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1.  Hardy exotics species in temperate zone: can “warm water” crayfish invaders establish regardless of low temperatures? 
Scientific Reports  2015;5:16340.
The spreading of new crayfish species poses a serious risk for freshwater ecosystems; because they are omnivores they influence more than one level in the trophic chain and they represent a significant part of the benthic biomass. Both the environmental change through global warming and the expansion of the pet trade increase the possibilities of their spreading. We investigated the potential of four “warm water” highly invasive crayfish species to overwinter in the temperate zone, so as to predict whether these species pose a risk for European freshwaters. We used 15 specimens of each of the following species: the red swamp crayfish (Procambarus clarkii), the marbled crayfish (Procambarus fallax f. virginalis), the yabby (Cherax destructor), and the redclaw (Cherax quadricarinatus). Specimens were acclimatized and kept for 6.5 months at temperatures simulating the winter temperature regime of European temperate zone lentic ecosystems. We conclude that the red swamp crayfish, marbled crayfish and yabby have the ability to withstand low winter temperatures relevant for lentic habitats in the European temperate zone, making them a serious invasive threat to freshwater ecosystems.
doi:10.1038/srep16340
PMCID: PMC4648075  PMID: 26572317
2.  The marbled crayfish as a paradigm for saltational speciation by autopolyploidy and parthenogenesis in animals 
Biology Open  2015;4(11):1583-1594.
ABSTRACT
The parthenogenetic all-female marbled crayfish is a novel research model and potent invader of freshwater ecosystems. It is a triploid descendant of the sexually reproducing slough crayfish, Procambarus fallax, but its taxonomic status has remained unsettled. By cross-breeding experiments and parentage analysis we show here that marbled crayfish and P. fallax are reproductively separated. Both crayfish copulate readily, suggesting that the reproductive barrier is set at the cytogenetic rather than the behavioural level. Analysis of complete mitochondrial genomes of marbled crayfish from laboratory lineages and wild populations demonstrates genetic identity and indicates a single origin. Flow cytometric comparison of DNA contents of haemocytes and analysis of nuclear microsatellite loci confirm triploidy and suggest autopolyploidisation as its cause. Global DNA methylation is significantly reduced in marbled crayfish implying the involvement of molecular epigenetic mechanisms in its origination. Morphologically, both crayfish are very similar but growth and fecundity are considerably larger in marbled crayfish, making it a different animal with superior fitness. These data and the high probability of a divergent future evolution of the marbled crayfish and P. fallax clusters suggest that marbled crayfish should be considered as an independent asexual species. Our findings also establish the P. fallax–marbled crayfish pair as a novel paradigm for rare chromosomal speciation by autopolyploidy and parthenogenesis in animals and for saltational evolution in general.
Summary: The triploid marbled crayfish is a rare animal example of speciation by autopolyploidisation and parthenogenesis. It seems to be a particularly suitable model to study how much genetic and epigenetic change is necessary to create a new species.
doi:10.1242/bio.014241
PMCID: PMC4728364  PMID: 26519519
Marbled crayfish; Autopolyploidy; Parthenogenesis; Epigenetics; Chromosomal speciation; Saltational evolution
3.  Old divergences in a boreal bird supports long-term survival through the Ice Ages 
Background
Unlike northern Europe and most of northern North America, the Eastern Palearctic and the northwesternmost tip of North America are believed to have been almost unglaciated during the Quarternary glacial periods. This could have facilitated long-term survival of many organisms in that area. To evaluate this, we studied the phylogeography in east Asia and Alaska of a boreal migratory passerine bird, the Arctic Warbler Phylloscopus borealis, and compared our results with published data on especially North American species.
Results
In a sample of 113 individuals from 18 populations we identified 42 haplotypes of the mitochondrial cytochrome b gene, which separated into three clades: A - Alaska and mainland Eurasia (except Kamchatka); B - Kamchatka, Sakhalin and Hokkaido; and C - Honshu, Shikoku and Kyushu (i.e. Japan except Hokkaido). The oldest split among these clades, between A/B and C, is estimated to have taken place sometime between the mid Pliocene and early Pleistocene, and the second divergence, between clades A and B, in the early to mid Pleistocene. Within all of the three main clades, there are signs of population expansion.
Conclusions
The Arctic Warbler separated into three main clades in close succession around the Pliocene/Pleistocene border, with the two northern clades diverging last. All three clades probably experienced population bottlenecks during the Pleistocene as a result of range shifts and contractions, but nevertheless survived and maintained their integrities. Several other clades of Northeastern Palearctic birds are noted to have diversified during the Pliocene. In contrast, avian species or phylogroups presently occupying formerly glaciated North American ground are generally younger. The differences between these regions could be due to slower speciation rates in the Eastern Palearctic due to less fragmentation of forest habitats during glacial periods, or to longer survival of Eastern Palearctic clades as a result of less severe conditions in that region compared to northern North America. Several other Palearctic organisms show concordant biogeographical patterns to that of the Arctic Warbler, indicating common causes of their diversifications.
doi:10.1186/1471-2148-10-35
PMCID: PMC2848155  PMID: 20128930
4.  The significance of droughts for hyporheic dwellers: evidence from freshwater crayfish 
Scientific Reports  2016;6:26569.
