Krings, Wencke, Brütt, Jan-Ole, Gorb, Stanislav N.
{"title":"Ontogeny of the elemental composition and the biomechanics of radular teeth in the chiton Lepidochitona cinerea","authors":"Krings, Wencke, Brütt, Jan-Ole, Gorb, Stanislav N.","doi":"10.1186/s12983-022-00465-w","DOIUrl":"https://doi.org/10.1186/s12983-022-00465-w","url":null,"abstract":"The radula, a chitinous membrane with embedded teeth, is one important molluscan autapomorphy. In some taxa (Polyplacophora and Patellogastropoda) one tooth type (the dominant lateral tooth) was studied intensively in the last decades with regard to its mechanical properties, chemical and structural composition, and the relationship between these parameters. As the dominant lateral tooth is probably one of the best studied biological materials, it is surprising, that data on elements and mechanical properties of the other tooth types, present on a chiton radula, is lacking. We provide data on the elemental distribution and mechanical properties (hardness and elasticity, i.e. Young’s modulus) of all teeth from the Polyplacophora Lepidochitona cinerea (Linnaeus, 1767) [Chitonidae: Ischnochitonidae]. The ontogeny of elements, studied by energy-dispersive X-ray spectroscopy, and of the mechanical properties, determined by nanoindentation, was analysed in every individual tooth type. Additionally, we performed breaking stress experiments with teeth under dry and wet condition, highlighting the high influence of the water content on the mechanical behaviour of the radula. We thereby could determine the forces and stresses, teeth can resist, which were previously not studied in representatives of Polyplacophora. Overall, we were able to relate the mineral (iron, calcium) content with the mechanical parameters (hardness and Young’s modulus) and the breaking force and stress in every tooth type. This led to a better understanding of the relationship between structure, material, and function in radular teeth. Further, we aimed at determining the role of calcium for the mechanical behaviour of the teeth: we decalcified radulae by ethylene diamine tetra acetic acid and performed afterwards elemental analyses, breaking stress experiments, and nanoindentation. Among other things, we detected that wet and decalcified radular teeth could resist highest forces, since teeth have a higher range of bending motion leading to a higher capability of teeth to gain mechanical support from the adjacent tooth row. This indicates, that the tooth material is the result of a compromise between failure reduction and the ability to transfer forces onto the ingesta. We present novel data on the elemental composition, mechanical properties, and the mechanical behaviour of chiton teeth, which allows conclusions about tooth function. We could also relate the parameters mentioned, which contributes to our understanding on the origins of mechanical property gradients and the processes reducing structural failure in radular teeth. Additionally, we add more evidence, that the elemental composition of radular is probably species-specific and could be used as taxonomic character.","PeriodicalId":55142,"journal":{"name":"Frontiers in Zoology","volume":"20 1","pages":""},"PeriodicalIF":2.8,"publicationDate":"2022-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138533125","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Sequence of chondrocranial development in basal anurans—Let’s make a cranium","authors":"Lukas, Paul, Ziermann, Janine M.","doi":"10.1186/s12983-022-00462-z","DOIUrl":"https://doi.org/10.1186/s12983-022-00462-z","url":null,"abstract":"The craniofacial skeleton is an evolutionary innovation of vertebrates. Due to its complexity and importance to protect the brain and aid in essential functions (e.g., feeding), its development requires a precisely tuned sequence of chondrification and/or ossification events. The comparison of sequential patterns of cartilage formation bears important insights into the evolution of development. Discoglossus scovazzi is a basal anuran species. The comparison of its chondrocranium (cartilaginous neuro- & viscerocranium) development with other basal anurans (Xenopus laevis, Bombina orientalis) will help establishing the ancestral pattern of chondrification sequences in anurans and will serve as basis for further studies to reconstruct ancestral conditions in amphibians, tetrapods, and vertebrates. Furthermore, evolutionary patterns in anurans can be studied in the light of adaptations once the ancestral sequence is established. We present a comprehensive overview on the chondrocranium development of D. scovazzi. With clearing and staining, histology and 3D reconstructions we tracked the chondrification