Genomic insights into the chromosomal elongation in a family of Collembola.

Collembola is a highly diverse and abundant group of soil arthropods with chromosome numbers ranging from 5 to 11. Previous karyotype studies indicated that the Tomoceridae family possesses an exceptionally long chromosome. To better understand chromosome size evolution in Collembola, we obtained a chromosome-level genome of Yoshiicerus persimilis with a size of 334.44 Mb and BUSCO completeness of 97.0% (n = 1013). Both genomes of Y. persimilis and Tomocerus qinae (recently published) have an exceptionally large chromosome (ElChr greater than 100 Mb), accounting for nearly one-third of the genome. Comparative genomic analyses suggest that chromosomal elongation occurred independently in the two species approximately 10 million years ago, rather than in the ancestor of the Tomoceridae family. The ElChr elongation was caused by large tandem and segmental duplications, as well as transposon proliferation, with genes in these regions experiencing weaker purifying selection (higher dN/dS) than conserved regions. Moreover, inter-genomic synteny analyses indicated that chromosomal fission/fusion events played a crucial role in the evolution of chromosome numbers (ranging from 5 to 7) within Entomobryomorpha. This study provides a valuable resource for investigating the chromosome evolution of Collembola.

Chromosomal-Level Genome Assembly of the Springtail Tomocerus qinae (Collembola: Tomoceridae).

The family Tomoceridae is among the earliest derived collembolan lineages, thus is of key importance in understanding the evolution of Collembola. Here, we assembled a chromosome-level genome of one tomocerid species Tomocerus qinae by combining Nanopore long reads and Hi-C data. The final genome size was 334.44 Mb with the scaffold/contig N50 length of 71.85/13.94 Mb. BUSCO assessment indicated that 96.80% of complete arthropod universal single-copy orthologs (n = 1,013) were present in the assembly. The repeat elements accounted for 26.11% (87.26 Mb) and 494 noncoding RNAs were identified in the genome. A total of 20,451 protein-coding genes were predicted, which captured 96.0% (973) BUSCO genes. Gene family evolution analyses identified 4,825 expanded gene families of T. qinae, among them, 47 experienced significant expansions, and these significantly expanded gene families mainly involved in proliferation and growth. This study provides an important genomic resource for future evolution and comparative genomics analyses of Collembola.

Multikingdom interactions govern the microbiome in subterranean cultural heritage sites.

SignificanceThe conservation of historical relics against microbial biodeterioration is critical to preserving cultural heritages. One major challenge is our limited understanding of microorganisms' dispersal, colonization, and persistence on relics after excavation and opening to external environments. Here, we investigate the ecological and physiological profiles of the microbiome within and outside the Dahuting Han Dynasty Tomb with a 1,800-y history. Actinobacteria dominate the microbiome in this tomb. Via interkingdom signaling mutualism, springtails carry Actinobacteria as one possible source into the tomb from surrounding environments. Subsequently, Actinobacteria produce cellulases combined with antimicrobial substances, which helps them to colonize and thrive in the tomb via intrakingdom competition. Our findings unravel the ecology of the microbiomes colonizing historical relics and provide help for conservation practices.

Phylogenomics of Elongate-Bodied Springtails Reveals Independent Transitions from Aboveground to Belowground Habitats in Deep Time.

Soil has become a major hotspot of biodiversity studies, yet the pattern and timing of the evolution of soil organisms are poorly known because of the scarcity of paleontological data. To overcome this limitation, we conducted a genome-based macroevolutionary study of an ancient, diversified, and widespread lineage of soil fauna, the elongate-bodied springtails (class Collembola, order Entomobryomorpha). To build the first robust backbone phylogeny of this previously refractory group, we sampled representatives of major higher taxa (6 out of 8 families, 11 out of 16 subfamilies) of the order with an emphasis on the most problematic superfamily Tomoceroidea, applied whole-genome sequencing methods, and compared the performance of different combinations of data sets (universal single-copy orthologs [USCO] vs. ultraconserved elements]) and modeling schemes. The fossil-calibrated timetree was used to reconstruct the evolution of body size, sensory organs, and pigmentation to establish a time frame of the ecomorphological divergences. The resultant trees based on different analyses were congruent in most nodes. Several discordant nodes were carefully evaluated by considering method fitness, morphological information, and topology test. The evaluation favored the well-resolved topology from analyses using USCO amino acid matrices and complex site-heterogeneous models (CAT$+$GTR and LG$+$PMSF (C60)). The preferred topology supports the monophyletic superfamily Tomoceroidea as an early-diverging lineage and a sister relationship between Entomobryoidea and Isotomoidea. The family Tomoceridae was recovered as monophyletic, whereas Oncopoduridae was recovered as paraphyletic, with Harlomillsia as a sister to Tomoceridae and hence deserving a separate family status as Harlomillsiidae Yu and Zhang fam. n. Ancestral Entomobryomorpha were reconstructed as surface-living, supporting independent origins of soil-living groups across the Paleozoic-Mesozoic, and highlighting the ancient evolutionary interaction between aboveground and belowground fauna. [Collembola; phylogenomics; soil-living adaptation; whole-genome sequencing.].

