AbstractPalm houses in Europe serve as urban biodiversity hot spots for alien spiders. As a result of several years of research in the Poznań Palm House, we documented the occurrence of 14 spider species, 9 of which were alien to Europe: Coleosoma floridanum, Hasarius adansoni, Howaia mogera, Ostearius melanopygius, Parasteatoda tabulata, Parasteatoda tepidariorum, Scytodes fusca, Spermophora kerinci and Triaeris stenaspis. The most abundant species was C. floridanum (39.9%). Three spider species were recorded for the first time in Poland: C. floridanum, S. fusca and S. kerinci. We studied the occurrence of endosymbiotic Wolbachia and Cardinium in parthenogenetic T. stenaspis and recorded for the first time the occurrence of Wolbachia in this spider. The endosymbiont was characterized based on the sequences of six bacterial housekeeping genes: 16S rRNA, coxA, fbpA, ftsZ, gatB and hcpA. Our phylogenetic reconstruction of Wolbachia supergroups revealed that the bacteria recovered from the spider formed distinct lineages in relation to all known supergroups. We assigned it to a novel supergroup X with unique sequences within the 16S rRNA and ftsZ genes. We discussed faunistic results in terms of long-term survival rates and the risk of invasion of alien species of spiders.
IntroductionSpiders disperse actively on land through their own locomotor abilities, passively in the air through air currents (ballooning)1,2 and with human involvement (anthropodispersal)3. They are among the first colonizers capable of finding suitable niches for settlement in a foreign environment. This ability makes introduced species potential invaders to local faunas2,3,4,5,6,7,8,9. Over the last 200 years, many alien species have been recorded in Europe, and some of them have become established3,8,10,11. They often arrive in Europe with global trade products10, predominantly with imported fruits and plants11. Spiders of tropical origin introduced to Europe, due to their preferences for high temperatures and humidity, usually find suitable places to settle and develop stable populations in palm houses and botanical gardens7,12,13,14,15,16,17,18,19. Such locations offer similar living conditions to those in the subtropics and tropics, turning them into unique urban ecological islands and hot spots of biodiversity for alien invaders20.Studies on alien invertebrates in the Poznań Palm House have been conducted extensively in the past20,21,22,23,24,25,26. Several alien species of arachnids have been documented, including those belonging to Acari27,28,29,30,31 and Schizomida32. Initial research on spiders was conducted by Woźniczko33 as part of her master’s thesis, but the results were never officially presented except the information on the occurrence of the jumping spider Hasarius adansoni (Audouin, 1826)34,35.Colonization of distant habitats far from the parental distribution range is much more intense and successful when invaders exhibit a parthenogenetic type of reproduction and have high ecological tolerance36,37,38,39. Parthenogenesis can be induced by bacterial endosymbionts, such as Wolbachia (phylum Pseudomonadota, class Alfaproteobacteria, order Rickettsiales, family Ehrlichiaceae) and Cardinium (phylum Bacteroidota, class Sphingobacteriia, order Sphingobacteriales, not assigned to family). Wolbachia is considered one of the most common bacterial endosymbiont among arthropods40,41. The associations between the microorganism and the host can take various forms, including changes induced by Wolbachia in the proportion of females and males in the invertebrate population. Wolbachia can induce several reproductive phenotypes in their hosts, including feminization, resulting in death of embryonic males42, or the conversion of genetic males into functional phenotypic females43. The bacteria can also lead to cytoplasmic incompatibility, which occurs after mating between males infected with certain bacterial strains and females either uninfected or infected with an incompatible bacterial strain. The consequence is embryonic death44. Wolbachia may also be the causative agent of parthenogenesis41,45 in host species by modifying mitosis or meiosis46.On the basis of the phylogeny of housekeeping genes or whole-genome typing methods, the genus Wolbachia has been divided into 21 supergroups (A-W). An examplary set of genes comprises 16S rRNA, coxA—coding for cytochrome c oxidase, gatB—coding for glutamyl-tRNA(Gln) amidotransferase, hcpA—coding for conserved hypothetical protein, ftsZ—coding for prokaryotic cell division protein and fbpA—coding for fructose-bisphosphate aldolase47,48,49.Although reproduction by parthenogenesis could