat Int 97–98:79–91.
Google Scholar
Shin Y, Min MS, Borzée A (2021) Driven to the edge: Species distribution modeling of a Clawed Salamander (Hynobiidae: Onychodactylus koreanus) predicts range shifts and drastic decrease of suitable habitats in response to climate change. Ecol Evol 11:14669–14688.
Google Scholar
Smith MA, Green DM (2005) Dispersal and the metapopulation paradigm in amphibian ecology and conservation: Are all amphibian populations metapopulations? Ecography 28:110–128.
Google Scholar
Song JY, Matsui M, Chung KH, Oh HS, Zhao W (2006) Distinct specific status of the Korean brown frog, Rana amurensis coreana (Amphibia: Ranidae). Zool Sci 23:219–224.
Google Scholar
Spearman C (1904) The proof and measurement of association between two things. Am J Psychol 15:72–101.
Google Scholar
Spicer RA, Su T, Valdes PJ, Farnsworth A, Wu FX, Shi G et al. (2021) Why ‘the uplift of the Tibetan Plateau’ is a myth. Natl Sci Rev 8:nwaa091.
Google Scholar
Sun X, Tian Y, Kuiper KF, Li C, Zhang Z, Wijbrans JR (2021) No Yangtze River prior to the Late Miocene: evidence from detrital muscovite and K-Feldspar 40Ar/39Ar geochronology. Geophys Res Lett 48:e2020GL089903.
Google Scholar
Sunday JM, Bates AE, Dulvy NK, Sunday JM, Bates AE, Dulvy NK (2011) Global analysis of thermal tolerance and latitude in ectotherms Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc B 278:1823–1830.
Google Scholar
Taira A (2001) Tectonic evolution of the Japanese Island arc system. Annu Rev Earth Planet Sci 29:109–134.
Google Scholar
Uyeda JC, Hansen TF, Arnold SJ, Pienaar J (2011) The million-year wait for macroevolutionary bursts. Proc Natl Acad Sci USA 108:15908–15913.
Google Scholar
Van der Meijden A, Vences M, Hoegg S, Boistel R, Channing A, Meyer A (2007) Nuclear gene phylogeny of narrow-mouthed toads (Family: Microhylidae) and a discussion of competing hypotheses concerning their biogeographical origins. Mol Phylogenet Evol 44:1017–1030.
Google Scholar
Wang GD, Zhang BL, Zhou WW, Li YX, Jin JQ, Shao Y et al. (2018) Selection and environmental adaptation along a path to speciation in the Tibetan frog Nanorana parkeri. Proc Natl Acad Sci USA 115:E5056–E5065.
Google Scholar
Wang J, Fuyuan WU, Zhang J, Khanal G, Yang L (2022) The Himalayan collisional orogeny: a metamorphic perspective. Acta Geol Sin 96:1842–1866.
Google Scholar
Wang Y, Li C, Wei H, Shan X (2003) Late Pliocene-recent tectonic setting for the Tianchi volcanic zone, Changbai Mountains, northeast China. J Asian Earth Sci 21:1159–1170.
Google Scholar
Wei X, Huang M, Yue Q, Ma S, Li B, Mu Z et al. (2021) Long-term urbanization impacts the eastern golden frog (Pelophylax plancyi) in Shanghai City: Demographic history, genetic structure, and implications for amphibian conservation in intensively urbanizing environments. Evol Appl 14:117–135.
Google Scholar
Wiens JJ, Sukumaran J, Pyron RA, Brown RM (2009) Evolutionary and biogeographic origins of high tropical diversity in Old World frogs (Ranidae). Evolution 63:1217–1231.
Google Scholar
Wogan GOU, Stuart BL, Iskandar DT, McGuire JA (2016) Deep genetic structure and ecological divergence in a widespread human commensal toad. Biol Lett 12:20150807.
Google Scholar
Xu M, Wang G, Liu P, He Z, He K, Cheng Z et al. (2024) Age structure and body size of two Tibetan toad (Bufo tibetanus) populations from different elevations in China. Ecol Evol 14:e11559.
Google Scholar
Yan F, Nneji LM, Jin JQ, Yuan ZY, Chen JM, Mi X et al. (2021) Multi-locus genetic analyses of Quasipaa from throughout its distribution. Mol Phylogenet Evol 163:107218.
Google Scholar
Yan P, Pan T, Wu G, Kang X, Ali I, Zhou W et al. (2020) Species delimitation and evolutionary history of tree frogs in the Hyla chinensis group (Hylidae, amphibian). Front Ecol Evol 8:234.
Google Scholar
Yang BT, Zhou Y, Min MS, Matsui M, Dong BJ, Li PP et al. (2017) Diversity and phylogeography of Northeast Asian brown frogs allied to Rana dybowskii (Anura, Ranidae). Mol Phylogenet Evol 112:148–157.
Google Scholar
Yang JX, Zhou WW, Rao DQ, Poyarkov AN, Kuzmin SL, Che J (2010) Validity and systematic position of Rana altaica (Rana: ranidae): results of a phylogenetic analysis. Dongwuxue Yanjiu 31:353–360.
