{"title":"Developmental Staging of Sexual Egg Formation in <i>Daphnia pulex</i>: Unmated Females Resorb Meiotic Oocytes to Resist Starvation.","authors":"Yugo Takahata, Hitoshi Miyakawa","doi":"10.2108/zs220010","DOIUrl":"https://doi.org/10.2108/zs220010","url":null,"abstract":"<p><p>Under favorable conditions, daphnids produce only female neonates by parthenogenesis, while they produce male neonates and start sexual reproduction when they detect cues signaling a deteriorating environment. Identifying the regulatory mechanisms of such cyclical parthenogenesis is important for understanding how organisms adapt to environments and expand their habitats. However, most previous studies using the model species <i>Daphnia magna</i> and <i>Daphnia pulex</i> have focused on production of male offspring (sex determination), whereas the process of meiosis induction in females has not been investigated. Here, we report a simple experimental method to induce meiosis effectively in <i>D. pulex</i> females. Through observations using the new method, we describe the process of sexual reproduction along an individual developmental time course. Meiotic oocytes are oviposited only when females mate within a certain time window, and failure to mate within that window results in subsequent resorption of oocytes, a measure that may increase resistance to starvation. These results further our understanding of regulatory mechanisms and evolutionary processes in the complicated life-history of <i>Daphnia</i>.</p>","PeriodicalId":24040,"journal":{"name":"Zoological Science","volume":"39 5","pages":"407-412"},"PeriodicalIF":0.9,"publicationDate":"2022-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"33492953","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Andy B Nofrianto, Sjamsu A Lawelle, Daniel F Mokodongan, Kawilarang W A Masengi, Nobuyuki Inomata, Yasuyuki Hashiguchi, Jun Kitano, Bayu K A Sumarto, Ryo Kakioka, Kazunori Yamahira
{"title":"Ancient Admixture in Freshwater Halfbeaks of the Genus <i>Nomorhamphus</i> in Southeast Sulawesi.","authors":"Andy B Nofrianto, Sjamsu A Lawelle, Daniel F Mokodongan, Kawilarang W A Masengi, Nobuyuki Inomata, Yasuyuki Hashiguchi, Jun Kitano, Bayu K A Sumarto, Ryo Kakioka, Kazunori Yamahira","doi":"10.2108/zs220023","DOIUrl":"https://doi.org/10.2108/zs220023","url":null,"abstract":"<p><p>Freshwater halfbeaks of the genus <i>Nomorhamphus</i> (Zenarchopteridae) uniquely diversified on Sulawesi Island, where tectonic movements have been very active since the Pliocene. Most species of this genus have quite limited distributions, which indicates that geographic isolations have contributed to their diversification. In this study, we demonstrated that secondary contacts and resultant admixtures between long-isolated species/populations may have also been important. We found that the mitochondrial phylogeny of a group of <i>Nomorhamphus</i> in Southeast Sulawesi was discordant with the nuclear phylogeny. Most notably, individuals in the upper and lower streams of the Moramo River, a small river in this region, clustered with each other in the mitochondrial phylogeny but not in the nuclear phylogeny; in the latter, the lower-stream individuals formed a clade with individuals in the Anduna River, a different river with no present water connection to the Moramo River. Phylogenetic network and population structure analyses using genomic data obtained from RNA-seq revealed that the lower-stream Moramo population admixed with the upper-stream Moramo lineage in ancient times. These findings indicate that the observed mito-nuclear discordance was caused by mitochondrial introgression and not incomplete lineage sorting. The phylogenetic network also revealed several other admixtures between ancient lineages. Repeated admixtures were also evidenced by topological incongruence in population trees estimated using the RNA-seq data. We propose that activities of many fault systems dissecting Southeast Sulawesi caused repeated secondary contact.