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-(A) Median-joining haplotype network of Myodes mitochondrial DNA cytochrome b gene (Cytb) sequences. The number of mutations between haplotypes is indicated by dots and numbers. The size of the circles is related to haplotype frequency. The groups enclosed in a shaded area correspond to the haplotype groups listed in Table 1 and Fig. 2. (B) Mismatch distribution of the mitochondrial Cytb sequences. Only clades or subclades that showed significant evidence of expansion are shown. Bars indicate the observed frequencies of mutations between haplotypes and a line denotes the expected frequency under the sudden expansion model.
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The Japanese archipelago is comprised of four main islands-Hokkaido, Honshu, Shikoku, and Kyushu-which contain high mountainous areas that likely allowed for lineage differentiation and population genetic structuring during the climatic changes of the late Pleistocene. Here, we assess the historical background of the evolutionary dynamics of herbiv...
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... the earlier divergence of M. rutilus (Lineage V, e.g., Luo et al. 2004). Lineage V contained a cluster represented by the haplotypes from the Hokkaido mainland (Vc), together with haplotypes from the Russian continent (Va) and Sakhalin (Vb), in accordance with previous work by of genetic diversity within each of the five species in Japan (Fig. 3A). Lineage IIId, representing M. smithii, was found to contain two clusters, IIId-1 and IIId-2 (Fig. ...
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... cluster represented by the haplotypes from the Hokkaido mainland (Vc), together with haplotypes from the Russian continent (Va) and Sakhalin (Vb), in accordance with previous work by of genetic diversity within each of the five species in Japan (Fig. 3A). Lineage IIId, representing M. smithii, was found to contain two clusters, IIId-1 and IIId-2 (Fig. ...
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... cluster of M. rufocanus (Ic-1) from the Hokkaido mainland showed a star-like structure. Similarly, the haplotypes of M. rutilus from Hokkaido tended to show a star-like feature (Vc). Significantly negative values of Tajima's D and Fu's Fs tests were obtained for the four clusters with star-like network patterns (Fig. 3A), including the clusters of M. rufocanus from the Hokkaido mainland (Ic-1, n = 59), M. smithii (IIId-1, n = 33; IIId-2, n = 13) from Honshu, and M. rutilus from Hokkaido (Vc, n = 35; Table 1). Additionally, expansion signals of the four clusters were depicted in mismatch distribution analysis (Fig. 3B); nonsignificant SSD and r-values ...
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... four clusters with star-like network patterns (Fig. 3A), including the clusters of M. rufocanus from the Hokkaido mainland (Ic-1, n = 59), M. smithii (IIId-1, n = 33; IIId-2, n = 13) from Honshu, and M. rutilus from Hokkaido (Vc, n = 35; Table 1). Additionally, expansion signals of the four clusters were depicted in mismatch distribution analysis (Fig. 3B); nonsignificant SSD and r-values suggestive of population expansion were obtained. The τ-values ranged from 4.1 to 6.3 and the elapsed times since expansion (T) covering the last 140,000 years were estimated to be 16,000 and 54,000-59,000 years ago (using the recommended μ-values of 0.11 and 0.047 substitutions/site/My, respectively; ...
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... (e.g., Kawai et al. 2013), here we provide evidence for signals of rapid expansion in four geographic lineages: Ic-1 (M. rufocanus, Hokkaido), IIId-1 (M. smithii, central Honshu), IIId-2 (M. smithii, southwestern Honshu), and Vc (M. rutilus, Hokkaido), revealing the presence of two ranges of the expansion indices, 4.1 and 5.8-6.3 (Table 1; Fig. 3). A similar trend was detected in our previous studies of Cytb (1,140 bp) variation in Japanese wood mice ( Suzuki et al. 2015;Hanazaki et al. 2017), in which τ-values were classified as 2.7-3.9, ~ 5.7, and 8.5 (Fig. 4C). In Japanese large flying squirrels (Petaurista leucogenys), Oshida et al. (2009) identified two regional haplotype ...