Freshwater biodiversity is globally threatened by various factors while severe weather events like long-term droughts may be substantially devastating. In order to remain in contact with the water or stay in a sufficiently humid environment at drying localities, the ability to withstand desiccation by dwelling in the hyporheic zone, particularly through vertical burrowing is crucial. We assessed the ability of three European native and five non-native crayfish as models to survive and construct vertical burrows in a humid sandy-clayey substrate under a simulated one-week drought. Three native species (Astacus astacus, A. leptodactylus, and Austropotamobius torrentium) suffered extensive mortalities. Survival of non-native species was substantially higher while all specimens of Cherax destructor and Procambarus clarkii survived. The native species and Pacifastacus leniusculus exhibited no ability to construct vertical burrows. Procambarus fallax f. virginalis and P. clarkii constructed bigger and deeper burrows than C. destructor and Orconectes limosus. In the context of predicted weather fluctuations, the ability to withstand desiccation through constructing vertical burrows into the hyporheic zone under drought conditions might play a significant role in the success of particular crayfish species, as well as a wide range of further hyporheic-dwelling aquatic organisms in general.
doi:10.1038/srep26569
PMCID: PMC4880899  PMID: 27225308
5.  Estimating the molecular evolutionary rates of mitochondrial genes referring to Quaternary ice age events with inferred population expansions and dispersals in Japanese Apodemus 
Background
Determining reliable evolutionary rates of molecular markers is essential in illustrating historical episodes with phylogenetic inferences. Although emerging evidence has suggested a high evolutionary rate for intraspecific genetic variation, it is unclear how long such high evolutionary rates persist because a recent calibration point is rarely available. Other than using fossil evidence, it is possible to estimate evolutionary rates by relying on the well-established temporal framework of the Quaternary glacial cycles that would likely have promoted both rapid expansion events and interisland dispersal events.
Results
We examined mitochondrial cytochrome b (Cytb) and control region (CR) gene sequences in two Japanese wood mouse species, Apodemus argenteus and A. speciosus, of temperate origin and found signs of rapid expansion in the population from Hokkaido, the northern island of Japan. Assuming that global warming after the last glacial period 7–10 thousand years before present (kyr BP) was associated with the expansion, the evolutionary rates (sites per million years, myr) of Cytb and CR were estimated as 11–16 % and 22–32 %, respectively, for A. argenteus, and 12–17 % and 17–24 %, respectively, for A. speciosus. Additionally, the significant signature of rapid expansion detected in the mtDNA sequences of A. speciosus from the remaining southern main islands, Honshu, Shikoku, and Kyushu, provided an estimated Cytb evolutionary rate of 3.1 %/site/myr under the assumption of a postglacial population expansion event long ago, most probably at 130 kyr BP. Bayesian analyses using the higher evolutionary rate of 11–17 %/site/myr for Cytb supported the recent demographic or divergence events associated with the Last Glacial Maximum. However, the slower evolutionary rate of 3.1 %/site/myr would be reasonable for several divergence events that were associated with glacial periods older than 130 kyr BP.
Conclusions
The faster and slower evolutionary rates of Cytb can account for divergences associated with the last and earlier glacial maxima, respectively, in the phylogenetic inference of murine rodents. The elevated evolutionary rate seemed to decline within 100,000 years.
doi:10.1186/s12862-015-0463-5
PMCID: PMC4571126  PMID: 26373638
6.  Invasive Crayfish Threaten the Development of Submerged Macrophytes in Lake Restoration 
PLoS ONE  2013;8(10):e78579.
Submerged macrophytes enhance water transparency and aquatic biodiversity in shallow water ecosystems. Therefore, the return of submerged macrophytes is the target of many lake restoration projects. However, at present, north-western European aquatic ecosystems are increasingly invaded by omnivorous exotic crayfish. We hypothesize that invasive crayfish pose a novel constraint on the regeneration of submerged macrophytes in restored lakes and may jeopardize restoration efforts. We experimentally investigated whether the invasive crayfish (Procambarus clarkii Girard) affects submerged macrophyte development in a Dutch peat lake where these crayfish are expanding rapidly. Seemingly favourable abiotic conditions for macrophyte growth existed in two 0.5 ha lake enclosures, which provided shelter and reduced turbidity, and in one lake enclosure iron was added to reduce internal nutrient loading, but macrophytes did not emerge. We transplanted three submerged macrophyte species in a full factorial exclosure experiment, where we separated the effect of crayfish from large vertebrates using different mesh sizes combined with a caging treatment stocked with crayfish only. The three transplanted macrophytes grew rapidly when protected from grazing in both lake enclosures, demonstrating that abiotic conditions for growth were suitable. Crayfish strongly reduced biomass and survival of all three macrophyte species while waterfowl and fish had no additive effects. Gut contents showed that crayfish were mostly carnivorous, but also consumed macrophytes. We show that P. clarkii strongly inhibit macrophyte development once favourable abiotic conditions for macrophyte growth are restored. Therefore, expansion of invasive crayfish poses a novel threat to the restoration of shallow water bodies in north-western Europe. Prevention of introduction and spread of crayfish is urgent, as management of invasive crayfish populations is very difficult.
doi:10.1371/journal.pone.0078579
PMCID: PMC3813481  PMID: 24205271
7.  New zoonotic cases of Onchocerca dewittei japonica (Nematoda: Onchocercidae) in Honshu, Japan 
Parasites & Vectors  2015;8:59.
Background
Zoonotic infections with Onchocerca species are uncommon, and to date only 25 clinical cases have been reported worldwide. In Japan, five previous zoonotic infections were concentrated in Oita, Kyushu (the southern island), with one previous case in Hiroshima in the western part of Honshu (the main island). The causative agent in Japan was identified as Onchocerca dewittei japonica Uni, Bain & Takaoka, 2001 from Japanese wild boars (Sus scrofa leucomystax Temminck, 1842). Here we report two infections caused by a female and male O. dewittei japonica, respectively, among residents of Hiroshima and Shimane Prefectures in the western part of Honshu.