</p>","PeriodicalId":24040,"journal":{"name":"Zoological Science","volume":"39 5","pages":"453-458"},"PeriodicalIF":0.9,"publicationDate":"2022-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"33493417","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Phylogeny of <i>g6pc1</i> Genes and Their Functional Divergence among Sarcopterygian Vertebrates: Implications for Thermoregulatory Strategies.","authors":"Genki Yamagishi, Min Kyun Park, Shinichi Miyagawa","doi":"10.2108/zs210113","DOIUrl":"https://doi.org/10.2108/zs210113","url":null,"abstract":"<p><p>Glucose-6-phosphatase catalytic subunit 1 (G6PC1) catalyzes the final rate-limiting step in endogenous glucose production and is critically important for glucose homeostasis. Although a single <i>g6pc1</i> gene is present in mammals, other vertebrates possess two to five paralogs. Functional divergence between paralogs has been reported in actinopterygians and has been implicated in the acquisition of adaptive characteristics. Such reports make sarcopterygian <i>g6pc1</i> an interesting research topic because unlike the aquatic habitat of actinopterygians, sarcopterygians have successfully adapted to terrestrial environments. However, little is known about the evolution of sarcopterygian <i>g6pc1</i>. In the present study, the evolutionary history of sarcopterygian <i>g6pc1</i> was investigated using molecular phylogeny, synteny analyses, and comparison of the genomic environment. Functional divergence between paralogs was also investigated in a reptilian species, the Japanese gecko, with a focus on gene expression in the liver. Evolutionary analyses suggested that amphibians and amniotes acquired duplicated genes independently. Among the amniotes, gene duplication occurred at the root of the reptilian-avian lineage, giving rise to <i>g6pc1-1</i> and <i>g6pc1-2</i> classes. While the avian lineage subsequently lost the <i>g6pc1-1</i>, the reptiles retained both classes. This co-occurrence of gene loss and endothermy acquisition, together with the observation that mammals possess only a single gene, suggests that the duplicated <i>g6pc1</i> is dispensable for endotherms. Quantitative RT-PCR analyses revealed that the two gecko genes respond differently to E2 administration, as the expression of <i>g6pc1-1</i> was downregulated by E2, whereas <i>g6pc1-2</i> showed no significant response. Such paralog-specific responses suggest functional divergence between paralogs, which is possibly related to reproduction.</p>","PeriodicalId":24040,"journal":{"name":"Zoological Science","volume":"39 5","pages":"419-430"},"PeriodicalIF":0.9,"publicationDate":"2022-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"33493414","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Iori Kawamura, Emmeline A Jamodiong, James Davis Reimer
{"title":"Sexual Reproduction in <i>Zoanthus kuroshio</i> and <i>Isaurus tuberculatus</i> (Cnidaria: Anthozoa: Zoanthidae) in Southern Japan.","authors":"Iori Kawamura, Emmeline A Jamodiong, James Davis Reimer","doi":"10.2108/zs220027","DOIUrl":"https://doi.org/10.2108/zs220027","url":null,"abstract":"<p><p>Among family Zoanthidae (Anthozoa: Hexacorallia: Zoantharia), <i>Zoanthus</i> and <i>Isaurus</i> are widespread benthos on coral reefs, but the reproductive biology of both genera is generally unknown. Accordingly, sexual reproduction of two Zoanthidae species in Japan, <i>Zoanthus kuroshio</i> in Okinawa, and <i>Isaurus tuberculatus</i> in Okinawa and Kochi, was investigated by annual sampling. Between 2012 and 2013, polyps of tagged colonies of <i>Z. kuroshio</i> and <i>I. tuberculatus</i> were sampled monthly, and gonads in mesenteries were examined under a stereomicroscope. In <i>Z. kuroshio</i>, sizes of oocytes were estimated and in situ spawning observations were conducted at night at Okinawa sites. Monthly sampling indicated that gametogenesis periods of both species in Okinawa were from May to August, and oogenesis set in earlier than spermatogenesis, and thus both species can be considered protogynous functional hermaphrodites. On the other hand, <i>I. tuberculatus</i> in Kochi had hermaphroditic polyps in July and August. Notably, fertile colonies of <i>Z. kuroshio</i> were not only hermaphrodites but also included exclusively male and female colonies. Overall, four sexual types were identified in <i>Z. kuroshio</i>: male, female, functional protogynous hermaphrodites, and unclassified sterile colonies. In situ gamete release of <i>Z. kuroshio</i> was observed in August 2012 and July to August 2013. First spawning of the year occurred 1 day after the new moon; colonies shed their bundles 3.5-4 h after sunset. We speculate that lunar phase and time after sunset influence spawning timing in <i>Z. kuroshio</i>. Basic knowledge on sexual reproduction of Zoanthidae is critically needed to better understand the basic biology of these benthic cnidarians.