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... respectively, have different time frames of rapid expansion (in the early MIS 3 and 1, respectively), as mentioned above. In addition, the other rare species, M. rex, which is a relic species displaced by the later M. rufocanus lineage (Nakata 1995), exhibited substantially less genetic diversity than did the predominant species M. rufocanus (Fig. 3). The consequences of the different responses to environmental changes can be explained in several ways. They may be more influential in rare species, increasing the strength of intraspecies competition and leading to bottlenecks in these species. Alternately, the ice age may have led to the formation of microhabitats on which vole ...
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... The authors discussed that a higher dispersal ability makes them less sensitive to geographical barriers and consequently affects their results. In our study, although several pairs of mammals, such as Craseomys smithii and C. andersoni, were distributed parapatrically (Ohdachi et al., 2015) by paleoclimatic events and geological barriers (Honda et al., 2019) in the HSK region, bats did not show such a distribution pattern. This suggests that Japanese bats are less sensitive to the dispersal limitations of terrestrial geographical barriers. ...
This study investigated the relative influences of environmental, spatial, and historical factors, including the island‐specific history of land connectivity, on bat assemblages in the Japanese Archipelago. We collected bat distribution data from 1408 studies and assigned them to Japan's First Standard Grid (approximately 6400 km ² ). Japanese bat assemblages were analyzed at two scales: the entire Japanese Archipelago comprised 16 islands and exclusively the four main islands. At first, we calculated taxonomic and functional total beta diversity ( β total ) by Jaccard pairwise dissimilarity and then divided this into turnover ( β repl ) and richness‐difference ( β rich ) components. We conducted hierarchical clustering of taxonomic beta diversity to examine the influence of the two representative sea straits, Tsugaru and Tokara, which are considered biogeographical borders. Variation partitioning was conducted to evaluate the relative effects of the three factors on the beta diversity. Clustering revealed that the Tokara Strait bordered the two major clades; however, the Tsugaru Strait did not act as a biogeographical border for bats. In the variation partitioning, shared fraction between spatial and historical factors significantly explained taxonomic and functional β total and taxonomic β repl at the entire archipelago scale, but not at the four main islands scale extending only Tsugaru Strait but not Tokara Strait. Pure environmental factors significantly explained functional β total at both scales and taxonomic β total only at the four main islands scale. These results suggest that spatial and historical factors are more pronounced in biogeographical borders, primarily structuring assemblage composition at the entire archipelago scale, especially in taxonomic dimension. However, current environmental factors primarily shape the assemblage composition of Japanese bats at the main island scale. The difference in results between the two scales highlights that the primary processes governing assemblages of both dimensions depend on the quality of the dispersal barriers between terrestrial and aquatic barriers for bats.
... 53,000 ya) marks another notable substantial environmental change (Batchelor et al., 2019;Doughty et al., 2021;Geibert et al., 2021;Biltekin et al., 2023). Indeed, among the affected species during MIS 3, instances of rapid population expansion events have been indicated, e.g., voles (genus Myodes, Kohli et al., 2015;Honda et al., 2019) and field mice (genus Apodemus, Hanazaki et al., 2017;Kozyra et al., 2021;. In contrast, although the response of populations to terrestrial environmental changes in subtropical regions has received relatively little attention, there is evidence suggesting rapid expansion events in subtropical RrC Lineage II rat populations in Southeast Asia during both the MIS 5e (post PGM period) and early MIS 3 (post MIS 4 period) timeframes (Maung Maung Theint et al., 2021). ...
... A maximum likelihood (ML) tree was constructed with 1000 bootstrap replications using the program MEGA version X (Kumar et al., 2018) with the HKY+ G + I model. This best fit model was determined using Akaike Information Criterion (AIC) implemented in MEGA X. Phylogenetic tree construction and divergence time estimation were done with the Bayesian inference (BI) analysis implemented in BEAST version 1.8.4 (Drummond and Rambaut, 2007), following the procedures described in our previous study (Honda et al., 2019). Our BEAST analysis employed the HKY+ G + I model to focus on estimating divergence times for nodes older than approximately 100,000 ya. ...
