Repeated and Time-Correlated Morphological Convergence in Cave-Dwelling Harvestmen (Opiliones, Laniatores) from Montane Western North America

BACKGROUND: Many cave-dwelling animal species display similar morphologies (troglomorphism) that have evolved convergent within and among lineages under the similar selective pressures imposed by cave habitats. Here we study such ecomorphological evolution in cave-dwelling Sclerobuninae harvestmen (Opiliones) from the western United States, providing general insights into morphological homoplasy, rates of morphological change, and the temporal context of cave evolution. METHODOLOGY/PRINCIPAL FINDINGS: We gathered DNA sequence data from three independent gene regions, and combined these data with Bayesian hypothesis testing, morphometrics analysis, study of penis morphology, and relaxed molecular clock analyses. Using multivariate morphometric analysis, we find that phylogenetically unrelated taxa have convergently evolved troglomorphism; alternative phylogenetic hypotheses involving less morphological convergence are not supported by Bayesian hypothesis testing. In one instance, this morphology is found in specimens from a high-elevation stony debris habitat, suggesting that troglomorphism can evolve in non-cave habitats. We discovered a strong positive relationship between troglomorphy index and relative divergence time, making it possible to predict taxon age from morphology. Most of our time estimates for the origin of highly-troglomorphic cave forms predate the Pleistocene. CONCLUSIONS/SIGNIFICANCE: While several regions in the eastern and central United States are well-known hotspots for cave evolution, few modern phylogenetic studies have addressed the evolution of cave-obligate species in the western United States. Our integrative studies reveal the recurrent evolution of troglomorphism in a perhaps unexpected geographic region, at surprisingly deep time depths, and in sometimes surprising habitats. Because some newly discovered troglomorphic populations represent undescribed species, our findings stress the need for further biological exploration, integrative systematic research, and conservation efforts in western US cave habitats

Phylogenomic reclassification of the world's most venomous spiders (Mygalomorphae, Atracinae), with implications for venom evolution

Here we show that the most venomous spiders in the world are phylogenetically misplaced. Australian atracine spiders (family Hexathelidae), including the notorious Sydney funnel-web spider Atrax robustus, produce venom peptides that can kill people. Intriguingly, eastern Australian mouse spiders (family Actinopodidae) are also medically dangerous, possessing venom peptides strikingly similar to Atrax hexatoxins. Based on the standing morphology-based classification, mouse spiders are hypothesized distant relatives of atracines, having diverged over 200 million years ago. Using sequence-capture phylogenomics, we instead show convincingly that hexathelids are non-monophyletic, and that atracines are sister to actinopodids. Three new mygalomorph lineages are elevated to the family level, and a revised circumscription of Hexathelidae is presented. Re-writing this phylogenetic story has major implications for how we study venom evolution in these spiders, and potentially genuine consequences for antivenom development and bite treatment research. More generally, our research provides a textbook example of the applied importance of modern phylogenomic research.Fil: Hedin, Marshal. San Diego State University; Estados UnidosFil: Derkarabetian, Shahan. University of California; Estados Unidos. San Diego State University; Estados UnidosFil: Ramirez, Martin Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”; ArgentinaFil: Vink, Cor. Canterbury Museum Christchurch; Nueva ZelandaFil: Bond, Jason E.. Auburn University; Estados Unido

Phylogenomic analysis and revised classification of atypoid mygalomorph spiders (Araneae, Mygalomorphae), with notes on arachnid ultraconserved element loci

The atypoid mygalomorphs include spiders from three described families that build a diverse array of entrance web constructs, including funnel-and-sheet webs, purse webs, trapdoors, turrets and silken collars. Molecular phylogenetic analyses have generally supported the monophyly of Atypoidea, but prior studies have not sampled all relevant taxa. Here we generated a dataset of ultraconserved element loci for all described atypoid genera, including taxa (Mecicobothrium and Hexurella) key to understanding familial monophyly, divergence times, and patterns of entrance web evolution. We show that the conserved regions of the arachnid UCE probe set target exons, such that it should be possible to combine UCE and transcriptome datasets in arachnids. We also show that different UCE probes sometimes target the same protein, and under the matching parameters used here show that UCE alignments sometimes include non-orthologs. Using multiple curated phylogenomic matrices we recover a monophyletic Atypoidea, and reveal that the family Mecicobothriidae comprises four separate and divergent lineages. Fossil-calibrated divergence time analyses suggest ancient Triassic (or older) origins for several relictual atypoid lineages, with late Cretaceous/early Tertiary divergences within some genera indicating a high potential for cryptic species diversity. The ancestral entrance web construct for atypoids, and all mygalomorphs, is reconstructed as a funnel-and-sheet web