offer advantages for the colonization of new environments by introduced species, it is a rare phenomenon in spiders. In most cases, it has been discussed speculatively rather than confirmed with results50,51,52,53,54,55,56. The only reliable studies were performed by Korenko et al.36, who studied a population of Triaeris stenaspis Simon, 1892, and Lake57, who maintained an immature female of the huntsman spider Isopoda insignis Simon, 1897 (currently included in the genus Holconia58). Both studies were conducted under laboratory conditions. It is known that no males of T. stenaspis have been collected together with females36,59. Although T. stenaspis reproduces by thelytokous parthenogenesis, the occurrence of endosymbiotic bacteria like Wolbachia or Cardinium, which could manipulate the sex ratio towards a lack of males and induce parthenogenesis, has not been confirmed36. This species is found in some tropical and subtropical areas of the world59 and has been introduced into Europe with cultivated pot plants60. Its presence has been observed exclusively in palm houses11,61. T. stenaspis has so far been reported from the aforementioned locations in Austria62, Czech Republic61, Finland15, Germany7,16, Hungary63, Ireland64, the Netherlands65, Poland60,66, Slovakia67,68, Switzerland65,69 and United Kingdom64. Some sites of occurrence (Danmark, France) were obtained from national checklists of spiders published online70,71.The primary objective of our study was to analyze the spider species composition, including the proportion of alien species inhabiting the Poznań Palm House. Additionally, we aimed to study the occurrence of Wolbachia and its genetic variability in T. stenaspis, as it may manipulate the spider’s reproduction towards parthenogenesis as an adaptation for survival in isolated conditions. Furthermore, we performed a phylogenetic analysis of Wolbachia to explore its relationships with other endosymbiont strains belonging to existing supergroups.Materials and methodsStudy sitesThe Poznań Palm House, established in 1911, serves as an educational and exhibition facility. It is the largest palm house in Poland and one of the largest in Europe. Comprising 12 pavilions, the facility showcases vegetation representative of subtropical climate (pavilion I), temperate climate (pavilions II and III), succulents of America (pavilion IV), vegetation of the tropics (pavilions V and VI), aquatic vegetation (pavilion VII), tropical forest undergrowth (pavilion VIII) and xerophytic vegetation and savannas (pavilion IX)72.Study materialSpiders were collected in 2013 (29/10 and 25/11), 2014 (17/11), 2015 (02/03, 20/04, 02/11, 17/11 and 14/12), 2016 (06/04), 2023 (13/03, 20/03 and 17/04). The collection sites included pavilions I, II, V, VI, VII, IX, as well as the breeding room and underground corridors with the heating system of the palm house. The species composition of spiders in the Poznań Palm House, indicating abundance and occupied habitats, is presented in Table 1. Additional data on the sampled material and collectors is shown in Table S1, available in the online Supplementary Material.Table 1 Composition of spider species in Poznań Palm House with notes on abundance and occupied habitat.Full size tableStudy techniquesThe collection process involved hand sorting from beneath stones, logs of trees, crevices, walls and window panes. Additionally, dry bamboo leaves and other litter material from the ground were sieved.Species identification was carried out using an Olympus SZX12 stereomicroscope, and specimens were photographed using an Artcam 500MI digital camera. Images were processed using Quick Photo Camera 2.3 software and Adobe Photoshop CS2. The reproductive organs of females of the species Coelosoma. floridanum Banks, 1900, Pholcus spp. and Howaia mogera (Yaginuma, 1972) were dissected and cleared with lactic acid. All specimens were stored in 75% ethanol.Genetic analysis of Triaeris stenaspis
Total DNA from the legs of one spider specimen was extracted using the Genomic Mini kit (A&A Biotechnology) for universal genomic DNA isolation according to the manufacturer’s recommendation. The COI gene was detected by PCR amplification with LEPF1 and LEPR1 primers, whose sequences and annealing temperature are described in Hebert et al.73. PCR reactions were carried out in mixtures containing: 3 µl DNA, 1.5 µl 10× DreamTaq Buffer (Thermo Scientific), 0.3 µl 10 mM dNTP (A&A Biotechnology), 0.75 µM each primer (Oligo.pl), 0.4 U DreamTaq DNA Polymerase (Thermo Scientific) and sterile bidistilled water to a final volume of 15 µl. Each reaction contained a sample without template DNA, which served as a negative control. PCR products were electrophoresed in an agarose gel (NOVA Mini, Novazym) and sequenced with BigDye Terminator v3.1 using an ABI Prism 3130XL Analyzer (Applied Biosystems).Identification of Wolbachia and Cardinium endosymbionts in Triearis stenaspis