Methods
In both cases, nodules were surgically removed. The parasites in nodules were identified on the basis of their histopathological characteristics. Identification was confirmed by sequencing the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene from worms in the tissues used in the histological preparations.
Results
Case 1 was a 61-year-old woman from Hiroshima Prefecture who complained of a painful subcutaneous nodule on the back of her right hand. The causative agent was identified as a female O. dewittei japonica owing to transverse ridges on the cuticle and molecular analysis. Case 2 was a 78-year-old woman from Shimane Prefecture who had a painful nodule in the left temporal region. Histopathological characteristics and cox1 sequencing of the worm indicated that the causative agent was a male O. dewittei japonica.
Conclusions
For Cases 1 and 2, we diagnosed the causative agents as a female and male O. dewittei japonica, respectively. These findings indicate the spread of a zoonosis caused by O. dewittei japonica in the western part of Honshu, where wild boars have recently extended their habitats because of decreased annual snowfall, unused rice fields and a decline in the number of hunters in Japan. The O. dewittei japonica infection rate among wild boars was reported as 78% in Shimane Prefecture, in the western part of Honshu. Therefore, in the near future, zoonotic onchocercosis is likely to occur in Honshu as well as Kyushu, where wild boars, blackfly vectors and humans share the same habitat.
doi:10.1186/s13071-015-0655-2
PMCID: PMC4323255  PMID: 25623081
Filarioid; Global warming; Japanese wild boar; Onchocerca dewittei japonica; Vector-borne disease; Zoonosis
8.  Geographical Distribution of the Herpes Simplex Virus Type 1 BgKL Variant in Japan Suggests Gradual Dispersion of the Virus from Shikoku Island to the Other Islands 
Journal of Clinical Microbiology  2006;44(6):2109-2118.
Restriction endonuclease fragment length polymorphism (RFLP) is useful for the epidemiological study of herpes simplex virus type 1 (HSV-1). We report here the identification of a major BglII RFLP variant of HSV-1, designated BgKL, found in 27.0% of 636 HSV-1 clinical isolates. We have also established its geographic distribution in Japan. BgKL has an unusually large BglII K fragment. SalI cleavage analyses showed that 97% of BgKL variant isolates lack both the SalI C-J and the F-J cleavage sites and have an unusually large SalI D or E fragment, and 91% of the BgKL variants lack both SalI G and H fragments. Furthermore, 96% of BgKL isolates have an unusually small KpnI M fragment. Therefore, BgKL is a marker for these five mutations in most HSV-1 isolates and is a useful HSV-1 RFLP marker. The BgKL variant was found in 59% of HSV-1 isolates from Shikoku Island, 44% of HSV-1 isolates from the Chugoku region of Honshu Island, 31% of HSV-1 isolates from Kyushu Island, 0% of HSV-1 isolates from Okinawa Island, 49% of HSV-1 isolates from Osaka, 27% of HSV-1 isolates from Shiga, 13% of HSV-1 isolates from the Chubu Region, and 9% of HSV-1 isolates from the Tohoku Region of Honshu Island. Differences in the frequency of BgKL between the Shikoku-Chugoku-Osaka area (49%) and Kyushu, between Kyushu and Okinawa, between the Shikoku-Chugoku-Osaka area and Shiga, and between Shiga and Tohoku are all statistically significant. The BgKL frequency decreases in a geographical gradient suggest that this HSV-1 variant was dispersed from Shikoku to the surrounding regions and then to more distant regions. The BgKL frequency in Tokyo was similar to the nationwide average. These are the first data to suggest a geographic and demographic dispersion pattern of HSV-1. Implications for the epidemiology and diversification of HSV-1 are discussed.
doi:10.1128/JCM.02064-05
PMCID: PMC1489417  PMID: 16757606
9.  Population-Level Metrics of Trophic Structure Based on Stable Isotopes and Their Application to Invasion Ecology 
PLoS ONE  2012;7(2):e31757.
Biological invasions are a significant driver of human-induced global change and many ecosystems sustain sympatric invaders. Interactions occurring among these invaders have important implications for ecosystem structure and functioning, yet they are poorly understood. Here we apply newly developed metrics derived from stable isotope data to provide quantitative measures of trophic diversity within populations or species. We then use these to test the hypothesis that sympatric invaders belonging to the same functional feeding group occupy a smaller isotopic niche than their allopatric counterparts. Two introduced, globally important, benthic omnivores, Louisiana swamp crayfish (Procambarus clarkii) and carp (Cyprinus carpio), are sympatric in Lake Naivasha, Kenya. We applied our metrics to an 8-year data set encompassing the establishment of carp in the lake. We found a strong asymmetric interaction between the two invasive populations, as indicated by inverse correlations between carp abundance and measures of crayfish trophic diversity. Lack of isotopic niche overlap between carp and crayfish in the majority of years indicated a predominantly indirect interaction. We suggest that carp-induced habitat alteration reduced the diversity of crayfish prey, resulting in a reduction in the dietary niche of crayfish. Stable isotopes provide an integrated signal of diet over space and time, offering an appropriate scale for the study of population niches, but few isotope studies have retained the often insightful information revealed by variability among individuals in isotope values. Our population metrics incorporate such variation, are robust to the vagaries of sample size and are a useful additional tool to reveal subtle dietary interactions among species. Although we have demonstrated their applicability specifically using a detailed temporal dataset of species invasion in a lake, they have a wide array of potential ecological applications.
doi:10.1371/journal.pone.0031757
PMCID: PMC3283663  PMID: 22363724
10.  Lanthanum from a Modified Clay Used in Eutrophication Control Is Bioavailable to the Marbled Crayfish (Procambarus fallax f. virginalis) 
PLoS ONE  2014;9(7):e102410.