of 44 elements from the first mesenchymal Anlagen to the premetamorphic cartilaginous head skeleton and illustrate the sequential changes of the skull. We identified several anuran and discoglossoid traits of cartilage development. In D. scovazzi the mandibular, hyoid, and first branchial arch Anlagen develop first followed by stepwise addition of the branchial arches II, III, and IV. Nonetheless, there is no strict anterior to posterior chondrification pattern within the viscerocranium of D. scovazzi. Single hyoid arch elements chondrify after elements of the branchial arch and mandibular arch elements chondrify after elements of the branchial arch I. In Osteichthyes, neurocranial elements develop in anterior to posterior direction. In the anurans investigated so far, as well as in D. scovazzi, the posterior parts of the neurocranium extend anteriorly, while the anterior parts of the neurocranium, extend posteriorly until both parts meet and fuse. Anuran cartilaginous development differs in at least two crucial traits from other gnathostomes which further supports the urgent need for more developmental investigations among this clade to understand the evolution of cartilage development in vertebrates.","PeriodicalId":55142,"journal":{"name":"Frontiers in Zoology","volume":"23 1","pages":""},"PeriodicalIF":2.8,"publicationDate":"2022-05-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138533127","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Goodheart, Jessica A., Barone, Vanessa, Lyons, Deirdre C.
{"title":"Movement and storage of nematocysts across development in the nudibranch Berghia stephanieae (Valdés, 2005)","authors":"Goodheart, Jessica A., Barone, Vanessa, Lyons, Deirdre C.","doi":"10.1186/s12983-022-00460-1","DOIUrl":"https://doi.org/10.1186/s12983-022-00460-1","url":null,"abstract":"Intracellular sequestration requires specialized cellular and molecular mechanisms allowing a predator to retain and use specific organelles that once belonged to its prey. Little is known about how common cellular mechanisms, like phagocytosis, can be modified to selectively internalize and store foreign structures. One form of defensive sequestration involves animals that sequester stinging organelles (nematocysts) from their cnidarian prey. While it has been hypothesized that nematocysts are identified by specialized phagocytic cells for internalization and storage, little is known about the cellular and developmental mechanisms of this process in any metazoan lineage. This knowledge gap is mainly due to a lack of genetically tractable model systems among predators and their cnidarian prey. Here, we introduce the nudibranch Berghia stephanieae as a model system to investigate the cell, developmental, and physiological features of nematocyst sequestration selectivity. We first show that B. stephanieae, which feeds on Exaiptasia diaphana, selectively sequesters nematocysts over other E. diaphana tissues found in their digestive gland. Using confocal microscopy, we document that nematocyst sequestration begins shortly after feeding and prior to the formation of the appendages (cerata) where the organ responsible for sequestration (the cnidosac) resides in adults. This finding is inconsistent with previous studies that place the formation of the cnidosac after cerata emerge. Our results also show, via live imaging assays, that both nematocysts and dinoflagellates can enter the nascent cnidosac structure. This result indicates that selectivity for nematocysts occurs inside the cnidosac in B. stephanieae, likely in the cnidophage cells themselves. Our work highlights the utility of B. stephanieae for future research, because: (1) this species can be cultured in the laboratory, which provides access to all developmental stages, and (2) the transparency of early juveniles makes imaging techniques (and therefore cell and molecular assays) feasible. Our results pave the way for future studies using live imaging and targeted gene editing to identify the molecular mechanisms involved in nematocyst sequestration. Further studies of nematocyst sequestration in B. stephanieae will also allow us to investigate how common cellular mechanisms like phagocytosis can be modified to selectively internalize and store foreign structures.","PeriodicalId":55142,"journal":{"name":"Frontiers in Zoology","volume":"28 1","pages":""},"PeriodicalIF":2.8,"publicationDate":"2022-04-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138533128","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Mashanov, Vladimir, Whaley, Lauren, Davis, Kenneth, Heinzeller, Thomas, Machado, Denis Jacob, Reid, Robert W., Kofsky, Janice, Janies, Daniel
