A genus-level taxonomic review of primitively segmented spiders (Mesothelae, Liphistiidae)

Abstract The spider suborder Mesothelae, containing a single extant family Liphistiidae, represents a species-poor and ancient lineage. These are conspicuous spiders that primitively retain a segmented abdomen and appendage-like spinnerets. While their classification history is nearly devoid of phylogenetic hypotheses, we here revise liphistiid genus level taxonomy based on original sampling throughout their Asian range, and on the evidence from a novel molecular phylogeny. By combining morphological and natural history evidence with phylogenetic relationships in the companion paper, we provide strong support for the monophyly of Liphistiidae, and the two subfamilies Liphistiinae and Heptathelinae. While the former only contains Liphistius Schiödte, 1849, a genus distributed in Indonesia (Sumatra), Laos, Malaysia, Myanmar, Thailand, we recognize and diagnose seven heptatheline genera, all but three removed from the synonymy of Heptathela: i) Ganthela Xu & Kuntner, gen. n. with the type species Ganthela yundingensis Xu, sp. n. is known from Fujian and Jiangxi, China; ii) a rediagnosed Heptathela Kishida, 1923 is confined to the Japanese islands (Kyushu and Okinawa); iii) Qiongthela Xu & Kuntner, gen. n. with the type species Qiongthela baishensis Xu, sp. n. is distributed disjunctly in Hainan, China and Vietnam; iv) Ryuthela Haupt, 1983 is confined to the Ryukyu archipelago (Japan); v) Sinothela Haupt, 2003 inhabits Chinese areas north of Yangtze; vi) Songthela Ono, 2000 inhabits southwest China and northern Vietnam; and vii) Vinathela Ono, 2000 (Abcathela Ono, 2000, syn. n.; Nanthela Haupt, 2003, syn. n.) is known from southeast China and Vietnam.


Introduction
The only extant family within the spider suborder Mesothelae, the family Liphistiidae consists of only 88 extant species-level taxa currently grouped in three genera, and displays an interesting geographical distribution confined to Southeast and East Asia (World Spider Catalog 2015). Liphistiids are relatively large, extremely long-lived (5-18 years), ground-dwelling spiders that build trapdoor burrows used for prey capture, shelter and protection (Bristowe 1976, Coddington and Levi 1991, Haupt 2003a. Despite being large and morphologically distinct, they are rarely encountered, making it difficult to secure taxonomically meaningful samples. Their natural history also suggests that liphistiids are confined to their burrows and that the spiders rarely move around, and phylogenetic and biogeographic analyses confirm that they are dispersallimited and highly genetically structured (Xu et al. in press).

nominated a new genus
Anadiasthothela, but the species A. thorelli was a synonym of Liphistius sumatranus Thorell, 1890(see Bristowe 1932. Kishida (1923) erected a new genus Heptathela (based on Liphistius kimurai Kishida, 1920), and divided the family Liphistiidae into two subfamilies, Liphistiinae (including the tribes Liphistiiae and Heptatheleae) and Anadiasthothelinae (Anadiasthothele Simon, 1903) based on details on spinnerets. In 1939, Petrunkevitch raised Heptathela to the family rank (Heptathelidae) to include Japanese and Chinese species. This classification system was retained until Haupt (1983Haupt ( , 1990 proposed dividing the group into three genera and two families (Liphistiidae (Liphistius), Heptathelidae (Heptathela and Ryuthela)). Ono's (2000) scheme treated the groups as two subfamilies: Liphistiinae and Heptathelinae. To Heptathela and Ryuthela, Ono (2000) added three new heptatheline genera, Abcathela, Songthela and Vinathela, solely based on the female genital morphology. However, Haupt (2003a) continued to prefer his two-family system (Haupt 1984(Haupt , 1990, rejected Abcathela and Vinathela, considered Songthela as a synonym of Sinothela Haupt, 2003, anderected Nanthela Haupt, 2003. In the most recent classification scheme of the family, Schwendinger and Ono (2011) rejected all but three genera: Liphistius (Liphistiinae), Heptathela (Heptathelinae) and Ryuthela (Heptathelinae). However, they expressed some doubt at the validity of the genus Heptathela, with no fewer than 33 nominal taxa. According to these authors, Heptathela may need to be split again if a comprehensive revision and/or phylogeny was to suggest this. A modern, species-level phylogeny of liphistiid spiders necessary for addressing taxonomic, evolutionary, and biogeographic questions has been long overdue. In a sister paper (Xu et al. in press), we used molecular data from our original extensive sampling to test the monophyly of the family Liphistiidae and the genera within. Based on a species-level multi-locus phylogeny reported in that paper, and on morphological and natural history diagnostic characters provided here, we revise below the higher level systematics of the family.