... The time-dependent evolutionary rates employed in this study were calibrated using the three historical climate change periods mentioned above, specifically 130,000 ya (post PGM), 53,000 ya (post MIS 4), and 10,000 ya (post LGM) (Suzuki et al., 2015;Hanazaki et al., 2017;Honda et al., 2019;Nakamoto et al., 2021;Suzuki, 2021). For the 1140 bp Cytb data set, τ values of approximately 8, 5, and 3 were obtained, and the corresponding τ values for the 945 bp data set were 6.8, 4.3, and 2.5. ...
... We employed the TN3 + G substitution model selected through model selection, as mentioned above, along with a single evolutionary rate. The evolutionary rate utilized in this study is timedependent and is generally consistent across rodent and mole species (Suzuki et al., 2015;Hanazaki et al., 2017;Honda et al., 2019;Nakamoto et al., 2021;Suzuki, 2021b). In this time-dependent evo-lutionary rate, the recommended rate for estimating older divergence times is 0.028 substitutions/site/million year (myr) for p-distances of cytb sequences. ...
The house shrew (Suncus murinus-S. montanus species complex) colonized regions across southern Asia and the Indian Ocean following human activity. The house shrew is distributed on islands of the Ryukyu Archipelago, the southernmost part of Japan, but the evolutionary history of the shrew on those islands and possible associations between these populations and humans remain unknown. In this study, we conducted phylogenetic and population genetic analyses based on both nuclear and mitochondrial genome sequences of house shrews. Phylogenetic analyses based on mitochondrial cytochrome b (cytb) sequences revealed that shrews from the Ryukyu Archipelago showed strong genetic affinity to Vietnamese and southern Chinese shrews. Demographic analyses of cytb sequences indicated a rapid population expansion event affecting the haplotype group in Vietnam, southern China, and the Ryukyu Archipelago 3300-7900 years ago. Furthermore, gene flow between Ryukyu (Yonaguni Island) and Taiwan and between Ryukyu and Vietnam inferred from f4 statistics of the nuclear genomes suggested repeated immigration to Ryukyu in recent years. The present study demonstrates that the Nagasaki population has a different origin from the Ryukyu population. These findings elucidate the complex pattern of genetic admixture in house shrews and provide insights into their evolutionary history.
... На островах Японского архипелага, как и на Сахалине отмечается экспансивный рост популяций C. rufocanus, Apodemus sp. и других мелких млекопитающих, начало которого соотносится с началом потепления около десяти тысяч лет назад [28]. По аналогии можно было бы предположить, что популяции Итурупа так же испытала экспансивный рост в данный период. ...
С целью исследования путей колонизации красно-серой полевкой о. Итуруп на основе распределения и численности гаплотипов фрагмента митохондриального гена цитохрома b (662 пн) проведен сравнительный анализ генетической изменчивости популяций полевок из разных локалитетов по периметру острова и полевок островов Хоккайдо, Кунашир и Сахалин, а также прилежащих районов материковой суши. Все изученные экземпляры красно-серой полевки с о. Итуруп (68) представлены единственным гаплотипом, наиболее близким к гаплотипам полевок с о. Сахалин. Только один экземпляр с о. Кунашир, ближайшего к Итурупу, обладал таким же гаплотипом. Еще три экземпляра с этого острова были близки к гаплотипам полевок с о. Сахалин и попадали с ними в одну кладу, большинство же гаплотипов полевок Кунашира близки к гаплотипам полевок Хоккайдо и составляют с ними одну самостоятельную кладу, сильно отличающуюся генетически от особей Сахалина и Итурупа. Полученные данные о генетической изменчивости полевок с о. Итуруп убедительно свидетельствуют в пользу недавнего завоза красно-серой полевки C. rufocanus на этот остров, вероятнее всего с морским транспортом с Сахалина.