Molecular phylogeny and trait evolution in an ancient terrestrial arthropod lineage: Systematic revision and implications for ecological divergence (Collembola, Tomocerinae).

Phylogenetic assessments of functional traits are important for mechanistically understanding the interactions between organisms and environments, but such practices are strongly limited by the availability of phylogenetic frameworks. The tomocerin springtails are an ancient, widespread and ecologically important group of terrestrial arthropods, whereas their phylogeny and trait evolution remained unaddressed. In the present study, we conducted the first comprehensive phylogenetic reconstruction of Tomocerinae, based on a multi-loci molecular dataset covering all major lineages within the subfamily, using Bayesian inference (BI), maximum-likelihood (ML) and maximum-parsimony (MP) approaches. Divergence time was estimated and ancestral character state reconstruction (ACSR) was performed to trace the evolutionary history of five ecomorphological traits correlated with sensory and locomotory functions. Our results support the monophyly of Tomocerinae, and indicate that current classification of Tomocerinae only partially reflects evolutionary relationships, notably the commonest and speciose genus Tomocerus is polyphyletic. The subfamily probably originated in Early Cretaceous and diversified in two Cretaceous and one Eocene radiation events. As indicated by the evolutionary patterns of functional traits, multiple ecological divergences took place during the diversification of Tomocerinae. The study suggests a potential underestimation of ecological divergence and functional diversity in terrestrial arthropods, calls for an update of present trait databases, and demonstrates the value of macroevolutionary knowledge for improving the trait-based ecology. In addition, Tomocerus, Tomocerina and Tritomurus are redefined, a new genus Yoshiicerusgen. n. and new subgenera Coloratomurussubgen. n., Ciliatomurussubgen. n., Striatomurussubgen. n. and Ocreatomurussubgen. n. are described in the appendix.

Phylomitogenomic analyses on collembolan higher taxa with enhanced taxon sampling and discussion on method selection.

Collembola are a basal group of Hexapoda renowned for both unique morphological characters and significant ecological roles. However, a robust and plausible phylogenetic relationship between its deeply divergent lineages has yet to be achieved. We carried out a mitophylogenomic study based on a so far the most comprehensive mitochondrial genome dataset. Our data matrix contained mitogenomes of 31 species from almost all major families of all four orders, with 16 mitogenomes newly sequenced and annotated. We compared the linear arrangements of genes along mitochondria across species. Then we conducted 13 analyses each under a different combination of character coding, partitioning scheme and heterotachy models, and assessed their performance in phylogenetic inference. Several hypothetical tree topologies were also tested. Mitogenomic structure comparison revealed that most species share the same gene order of putative ancestral pancrustacean pattern, while seven species from Onychiuridae, Poduridae and Symphypleona bear different levels of gene rearrangements, indicating phylogenetic signals. Tomoceroidea was robustly recovered for the first time in the presence of all its families and subfamilies. Monophyly of Onychiuroidea was supported using unpartitioned models alleviating LBA. Paronellidae was revealed polyphyletic with two subfamilies inserted independently into Entomobryidae. Although Entomobryomorpha has not been well supported, more than half of the analyses obtained convincing topologies by placing Tomoceroidea within or near remaining Entomobryomorpha. The relationship between elongate-shaped and spherical-shaped collembolans still remained ambiguous, but Neelipleona tend to occupy the basal position in most trees. This study showed that mitochondrial genomes could provide important information for reconstructing the relationships among Collembola when suitable analytical approaches are implemented. Of all the data refining and model selecting schemes used in this study, the combination of nucleotide sequences, partitioning model and exclusion of third codon positions performed better in generating more reliable tree topology and higher node supports than others.