Detection of Wolbachia and Cardinium endosymbionts68 was performed for four spider specimens. DNA isolation from individual specimens was performed as described above. Endosymbiont genes were detected by PCR amplification using primers whose sequences and annealing temperatures were reported by Brown et al.69 and Zchori-Fein & Perlman70. PCR reactions, gel electrophoresis in agarose gel and sequencing was carried out as described above. The BLASTn algorithm was used to compare DNA sequences with data deposited in GenBank.Molecular analysis of Wolbachia genes in Triaeris stenaspis
Molecular characterization of Wolbachia was based on the analysis of the following housekeeping gene sequences: 16S rRNA69,74, coxA, fbpA, gatB, hcpA47 and ftsZ75. The primer sequences and annealing temperatures are presented in Table S2.Amplifications were performed in a 15 µl mixtures as described above. The PCR cycling profile was as follows: 95 °C for 5 min; 40 cycles at 95 °C for 30 s, annealing (Table S2) for 30 s, and 72 °C for 45 s, and a final elongation at 72 °C for 5 min. Subsequently, the amplified products were subjected to electrophoresis, sequencing and BLASTn analysis as described above. The sequences of the 16 S rRNA, coxA, fbpA, ftsZ, gatB and hcpA genes derived from Wolbachia inhabiting T. stenaspis have been deposited in GenBank.The 16S rRNA sequence of Wolbachia from T. stenaspis was analyzed for nucleotide variations between bacterial strains from different Wolbachia supergroups, with specific focus on regions corresponding to individual positions in Escherichia coli 16S rRNA. Additionally, 16S rRNA was analyzed for the presence of a unique sequence specific to Wolbachia from the spider. The ftsZ gene sequence was also examined for the presence of a specific sequence characteristic for Wolbachia from T. stenaspis.Phylogeny of Wolbachia from Triaeris stenaspis
The sequences of the 16S rRNA, coxA, fbpA, ftsZ, gatB and hcpA genes of Wolbachia isolated from T. stenaspis were aligned with Wolbachia loci representing different phylogenetic supergroups (A–W) using MEGA 11 software76. NCBI accession numbers for sequences used in the phylogenetic analysis are presented in Figs. S1–S6 and Table S3 available in the online Supplementary Material. The alignments of the obtained sequences were constructed using ClustalW77. Single gene sequences were aligned, and then a multigene alignment was created using data of 33 Wolbachia strains from various hosts together with T. stenaspis. An outgroup of Ehrlichia spp. sequences was added to the analysis. The jModelTest 2 software78,79 was used to select the appropriate model of sequence evolution. The maximum likelihood bootstrap support was determined using 1000 bootstrap replicates. The HKY + G + I model was chosen for the 16S rRNA sequence data. For the coxA and fbpA genes, the HKY + G model was used. The GTR + G model was selected for the gatB and hcpA genes, as well as for concatenated sequence data of the six loci (16S rRNA, coxA, fbpA, ftsZ, gatB and hcpA). The TrN + G model was selected for the ftsZ sequence. Gene recombination between strains was detected by the φ test using SplitsTree4 software80.Additional phylogenetic analysis was performed based on concatenated sequence data of the 16S rRNA, coxA, fbpA, ftsZ, gatB and hcpA genes of Wolbachia from T. stenaspis and Wolbachia supergroups A and B from other spider species using MEGA 11, ClustalW and jModeltest as described above. The GTR + G model was selected for this analysis. NCBI accession numbers for sequences used in the phylogenetic analysis are listed in Table S4 available in the online Supplementary Material.ResultsComposition of speciesThe material for analysis included 223 spider specimens collected between 2013 and 2023. Fourteen spider species were identified to the species level, including 9 belonging to species alien to Europe: C. floridanum, H. adansoni, H. mogera, Ostearius melanopygius (O. P.-Cambridge, 1879), Parasteatoda tabulata (Levi, 1980), Parasteatoda tepidariorum (C. L. Koch, 1841), Scytodes fusca Walckenaer, 1837, Spermophora kerinci Huber, 2005 and T. stenaspis (Table 1; Fig. 2a–o).Abundance of alien speciesThe most numerous species in our study was C. floridanum, constituting 39.9% of all spiders. This species was predominantly found at ground level, specifically in fallen, dry banana leaves. The proportion of the next four most abundant species was in the range of 6.3–13.9%: H. mogera (13.9%), S. fusca (12.6%), O. melanopygius (6.7%) and P. tabulata (6.3%) (Table 1).Sex ratio of alien species and sexual dimorphism in C. floridanum