{"title":"A subterminal growth zone at arm tip likely underlies life-long indeterminate growth in brittle stars","authors":"Mashanov, Vladimir, Whaley, Lauren, Davis, Kenneth, Heinzeller, Thomas, Machado, Denis Jacob, Reid, Robert W., Kofsky, Janice, Janies, Daniel","doi":"10.1186/s12983-022-00461-0","DOIUrl":"https://doi.org/10.1186/s12983-022-00461-0","url":null,"abstract":"Echinoderms are a phylum of marine invertebrates with close phylogenetic relationships to chordates. Many members of the phylum Echinodermata are capable of extensive post-traumatic regeneration and life-long indeterminate growth. Different from regeneration, the life-long elongation of the main body axis in adult echinoderms has received little attention. The anatomical location and the nature of the dividing progenitor cells contributing to adults’ growth is unknown. We show that the proliferating cells that drive the life-long growth of adult brittle star arms are mostly localized to the subterminal (second from the tip) arm segment. Each of the major anatomical structures contains dividing progenitors. These structures include: the radial nerve, water-vascular canal, and arm coelomic wall. Some of those proliferating progenitor cells are capable of multiple rounds of cell division. Within the nervous system, the progenitor cells were identified as a subset of radial glial cells that do not express Brn1/2/4, a transcription factor with a conserved role in the neuronal fate specification. In addition to characterizing the growth zone and the nature of the precursor cells, we provide a description of the microanatomy of the four distal-most arm segments contrasting the distal with the proximal segments, which are more mature. The growth of the adult brittle star arms occurs via proliferation of progenitor cells in the distal segments, which are most abundant in the second segment from the tip. At least some of the progenitors are capable of multiple rounds of cell division. Within the nervous system the dividing cells were identified as Brn1/2/4-negative radial glial cells.","PeriodicalId":55142,"journal":{"name":"Frontiers in Zoology","volume":"72 1","pages":""},"PeriodicalIF":2.8,"publicationDate":"2022-04-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138533064","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Frankowski, Karina, Miyazaki, Katsumi, Brenneis, Georg
{"title":"A microCT-based atlas of the central nervous system and midgut in sea spiders (Pycnogonida) sheds first light on evolutionary trends at the family level","authors":"Frankowski, Karina, Miyazaki, Katsumi, Brenneis, Georg","doi":"10.1186/s12983-022-00459-8","DOIUrl":"https://doi.org/10.1186/s12983-022-00459-8","url":null,"abstract":"Pycnogonida (sea spiders) is the sister group of all other extant chelicerates (spiders, scorpions and relatives) and thus represents an important taxon to inform early chelicerate evolution. Notably, phylogenetic analyses have challenged traditional hypotheses on the relationships of the major pycnogonid lineages (families), indicating external morphological traits previously used to deduce inter-familial affinities to be highly homoplastic. This erodes some of the support for phylogenetic information content in external morphology and calls for the study of additional data classes to test and underpin in-group relationships advocated in molecular analyses. In this regard, pycnogonid internal anatomy remains largely unexplored and taxon coverage in the studies available is limited. Based on micro-computed X-ray tomography and 3D reconstruction, we created a comprehensive atlas of in-situ representations of the central nervous system and midgut layout in all pycnogonid families. Beyond that, immunolabeling for tubulin and synapsin was used to reveal selected details of ganglionic architecture. The ventral nerve cord consistently features an array of separate ganglia, but some lineages exhibit extended composite ganglia, due to neuromere fusion. Further, inter-ganglionic distances and ganglion positions relative to segment borders vary, with an anterior shift in several families. Intersegmental nerves target longitudinal muscles and are lacking if the latter are reduced. Across families, the midgut displays linear leg diverticula. In Pycnogonidae, however, complex multi-branching diverticula occur, which may be evolutionarily correlated with a reduction of the heart. Several gross neuroanatomical features are linked to external morphology, including intersegmental nerve reduction in concert with trunk segment fusion, or antero-posterior ganglion shifts in partial correlation to trunk elongation/compaction. Mapping on a recent phylogenomic phylogeny shows disjunct distributions of these traits. Other characters