Molecular phylogeny of Entomobrya (Collembola: Entomobryidae) from China: Color pattern groups and multiple origins.

Highly diversified colorations among springtails (Collembola) have been widely used for species diagnosis, but their phylogenetic significance is poorly known. We addressed this issue in the largest Entomobryinae genus Entomobrya, which possesses variable color patterns among species. The relationships within the genus and to other genera have also rarely been studied. Based on material mainly from China, we have conducted a multilocus phylogeny and topology tests with likelihood and Bayesian algorithms, and accordingly demonstrated the non-monophyly of Chinese Entomobrya. The division of five clades, including Entomobrya and several related genera, coincided well with five types of colorations, respectively. Further analyses of divergence time and historical biogeography revealed that Chinese Entomobrya originated mainly from Palearctic (northern and western) China in the Paleocene and Eocene. This study highlights the great phylogenetic values as well as taxonomic uses of coloration in Chinese Entomobrya. Multiple phylogenetic and biogeographic origins of Entomobrya imply its complicated relationships with both scaled and unscaled genera of Entomobryinae.

Three new species of Tomocerus from tropical zone of China (Collembola, Tomoceridae).

Tomocerids are world-widely distributed, but were seldom reported from tropics. In the present paper, three new species of Tomocerus Nicolet are described from Hainan and Yunnan Provinces, tropical zone of China. All three species have compound-type dental spines and belong to Tomocerus ocreatus species-group. Tomocerus tropicus sp. nov. resembles Tomocerus pseudocreatus Yu, but differs from the latter in mesothoracic macrochaetotaxy, manubrial dorsal scales and denticles on the dental spines. Tomocerus nan sp. nov. resembles Tomocerus virgatus Yu, but differs from the latter in colour pattern, cephalic dorsal macrochaetotaxy, manubrial dorsal scales and denticles on the dental spines. Tomocerus nabanensis sp. nov. resembles T. postantennalis Yu, Zhang Deharveng, Tomocerus dong Yu Li and Tomocerus deharvengi Yu Li, but differs from the three species in PAO, cephalic and tergal dorsal macrochaetotaxy and tenent hairs. Our studies including the present work indicate the importance of future survey on Tomocerinae in and near tropics where diversity of this group was historically underestimated.

Two new species of Tomocerus ocreatus group with a single large distal dental spine (Collembola, Tomoceridae).

Most members of Tomocerus ocreatus group have two distal large spines on dens, so far, only Tomocerus spinulus Chen Christiansen, 1998 and Tomocerus leyensis Yu Deharveng, 2018 have been described with only one distal large spine and are thus exceptional in this group. In the present paper, we report two other species with the same form. The two new species resemble T. spinulus in chaetotaxy, dental spine formula and general shape of the dental spines, but differ from it in several other characters, including position and shape of the prominent dorsal chaetae on the manubrium and dens. Also, T. pseudospinulus sp. nov. differs from T. spinulus in having larger denticles on the dental spines, and T. paraspinulus sp. nov. differs from T. spinulus in having longer antenna and more chaetae on the tenaculum. The two new species are similar, but can be distinguished by length of the antenna, number of the chaetae on tenaculum, status of the prominent manubrial dorsal chaetae and fine sculpture of the dental spines. Distances of COI mtDNA also support the validation of two new species. A key to species of T. ocreatus species-group with single large dental spine is provided.

Two new Chinese species of Tomocerus at different stages of troglomorphic adaptation (Collembola, Tomoceridae).