For C. floridanum, H. mogera, O. melanopygius and S. fusca, sex ratio was over 2, while for H. adansoni, it was 0.2. An equal sex ratio was observed for P. tabulata, while only females were recorded for P. tepidariorum, S. kerinci and T. stenaspis (Fig. 1). In the case of the latter species, only single specimens were recorded.Fig. 1Sex ratio of alien species.Full size imageColeosoma floridanum was characterized by the highest sexual dimorphism among the species studied. Females had a slightly oval, sometimes spherical abdomen with black spots running in two rows on the dorsum (Fig. 2a). Male abdomen was elongated and slightly narrow in 2/3 of its length, with a light transverse stripe on a dark background (Fig. 2b). The coloration may include a combination of dark and white spots. Additionally, males possessed characteristic two appendages on the sclerotized ring located anteriorly in the abdomen (Fig. 2c). The terminal apophysis of the male palp extended over the bulbus (Fig. 2e).Fig. 2Alien spiders in the Palm House in Poznan, Poland. (a) Coleosoma floridanum, female, dorsal view, (b) C. floridanum, male, dorsal view, (c) C. floridanum, male sclerotized appendages located anteriorly on the abdomen, (d) C. floridanum, epigyne, (e) C. floridanum male palp, ventral view, (f) Hasarius adansoni, male and female, dorsal view, (g) H. adansoni, cephalothorax of female, frontal view, (h) Howaia mogera, male, dorsal view, (i) H. mogera, male palp, (j) H. mogera, epigyne, (k) Ostearius melanopygius, lateral view, (l) Scytodes fusca, female, dorsal view, (m) S. fusca, cephalothorax of female, frontal view, (n) Spermophora kerinci, cephalothorax of female, frontal view, (o) Triaeris stenaspis, female, dorsal view.Full size imageColeosoma floridanum, S. fusca and S. kerinci were recorded for the first time in Poznań Palm House. They are new species in the fauna of Poland.Genetic analysis of Triaeris stenaspis
The 619-bp sequence of T. stenaspis COI gene has been deposited in GenBank under accession no. OR456447 and is an important source of molecular data for comparative studies. Comparative analysis showed the highest identity of 82.57% to Oonopidae sp. (accession no. OP242080) and 82.47% with Aranea sp. (accession no. OL694580). The sequence also exhibited identities of 80% and 80.78% with T. stenaspis (accession nos. KX536938 and KX536955, respectively).Identification of parthenogenesis-inducing bacterial endosymbionts in Triaeris stenaspis
For the first time, we have identified Wolbachia in the parthenogenetic spider species T. stenaspis. Three females out of four collected were infected. Cardinum was not found.Molecular characterization of Wolbachia from Triaeris stenaspis
We successfully amplified six Wolbachia housekeeping genes in T. stenaspis: 16S rRNA, coxA, fbpA, ftsZ, gatB and hcpA. All six genes were identified in three studied females of T. stenaspis. The obtained sequences were identical in studied specimens. Wolbachia genes originated from one female were used for phylogenetic analyses. NCBI accession numbers for the obtained Wolbachia sequences are as follow: OR457752 (16S rRNA), OR450018 (coxA), OR462179 (fbpA), OR462180 (ftsZ), OR462181 (gatB) and OR462182 (hcpA). The 443-bp region of the Wolbachia 16S rRNA sequence in T. stenaspis showed 99% identity to Wolbachia 16S rRNA from the isopteran insect Nasutitermes takasagoensis (Shiraki, 1911) deposited in GenBank under accession no. DQ837200. The amplicon of coxA (429 bp) showed the highest identity (93.56%) with bacterial sequences of the hemipteran insect Nilaparvata muiri (accession no. GU289807). The fbpA sequence of 436 bp showed the highest identity of 92.36% with the Wolbachia gene from the lepidopteran insect Apotomis betuletana (Haworth, 1811) (accession no. OX366320). The 330-bp sequence of the ftsZ gene of Wolbachia in T. stenaspis revealed the highest identity of 91.52% with the sequence of Wolbachia in the siphonapteran insects Ctenocephalides felis (Bouche, 1835) [accession nos. (1) CP051157—DNA sequence of Wolbachia strain wCfeJ, (2) CP116768—strain wCfeJ and (3) AJ628415—strain wCfe]. The gatB sequence of 393 bp showed the highest identity (91.49%) with the endosymbiont gene from the hemipteran insect Cystococcus echiniformis Fuller, 1897 (accession no. MW511352). The PCR product of hcpA (469 bp) revealed the highest identity of 90.17% with the Wolbachia sequence from the odonate insect Ischnura elegans (Vander Linden, 