To mitigate eutrophication in fresh standing waters the focus is on phosphorus (P) control, i.e. on P inflows to a lake as well as a lake's sediment as internal P source. The in-lake application of the lanthanum (La) modified clays – i.e. La modified bentonite (Phoslock) or La modified kaolinite, aim at dephosphatising the water column and at reducing the release of P from a lake's sediment. Application of these clays raises the question whether La from these clays can become bioavailable to biota. We investigated the bioavailability of La from Phoslock in a controlled parallel groups experiment in which we measured the La in carapace, gills, ovaries, hepatopancreas and abdominal muscle after 0, 14 and 28 days of exposure to Phoslock. Expressing the treatment effect as the difference of the median concentration between the two treatment groups (Phoslock minus control group) yield the following effects, the plus sign (+) indicating an increase, concentrations in µg g−1 dry weight: Day 14: carapace +10.5 µg g−1, gills +112 µg g−1, ovaries +2.6 µg g−1, hepatopancreas +32.9 µg g−1 and abodminal muscle +3.2 µg g−1. Day 28: carapace +17.9 µg g−1; gills +182 µg g−1; ovaries +2.2 µg g−1; hepatopancreas +41.9 µg g−1 and abodminal muscle +7.6 µg g−1, all effects were statistically significant. As La from Phoslock is bio-available to and taken up by the marbled crayfishes (Procambarus fallax f. virginalis), we advocate that the application of in-lake chemical water treatments to mitigate eutrophication should be accompanied by a thorough study on potential side effects.
doi:10.1371/journal.pone.0102410
PMCID: PMC4113486  PMID: 25068309
11.  Phylogeographic insights into the invasion history and secondary spread of the signal crayfish in Japan 
Ecology and Evolution  2016;6(15):5366-5382.
Abstract
Successful invasion by nonindigenous species is often attributed to high propagule pressure, yet some foreign species become widespread despite showing reduced genetic variation due to founder effects. The signal crayfish (Pacifastacus leniusculus) is one such example, where rapid spread across Japan in recent decades is believed to be the result of only three founding populations. To infer the history and explore the success of this remarkable crayfish invasion, we combined detailed phylogeographical and morphological analyses conducted in both the introduced and native ranges. We sequenced 16S mitochondrial DNA of signal crayfish from across the introduced range in Japan (537 samples, 20 sites) and the native range in western North America (700 samples, 50 sites). Because chela size is often related to aggressive behavior in crayfish, and hence, their invasion success, we also measured chela size of a subset of specimens in both introduced and native ranges. Genetic diversity of introduced signal crayfish populations was as high as that of the dominant phylogeographic group in the native range, suggesting high propagule pressure during invasion. More recently established crayfish populations in Japan that originated through secondary spread from one of the founding populations exhibit reduced genetic diversity relative to older populations, probably as a result of founder effects. However, these newer populations also show larger chela size, consistent with expectations of rapid adaptations or phenotypic responses during the invasion process. Introduced signal crayfish populations in Japan originate from multiple source populations from a wide geographic range in the native range of western North America. A combination of high genetic diversity, especially for older populations in the invasive range, and rapid adaptation to colonization, manifested as larger chela in recent invasions, likely contribute to invasion success of signal crayfish in Japan.
doi:10.1002/ece3.2286
PMCID: PMC4984510  PMID: 27551389
Biological invasion; freshwater; mitochondrial DNA; Pacifastacus leniusculus; population genetics; propagule pressure
12.  Regional disparities in interferon therapy for chronic hepatitis C in Japan: a nationwide retrospective cohort study 
BMC Public Health  2015;15:566.
Background
Many patients with chronic hepatitis C have been treated with interferon (IFN) therapy in Japan, especially after the introduction of subsidies for medical expenses in 2008. However, its performance and outcome have never been evaluated. Therefore, a nationwide, mail-based, retrospective cohort study was conducted.
Methods
Regional disparities in the demographic features, treatment performance, and virological response were evaluated using an intent-to-treat design. The participating prefectures were classified into nine regions from north to south (Hokkaido/Tohoku, Kanto, Shin-etsu, Hokuriku, Tokai, Kinki, Chugoku, Shikoku, and Kyushu). Multivariate logistic regression analysis was performed to select predictive factors for treatment performance and outcome.
Results
From December 2009 to May 2013, 16,854 patients with chronic hepatitis C were registered from 37 prefectures in Japan (median age: 60 years; 50.4 % male; 74.8 % IFN-naïve; HCV genotype [1 or 2]/viral load [high (≥5 log IU/mL) or low (<5 log IU/mL)]: 1/high = 58.2 %, 1/low = 5.2 %, 2/high = 27.3 %, 2/low = 7.5 %; 83.4 % treated with peginterferon-α and ribavirin). Mean age, proportion of elderly patients (≥65 years), male sex, IFN-experienced, and HCV genotype were significantly different among the nine regions (all P < 0.001). Regional disparities were independently selected as one of the predictive factors for treatment performance and outcome in patients treated with peginterferon-α and ribavirin, which revealed two regions that required further investigation.