Two new species of Tomocerus are described from caves in Guizhou and Guangxi Province, China. Tomocerus troglodytes sp. nov. is highly troglomorphic. It belongs to the kinoshitai complex, and is most similar to another eyeless and colourless species Tomocerus caecus, from which it differs as it has longer antennae; 2,2/2,2/2+2/0 versus 2,2/2,5/0/0 cephalic dorsal chaetotaxy formula; 6 versus 4 central macrochaetae on Th. II; 0 versus 2 ungual teeth; unguis devoid of baso-internal ridges; 3-5/3-5, I, 0-1, I versus 4-5/1-2,I-II,0-1,I-II dental spines formula; 2-4 versus 1 tenacular chaetae; and 0 versus 1 mucronal intermediate teeth. In contrast, Tomocerus leyensis sp. nov. is at an earlier stage of troglomorphic adaptation. It resembles several cave-dwelling species of the ocreatus complex in habitus and shape of dental spines, but differs in the following characters: absence of large postantennal organ; cephalic dorsal chaetotaxy formula 2/2,4/2+2/2+2 versus other patterns; larger number of ungual teeth; and only 1 large distal dental spine. The troglomorphic characteristics of the two species are discussed with emphasis on their potential adaptation to cave habitats.

Revision of Tomocerus similis Chen & Ma, with discussion of the kinoshitai complex and the distal tibiotarsal chaetae in Tomocerinae (Collembola, Tomoceridae).

Molecular analysis and a detailed morphological comparison revealed that Tomocerus similis Chen & Ma was described from individuals belonging to several species from several localities. Based on both old and new material from Anhui and Jiangsu Provinces, China, T. similis is redescribed and two new species are described. The three species are morphologically similar. Tomocerus persimilis sp. nov. differs from the others by the presence of central macrochaeta on head and of several distinct distal inner teeth on unguis. Tomocerus dissimilis sp. nov. is characterised by pointed tenent hairs on anterior legs. Remarks are made on the systematics and ecology of the kinoshitai complex, and on the taxonomic value of tenent hair and its adjacent chaetae.

New troglomorphic species of Tomocerus with well-developed postantennal organs (Collembola: Tomoceridae).

Three new troglobitic species of Tomocerus are described from the southwestern karsts of China. All of them have well developed postantennal organs. Tomocerus dong sp. nov. is similar to Tomocerus postantennalis Yu, Zhang & Deharveng and Tomocerus deharvengi sp. nov., but is different from them mainly in the number of prelabral chaetae and the dorsal body chaetotaxy. T. deharvengi sp. nov. is very similar to T. postantennalis but differs from the latter in the cephalic chaetotaxy, the number of manubrial pseudopores and the number of dental spines. T. cthulhu sp. nov. is peculiar for the multi-furcated vesicles of ventral tube, and is different from the three aforementioned species mainly in the dorsal body chaetotaxy. The position of the new species and the relationships between them are discussed.

Two new species of Tomocerus ocreatus complex (Collembola, Tomoceridae) from Nanjing, China.

Two new species of Tomocerus Nicolet, 1842 are described from Nanjing, China. Tomocerus qinae sp. nov. is similar to the Vietnamese species Tomocerus ocreatus, but is different from the latter mainly in the colour pattern, the length of antennae, and the pattern of ungual teeth. Tomocerus qixiaensis sp. nov. is similar to Tomocerus ocreatus and Tomocerus qinae sp. nov., but can be distinguished from them by the short antennae and the blunt prominent macrochaetae on manubrium and dens. DNA barcode sequences of the new species are provided.

New cave-dwelling species of Tomoceridae from China, with a study on the pattern of mesothoracic bothriotricha in Tomocerinae (Collembola, Entomobryomorpha).

Two new troglobitic species of Tomoceridae are described from Guizhou and Guangxi provinces, China. Tomocerus tiani sp. n. resembles Tomocerus kinoshitai Yosii, 1954, Tomocerus caecus Yu & Deharveng, 2015 and Tomocerus similis Chen & Ma, 1997 but differs from them mainly in the body colour, the cephalic chaetotaxy and the number of manubrial pseudopores. Monodontocerus cinereus sp. n. is similar to Monodontocerus mulunensis Yu, Deharveng & Zhang, 2014 but is different from the latter in the body colour, the length of antennae, the number of ungual teeth and the chaetotaxy on Abd. III and Abd. IV. Special remarks are made on the mesothoracic bothriotricha in Tomocerinae.

Molecular phylogeny supports S-chaetae as a key character better than jumping organs and body scales in classification of Entomobryoidea (Collembola).