1820) (accession no. OX366371).The 16S rRNA sequences of Wolbachia from T. stenaspis and bacteria from other hosts representing supergroups A–W were compared based on nucleotide differences. In the gene of the spider-derived microorganism, we recorded a T nucleotide at position corresponding to position 747 in 16S rRNA of E. coli. Nucleotides A or C were found in the same position of Wolbachia 16S rRNA from supergroups A–W. Additionally, a unique 5’TCATATC-3’ sequence was found in the 16S rRNA gene of the endosymbiont from T. stenaspis. The sequence was located at positions 745–749 corresponding to the sequence of the 16S rRNA gene of E. coli (Fig. S7). We have also identified a unique 5’-CTTACAC-3’ sequence for Wolbachia from the spider in the ftsZ gene. The location of this sequence was determined at positions 612–616 in relation to ftsZ of Wolbachia from Drosophila sturtevanti Duda, 1927 (accession no. CP050531). An alignment showing the unique ftsZ sequence of Wolbachia supergroup A is illustrated in Fig. S8.
Wolbachia phylogenyThe phylogeny of Wolbachia in T. stenaspis was based on sequence analysis of six bacterial genes: 16S rRNA, coxA, fbpA, ftsZ, gatB and hcpA (2523 bp in total). Both individual gene sequences, as well as the six-gene phylogenetic characterization indicated that bacteria from the spider formed a separate supergroup. Our research revealed that Wolbachia from T. stenaspis belongs to a new Wolbachia supergroup X (Fig. 3). We ruled out the possibility that the spider endosymbiont could be a recombinant between strains of other subgroups, as the φ test did not reveal statistically significant evidence for recombination (p = 1).Fig. 3Maximum likelihood reconstruction of Wolbachia supergroup phylogeny based on concatenated sequence alignments of six bacterial loci (16S rRNA, coxA, fbpA, ftsZ, gatB, hcpA) using MEGA 11 software. Strains are denoted by their host names, except for outgroup bacteria. Capital letters indicate individual Wolbachia supergroups. Bar, substitutions per nucleotide. Bootstrap values based on 1000 replicates are shown on branches. 1complete genome of the strain wCfeJ deposited in GenBank under accession no. CP051157. 2complete genome of the strain wCfeJ deposited in GenBank under accession no. CP116768. 3supergroup V assigned by Sharma & Som116. 4supergroup V assigned by Mioduchowska et al.115. 5supergroup W assigned by Beliavskaia et al.117. 6supergroup W assigned by Sharma & Som116.Full size imagePhylogenetic trees reconstructing the relationships of bacteria based on the analyses of individual genes are shown in Figs. S1–S6 available in the online Supplementary Material. The phylogeny based on the concatenated set of 16S rRNA, coxA, fbpA, ftsZ, gatB and hcpA gene sequences is depicted in Fig. 3. An additional phylogenetic tree showing that Wolbachia from T. stenaspis does not group with Wolbachia supergroups discovered so far in spiders, i.e. supergroups A and B is presented in Fig. S9 available in the online Supplementary Material.DiscussionLong-term spider survival ratesPresently, we compare the old findings originated from 1966 with the results of our studies carried out in 2013–2023. Woźniczko33 listed 11 spider species, of which 2 were designated as spiders of foreign origin: H. adansoni and P. tepidariorum, with the latter one being most numerous (77%). As a result of the current series of studies conducted after more than 50 years, 18 taxa have been identified, of which 14 were classified to the species level. The material acquired included 9 species of spiders characterized as allochthonous to the European fauna. Despite potential fluctuations in environmental conditions between the two distant study, attributed to factors such as the introduction of novel elements through horticultural plants (inclusive of substrate-dwelling invertebrates, bacteria and fungi), routine utility works, unpredictable variations in temperature and humidity, a restricted and simplified food base, and frequent application of plant protection pesticides, the persistence of 5 spider species has been confirmed between 1966 and the current survey cycle. Among them, 2 were alien species of spiders: H. adansoni and P. tepidariorum, and 3 were native species: Amaurobius ferox (Walckenaer, 1830), Steatoda grossa (C. L. Koch, 1838) and Tegenaria domestica (Clerck, 1758) (Fig. 4).Fig. 4Percentages of spider species in the Poznań Palm House in 2013–2023 compared to unpublished data of Woźniczko33.Full size imageBased on these findings, we considered the aforementioned species a stable faunistic element of the Poznań Palm House. Although two of them are native to remote