HeredityPub Date : 2024-08-02DOI: 10.1038/s41437-024-00711-3
Hui Zhen Tan, Phoebe Scherer, Katarina C. Stuart, Sarah Bailey, Kate D. Lee, Patricia Brekke, John G. Ewen, Annabel Whibley, Anna W. Santure
{"title":"A high-density linkage map reveals broad- and fine-scale sex differences in recombination in the hihi (stitchbird; Notiomystis cincta)","authors":"Hui Zhen Tan, Phoebe Scherer, Katarina C. Stuart, Sarah Bailey, Kate D. Lee, Patricia Brekke, John G. Ewen, Annabel Whibley, Anna W. Santure","doi":"10.1038/s41437-024-00711-3","DOIUrl":"10.1038/s41437-024-00711-3","url":null,"abstract":"Recombination, the process of DNA exchange between homologous chromosomes during meiosis, plays a major role in genomic diversity and evolutionary change. Variation in recombination rate is widespread despite recombination often being essential for progression of meiosis. One such variation is heterochiasmy, where recombination rates differ between sexes. Heterochiasmy has been observed across broad taxonomic groups, yet it remains an evolutionary enigma. We used Lep-MAP3, a pedigree-based software that is efficient in handling large datasets, to generate linkage maps for the hihi or stitchbird (Notiomystis cincta), utilising information from >36 K SNPs and 36 families. We constructed 29 linkage maps, including for the previously unscaffolded Z chromosome. The hihi is an endangered passerine endemic to Aotearoa New Zealand that is sexually dimorphic and exhibits high levels of sexual conflict, including sperm competition. Patterns in recombination in the hihi are consistent with those in other birds, including higher recombination rates in micro-chromosomes. Heterochiasmy in the hihi is male-biased, in line with predictions of the Haldane-Huxley rule, with the male linkage map being 15% longer. Micro-chromosomes exhibit heterochiasmy to a greater extent, contrary to that reported in other birds. At the intra-chromosomal level, heterochiasmy is higher nearer to chromosome ends and in gene-rich regions. Regions of extreme heterochiasmy are enriched for genes implicated in cell structure. This study adds an important contribution in assessing evolutionary theories of heterochiasmy and provides a framework for future studies investigating fine-scale heterochiasmy.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"133 4","pages":"262-275"},"PeriodicalIF":3.1,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41437-024-00711-3.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141878593","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}
{"title":"Secondary contact zone and genetic introgression in closely related haplodiploid social spider mites","authors":"Shota Konaka, Shun K. Hirota, Yukie Sato, Naoki Matsumoto, Yoshihisa Suyama, Yoshihiko Tsumura","doi":"10.1038/s41437-024-00708-y","DOIUrl":"10.1038/s41437-024-00708-y","url":null,"abstract":"How frequently hybridisation and gene flow occur in the contact zones of diverging taxa is important for understanding the speciation process. Stigmaeopsis sabelisi and Stigmaeopsis miscanthi high-aggression form (hereafter, S. miscanthi HG) are haplodiploid, social spider mites that infest the Chinese silver grass, Miscanthus sinensis. These two species are closely related and parapatrically distributed in Japan. In mountainous areas, S. sabelisi and S. miscanthi HG are often found in the highlands and lowlands, respectively, suggesting that they are in contact at intermediate altitudes. It is estimated that they diverged from their common ancestors distributed in subtropical regions (south of Japan) during the last glacial period, expanded their distribution into the Japanese Archipelago, and came to have such a parapatric distribution (secondary contact). As their reproductive isolation is strong but incomplete, hybridisation and genetic introgression are expected at their distributional boundaries. In this study, we investigated their spatial distribution patterns along the elevation on Mt. Amagi using male morphological differences, and investigated their hybridisation status using single-nucleotide polymorphisms by MIG-seq. We found their contact zone at altitudes of 150–430 m, suggesting that their contact zone is prevalent in the parapatric area, which is in line with a previous study. Interspecific mating was predicted based on the sex ratio in the contact zone. No obvious hybrids were found, but genetic introgression was detected although it was extremely low.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"133 4","pages":"227-237"},"PeriodicalIF":3.1,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141874669","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}