Google Scholar
Yu TL, Guo YS (2010) Overwintering habitat selection of Asiatic toad, Bufo gargarizans in southwestern China. Biharean Biol 4:15–18.
Yu TL, Deng YH (2020) Geographic variation in maternal investment and trade-offs between egg size and clutch size in an endemic toad of the Qinghai-Tibet Plateau. Sci Rep 10:6838.
Google Scholar
Yu TL, Han YT, Zhang SP (2016) Plasticity in metamorphic traits of Rana kukunoris tadpoles: The interactive effects of food level and rearing temperature. Russ J Ecol 47:552–556.
Google Scholar
Yuan ZY, Zhou WW, Chen X, Poyarkov NA, Chen HM, Jang-Liaw NH et al. (2016) Spatiotemporal diversification of the True Frogs (Genus Rana): A historical framework for a widely studied group of model organisms. Syst Biol 65:824–842.
Google Scholar
Zamudio KR, Bell RC, Mason NA (2016) Phenotypes in phylogeography: species’ traits, environmental variation, and vertebrate diversification. Proc Natl Acad Sci USA 113:8041–8048.
Google Scholar
Zhang H, Yan J, Zhang G, Zhou K (2008b) Phylogeography and demographic history of Chinese black-spotted frog populations (Pelophylax nigromaculata): evidence for independent refugia expansion and secondary contact. BMC Evol Biol 8:21.
Google Scholar
Zhang M, Chen X, Ye C, Fei L, Li P, Jiang J et al. (2020) Osteology of the Asian narrow-mouth toad Kaloula borealis (Amphibia, Anura, Microhylidae) with comments on its osteological adaptation to fossorial life. Acta Zool 101:366–383.
Google Scholar
Zhang X, Othman SN, Kohler DB, Wu Z, Wang Z, Borzée A (2024) Combined climate change and dispersal capacity positively affect Hoplobatrachus chinensis occupancy of agricultural wetlands. iScience 27:110732.
Google Scholar
Zhang YH, Zhao YY, Li XY, Li XC (2014) Evolutionary history and population genetic structure of the endemic tree frog Hyla tsinlingensis (Amphibia: Anura: Hylidae) inferred from mitochondrial gene analysis. Mitochondr DNA 27:1348–1357.
Google Scholar
Zhang YJ, Stöck M, Zhang P, Wang XL, Zhou H, Qu LH (2008a) Phylogeography of a widespread terrestrial vertebrate in a barely-studied Palearctic region: Green toads (Bufo viridis subgroup) indicate glacial refugia in Eastern Central Asia. Genetica 134:353–365.
Google Scholar
Zheng H, Powell CM, An Z, Zhou J, Dong G (2000) Pliocene uplift of the northern Tibetan Plateau. Geology 28:715–718.
Google Scholar
Zhigileva ON, Kirina IY (2015) First data on genetic variability of the Siberian Wood Frog Rana amurensis in Western Siberia and its differentiation from the Moor frog Rana arvalis Population. Ecol Genet 13:23.
Google Scholar
Zhou WW, Wen Y, Fu J, Xu YB, Jin JQ, Ding L et al. (2012) Speciation in the Rana chensinensis species complex and its relationship to the uplift of the Qinghai-Tibetan Plateau. Mol Ecol 21:960–973.
Google Scholar
Zhou Y, Wang S, Zhu H, Li P, Yang B, Ma J (2017) Phylogeny and biogeography of South Chinese brown frogs (Ranidae, Anura). PLoS One 12:e0175113.
Google Scholar
Acknowledgements
We thank Professor Yikweon Jang and Professor Yuseob Kim (Ewha Womans University, Republic of Korea) for inspiring the fundamental idea behind this study. We express gratitude to Jiaqi Liu (Nanjing University of Information Science and Technology, China) for assistance with data curation, and Xiaoli Zhang (Nanjing Forestry University, China), for providing the spatial data layers used in the compilation of divergence-dating information and mapping. We thank the reviewers for their constructive comments, which helped improve the manuscript.
Funding
The study was funded by the Research Fund for International Scientists (RFIS) from the National Natural Science Foundation of China (grant number 32350410398), and by Foreign Young Talent under the Ministry of Science and Technology of the People’s Republic of China (grant number QN2023014005L), both awarded to SNO. It was additionally supported by the Research Fund for International Scientists (RFIS) of the National Natural Science Foundation of China (grant number W2432021) awarded to AB.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Research ethics statement
N.A.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Associate editor: Frank Hailer.
Supplementary information
Supplementary information (download DOCX )
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
Reprints and permissions
About this article
Cite this article
Othman, S.N., Borzée, A. From Paleogene to Anthropocene: phylogeography, geographic patterns of traits, and chronology of evolutionary drivers in northeast Asian anurans.
Heredity (2026). https://doi.org/10.1038/s41437-026-00856-3
Received:
Revised:
Accepted:
Published:
Version of record:
DOI: https://doi.org/10.1038/s41437-026-00856-3
Source: Ecology - nature.com