geographic zones (H. adansoni—African origin, P. tepidariorum—Asian origin), and despite frequent use of insecticides, which could limit spider abundance and their predation rate81,79,80,81,85, they have not caused lethal effects to these two species. Our suggestion posits that H. adansoni and P. tepidariorum may exhibit resistance to these chemical agents, which is consistent with the findings of Wilczek et al.86, Babczyńska et al.87 and Řezáč et al.88. These authors confirmed the relative resistance of certain spider species to chemical contamination and tolerance for high concentrations of heavy metals and some pesticides. All alien species recorded in the Poznań Palm House should be regarded as highly acclimated to demanding and fluctuating conditions, notably distinct from their natural habitats. This adaptability is especially important for spiders from tropical regions, as their occurrence has been confirmed in similar places like palm houses, greenhouses (butterfly, orchid etc.) and botanical gardens across Europe7,14,15,18,19,62,64,65,89,87,91,,71,92,93,94,95,96.Risk of colonization of synanthropic and natural habitats by alien speciesThe likelihood of alien spider species invading natural habitats located outside urban tropical island appears to be low3. This is due to the prevailing unfavorable thermal and humidity conditions of such habitats and highly competitive pressure of native species. Nevertheless, some species of non-native spiders, demonstrating broad ecological adaptability, have successfully acclimated to synanthropic and natural biotopes in Central Europe97. In the present study, we have found O. melanopygius, which inhabits natural and seminatural habitats in Poland and continues to expand its range66,98,99,100. It was originally described in New Zealand by Pickard-Cambridge101. This species successfully disseminated in Europe in the 20th century and has also recently spread rapidly in Poland66,89. The probable introduction of O. melanopygius into the palm house occurred through the transport of non native horticultural plants or substrates; however, it cannot be excluded that it could have entered the palm house with local plants and other materials delivered to the pavilion with temperate zone vegetation. An alternate scenario for its settlement was presented by Rozwałka & Stachowicz100. The latter authors suggested that O. melanopygius initially spread in the eastern part of Poland, primarily inhabiting greenhouses of horticultural farms and expanded to neighboring biotopes after the population stabilized. Passive dispersal by ballooning is an advantageous phenomenon that may allow the species to spread rapidly and colonize synanthropic and natural biotopes66,89,98. Another alien species, H. mogera, originated from Asian and was recorded for the first time in Europe in 20097. In Poland, it has been identified in locations such as a botanical garden, garden store and butterfly house in zoological garden, where stable and numerous populations have been observed60,66,102. Considering that Jung et al.103 have found that this species inhabits stream banks with ruderal vegetation in agricultural, residential and industrial areas in South Korea, it is quite possible that this spider can also colonize seminatural habitats in Europe. Some species, due to their adaptation to environments heavily transformed by humans, are able to more easily colonize new synanthropic habitats. Two such examples are P. tabulata and P. tepidariorum, with P. tabulata being significantly more expansive104 and showing higher adaptability to natural biotopes105. P. tabulata has been recorded in cities, inhabiting building walls and fences, but also occurring in synanthropic habitats like roadside trees or forest car parks. Moreover, H. adansoni and T. stenaspis have also been found outside the Palm House in Poland. Thus far, they have been recorded in garden centers, ornamental plant markets and greenhouses. H. adansoni was found to be particularly numerous in a horticultural farm60,66, while T. stenaspis in a greenhouse with orchids60.Although negative impact of alien invaders on spider assemblages in natural habitats has not been observed in Europe8,106,107, such risks continue to increase due to climate change. There is a general consensus that global warming will potentially promote the spread, colonization and development of invasive alien species in terrestrial as well as subterranean (caves) habitats108,109,110. Given the progressive climate warming in Poland111,112, it is possible that the thermophilic alien species found in the Poznań Palm House could extend their range to open land in the near future, potentially becoming invasive in both disturbed and natural habitats. Considering the potential for the rapid spread of certain alien spider species in Europe, such as the highly invasive Mermessus trilobatus (Emerton, 1882)113,114, it is crucial to exercise special care and monitor the abundance of invaders living in urban ecological islands such as palm houses.Endosymbiotic Wolbachia in Triaeris stenaspis