HeredityPub Date : 2024-08-02DOI: 10.1038/s41437-024-00712-2
Ivan Jakovlić, Tong Ye, Hong Zou, Fengyue Zhu, Yuying Shi, Yiwen Ma, Gui-Tang Wang, Wen-Xiang Li, Dong Zhang
{"title":"Drivers of interlineage variability in mitogenomic evolutionary rates in Platyhelminthes","authors":"Ivan Jakovlić, Tong Ye, Hong Zou, Fengyue Zhu, Yuying Shi, Yiwen Ma, Gui-Tang Wang, Wen-Xiang Li, Dong Zhang","doi":"10.1038/s41437-024-00712-2","DOIUrl":"10.1038/s41437-024-00712-2","url":null,"abstract":"Studies of forces driving interlineage variability in the evolutionary rates (both sequence and architecture) of mitochondrial genomes often produce contradictory results. Flatworms (Platyhelminthes) exhibit the fastest-evolving mitogenomic sequences among all bilaterian phyla. To test the effects of multiple factors previously associated with different aspects of mitogenomic evolution, we used mitogenomes of 223 flatworm species, phylogenetic multilevel regression models, and causal inference. Thermic host environment (endothermic vs. ectothermic) had nonsignificant impacts on both sequence evolution and mitogenomic size. Mitogenomic gene order rearrangements (GORR) were mostly positively correlated with mitogenomic size (R2 ≈ 20–30%). Longevity was not (negatively) correlated with sequence evolution in flatworms. The predominantly free-living “turbellaria” exhibited much shorter branches and faster-evolving mitogenomic architecture than parasitic Neodermata. As a result, “parasitism” had a strong explanatory power on the branch length variability (>90%), and there was a negative correlation between GORR and branch length. However, the stem branch of Neodermata comprised 63.6% of the total average branch length. This evolutionary period was also marked by a high rate of gene order rearrangements in the ancestral Neodermata. We discuss how this period of rapid evolution deep in the evolutionary history may have decoupled sequence evolution rates from longevity and GORR, and overestimated the explanatory power of “parasitism”. This study shows that impacts of variables often vary across lineages, and stresses the importance accounting for the episodic nature of evolutionary patterns in studies of mitogenomic evolution.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"133 4","pages":"276-286"},"PeriodicalIF":3.1,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41437-024-00712-2.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141878594","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}
HeredityPub Date : 2024-08-01DOI: 10.1038/s41437-024-00709-x
Dieu - Merci Assumani Angbonda, Crispin M. Ilunga-Mulala, Nils Bourland, Hans Beeckman, Faustin Boyemba, Hulda Hatakiwe, Jean Pierre Ngongo, Olivier J. Hardy
{"title":"Inbreeding depression affects the growth of seedlings of an African timber species with a mixed mating reproductive system, Pericopsis elata (Harms) Meeuwen","authors":"Dieu - Merci Assumani Angbonda, Crispin M. Ilunga-Mulala, Nils Bourland, Hans Beeckman, Faustin Boyemba, Hulda Hatakiwe, Jean Pierre Ngongo, Olivier J. Hardy","doi":"10.1038/s41437-024-00709-x","DOIUrl":"10.1038/s41437-024-00709-x","url":null,"abstract":"Selfing or mating between related individuals can lead to inbreeding depression (ID), which can influence the survival, growth and evolution of populations of tree species. As selective logging involves a decrease in the density of congeneric partners, it could lead to increasing biparental inbreeding or self-fertilization, exposing the population to higher ID. We assessed the influence of inbreeding on the growth of a commercial timber species, Pericopsis elata (Fabaceae), which produced about 54% of self-fertilized seedlings in a natural population of the Congo basin. We followed the survival and growth of 540 plants raised in a plantation along a gradient of plant density (0.07–15.9 plants per m2). Parentage analysis allowed us distinguishing selfed and outcrossed seedlings. The annual growth was higher for outcrossed than selfed plants, on average by 10.8% for diameter and 12.9% for height growth. Based on the