... Since the evolutionary rate of Cytb is estimated at 0.028-0.11/Myr for Myodes species(Honda et al. 2019), around 0.1/Myr or higher rates are expected for the CR of Myodes species (but seeMatson and Baker 2001, Table 5). The current estimates for the CR (0.196 for M. rufocanus and 0.101 for M. rex) are consistent with these studies. ...
... Wakana et al. (1996) suggested that M. rufocanus colonized Hokkaido 10 000-20 000 years ago using the restriction fragments of rDNA and mtDNA. In contrast, Honda et al. (2019) estimated that M. rufocanus expanded its population around 60 000 years ago in Hokkaido using Cytb of mtDNA. It is difficult for the colonization year of Wakana et al. (1996) to explain that Haplo_ruf26 originating from the Rishiri haplotype group was found in the Hokkaido mainland because a land bridge should be formed two times at least to explain this finding. ...
... Myodes rufocanus immigrated to Rishiri Island through first land bridge and evolved Haplo_ruf26 on Rishiri Island before the second land bridge formation, which may have occurred during LGM (26 500 to 19 000 years ago). Therefore, the present results support the estimation of Honda et al. (2019). ...
The sequence variation of the mtDNA control region (CR) was analyzed for the two sibling species of Myodes (the gray-sided vole M. rufocanus and the dark red-backed vole M. rex) in Hokkaido mainland and its adjacent islands of Japan. The evolutionary rate of the CR was estimated using the island–island connections during the Quaternary. The 737–741-bp were determined for 1196 individuals of M. rufocanus from 65 localities and 315 individuals of M. rex from 26 localities. The CR was highly variable in both species: 330 and 79 haplotypes were identified for M. rufocanus and M. rex, respectively. The genetic distances were estimated for six island population pairs of M. rufocanus and two pairs of M. rex. The genetic distances log-linearly increased with an increase in the separation time. Although the evolutionary rates (substitutions/site/Myr) varied around 10 000 years ago, they became less variable further back in time. The representative evolutionary rate was estimated at 0.196/Myr with 0.139–0.254 (95% CI) for M. rufocanus 40 000 years ago and 0.101/Myr with 0.068–0.134 (95% CI) for M. rex 120 000 years ago. These estimates open opportunities for comparative studies on the evolutionary history of the sibling species.
... Such changes occurred at a 100 000-year cycle, affecting species distribution ranges and facilitating the movement of individuals between islands by lowering the sea level by ~120 m to form land bridges (Hewitt 2000). It has been found that the extent and timing of the effects of Quaternary environmental changes on population dynamics, such as rapid demographic growth, were influenced by local topography, ocean currents, and latitude and also varied among species and populations (Hewitt 2000;Oshida et al. 2009;Burbrink et al. 2016;Honda et al. 2019;Nakamoto et al. 2021). However, it remains to be well documented how the population expansion events have shaped the spatial structure of genetic diversity in response to environmental changes. ...
... These islands are arranged along a north-south axis, and each has a different climate. Numerous species exist in the Japanese archipelago, many of which have colonized the archipelago since millions of years ago (Serizawa et al. 2000;Nunome et al. 2007Nunome et al. , 2010Kirihara et al. 2013;Honda et al. 2019;Nakamoto et al. 2021), allowing comparison of the effects of Quaternary environmental changes within and between species. Several evolutionary studies *To whom correspondence should be addressed. ...
... There is growing evidence to support that the rate of evolution of mtDNA in animals is not constant and is time-dependent, especially in the early stages of divergence, partly due to the involvement of mild deleterious mutations (e.g., Ho et al. 2005Ho et al. , 2011Inoue and Suzuki 2022). Hence, here we used the timedependent evolutionary rate of Cytb in small mammals (Honda et al. 2019;Suzuki 2021). ...