The capacity for parthenogenesis and high ecological tolerance appear to be pivotal factors enabling some arachnids to colonize such ecological islands as tropical palm houses39. Zawierucha et al.32 reported the occurrence of parthenogenetic species of Schizomida (Stenochrus portoricensis Chamberlin, 1922) in the Poznań Palm House in the past. The ability of females to reproduce without a male can be induced by endosymbiotic bacteria, with Wolbachia being the most prevalent among them40,41. Considering the fact that this type of reproduction is advantageous for species to become successful colonizers11, we focused on the parthenogenetic alien spider T. stenaspis. Until now, the presence of endosymbiotic bacteria like Wolbachia or Cardinium in T. stenaspis has not been confirmed36. This report marks the first identification of Wolbachia in this species. The endosymbiont was characterized based on the sequences of six bacterial housekeeping genes: 16S rRNA, coxA, fbpA, ftsZ, gatB and hcpA. Sequence identity analysis of single genes revealed the highest complementarity to DNA of different Wolbachia supergroups from insect hosts representing various orders, including Isoptera, Hemiptera, Lepidoptera, Siphonaptera and Odonata. Specifically, the DNA sequences of the endosymbiont from T. stenaspis showed the highest identity with the genes of the following Wolbachia supergroups: B (Wolbachia from A. betuletana and I. elegans), I (Wolbachia wCfe from C. felis), F (Wolbachia from N. takasagoensis and C. echiniformis), V (Wolbachia wCfeJ from C. felis), and additionally to an unassigned supergroup (Wolbachia from N. muiri). Our phylogenetic reconstruction of Wolbachia supergroups based on six loci revealed that the bacteria recovered from the spider clearly formed distinct Wolbachia lineages, differing from the known Wolbachia supergroups (Fig. 3). Furthermore, there is compelling evidence supporting the identification of a novel Wolbachia supergroup X from T. stenaspis characterized by unique 5’-TCATATC-3’ and 5’-GACTTCG-3’ sequences within the 16S rRNA and the ftsZ genes, respectively.Supergroups V and W were duplicated due to the publication of independent supergroups with the same designation at the same time. Thus, there are currently two distinct supergroups V described in different groups of arthropods: Mioduchowska et al.115 discovered supergroup V in Unio crassus Philipsson, 1788 (Mollusca, Bivalvia) and Streptocephalus cafer Lovén, 1847 (Arthropoda, Branchipoda). Concurrently, Sharma & Som116 introduced a new Wolbachia supergroup V from C. felis (Arthropoda, Insecta). Similarly, Sharma & Som116 and Beliavskaia et al.117 designated two independent supergroups with the same name “supergroup W” from various host groups: C. felis and Howardula sp. (Nematoda, Secementea), respectively. It should be noted that although two independent supergroups V and W were detected in one host, i.e. C. felis, the Wolbachia strains were designated as wCfeJ (accession no. CP011157) and wCfeT (accession no. CP051156), respectively. In light of the duplication of supergroup names assigned to independent bacterial strains, it seems necessary to establish a committee to update the nomenclature of newly described Wolbachia supergroups. Researchers discovering a novel supergroup would be encouraged to submit relevant information to the committee to assign a logical designation for new supergroup.The detection of Wolbachia in T. stenaspis leads us to propose a strong influence of this endosymbiont on the manipulation of the reproduction of this species towards parthenogenesis. This adaptation could potentially facilitate the colonization and establishment in the Poznań Palm House and similar “tropical islands” in Europe.Conclusions(1) Thermophilic alien spider species are present in the Poznań Palm House. Given the progressive climate warming in Poland, it is possible that they could extend their range to open land in the near future, potentially becoming invasive in both disturbed and natural habitats. (2) We have detected the new Wolbachia supergroup X in T. stenaspis. The presence of the bacteria may be related to the induction of parthenogenesis in the spider as an adaptation for survival in isolated conditions.