difference in above ground biomass between selfed and outcrossed seedlings after 41 months, we estimated the level of ID at δ = 0.33, while a lifetime estimate of ID based on the proportions of selfed plants at seedling and adult stages led to δ = 0.7. The level of ID on growth rate did not change significantly with age but tended to vanish under high competition. Pericopsis elata is a particularly interesting model because inbreeding depression is partial, with about 26% of reproducing adults resulting from selfing, contrary to most tropical tree species where selfed individuals usually die before reaching adulthood. Hence, the risks of ID must be considered in the management and conservation of the species.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"133 4","pages":"238-248"},"PeriodicalIF":3.1,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41437-024-00709-x.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141870882","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}
HeredityPub Date : 2024-07-29DOI: 10.1038/s41437-024-00699-w
Marc-Alexander Gose, Emily Humble, Andrew Brownlow, Dave Wall, Emer Rogan, Guðjón Már Sigurðsson, Jeremy J. Kiszka, Charlotte Bie Thøstesen, Lonneke L. IJsseldijk, Mariel ten Doeschate, Nicholas J. Davison, Nils Øien, Rob Deaville, Ursula Siebert, Rob Ogden
{"title":"Correction: Population genomics of the white-beaked dolphin (Lagenorhynchus albirostris): implications for conservation amid climate-driven range shifts","authors":"Marc-Alexander Gose, Emily Humble, Andrew Brownlow, Dave Wall, Emer Rogan, Guðjón Már Sigurðsson, Jeremy J. Kiszka, Charlotte Bie Thøstesen, Lonneke L. IJsseldijk, Mariel ten Doeschate, Nicholas J. Davison, Nils Øien, Rob Deaville, Ursula Siebert, Rob Ogden","doi":"10.1038/s41437-024-00699-w","DOIUrl":"10.1038/s41437-024-00699-w","url":null,"abstract":"","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"133 3","pages":"206-206"},"PeriodicalIF":3.1,"publicationDate":"2024-07-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41437-024-00699-w.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141792333","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}
HeredityPub Date : 2024-07-24DOI: 10.1038/s41437-024-00706-0
Elizabeth Tapanes, Diana J. Rennison
{"title":"The genetic basis of divergent melanic pigmentation in benthic and limnetic threespine stickleback","authors":"Elizabeth Tapanes, Diana J. Rennison","doi":"10.1038/s41437-024-00706-0","DOIUrl":"10.1038/s41437-024-00706-0","url":null,"abstract":"Pigmentation is an excellent trait to examine patterns of evolutionary change because it is often under natural selection. Benthic and limnetic threespine stickleback (Gasterosteus aculeatus) exhibit distinct pigmentation phenotypes, likely an adaptation to occupation of divergent niches. The genetic architecture of pigmentation in vertebrates appears to be complex. Prior QTL mapping of threespine stickleback pigmentation phenotypes has identified several candidate loci. However—relative to other morphological phenotypes (e.g., spines or lateral plates)—the genetic architecture of threespine stickleback pigmentation remains understudied. Here, we performed QTL mapping for two melanic pigmentation traits (melanophore density and lateral barring) using benthic-limnetic F2 crosses. The two traits mapped to different chromosomes, suggesting a distinct genetic basis. The resulting QTLs were additive, but explained a relatively small fraction of the total variance (~6%). QTLs maps differed by F1 family, suggesting variation in genetic architecture or ability to detect loci of small effect. Functional analysis identified enriched pathways for candidate loci. Several of the resulting candidate loci for pigmentation, including three loci in enriched pathways (bco1, sulf1, and tyms) have been previously indicated to affect pigmentation in other vertebrates. These findings add to a growing body of evidence suggesting pigmentation is often polygenic.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"133 4","pages":"207-215"},"PeriodicalIF":3.1,"publicationDate":"2024-07-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41437-024-00706-0.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141758404","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}
HeredityPub Date : 2024-07-22DOI: 10.1038/s41437-024-00707-z