Conclusions
Regional disparities still exist in IFN therapy, and are strongly associated with treatment performance and outcome. Since the accessibility to medical resources for individual patients seemed to be different among the nine regions, public health actions should be focused on how to construct and properly manage consultation networks between base hospitals and local clinics, especially in those regions with low population density.
Electronic supplementary material
The online version of this article (doi:10.1186/s12889-015-1891-2) contains supplementary material, which is available to authorized users.
doi:10.1186/s12889-015-1891-2
PMCID: PMC4474553  PMID: 26088426
Treatment performance; Treatment outcome; Peginterferon-α; Ribavirin; Subsidy policy
13.  Prevalence of the Crayfish Plague Pathogen Aphanomyces astaci in Populations of the Signal Crayfish Pacifastacus leniusculus in France: Evaluating the Threat to Native Crayfish 
PLoS ONE  2013;8(7):e70157.
Aphanomyces astaci, the crayfish plague pathogen, first appeared in Europe in the mid-19th century and is still responsible for mass mortalities of native European crayfish. The spread of this parasite across the continent is especially facilitated by invasive North American crayfish species that serve as its reservoir. In France, multiple cases of native crayfish mortalities have been suggested to be connected with the presence of the signal crayfish Pacifastacus leniusculus, which is highly abundant in the country. It shares similar habitats as the native white-clawed crayfish Austropotamobius pallipes and, when infected, the signal crayfish might therefore easily transmit the pathogen to the native species. We investigated the prevalence of A. astaci in French signal crayfish populations to evaluate the danger they represent to local populations of native crayfish. Over 500 individuals of Pacifastacus leniusculus from 45 French populations were analysed, plus several additional individuals of other non-indigenous crayfish species Orconectes limosus, O. immunis and Procambarus clarkii. Altogether, 20% of analysed signal crayfish tested positive for Aphanomyces astaci, and the pathogen was detected in more than half of the studied populations. Local prevalence varied significantly, ranging from 0% up to 80%, but wide confidence intervals suggest that the number of populations infected by A. astaci may be even higher than our results show. Analysis of several individuals of other introduced species revealed infections among two of these, O. immunis and P. clarkii. Our results confirm that the widespread signal crayfish serves as a key reservoir of Aphanomyces astaci in France and therefore represents a serious danger to native crayfish species, especially the white-clawed crayfish. The prevalence in other non-indigenous crayfish should also be investigated as they likely contribute to pathogen transmission in the country.
doi:10.1371/journal.pone.0070157
PMCID: PMC3720925  PMID: 23894606
14.  Host resistance does not explain variation in incidence of male-killing bacteria in Drosophila bifasciata 
Background
Selfish genetic elements that distort the sex ratio are found widely. Notwithstanding the number of records of sex ratio distorters, their incidence is poorly understood. Two factors can prevent a sex ratio distorter from invading: inability of the sex ratio distorter to function (failure of mechanism or transmission), and lack of drive if they do function (inappropriate ecology for invasion). There has been no test to date on factors causing variation in the incidence of sex ratio distorting cytoplasmic bacteria. We therefore examined whether absence of the male-killing Wolbachia infection in D. bifasciata in Hokkaido island of Japan, in contrast to the presence of infection on the proximal island of Honshu, was associated with failure of the infection to function properly on the Hokkaido genetic background.
Results
The male-killer both transmitted and functioned well following introgression to each of 24 independent isofemale inbred lines carrying Hokkaido genetic backgrounds. This was maintained even under stringent conditions of temperature. We therefore reject the hypothesis that absence of infection is due to its inability to kill males and transmit on the Hokkaido genetic background. Further trap data indicates that D. bifasciata may occur at different densities in Hokkaido and Honshu populations, giving some credence to the idea that ecological differentiation could be important.
Conclusions
The absence of the infection from the Hokkaido population is not caused by failure of the male-killer to function on the Hokkaido genetic background.
doi:10.1186/1471-2148-4-52
PMCID: PMC535909  PMID: 15571631
15.  Macrogenomic Evidence for the Origin of the Black Fly Simulium suzukii (Diptera: Simuliidae) on Okinawa Island, Japan 
PLoS ONE  2013;8(8):e70765.
To determine the geographic origin of the black fly Simulium suzukii on Okinawa Island, Japan, macrogenomic profiles derived from its polytene chromosomes were compared with those of mainland and other insular populations of S. suzukii and of the isomorphic Simulium tani species complex. The Okinawan population is a chromosomally unique cytoform, designated ‘D,’ which is essentially monomorphic and differs by about 27 fixed rearrangements from the chromosomal standard sequence for the subgenus Simulium and by two fixed differences from its nearest known relative, representing the type of S. suzukii, on the main islands of Japan. Chromosomal band sequences revealed two additional, sympatric cytoforms of S. suzukii, designated ‘A’ and ‘B,’ each with species status, in Korea, and a third cytoform, designated ‘C,’ on Hokkaido, Japan. A new cytoform, ‘K,’ of S. tani from Malaysia, representing the type of S. tani, is more closely related to cytoforms in Thailand, as are populations from Taiwan previously treated as S. suzukii but more closely aligned with S. tani and newly recognized as cytoform ‘L’ of the latter nominal species. Rooting of chromosomal band sequences by outgroup comparisons allowed directionality of chromosomal rearrangements to be established, enabling phylogenetic inference of cytoforms. Of 41 macrogenomic rearrangements discovered in the five new cytoforms, four provide evidence for a stepwise origin of the Okinawan population from populations characteristic of the main islands of Japan. The macrogenomic approach applied to black flies on Okinawa Island illustrates its potential utility in defining source areas for other species of flies including those that might pose medical and veterinary risks.
doi:10.1371/journal.pone.0070765
PMCID: PMC3739796  PMID: 23951001
16.  Lineage admixture during postglacial range expansion is responsible for the increased gene diversity of Kalopanax septemlobus in a recently colonised territory 
Heredity  2011;107(4):338-348.