Quaternary environmental change provided opportunities for rapid population expansion; however, the process of building the population spatial structures remains poorly understood. In this study, we determined the mitochondrial cytochrome b and control region sequences of 43 individuals of the large Japanese wood mouse (Apodemus speciosus) from Hokkaido, northern Japan and analyzed these data along with those from 40 other individuals. Consistent with the findings of our previous study, we found that two rapid expansion events, after the last glacial maximum (LGM) and Marine Isotope Stage (MIS) 4, shaped population genetic pattern of A. speciosus in Hokkaido. In northeastern Hokkaido, several ancient lineages that originated during MIS 3 were detected, whereas central Hokkaido was dominated by haplotypes descended from a single lineage that survived the LGM, suggesting that the populations of western part of Hokkaido were newly formed by westward migration from eastern Hokkaido during the post-LGM warm period. Alternatively, as post-LGM vegetation recovery is thought to have occurred gradually from west to east in Hokkaido, population expansion started in the west and moved gradually to the east, resulting in eastward haplotype movement; thus, western and eastern Hokkaido may have served as the haplotype source and sink, respectively.
... Comparing such clusters that arose at different times is helpful for understanding the dynamics. In our previous studies on wild rodents and moles (Suzuki et al., 2015;Hanazaki et al., 2017;Honda et al., 2019;Nakamoto et al., 2021), we revealed several Cytb haplogroups exhibiting a rapid expansion event signature. These haplogroups can be classified into three groups based on the estimated expansion start time, i.e., post-last glacial maximum (LGM) ( < 15,000 years ago), early marine isotope stage (MIS) 3 (53,000 years ago) and post-penultimate glacial maximum (PGM) (130,000 years ago) events. ...
... These in turn allow us to calculate evolutionary rates, based on the modal (peak) values of a unimodal mismatch distribution, defined as τ, which is a statistical value proportional to the time since expansion. The resulting evolutionary rate is 0.11 substitutions/site/million years (myr) for divergence within the past 10,000 years, followed by a sharp decrease to approximately 0.03 substitutions/site/myr for divergence that occurred more than 130,000 years ago (Suzuki et al., 2015;Hanazaki et al., 2017;Honda et al., 2019;Suzuki, 2021). To trace the dynamics of nonsynonymous substitutions, it is also reasonable to address those lying on the younger and older branches of the haplogroup network. ...
... Several haplogroups exhibiting rapid expansion signals have been detected in wood mice (Apodemus) and voles (Myodes) inhabiting the Japanese Archipelago (Suzuki et al., 2015;Hanazaki et al., 2017;Honda et al., 2019). It is also possible to obtain sequence data showing rapid expansion signals in other Apodemus species from Europe (Michaux et al., 2003). ...
We have previously estimated the evolutionary rate (number of substitutions/site/million years) of mitochondrial cytochrome b gene (Cytb) sequences in rodents and moles to be about 0.11 at more recent divergence times of tens of thousands of years, and to decrease rapidly to about 0.03 at more distant divergence times. Because this time dependency is thought to be caused by the removal of mildly deleterious substitutions in later generations, we focused in this study on the abundance of nonsynonymous substitutions. We collected 23 haplogroups of Cytb with signals of late Quaternary population expansion events from rodents and moles and categorized them into three groups for comparison based on predicted expansion start time: 5,000-15,000 years ago (Group I), ca. 53,000 years ago (Group II) and 130,000-230,000 years ago (Group III). We counted the numbers of nonsynonymous and synonymous substitutions in all haplogroups. The rates of nonsynonymous substitutions were lowest in Groups II and III (0.08-0.22), whereas those in Group I varied markedly. We further classified Group I into two subgroups based on high (0.29-0.43) and low (0.09-0.20) nonsynonymous substitution rates, which were likely to be associated with the start of the expansion within 10,000 years and at around 15,000 years ago, respectively. The Group II and III networks had two- or three-step star-shaped structures and tended to exhibit frequent and less frequent nonsynonymous substitutions on exterior and interior branches, respectively. Based on temporal dynamics, nonsynonymous mitochondrial DNA (mtDNA) substitutions in small mammals accounted for at most 40% of all substitutions during the early evolutionary stage and then rapidly declined, dropping to approximately 15%. The results of this study provide a good explanation of the time-dependent trend in the mtDNA evolution rate predicted in previous work.