show no such dependency and help to underpin closer affinities in sub-branches of the pycnogonid tree, as exemplified by the tripartite subesophageal ganglion of Pycnogonidae and Rhynchothoracidae. Building on this gross anatomical atlas, future studies should now aim to leverage the full potential of neuroanatomy for phylogenetic interrogation by deciphering pycnogonid nervous system architecture in more detail, given that pioneering work on neuron subsets revealed complex character sets with unequivocal homologies across some families.","PeriodicalId":55142,"journal":{"name":"Frontiers in Zoology","volume":"47 1","pages":""},"PeriodicalIF":2.8,"publicationDate":"2022-03-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138533126","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Sexual dimorphism in ritualized agonistic behaviour, fighting ability and contest costs of Sus scrofa","authors":"I. Camerlink, M. Farish, G. Arnott, S. Turner","doi":"10.1186/s12983-022-00458-9","DOIUrl":"https://doi.org/10.1186/s12983-022-00458-9","url":null,"abstract":"","PeriodicalId":55142,"journal":{"name":"Frontiers in Zoology","volume":"19 1","pages":""},"PeriodicalIF":2.8,"publicationDate":"2022-03-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"65725018","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Effects of host state and body condition on parasite infestation of bent-wing bats.","authors":"Yik Ling Tai, Ya-Fu Lee, Yen-Min Kuo, Yu-Jen Kuo","doi":"10.1186/s12983-022-00457-w","DOIUrl":"10.1186/s12983-022-00457-w","url":null,"abstract":"<p><strong>Background: </strong>Ectoparasites inhabit the body surface or outgrowths of hosts and are usually detrimental to host health and wellbeing. Hosts, however, vary in quality and may lead ectoparasites to aggregate on preferred hosts, resulting in a heterogeneous distribution of parasite load among hosts.</p><p><strong>Results: </strong>We set out to examine the effects of host individual state and body condition on the parasite load of multiple nycteribiid and streblid bat flies and Spinturnix wing mites on eastern bent-wing bats Miniopterus fuliginosus in a tropical forest in southern Taiwan. We detected a high parasite prevalence of 98.9% among the sampled bats, with nearly 75% of the bats harboring three or more species of parasites. The parasite abundance was higher in the wet season from mid spring to early fall, coinciding with the breeding period of female bats, than in the dry winter season. In both seasonal periods, the overall parasite abundance of adult females was higher than that of adult males. Among the bats, reproductive females, particularly lactating females, exhibited a higher body condition and were generally most infested. The Penicillidia jenynsii and Nycteribia parvula bat flies showed a consistent female-biased infection pattern. The N. allotopa and Ascodipteron speiserianum flies, however, showed a tendency towards bats of a moderate to higher body condition, particularly reproductive females and adult males.</p><p><strong>Conclusions: </strong>We found an overall positive correlation between parasite abundance and reproductive state and body condition of the host and female-biased parasitism for M. fuliginosus bats. However, the effects of body condition and female-biased infestation appear to be parasite species specific, and suggest that the mobility, life history, and potential inter-species interactions of the parasites may all play important roles.</p>","PeriodicalId":55142,"journal":{"name":"Frontiers in Zoology","volume":"19 1","pages":"12"},"PeriodicalIF":2.6,"publicationDate":"2022-03-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8898463/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"65725000","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Guilherme Gainett, Audrey R Crawford, Benjamin C Klementz, Calvin So, Caitlin M Baker, Emily V W Setton, Prashant P Sharma
{"title":"Eggs to long-legs: embryonic staging of the harvestman Phalangium opilio (Opiliones), an emerging model arachnid.","authors":"Guilherme Gainett, Audrey R Crawford, Benjamin C Klementz, Calvin So, Caitlin M Baker, Emily V W Setton, Prashant P Sharma","doi":"10.1186/s12983-022-00454-z","DOIUrl":"10.1186/s12983-022-00454-z","url":null,"abstract":"<p><strong>Background: </strong>The comparative embryology of Chelicerata has greatly advanced in recent years with the integration of classical studies and genetics, prominently spearheaded by developmental genetic works in spiders. Nonetheless, the understanding of the evolution of development and polarization of embryological characters in Chelicerata is presently limited, as few non-spider species have been well studied. A promising focal species for chelicerate evo-devo is the daddy-long-legs (harvestman) Phalangium opilio, a member of the order Opiliones. Phalangium opilio, breeds prolifically and is easily accessible in many parts of the world, as well as tractable in a laboratory setting. Resources for this species include developmental transcriptomes, a draft genome, and protocols for RNA interference, but a modern staging system is critically missing for this emerging model system.