We aimed to reveal the effects of range expansion and subsequent lineage admixture from separated glacial refugia on genetic diversity of Kalopanax septemlobus in Japan, by combining nuclear microsatellite data and ecological niche modelling. Allelic richness and gene diversity were compared at the population and regional level. We also statistically examined these indices as a function of population accessibility to the last glacial maximum (LGM) palaeodistribution reconstructed by ecological niche modelling to test a simple range expansion scenario from glacial refugia. Genetic diversity was highest in the populations of southern Japan and gradually decreased towards the north. However, an additional centre of genetic diversity, when measured as gene diversity, was found in northern Honshu Island, where distinct lineages were shown to be in contact. Positive effects of population accessibility to the LGM range were detected in both diversity indices at different spatial scales. The combined data support independent postglacial range expansions towards the north from the edge populations on the exposed coastal shelf of Pacific and Sea of Japan in northern Honshu during the LGM, which subsequently resulted in markedly low genetic diversity in the northernmost extant range, Hokkaido. The regional increase in gene diversity in northern Honshu is likely to be the result of postglacial lineage admixture. Relative difference in the spatial scales best relating population genetic diversity with the LGM distribution can be explained by a higher rate of allelic richness diversity loss during range expansions and stronger effects of lineage admixture on gene diversity.
doi:10.1038/hdy.2011.20
PMCID: PMC3182501  PMID: 21427749
accessibility to palaeodistribution; ecological niche model; exposed coastal landscape; lineage admixture; nuclear microsatellite; postglacial colonisation
17.  Spread of Aedes japonicus japonicus (Theobald, 1901) in Austria, 2011–2015, and first records of the subspecies for Hungary, 2012, and the principality of Liechtenstein, 2015 
Parasites & Vectors  2016;9:356.
Background
The Asian bush mosquito, Aedes (Hulecoeteomyia) japonicus japonicus (Theobald, 1901) (Diptera: Culicidae), was first identified in Austria in August 2011 in the federal state of Styria at the border to Slovenia.
Methods
Between 2011 and 2015 the spread of Ae. j. japonicus was monitored in southern, eastern and western Austrian provinces as well as in neighbouring countries by checking natural and man-made container habitats for the aquatic stages. The search concentrated around the most recent occurrence of Ae. j. japonicus and extended up to several kilometres until the subspecies could not be found anymore.
Results
Between May and July 2012 the distribution area of Ae. j. japonicus was found to be extended westwards into Carinthia, and eastwards towards the federal state of Burgenland. In August 2012, the subspecies was found in Hungary, representing the first record of an invasive mosquito species in this country. In 2013 its expansion was confirmed at several sites in Austria. Additionally, between April and July 2015, the subspecies was detected in all districts of the westernmost Austrian state Vorarlberg reaching the alpine Montafon valley at the end of October 2015, at all three examined sites in southern Bavaria bordering Vorarlberg, and in the adjacent Principality of Liechtenstein, for which it also represents the first record of an invasive mosquito species. One remarkable finding of the subspecies was located close to the city of Kufstein in the lower Inn valley of the Tyrol in September 2015, which is an isolated occurrence without spatial connection to any known established population.
Conclusions
Our findings demonstrate the ongoing spread of Ae. j. japonicus towards all directions within Austria and beyond. Together with the absence of supposed natural barriers, e.g. high mountain chains, at the borders of the current subspecies’ distribution area in south-eastern Austria, these findings suggest a further spread to the Austrian capital Vienna and the Hungarian tourist region of Lake Balaton within the upcoming few years. The observed intrusions in western Austria represent most probably extensions of the population established and spreading in eastern Switzerland and southern Germany. The putative role of the subspecies in pathogen transmission together with its rapid spread observed argues for the implementation of comprehensive nation-wide surveillance and response preparedness.
doi:10.1186/s13071-016-1645-8
PMCID: PMC4919864  PMID: 27343074
Aedes japonicus; Asian bush mosquito; Invasive mosquito species; Active spread; First record; Austria; Hungary; Bavaria; Liechtenstein
18.  Population Genetic Structure and Post-Establishment Dispersal Patterns of the Red Swamp Crayfish Procambarus Clarkii in China 
PLoS ONE  2012;7(7):e40652.
The red swamp crayfish (Procambarus clarkii) was introduced to China in the early 20th century. It has been spread to almost all forms of fresh water bodies including lakes, rivers and even paddyfields in most provinces of China. To clarify issues such as the initial entry point(s), dispersal pattern, genetic diversity and genetic structure of Procambarus clarkii in China, the genetic structure and diversity of P. clarkii populations at 37 sampling sites (35 from China, one from the USA and one from Japan) were analyzed using both mitochondrial gene sequences (COI and 16S rRNA) and 12 nuclear microsatellites. Multiple tests including phylogenetic analyses, Bayesian assignment and analysis of isolation by distance showed that (i) the population from Japan and those collected from China, particularly from NanJing (BGt and XG) and its some neighboring sites (CJr, NT and NB), have similar genetic composition, (ii) relatively high genetic diversity was detected in Chinese populations, (iii) the P. clarkii populations in China did not experience significant population expansions. Taken together, Nanjing, Jiangsu province is the presumed initial entry point, and human-mediated dispersal and adaptive variation are likely responsible for the observed genetic pattern of P. clarkii in China.
doi:10.1371/journal.pone.0040652
PMCID: PMC3393698  PMID: 22808222
19.  Current status of nontuberculous mycobacterial surgery in Japan: analysis of data from the annual survey by the Japanese Association for Thoracic Surgery 
Objective
The prevalence of pulmonary disease caused by nontuberculous mycobacteria (NTM) has been increasing in Japan. Adjuvant resectional surgery is often recommended to lessen disease progression when the response to drug therapy is poor. In all likelihood, as affected cases of NTM disease increase, so will the number of operations. The goal of this study was to determine the current status of NTM surgery in Japan by analyzing data from the annual survey of the Japanese Association for Thoracic Surgery (JATS).