Fernando H. S. Souza, Manolo F. Perez, Pedro H. N. Ferreira, Luiz A. C. Bertollo, Tariq Ezaz, Deborah Charlesworth, Marcelo B. Cioffi
{"title":"Multiple karyotype differences between populations of the Hoplias malabaricus (Teleostei; Characiformes), a species complex in the gray area of the speciation process","authors":"Fernando H. S. Souza, Manolo F. Perez, Pedro H. N. Ferreira, Luiz A. C. Bertollo, Tariq Ezaz, Deborah Charlesworth, Marcelo B. Cioffi","doi":"10.1038/s41437-024-00707-z","DOIUrl":"10.1038/s41437-024-00707-z","url":null,"abstract":"Neotropical fishes exhibit remarkable karyotype diversity, whose evolution is poorly understood. Here, we studied genetic differences in 60 individuals, from 11 localities of one species, the wolf fish Hoplias malabaricus, from populations that include six different “karyomorphs”. These differ in Y-X chromosome differentiation, and, in several cases, by fusions with autosomes that have resulted in multiple sex chromosomes. Other differences are also observed in diploid chromosome numbers and morphologies. In an attempt to start understanding how this diversity was generated, we analyzed within- and between-population differences in a genome-wide sequence data set. We detect clear genotype differences between karyomorphs. Even in sympatry, samples with different karyomorphs differ more in sequence than samples from allopatric populations of the same karyomorph, suggesting that they represent populations that are to some degree reproductively isolated. However, sequence divergence between populations with different karyomorphs is remarkably low, suggesting that chromosome rearrangements may have evolved during a brief evolutionary time. We suggest that the karyotypic differences probably evolved in allopatry, in small populations that would have allowed rapid fixation of rearrangements, and that they became sympatric after their differentiation. Further studies are needed to test whether the karyotype differences contribute to reproductive isolation detected between some H. malabaricus karyomorphs.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"133 4","pages":"216-226"},"PeriodicalIF":3.1,"publicationDate":"2024-07-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141748029","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}
HeredityPub Date : 2024-07-12DOI: 10.1038/s41437-024-00703-3
Cleiton A. Wartha, Aaron J. Lorenz
{"title":"Genomic predictions of genetic variances and correlations among traits for breeding crosses in soybean","authors":"Cleiton A. Wartha, Aaron J. Lorenz","doi":"10.1038/s41437-024-00703-3","DOIUrl":"10.1038/s41437-024-00703-3","url":null,"abstract":"Parental selection is perhaps the most critical decision a breeder makes, establishing the foundation of the entire program for years to come. Cross selection based on predicted mean and genetic variance can be further expanded to multiple-trait improvement by predicting the genetic correlation ( $${r}_{G}$$ ) between pairs of traits. Our objective was to empirically assess the ability to predict the family mean, genetic variance, superior progeny mean and genetic correlation through genomic prediction in a soybean population. Data made available through the Soybean Nested Association Mapping project included phenotypic data on seven traits (days to maturity, lodging, oil, plant height, protein, seed size, and seed yield) for 39 families. Training population composition followed a leave-one-family-out cross-validation scheme, with the validation family genetic parameters predicted using the remaining families as the training set. The predictive abilities for family mean and superior progeny mean were significant for all traits while predictive ability of genetic variance was significant for four traits. We were able to validate significant predictive abilities of $${r}_{G}$$ for 18 out of 21 (86%) pairwise trait combinations (P < 0.05). The findings from this study support the use of genome-wide marker effects for predicting $${r}_{G}$$ in soybean biparental crosses. If successfully implemented in breeding programs, this methodology could help to increase the rate of genetic gain for multiple correlated traits.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"133 3","pages":"173-185"},"PeriodicalIF":3.1,"publicationDate":"2024-07-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41437-024-00703-3.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141599259","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}