The jumping organ (furcula) is the most characteristic structure among collembolans, and it is of great taxonomical values at higher levels. The largest superfamily Entomobryoidea is traditionally classified into four families only by the morphology of the furcula. Actually, many taxa among these families are strikingly similar in morphology without considering furcula. The phylogeny of Entomobryoidea was reconstructed here based on mitochondrial and ribosomal fragments. This indicated that both Paronellidae and Cyphoderidae were ingroups within Entomobryidae with the former polyphyletic. Topology tests, which used the likelihood and Bayesian approaches, also rejected the traditional hypotheses relying on furcula morphology. Further ancestral state reconstructions have revealed that traditional taxonomical characters, i.e., furcula and body scales, had multiple independent origins in Entomobryoidea whereas tergal specialized chaetae (S-chaetae) exhibited strong phylogenetic signals. By integrating both molecular and morphological evidence, the results of this study drastically undermine the present classification of Entomobryoidea. Tergal S-chaetotaxic pattern in combination with other characters are more reasonable in taxonomy at suprageneric levels than convergent furcula. This study provides new insights of the jumping organ, which could be adaptively modified during evolution of Collembola.

The first eyeless species of Tomocerus from China (Collembola, Tomoceridae) with notes on genera Tomocerus and Pogonognathellus.

A new cave tomocerid from Guangxi Zhuang Autonomous Region, South China is described. Tomocerus caecus sp. nov. is characterized by the absence of ocelli, the absence of posterior macrochaetae on head and the reduced number of teeth on unguis and mucro. The generic position of the new species is discussed. Tomocerus caecus sp. nov. is similar to the East Asian species Tomocerus kinoshitai Yosii, 1954 and Tomocerus similis Chen & Ma, 1997 mainly in the shape of dental spines and the small number of teeth on unguis and mucro, but different from the latters in the absence of ocelli and pigment. The differences between the genera Tomocerus Nicolet, 1842 and Pogonognathellus (Börner, 1908) are discussed with a special focus on the work of Massoud & Ellis (1974) that was long ignored by collembologists. 

A peculiar cave species of Tomocerus (Collembola, Tomoceridae, Tomocerinae) from Vietnam, with a discussion of the postantennal organ and prelabral chaetae in Tomocerinae.

The first Tomocerus species with a postantennal organ (PAO) in the adult stage is described from Vietnam. Tomocerus postantennalis sp. n. differs from the other PAO-possessing tomocerid, Tomolonus reductus Mills, 1948, mainly in the morphology of PAO, the number of ocelli, the number of chaetae in trochantero-femoral organ and several features of the furca. The new species is placed in Tomocerus because of the presence of a toothlet on the outer basal mucronal tooth and the absence of the diagnostic character states of Plutomurus Yosii, 1956 and Aphaenomurus Yosii, 1956. Besides the presence of PAO, the new species is peculiar in having six prelabral chaetae, instead of four as in other Tomocerus species. The new species is similar to Tomocerus folsomi Denis, 1929 and Tomocerus ocreatus Denis, 1948 in the type of dental spines but different from them in the body colour, the relative length of antennae to body, the number of unguis inner teeth and the number of mucronal intermediate teeth.

New species of Monodontocerus (Collembola: Tomoceridae) from southern China with diagnostic notes on the genus and introduction of new taxonomic characters.

Three new species of Monodontocerus are described from caves in southern China: M. absens sp. nov. is characterized by its cephalic chaetotaxy and the absence of chaetae from the tenaculum; M. mulunensis sp. nov. is characterized by a combination of characters including chaetotaxy, foot complex and furca; M. trigrandis sp. nov. is different from other species in the formula of dental spines and the reduction of the ungual teeth. A key to the species of Monodontocerus is provided. Potential diagnostic characters for this genus are proposed. Troglomorphy and interspecific variability are discussed. Pseudopores and the dorsal disto-lateral chaeta on the manubrium are introduced as new taxonomic characters for Tomocerinae. 

[A study on the interpolation algorithm for the serial-parallel robot-controlled HIFU].

According to the hardware characters of the high intensive focused ultrasound (HIFU) serial-parallel robots, this paper presents an algorithm of 2-grade interpolation scheme which includes the rough and fine interpolations. Both pre-acceleration and post-acceleration are employed to meet the restrictive requirements of coordinated dynamic performance and the detailed procedure of the interpolation algorithm is given too.