</p>","PeriodicalId":24040,"journal":{"name":"Zoological Science","volume":"39 5","pages":"477-488"},"PeriodicalIF":0.9,"publicationDate":"2022-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"33493420","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ko Tomikawa, Yuichiro Nishimoto, Naoyuki Nakahama, Takafumi Nakano
{"title":"A New Species of the Genus <i>Pseudocrangonyx</i> (Crustacea: Amphipoda: Pseudocrangonyctidae) from Yonaguni Island, Southwestern Japan, and Historical Biogeographic Insights of Pseudocrangonyctids.","authors":"Ko Tomikawa, Yuichiro Nishimoto, Naoyuki Nakahama, Takafumi Nakano","doi":"10.2108/zs220030","DOIUrl":"https://doi.org/10.2108/zs220030","url":null,"abstract":"<p><p>The subterranean amphipod genus <i>Pseudocrangonyx</i> is diverse in Far East Asia, including the Japanese Archipelago. However, <i>Pseudocrangonyx</i> species have not been recorded from the Ryukyu Islands, which extend southwest of the Japanese Archipelago. This study describes a new species of <i>Pseudocrangonyx</i>, <i>Pseudocrangonyx dunan</i> sp. nov., from Yonaguni Island, Ryukyu Islands, Japan. Phylogenetic analyses revealed that <i>P. dunan</i> sp. nov. is a sister species to <i>Pseudocrangonyx</i> sp. 4 from Honshu Island, Japan. In addition, three monophyletic groups were found in <i>Pseudocrangonyx</i>, although the phylogenetic positions of several species remain unknown. Our divergence dating indicates that the differentiation of major lineages of <i>Pseudocrangonyx</i>, which contains species from both the Asian continent and the Japanese Archipelago, is concentrated around 20 MYA. These results suggest that the opening of the Sea of Japan is one of the major factors promoting the speciation of <i>Pseudocrangonyx</i> endemic to the archipelago.</p>","PeriodicalId":24040,"journal":{"name":"Zoological Science","volume":"39 5","pages":"489-499"},"PeriodicalIF":0.9,"publicationDate":"2022-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"33493841","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Kimiko Hirose, Hajime Itoh, Tsuyoshi Takano, Tomoko Yamamoto, Shigeaki Kojima
{"title":"Reproductive Isolation and a Change in the Development Mode of the Tideland Snail <i>Batillaria flectosiphonata</i> (Gastropoda: Batillariidae).","authors":"Kimiko Hirose, Hajime Itoh, Tsuyoshi Takano, Tomoko Yamamoto, Shigeaki Kojima","doi":"10.2108/zs210125","DOIUrl":"https://doi.org/10.2108/zs210125","url":null,"abstract":"<p><p>Microsatellite analyses of sympatric populations of a tideland snail endemic to the Nansei Islands, Japan, <i>Batillaria flectosiphonata</i>, and its sister species, <i>Batillaria multiformis</i>, from a tideland on Amami-Oshima Island, indicated that the two species are reproductively isolated from each other, confirming the validity of <i>B. flectosiphonata</i>, whose monophyly was supported only by a low bootstrap probability in the previous molecular phylogenetic analysis. Egg capsules of <i>B. flectosiphonata</i> from Tokunoshima Island of the Amami insular group and Okinawajima Island of the Okinawa insular group were examined, which revealed that this species is a direct developer. Thus, the direct development has evolved twice within batillariids in Japanese waters. The lower genetic diversity of <i>B. flectosiphonata</i> than that of <i>B. multiformis</i> in the sympatric habitat might be attributed to its long-term isolation within the Amami insular group.