HeredityPub Date : 2024-07-09DOI: 10.1038/s41437-024-00705-1
Cris L. Wijnen, Ramon Botet, José van de Belt, Laurens Deurhof, Hans de Jong, C. Bastiaan de Snoo, Rob Dirks, Martin P. Boer, Fred A. van Eeuwijk, Erik Wijnker, Joost J. B. Keurentjes
{"title":"A complete chromosome substitution mapping panel reveals genome-wide epistasis in Arabidopsis","authors":"Cris L. Wijnen, Ramon Botet, José van de Belt, Laurens Deurhof, Hans de Jong, C. Bastiaan de Snoo, Rob Dirks, Martin P. Boer, Fred A. van Eeuwijk, Erik Wijnker, Joost J. B. Keurentjes","doi":"10.1038/s41437-024-00705-1","DOIUrl":"10.1038/s41437-024-00705-1","url":null,"abstract":"Chromosome substitution lines (CSLs) are tentatively supreme resources to investigate non-allelic genetic interactions. However, the difficulty of generating such lines in most species largely yielded imperfect CSL panels, prohibiting a systematic dissection of epistasis. Here, we present the development and use of a unique and complete panel of CSLs in Arabidopsis thaliana, allowing the full factorial analysis of epistatic interactions. A first comparison of reciprocal single chromosome substitutions revealed a dependency of QTL detection on different genetic backgrounds. The subsequent analysis of the complete panel of CSLs enabled the mapping of the genetic interactors and identified multiple two- and three-way interactions for different traits. Some of the detected epistatic effects were as large as any observed main effect, illustrating the impact of epistasis on quantitative trait variation. We, therefore, have demonstrated the high power of detection and mapping of genome-wide epistasis, confirming the assumed supremacy of comprehensive CSL sets. Development of a complete panel of chromosome substitution lines enables high power mapping of epistatic interactions in Arabidopsis thaliana.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"133 3","pages":"198-205"},"PeriodicalIF":3.1,"publicationDate":"2024-07-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41437-024-00705-1.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141563298","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}
HeredityPub Date : 2024-07-05DOI: 10.1038/s41437-024-00704-2
Joseph J. Dubie, Vaishali Katju, Ulfar Bergthorsson
{"title":"Dissecting the sequential evolution of a selfish mitochondrial genome in Caenorhabditis elegans","authors":"Joseph J. Dubie, Vaishali Katju, Ulfar Bergthorsson","doi":"10.1038/s41437-024-00704-2","DOIUrl":"10.1038/s41437-024-00704-2","url":null,"abstract":"Mitochondrial genomes exist in a nested hierarchy of populations where mitochondrial variants are subject to genetic drift and selection at each level of organization, sometimes engendering conflict between different levels of selection, and between the nuclear and mitochondrial genomes. Deletion mutants in the Caenorhabditis elegans mitochondrial genome can reach high intracellular frequencies despite strongly detrimental effects on fitness. During a mutation accumulation (MA) experiment in C. elegans, a 499 bp deletion in ctb-1 rose to 90% frequency within cells while significantly reducing fitness. During the experiment, the deletion-bearing mtDNA acquired three additional mutations in nd5, namely two single insertion frameshift mutations in a homopolymeric run, and a base substitution. Despite an additional fitness cost of these secondary mutations, all deletion-bearing molecules contained the nd5 mutations at the termination of the MA experiment. The presence of mutant mtDNA was associated with increased mtDNA copy-number. Variation in mtDNA copy-number was greater in the MA lines than in a wildtype nuclear background, including a severe reduction in copy-number at one generational timepoint. Evolutionary replay experiments using different generations of the MA experiment as starting points suggests that two of the secondary mutations contribute to the proliferation of the original ctb-1 deletion by unknown mechanisms.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"133 3","pages":"186-197"},"PeriodicalIF":3.1,"publicationDate":"2024-07-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41437-024-00704-2.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141537841","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}