Materials and methods
In order to secure a comparative sample of these seemingly rare spiders, we sampled liphistiids through China, Japan and Vietnam both at type locations and in areas with suitable habitat. We collected adults and immature spiders by excavating them from their subterranean burrows, then reared juveniles to adulthood in the laboratory. Since we primarily focused on heptathelines (the liphistiids of East Asia), our sample is biased toward China, Japan, and Vietnam ( Figure 1).
Specimens were studied using an Olympus SZX16 stereomicroscope, and anatomical details were examined and photographed with Leica M205C stereomicroscope and Olympus BX51 compound microscope. Genitalia were cleared in boiling KOH for a few minutes to dissolve soft tissues. Unless otherwise noted left palps were depicted. All measurements are in millimeters. Leg and palp measurements are given in the following order: total length (femur + patella + tibia + metatarsus + tarsus).

Results
In three years we accumulated 1,455 specimens (786 females, 118 males and 551 juveniles) from 145 localities in China, Japan, Laos, Malaysia and Vietnam. These vouchers, deposited at the Centre for Behavioural Ecology and Evolution (CBEE), College of Life Sciences, Hubei University, Wuhan, China, were the basis for our morphological examinations (reported here) and for molecular analyses (Xu et al. in press). Examined and illustrated specimens were labelled with unique codes (Appendix 1; see also Figure legends), which will be reused in the upcoming genus-level revisions. All designated type specimens were deposited at the National Zoological Museum of China (NZMC), Institute of Zoology, Chinese Academy of Sciences, Beijing, China.
In a concurrent paper (Xu et al. in press), we report on phylogenetic analyses using original five-gene nucleotide data for 75 species. These results, summarized in Figure 2, form the phylogenetic basis for a revised classification of the family. The family and subfamily monophyly were well supported in all phylogenetic analyses (for details, see Xu et al. in press). The current classification of Liphistiidae, based on morphological features, treats as valid three genera (see World Spider Catalog 2015): Heptathela s.l., Liphistius and Ryuthela. Our phylogenetic results strongly support the monophyly of Liphistius and Ryuthela, but not of Heptathela s.l., and thus require substantial taxonomic emendations. Below, we classify the species currently in paraphyletic Heptathela s.l. in six genera-the monophyly of each strongly supported (for details, see Xu et al. in press)-of which two are new, describe two new species that become the type for the new genera, and propose further synonymies.

Figure 2.
A simplified genus level phylogeny derived from the summary tree in the accompanying paper (Xu et al. submitted), as the basis for newly proposed classification. Images on the right depict typical generic characteristics (female habitus and trapdoor).

Suborder Mesothelae Pocock, 1892
Phylogenetic definition (for details, see Xu et al. in press). In the analysis of divergence times, we treated Mesothelae as a stem group leading from the root of all spiders to the node-based clade Liphistiidae. Therefore, Mesothelae accommodates the fossil genus Palaeothele Selden, 2000, which does not share one of the synapomorphies of Liphistiidae (single row of teeth on cheliceral fang groove). Although the morphological diagnosis resembles that of Liphistiidae, Mesothelae is inclusive of Liphistiidae but the two groups are phylogenetically not identical.
Composition. Mesothelae includes the crown group Liphistiidae with extant species from East and Southeast Asia, and the fossil Palaeothele montceauensis (Selden 1996a, b) from the Upper Carboniferous of Montceau-les-Mines, France around 295 Ma.

Family Liphistiidae Thorell, 1869
Diagnosis. Unlike all other extant spiders, Liphistiidae possess tergites on all abdominal segments (Figure 3), their spinnerets are located in the middle of abdominal venter (Figure 4), and in addition to a narrow sternum they also possess another narrow ventral plate, the sternite, located adjacent to coxae IV ( Figure 4).
Description. Medium to large sized ground dwelling and burrowing spiders, chelicerae with a single row of teeth, two pairs of book lungs (Figure 4), tibial spurs specialized as sense organs. Their ground burrows are closed with trapdoors, with or without additional concentric signal lines (Figure 2b, d, f, h, j, l, n, p).

Subfamily Liphistiinae Thorell, 1869
Diagnosis. In contrast to the members of the subfamily Heptathelinae, Liphistiinae spiders construct signal lines radiating from the burrow entrance (Figure 2b), the male palp possesses a tibial apophysis ( Figures 5-7), and the female genitals have a poreplate and unpaired receptacular clusters (Figures 8-9). Platnick and Sedgwick (1984) also report the unique presence of clavate trichobothria on the tarsi and metatarsi of all legs and on the palpal tarsi.

Genus
Diagnosis. Males of Ganthela differs from all other Heptathelinae genera by a smooth conductor with a distal spiniform apex (Figures 10-11), a flat opening embolus and scale-like contrategulum (Figures 10-11), females can be identified by a single pair of similar receptacular clusters (Figures 13-14).
Distribution. China (Fujian, Jiangxi). Remarks. Wang (1989) placed G. cipingensis in Liphistius based on the presence of eight spinnerets. Our collections from the type locality contain specimens with seven spinnerets. The number of spinnerets thus varies intraspecifically. Etymology. 'Yunding' refers to the type locality of this species, Mt. Yunding. Diagnosis. Females can be distinguished from G. cipingensis and the five undescribed Ganthela species we are aware of by lacking genital stalks (Figures 13-14), and the males, uniquely among heptathelines, possess the contrategulum with two marginal apophyses (Figures 11-12), the prolateral one being scale-like ( Figure 11).
Female genitalia: The posterior part of the genital area rectangular (Figure 13-14), a pair of receptacular clusters close to each other, without stalks (Figures 13-14).