Methods
Data were obtained from annual surveys conducted between 2008 and 2012. The annual number of operations for pulmonary NTM disease was tabulated nationwide and in each region (Hokkaido, Tohoku, Kanto, Tokyo, Chubu, Kinki, Chugoku/Shikoku, and Kyushu). For comparison, the numbers for pulmonary tuberculosis and tuberculoma operations were also obtained.
Results
The annual number of operations for pulmonary NTM disease nationwide increased each year between 2008 and 2012: 292 (2008), 323 (2009), 452 (2010), 440 (2011), and 514 (2012); an overall increase of 76 %. Conversely, the annual numbers of operations for pulmonary tuberculosis were stable: 145 (2008), 181 (2009), 117 (2010), 113 (2011), and 107 (2012), as were the annual numbers of operations for tuberculoma: 386 (2008), 341 (2009), 320 (2010), 390 (2011), and 351 (2012).
Conclusion
Data from the JATS annual survey demonstrate a steady increase in the number of NTM surgeries in Japan. General thoracic surgeons will continue to increasingly encounter NTM patients who are candidates for surgery until a magic bullet against NTM disease is available.
doi:10.1007/s11748-015-0594-z
PMCID: PMC4700056  PMID: 26433726
Nontuberculous mycobacteriosis; Tuberculosis; Tuberculoma; Resectional surgery
20.  Where to deliver baits for deworming urban red foxes for Echinococcus multilocularis control: new protocol for micro-habitat modeling of fox denning requirements 
Parasites & Vectors  2014;7:357.
Background
Deworming wild foxes by baiting with the anthelmintic praziquantel is being established as a preventive technique against environmental contamination with Echinococcus multilocularis eggs. Improvement of the cost-benefit performance of baiting treatment is required urgently to raise and maintain the efficacy of deworming. We established a spatial model of den site selection by urban red foxes, the definitive host, to specify the optimal micro-habitats for delivering baits in a new modeling approach modified for urban fox populations.
Methods
The model was established for two cities (Obihiro and Sapporo) in Hokkaido, Japan, in which a sylvatic cycle of E. multilocularis is maintained. The two cities have different degrees of urbanization. The modeling process was designed to detect the best combination of key environmental factors and spatial scale that foxes pay attention to most (here named ‘heeding range’) when they select den sites. All possible models were generated using logistic regression analysis, with “presence” or “absence” of fox den as the objective variable, and nine landscape categories customized for urban environments as predictor variables to detect the best subset of predictors. This procedure was conducted for each of ten sizes of concentric circles from dens and control points to detect the best circle size. Out of all models generated, the most parsimonious model was selected using Akaike’s Information Criterion (AIC) inspection.
Results
Our models suggest that fox dens in Obihiro are located at the center of a circle with 500 m radius including low percentages of wide roads, narrow roads, and occupied buildings, but high percentages of green covered areas; the dens in Sapporo within 300 m radius with low percentages of wide roads, occupied buildings, but high percentages of riverbeds and green covered areas. The variation of the models suggests the necessity of accumulating models for various types of cities in order to reveal the patterns of the model.
Conclusions
Our denning models indicating suitable sites for delivering baits will improve the cost-benefit performance of the campaign. Our modeling protocol is suitable for the urban landscapes, and for extracting the heeding range when they select the den sites.
Electronic supplementary material
The online version of this article (doi:10.1186/1756-3305-7-357) contains supplementary material, which is available to authorized users.
doi:10.1186/1756-3305-7-357
PMCID: PMC4262088  PMID: 25095789
Echinococcus multilocularis; Baiting strategy; Cost-benefit performance; Vulpes vulpes; Urban red fox; Den site selection; Key environmental factors; Key spatial scale; Requisite spatial scale; Heeding range
21.  Invasion Biology of Aedes japonicus japonicus (Diptera: Culicidae) 
Aedes japonicus japonicus (Theobald) (Diptera: Culicidae) has recently expanded beyond its native range of Japan and Korea into large parts of North America and Central Europe. Population genetic studies begun immediately after the species was detected in North America revealed genetically distinct introductions that subsequently merged, likely contributing to the successful expansion. Interactions, particularly in the larval stage, with other known disease vectors give this invasive subspecies the potential to influence local disease dynamics. Its successful invasion likely does not involve superior direct competitive abilities, but it is associated with the use of diverse larval habitats and a cold tolerance that allows an expanded seasonal activity range in temperate climates. We predict a continued but slower expansion of Ae. j. japonicus in North America and a continued rapid expansion into other areas as this mosquito will eventually be considered a permanent resident of much of North America, Europe, Asia, and parts of Hawaii.
doi:10.1146/annurev-ento-011613-162012
PMCID: PMC4106299  PMID: 24397520
Aedes japonicus or Ochlerotatus japonicus; invasive mosquitoes; disease vectors; container habitats; mosquito larvae interactions
22.  Genome-wide association mapping focusing on a rice population derived from rice breeding programs in a region 
Breeding Science  2015;65(5):403-410.