... In the insular and coastal world, fluctuations in climate and ocean level are especially noticeable since they systematically influenced changes to the landscape and dependent species of flora and fauna (Rudaya et al., 2013;Vasilevski et al., 2010). The most important factors determining the dynamics of mammals, including humans, in the Japanese Islands were changes in the environment of the Pleistocene with accompanying glacial-interglacial cycles and sea level fluctuations (Honda et al., 2019;Vasilevski, 2008b). In the Paleo-SHK most of the natural history of the region was inhabited by modern humans, starting from 34 to 28 ka from the present day (Buvit et al., 2014; see Chapter "Synthetic Perspective on Prehistoric Hunter-Gatherer Adaptations and Landscape Change in Northern Japan" herein). ...
During the period between ~40 and 13 ka BP (all dates are calibrated), Homo sapiens travelled across the aquatic straights between islands in the Far East either by some form of boat or on foot during the last glacial period. The southern Kuril, Hokkaido, Sakhalin islands and the continental Russian Far East merged together during the Last Glacial Maximum (LGM) and formed the Paleo-peninsula of Sakhalin, Hokkaido, Lesser and South Kurils (Paleo-SHK). Also, this glacial process merged together the Kamchatka Peninsula and the Northern Kuril Islands, herein termed the Paleo-KK. These land-bridges existed until the Early Holocene warming. The number and width of the remaining straits were reduced in size and did not represent significant obstacles to human migrations. The interrelationship between these islands and the coastal world of the Sea of Japan and the Sea of Okhotsk is evident in their proximity to each other and the synchronous development of adjacent Stone Age populations. Those groups were connected by contact zones within the boundaries of the overlapping territories reaching from the mouth of the Amur River to eastern Hokkaido and the Middle Kurils, across the Tsugaru Strait to the Nemuro Peninsula and Iturup Island onward, and from Urup Island to Kamchatka. Neolithic processes in this region began in the post-Paleolithic period and were temporarily interrupted by catastrophic climate changes. Sometimes the insular world played a role as the last refugium for people from the continent. The resumption of Neolithization processes took place during conditions of a changes in their economic systems during the climatic warming, which occurred after the end of global cooling that took place during the Kenbuchi stadial around 11.5–11 ka BP. The renaissance of the blade stone tool industry marks the migration of populations from the continent to the insular world of the Far East about 9–8.5 ka BP. Human migrations related to the Paleolithic and the Initial-Early Neolithic insular world were associated with the extreme nature of marine environments and the influx of continental populations into the North and East from the adjacent regions of Eurasia.KeywordsSakhalinPaleo-SHKKuril archipelagoPaleo-KKLGMEUPTUP 1–2Post PaleolithicNeolithicMigrationsEco-social systems
... Population expansion events have been deduced for rodents dwelling in temperate forests (genus Apodemus) (Hanazaki et al. 2017). In addition, population expansion events have been inferred for subarctic grassland-dwelling rodents (genus Myodes) (Kohli et al. 2015;Honda et al. 2019) during the intermediate period 50,000-60,000 years ago, when warmer conditions were beginning during early marine oxygen isotope stage 3 (MIS 3) after a substantially colder period (MIS 4) (e.g., Sawagaki et al. 2004;Shang et al. 2018). Therefore, we sought to determine whether these critical periods of drastic environmental change during the late Quaternary affected the population dynamics of species in subtropical areas. ...