Diagnosis.
Heptathela males differ from all other Heptathelinae genera by a leafshaped conductor (Figures 18-19), a thumb-shaped embolus (Figures 15, 18) and a wide tegulum with a rugate margin (Figures 16, 18-19). Heptathela females can be distinguished from all other Heptathelinae genera by a single paired depression on the ventro-lateral part of genital atrium (Figure 20), and by the one pair of main receptacular cluster and secondary, lateral, irregular receptacular clusters (Figures 20-21).
Diagnosis. Qiongthela males differ from all other Heptathelinae genera by the conductor with a narrow, blade-like, slightly hooked apex (Figures 22, 25-26), and by tegulum with two apophyses (Figures 23, 25-26). Qiongthela females can be distinguished from all other Heptathelinae by two paired receptacular clusters located at the anterior margin of the bursa copulatrix ( Figure 27).
Distribution. Hainan (China) and Vietnam. Remarks. Based on morphological descriptions, but not on phylogenetic analyses, we include two species from Vietnam in this genus, originally described as Songthela australis Ono, 2002 andHeptathela nui Schwendinger &Ono, 2011. Etymology. The species epithet refers to Baisha, the species type locality. Diagnosis. Unlike other Qiongthela species, males of Q. baishensis possess three parallel serrated distal edges of the contrategulum (Figures 25, 26), and females have two pairs of receptacular clusters, the median pair larger than the lateral one, with very short or no stalks ( Figure 27).
Palp: Cymbium with a projection; prolateral side of paracymbium unpigmented and unsclerotised, numerous setae and spines at the tip of paracymbium (Figures 22,  24). Contrategulum with three parallel distal edges, row of denticles on inner edge running down to ventro-proximal margin of contrategulum and the outer row forming a sharp edge without denticles (Figures 22,(25)(26). Tegulum with a very long, wide base, pointed, distally directed marginal apophysis with a sharp edge, and retrolaterally with a proximally directed terminal apophysis with a slightly short dentate row and continuously narrowing to a rounded, hooked apex (Figures 22-26). Conductor situated ventro-proximally on embolus, with a bent apex (Figures 22, 25-26). Embolus largely sclerotised, prolaterally with numerous longitudinal ribs (Figures 22-26).
Female (paratype). Colouration as in male; promargin of robust chelicerae with 9 strong denticles variable in size; legs and opisthosoma as in the male; 7 spinnerets. Measurements: BL 13.  Female genitalia: Two pairs of receptacular clusters along the anterior margin of bursa copulatrix, the median pair larger than the lateral one, with very short or no stalks ( Figure 27). Genus Ryuthela Haupt, 1983Figures 28-34 Ryuthela Haupt, 1983, type species Heptathela nishihirai Haupt, 1979, P. 286. Diagnosis. Ryuthela males differ from all other Heptathelinae genera by lacking the conductor and by the contrategulum with an enlongate spine (Figures 28, 30). The females differ from Heptathela, Qiongthela, Sinothela, Songthela and Vinathela by one paired receptacular cluster close to each other (Figures 31-32), located at the anterior margin of the bursa copulatrix, and from Ganthela by receptacular clusters without stems that may or may not be fused (Figures 31-34).

Remarks. In
Ryuthela, female genital anatomy shows considerable intraspecific variation, therefore the structure of the male palp appears more reliable for diagnostics and identification.
Distribution. China north of Yangzi River (Hebei, Henan, Hubei, Shandong, Shaanxi, and Shanxi).   Diagnosis. Songthela males differ from all other heptatheline genera by the conductor with a smooth surface and with the proximal portion relatively narrow, the distal portion with more than one apical spine (45)(46), and by the embolus with a flat opening (Figures 40-41, 45-46). Songthela females differ from all other heptatheline genera by two paired receptacular clusters, all four of similar size or median ones larger than laterals, median pair with tubular stems situated at the anterior margin of bursa copulatrix, lateral ones situated more dorsally (Figures 43-44, 47).
Distribution. China (Chongqing, Guizhou, Hubei, Hunan, Jiangxi, Sichuan, Zhejiang, and Yunnan) and northern Vietnam. Diagnosis. Males of Vinathela differ from all other Heptathelinae genera by a wide proximal portion of the conductor, its distal portion being bent (Figure 50), and embolus with two peaks (Figures 49-50); females of Vinathela can be distinguished from all other Heptathelinae by three or four receptacular clusters situated at the anterior margin of bursa copulatrix, three of the same size or median pair small and lateral pair large (Figures 52-55).