</p>","PeriodicalId":24040,"journal":{"name":"Zoological Science","volume":"39 5","pages":"413-418"},"PeriodicalIF":0.9,"publicationDate":"2022-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"33493413","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Constant Light, <i>Pdp1</i>, and <i>Tim</i> Exert Influence on Free-Running Period of Locomotor Rhythms in the Cricket <i>Gryllus bimaculatus</i>.","authors":"Yoshiyuki Moriyama, Kazuki Takeuchi, Kenji Tomioka","doi":"10.2108/zs220014","DOIUrl":"https://doi.org/10.2108/zs220014","url":null,"abstract":"<p><p>Most insects show circadian rhythms of which the free-running period changes in a light-dependent manner and is generally longer under constant light (LL) than under constant dark conditions in nocturnal animals. However, the mechanism underlying this LL-dependent period change remains unclear. Here, using the cricket <i>Gryllus bimaculatus</i>, we examined the effects of long-term LL exposure on the free-running period of locomotor rhythms. Initially, the free-running period was considerably longer than 24 h but it gradually became shorter during long-term exposure to LL. The initial lengthening and ensuing gradual shortening under long-term LL exposure were observed even after unilateral removal of the optic lobe. Thus, these changes in the free-running period could be attributable to a single optic lobe clock. RNA interference (RNAi)-mediated silencing of the clock genes <i>Par domain protein 1</i> (<i>Pdp1</i>) and <i>timeless</i> (<i>tim</i>) revealed that the treatments eliminated the initial period lengthening by LL without reducing circadian photoreceptor gene expression. However, they did not affect the period shortening during long-term LL exposure. The slopes of the regression line for the period change during long-term LL for <i>Pdp1</i><sup>RNAi</sup>-treated and <i>tim</i><sup>RNAi</sup>-treated crickets were not different from that of the ds<i>DsRed2</i>-treated control. These results suggest that the initial period lengthening after transfer to LL requires <i>tim</i> and <i>Pdp1</i>, while the ensuing period shortening during long-term LL exposure is caused by a mechanism independent of <i>tim</i> and <i>Pdp1</i>.</p>","PeriodicalId":24040,"journal":{"name":"Zoological Science","volume":"39 5","pages":"459-467"},"PeriodicalIF":0.9,"publicationDate":"2022-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"33493418","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"CD34 is Expressed in Endothelial Cells in Embryonic Testes and is Additionally Expressed in Non-Endothelial Cells in Postnatal Mouse Testes.","authors":"Kazuko Abe, Hiroki Kameyama, Shin-Ichi Abe","doi":"10.2108/zs220026","DOIUrl":"https://doi.org/10.2108/zs220026","url":null,"abstract":"<p><p>CD34 is expressed in various cell types in various tissues/organs, and has been regarded as being expressed in progenitors in various differentiation pathways. On the other hand, morphological studies have reported the presence of a special type of interstitial cells, telocytes, which generally express CD34, and have extremely long moniliform prolongations in various tissues/organs in vertebrates. We have recently reported the successful reconstruction of testicular structures by 3-D re-aggregation culture of dissociated prepubertal mouse testicular cells, and the roles of CD34 <sup>+</sup> cells in the reconstruction. However, it was unknown whether CD34 is expressed in embryonic through adult testes, and if so, in what cell type it is expressed. In order to clarify the expression of CD34 and behavior of CD34 <sup>+</sup> cells during development of mouse testes, we performed immunohistochemical studies. The results show that CD34 is expressed in two cell types in testes; one is endothelial cells which co-express CD31, VE-cadherin, and integrin β1, but barely express PDGFRα and integrin α4 and α9, throughout development, while the other one is non-endothelial cells in which CD34 expression is initiated after birth, and which co-express PDGFRα and integrin α4, α9, and β1. The latter corresponds to telocytes. The present findings will lead to clarifying the roles of these two types of CD34 <sup>+</sup> cells in spermatogenesis.</p>","PeriodicalId":24040,"journal":{"name":"Zoological Science","volume":"39 5","pages":"468-476"},"PeriodicalIF":0.9,"publicationDate":"2022-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"33493419","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Rio Kashimoto, Miyako Tanimoto, Saori Miura, Noriyuki Satoh, Vincent Laudet, Konstantin Khalturin