... The cluster exhibited a star-like structure and possessed significant signals of rapid expansion, with a τ value of 6.79 (1140 bp; Table 2). Using an evolutionary rate of 0.047 substitutions/site/myr for Cytb sequences (Honda et al. 2019), the expansion time was estimated as 63,000 years BP (CI: 44,000-77,000 years ago), corresponding to the rapid warming period during early MIS 3, following a bottleneck event during the colder period of MIS 4 (e.g., Woltering et al. 2011) (Fig. 4). Notably, the entire set of haplotypes from Myanmar and Manipur exhibited expansion signals (Table 2), with a τ value of 8.06 and an estimated expansion start time of ca. ...
... Employing a time-dependent evolutionary rate, the expansion start times based on nucleotide substitution levels were calculated to be 63,000 (CI: 44,000-77,000) and 140,000 (CI: 101,000-183,000) years ago, suggesting that both the colder period and subsequent warmer period during the transition from MIS 4 to MIS 3 and MIS 5e were involved, respectively (Fig. 4). This finding implies that species found in subtropical areas had been affected by late Quaternary environmental fluctuations, as had those in areas of higher latitude Hanazaki et al. 2017;Honda et al. 2019). ...
We addressed the spatiotemporal characteristics of four commensal rodent species occurring in Myanmar in comparison with other areas of the Indo-Malayan region. We examined sequence variations of the mitochondrial cytochrome b gene (Cytb) in the Pacific rat (Rattus exulans), roof rat (Rattus rattus complex, RrC), lesser bandicoot rat (Bandicota bengalensis), and house mouse (Mus musculus) using the recently developed time-dependent evolutionary rates of mtDNA. The Cytb sequences of RrC from Myanmar were shown to belong to RrC Lineage II, and their level of genetic diversity was relatively high compared to those of the other three species. RrC was found to have experienced bottleneck and rapid expansion events at least twice in the late Pleistocene period in Myanmar and a nearby region. Accordingly, paleoclimatic environmental fluctuations were shown to be an important factor affecting rodents in the subtropics of the Indo-Malayan region. Our results show that human activities during the last 10,000 years of the Holocene period affected the population dynamics of the rodent species examined, including introducing them to Myanmar from neighboring countries. Further study of these four commensal rodents in other geographic areas of the Indo-Malayan region would allow us to better understand the factors that drove their evolution and their ecological trends.
... Gómez and Lunt 4 proposed that within a big refugium composed of complex mountain ranges, multiple small refugia could form. The idea of small refugia existing within a big refugium has been proposed in many studies 5,[96][97][98] , including empirical studies on plethodontids 99,100 and other East Asian animals [101][102][103][104][105] . This scenario also provides a reasonable interpretation of our data, i.e., genetically distinct K. koreana populations exist in small refugia that are distributed in or around the mountainous terrain of the Korean Peninsula, which in total may be considered one big refugium. ...
The Korean Peninsula, located at the southern tip of Northeast Asia, has never been covered by ice sheets and was a temperate refugium during the Pleistocene. Karsenia koreana, the sole Asian plethodontid salamander species, occurs only on the southern half of the Korean Peninsula and is thought to have found various climatic refugia. Despite its phylogenetic and biogeographic importance, no population-level genetic analysis has been performed on this species. Here we study the population genetic structure of K. koreana using mitochondrial and microsatellite loci to understand the recent historical dispersion process that shaped its current distribution. Overall, the genetic distance between populations correlated well with the spatial distance, and the genetic structure among populations showed signs of a unilateral northward expansion from a southernmost refugium population. Given the distinct genetic structure formed among the populations, the level of historical gene flow among populations appears to have been very low. As the estimated effective population size of K. koreana was also small, these results suggest that the small, restricted populations of K. koreana are extremely vulnerable to environmental changes that may require high levels of genetic diversity to cope with. Thus, special management strategies are needed to preserve these remnant populations.