Plant breeding programs in local regions may generate genetic variations that are desirable to local populations and shape adaptability during the establishment of local populations. To elucidate genetic bases for this process, we proposed a new approach for identifying the genetic bases for the traits improved during rice breeding programs; association mapping focusing on a local population. In the present study, we performed association mapping focusing on a local rice population, consisting of 63 varieties, in Hokkaido, the northernmost region of Japan and one of the northern limits of rice cultivation worldwide. Six and seventeen QTLs were identified for heading date and low temperature germinability, respectively. Of these, 13 were novel QTLs in this population and 10 corresponded to the QTLs previously reported based on QTL mapping. The identification of QTLs for traits in local populations including elite varieties may lead to a better understanding of the genetic bases of elite traits. This is of direct relevance for plant breeding programs in local regions.
doi:10.1270/jsbbs.65.403
PMCID: PMC4671701  PMID: 26719743
genome-wide association mapping; local population; Oryza sativa L.; plant breeding programs; rice
23.  Interspecific Larval Competition Between Aedes albopictus and Aedes japonicus (Diptera: Culicidae) in Northern Virginia 
Journal of medical entomology  2008;45(4):629-637.
Aedes albopictus (Skuse) and Aedes japonicus (Theobald) are two of the most recent and widespread invasive mosquito species to have become established in the United States. The two species co-occur in water-filled artificial containers, where crowding and limiting resources are likely to promote inter- or intraspecific larval competition. The performance of northern Virginia populations of Ae. japonicus and Ae. albopictus competing as larvae under field conditions was evaluated. Per capita rates of population increase for each species were estimated, and the effects of species composition and larval density were determined. In water-containing cups provided with oak leaves, Ae. albopictus larvae exhibited a competitive advantage over Ae. japonicus as a consequence of higher survivorship, shorter developmental time, and a significantly higher estimated population growth rate under conditions of interspecific competition. Intraspecific competition constrained population performance of Ae. albopictus significantly more than competition with Ae. japonicus. In the context of the Lotka-Volterra model of competition, these findings suggest competitive exclusion of Ae. japonicus in those habitats where this species co-occurs with Ae. albopictus.
PMCID: PMC2631177  PMID: 18714861
invasive; mosquito; containers; competition
24.  Impacts of the North American signal crayfish (Pacifastacus leniusculus) on European ecosystems 
As a vector of the crayfish plague (Aphanomyces astaci), invasive crayfish pose a major threat to endemic crayfish species in Europe. But do they affect whole ecosystems and fish species as well? A comprehensive review was done using online search engines on current literature to elucidate possible crayfish effects. It showed that they have the potential to decimate benthic invertebrate populations as well as submerged plants—the first a necessary food source, the second an important part of the habitat of fish, functioning as hiding space for their fry as well as their prey. Crayfish are suspected to act as bioturbators as well, by influencing preconditions to certain algae and animals while sorting through the substrate of a river. Their long-term effects on fish so far are inconclusive. Studies on this matter showed no effect, selective impact on fish that share prey with the crayfish, as well as significantly negative effects on fish in general. In shorter examinations, invasive crayfish have proven to displace fish from shelters, putting them at a higher risk for predation. Moreover, comparisons to native crayfish species showed that these had less negative effects on fish—due to lower consumption and reproduction rates and population densities.
doi:10.1186/s12302-015-0065-2
PMCID: PMC5044948  PMID: 27752434
Signal crayfish; Benthos; Fish species; Biological invasion
25.  Molecular and genealogical analysis of grain dormancy in Japanese wheat varieties, with specific focus on MOTHER OF FT AND TFL1 on chromosome 3A 
Breeding Science  2015;65(1):103-109.
In the wheat (Triticum aestivum L.) cultivar ‘Zenkoujikomugi’, a single nucleotide polymorphism (SNP) in the promoter of MOTHER OF FT AND TFL1 on chromosome 3A (MFT-3A) causes an increase in the level of gene expression, resulting in strong grain dormancy. We used a DNA marker to detect the ‘Zenkoujikomugi’-type (Zen-type) SNP and examined the genotype of MFT-3A in Japanese wheat varieties, and we found that 169 of 324 varieties carry the Zen-type SNP. In Japanese commercial varieties, the frequency of the Zen-type SNP was remarkably high in the southern part of Japan, but low in the northern part. To examine the relationship between MFT-3A genotype and grain dormancy, we performed a germination assay in three wheat-growing seasons. On average, the varieties carrying the Zen-type SNP showed stronger grain dormancy than the varieties carrying the non-Zen-type SNP. Among commercial cultivars, ‘Iwainodaichi’ (Kyushu), ‘Junreikomugi’ (Kinki-Chugoku-Shikoku), ‘Kinuhime’ (Kanto-Tokai), ‘Nebarigoshi’ (Tohoku-Hokuriku), and ‘Kitamoe’ (Hokkaido) showed the strongest grain dormancy in each geographical group, and all these varieties, except for ‘Kitamoe’, were found to carry the Zen-type SNP. In recent years, the number of varieties carrying the Zen-type SNP has increased in the Tohoku-Hokuriku region, but not in the Hokkaido region.
doi:10.1270/jsbbs.65.103
PMCID: PMC4374559  PMID: 25931984
Triticum aestivum L.; grain dormancy; pre-harvest sprouting; MFT; genealogical pedigree

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