{"title":"Transcriptomes of Giant Sea Anemones from Okinawa as a Tool for Understanding Their Phylogeny and Symbiotic Relationships with Anemonefish.","authors":"Rio Kashimoto, Miyako Tanimoto, Saori Miura, Noriyuki Satoh, Vincent Laudet, Konstantin Khalturin","doi":"10.2108/zs210111","DOIUrl":"https://doi.org/10.2108/zs210111","url":null,"abstract":"<p><p>The relationship between anemonefish and sea anemones is one of the most emblematic examples of mutualistic symbiosis in coral reefs. Although this is a textbook example, the major aspects of this symbiosis are still not fully understood in mechanistic terms. Moreover, since studies of this relationship have usually been focused on anemonefish, much less is known about giant sea anemones, their similarities, their phylogenetic relationships, and their differences at the molecular level. Since both partners of the symbiotic relationship are important, we decided to explore this well-known phenomenon from the perspective of giant sea anemones. Here, we report reference transcriptomes for all seven species of giant sea anemones that inhabit fringing reefs of Okinawa (Japan) and serve as hosts for six species of local anemonefish. Transcriptomes were used to investigate their phylogenetic relations, genetic differences and repertoires of nematocyte-specific proteins. Our data support the presence of three distinct groups corresponding to three genera: <i>Entacmaea</i>, <i>Heteractis</i>, and <i>Stichodactyla</i>. The basal position among the three groups belongs to <i>Entacmaea</i>, which was the first to diverge from a common ancestor. While the magnitude of genetic difference between the representatives of <i>Entacmaea</i> and <i>Stichodactyla</i> is large, intra-specific variation within <i>Stichodactyla</i> is much smaller and seems to result from recent speciation events. Our data reconfirms that <i>Heteractis magnifica</i> belongs to the genus <i>Stichodactyla</i>, despite an overall morphological similarity with representatives of the genus <i>Heteractis</i>. The availability of reference transcriptomes will facilitate further research into the fascinating relationship between sea anemones and anemonefish.</p>","PeriodicalId":24040,"journal":{"name":"Zoological Science","volume":"39 4","pages":""},"PeriodicalIF":0.9,"publicationDate":"2022-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40718056","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Periodic Stretching of Cultured Myotubes Enhances Myofibril Assembly.","authors":"Takahiro Nomura, Kimihide Hayakawa, Naruki Sato, Takashi Obinata","doi":"10.2108/zs220015","DOIUrl":"https://doi.org/10.2108/zs220015","url":null,"abstract":"<p><p>The effects of mechanical stress on cultured muscle cells were examined with particular interest in myofibril assembly by using a cell-stretching system. We observed that formation and maintenance of cross-striated myofibrils in chick muscle cell cultures was suppressed in the media containing higher concentration of KCl, tetrodotoxin, or ML-9 (an inhibitor of myosin light chain kinase), but periodic stretching of myotubes for several days enabled formation of striated myofibrils just as in standard muscle cultures. However, ryanodine (a blocker of the Ca<sup>2</sup> <sup>+</sup> channel in sarcoplasmic reticulum) and BDM (an inhibitor of myosin-actin interaction) suppressed the stretch-induced myofibrillogenesis. We further found that stretching of myotubes causes quick and transient elevation of the intracellular Ca<sup>2</sup> <sup>+</sup> concentration and this elevation is disturbed by inhibition of Ca<sup>2</sup> <sup>+</sup> channels of sarcoplasmic reticulum and suppression of Ca<sup>2</sup> <sup>+</sup> influx from culture medium. These observations indicate that periodic stretching induces elevation of intracellular Ca<sup>2</sup> <sup>+</sup> concentration and that this elevation may be due to release of Ca<sup>2</sup> <sup>+</sup> from sarcoplasmic reticulum and Ca<sup>2</sup> <sup>+</sup> influx from outside of the cells. The increased Ca<sup>2</sup> <sup>+</sup> may activate actin-myosin interaction by interacting with troponin that is located along actin filaments and/or inducing phosphorylation of myosin light chains and thereby promote myofibril assembly.</p>","PeriodicalId":24040,"journal":{"name":"Zoological Science","volume":"39 4","pages":""},"PeriodicalIF":0.9,"publicationDate":"2022-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40718058","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}