</p><p><strong>Results: </strong>We present a staging system of P. opilio embryogenesis that spans the most important morphogenetic events with respect to segment formation, appendage elongation and head development. Using time-lapse imaging, confocal microscopy, colorimetric in situ hybridization, and immunohistochemistry, we tracked the development of synchronous clutches from egg laying to adulthood. We describe key events in segmentation, myogenesis, neurogenesis, and germ cell formation.</p><p><strong>Conclusion: </strong>Considering the phylogenetic position of Opiliones and the unduplicated condition of its genome (in contrast to groups like spiders and scorpions), this species is poised to serve as a linchpin for comparative studies in arthropod development and genome evolution. The staging system presented herein provides a valuable reference for P. opilio that we anticipate being useful to the arthropod evo-devo community, with the goal of revitalizing research in the comparative development of non-spider arachnids.</p>","PeriodicalId":55142,"journal":{"name":"Frontiers in Zoology","volume":"19 1","pages":"11"},"PeriodicalIF":2.6,"publicationDate":"2022-03-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8896363/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"65724954","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
A. Arct, S. Drobniak, A. Dubiec, R. Martyka, Joanna Sudyka, L. Gustafsson, M. Cichoń
{"title":"The interactive effect of ambient temperature and brood size manipulation on nestling body mass in blue tits: an exploratory analysis of a long-term study","authors":"A. Arct, S. Drobniak, A. Dubiec, R. Martyka, Joanna Sudyka, L. Gustafsson, M. Cichoń","doi":"10.1186/s12983-022-00456-x","DOIUrl":"https://doi.org/10.1186/s12983-022-00456-x","url":null,"abstract":"","PeriodicalId":55142,"journal":{"name":"Frontiers in Zoology","volume":"19 1","pages":""},"PeriodicalIF":2.8,"publicationDate":"2022-02-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"65724970","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Differential time allocation of foraging workers in the subterranean termite.","authors":"Sang-Bin Lee, Thomas Chouvenc, Nan-Yao Su","doi":"10.1186/s12983-021-00446-5","DOIUrl":"https://doi.org/10.1186/s12983-021-00446-5","url":null,"abstract":"<p><strong>Background: </strong>Foraging in group living animals such as social insects, is collectively performed by individuals. However, our understanding on foraging behavior of subterranean termites is extremely limited, as the process of foraging in the field is mostly concealed. Because of this limitation, foraging behaviors of subterranean termites were indirectly investigated in the laboratory through tunnel geometry analysis and observations on tunneling behaviors. In this study, we tracked subsets of foraging workers from juvenile colonies of Coptotermes formosanus (2-yr-old) to describe general foraging behavioral sequences and to find how foraging workers allocate time between the foraging site (food acquisition or processing) and non-foraging site (food transportation).</p><p><strong>Results: </strong>Once workers entered into the foraging site, they spent, on average, a significantly longer time at the foraging site than the non-foraging site. Our clustering analysis revealed two different types of foraging workers in the subterranean termite based on the duration of time they spent at the foraging site and their foraging frequency. After entering the foraging site, some workers (cluster 1) immediately initiated masticating wood fragments, which they transferred as food boluses to recipient workers at the foraging site. Conversely, the recipient workers (cluster 2) moved around after entering the foraging site and received food from donating workers.</p><p><strong>Conclusions: </strong>This study provides evidence of task specialization within foraging cohorts in subterranean termites.</p>","PeriodicalId":55142,"journal":{"name":"Frontiers in Zoology","volume":"18 1","pages":"61"},"PeriodicalIF":2.8,"publicationDate":"2021-12-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8670135/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39723097","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}