Data availability
Sequencing data generated and analyzed in this study are deposited to NCBI Nucleotide Database (accession nos. OR456447, OR457752, OR450018, and OR462179–OR462182).
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Download referencesAcknowledgementsWe would like to dedicate this work to Dr. Andrzej Dziabaszewski, a distinguished Polish arachnologist who conducted the initial studies on spiders in the Poznań Palm House. We express our gratitude to Dr. Ziemowit Olszanowski (1961-2019), a co-discoverer of Wolbachia and Cardinium in Oribatida, whose inspiration fueled our research on endosymbiotic bacteria in spiders. It is thanks to his influence that our study has become fruitful. The completion of our study was also made possible by the invaluable assistance of Dr. Szymon Konwerski and members of the Invertebrate Research Group of the Naturalist Science Club at Adam Mickiewicz University, Poznań, Poland, with special acknowledgment to Maria Śmigiel and Maria Tsiareshyna, who played crucial roles in the comprehensive collection of material for this research.FundingThis research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.Author informationAuthors and AffiliationsDepartment of Animal Taxonomy and Ecology, Faculty of Biology, Adam Mickiewicz University Poznań, Uniwersytetu Poznańskiego 6, 61-614, Poznań, PolandPaweł Szymkowiak & Aleksandra PecynaDepartment of Microbiolgy, Faculty of Biology, Adam Mickiewicz University Poznań, Uniwersytetu Poznańskiego 6, 61-614, Poznań, PolandEdyta KoneckaDepartment of General Zoology, Faculty of Biology, Adam Mickiewicz University Poznań, Uniwersytetu, Poznańskiego 6, 61-614, Poznań, PolandTomasz RutkowskiPoznań Palm House, Matejki 18, 60-767, Poznań, PolandPrzemysław SzwajkowskiAuthorsPaweł SzymkowiakView author publicationsYou can also search for this author inPubMed Google ScholarEdyta KoneckaView author publicationsYou can also search for this author inPubMed Google ScholarTomasz RutkowskiView author publicationsYou can also search for this author inPubMed Google ScholarAleksandra PecynaView author publicationsYou can also search for this author inPubMed Google ScholarPrzemysław SzwajkowskiView author publicationsYou can also search for this author inPubMed Google ScholarContributionsP.S1. conceptualization, data analysis, original draft preparation, writing, specimens collection and identyfication; E. K. concept of bacterial research, molecular techniques, data analysis, reviewing; T. R. specimens collection, reviewing; A. P. specimens collection; P. S.4 access to the Palm House and permission to collect specimens for study.Corresponding authorCorrespondence to
Paweł Szymkowiak.Ethics declarations
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Reprints and permissionsAbout this articleCite this articleSzymkowiak, P., Konecka, E., Rutkowski, T. et al. Alien spiders in a palm house with the first report of parthenogenetic Triaeris stenaspis (Araneae: Oonopidae) infected by Wolbachia from new supergroup X.
Sci Rep 15, 9512 (2025). https://doi.org/10.1038/s41598-025-93540-1Download citationReceived: 12 June 2024Accepted: 07 March 2025Published: 19 March 2025DOI: https://doi.org/10.1038/s41598-025-93540-1Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard
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KeywordsColonizationEndosymbiontsInvasive speciesNew species to PolandNovel bacterial phylogeny lineageUrban ecological island