Phylogenomics, Integrative Taxonomy, and Population Genomics in the Travunioidea (Arachnida, Opiliones, Laniatores)

My dissertation research utilizes next-generation sequencing (NGS) technology and associated bioinformatics processing to answer systematic and evolutionary questions in Opiliones (harvestmen) at different taxonomic scales, focusing on the Laniatores superfamily Travunioidea and particularly the travunioid genus Sclerobunus. Opiliones are a diverse group of arachnids with over 6500 described species distributed on every continent except Antarctica. Despite relatively high diversity (e.g., more described species than mammals), harvestmen are poorly studied. This dissertation research has three main projects. The first chapter is a higher-level phylogenetics and taxonomic study of the Travunioidea, a clade of ~80 species of harvestmen distributed throughout the Holarctic. Here I utilized ultraconserved elements (UCE) for phylogenomic reconstruction using multiple types of phylogenetic reconstruction methods. Based on results, a new taxonomic classification is proposed for the Travunioidea, including the identification and diagnosis of a new family, and I reassess the phylogenetic utility of morphological characters used to differentiate and diagnose travunioid taxa. The second chapter focuses on species delimitation of the western North American travunioid genus Sclerobunus. I utilized modern integrative taxonomic methods, using both discovery-based and validation-based approaches by combining morphometrics, mitochondrial genetic data, genitalic morphology, and nuclear genetic data derived from newly developed genes based on a comparative transcriptomics approach. This research resulted in a revision of the genus including synonymy of the genus Cyptobunus, elevation of four subspecies, and the description of five new species. The third chapter is a phylogeographic analysis of Sclerobunus robustus, a species distributed throughout the southwestern United States. A hypothesis-based framework was adopted, where stable habitats (i.e., potential refugia) were identified through ecological niche modeling, and hypotheses regarding genetic patterns associated with these refugia were developed. Hypotheses were tested by using genetic data in the form of loci and SNPs derived from double-digest RAD sequencing methods. Two large refugial regions were identified and population genomic analyses supported the presence of both

Data from: Integrative taxonomy and species delimitation in harvestmen: a revision of the western North American genus Sclerobunus (Opiliones: Laniatores: Travunioidea)

Alpha taxonomy, and specifically the delimitation of species, is becoming increasingly objective and integrative. The use of coalescent-based methods applied to genetic data is providing new tools for the discovery and delimitation of species. Here, we use an integrative approach via a combination of discovery-based multivariate morphological analyses to detect potential new species. These potential species are then used as a priori species in hypothesis-driven validation analyses with genetic data. This research focuses on the harvestmen genus Sclerobunus found throughout the mountainous regions of western North America. Based on our analyses, we conduct a revision of Sclerobunus resulting in synonymy of Cyptobunus with Sclerobunus including transfer of S. cavicolens comb. nov. and elevation of both subspecies of S. ungulatus: S. ungulatus comb. nov. and S. madhousensis comb. nov., stat. nov. The three subspecies of S. robustus are elevated, S. robustus, S. glorietus stat. nov., and S. idahoensis stat. nov. Additionally, five new species of Sclerobunus are described from New Mexico and Colorado, including S. jemez sp. nov., S. klomax sp. nov., S. skywalkeri sp. nov., S. speoventus sp. nov., and S. steinmanni sp. nov. Several of the newly described species are single-cave endemics, and our findings suggest that further exploration of western North American cave habitats will likely yield additional new species

Sinonychia Zhang & Derkarabetian 2021, gen. n.

Sinonychia gen. n. Figs 1–31, 33 ZooBank LSID: urn:lsid:zoobank.org:act: 3E5B75D9-94F0-4B4E-8D09-89A5A916495C Type species: Sinonychia martensi sp. n. Diagnosis. Sinonychia gen. n. can be differentiated from all other Cladonychiidae genera on the basis of penis morphology, having a combination of two pairs of relatively thick lateral setae on the glans, a cylindrical, basally widening glans, and an elongate stylus arising apically. Morphologically the new genus is most similar to Speleonychia from the Pacific Northwest of North America but can be distinguished by several characters. First, in spination of the penis: in Sinonychia gen. n. two pairs of apical setae on the penis are thick and at a 90˚ or larger angle to the stylus, whereas in Speleonychia these setae are at a much smaller angle, directed apicad (Briggs 1974: figs 7–8). Second, the shape of the glans: in Sinonychia gen. n. the glans is almost cylindrical, with a wide, blunt apex and with the stylus arising sub-terminally, while in Speleonychia the glans is more triangular, with a more pointed apex and a stylus arising terminally. Third, in spination of the pedipalpal femur: Sinonychia gen. n. has multiple distal SBTs on the ventral surface at the distal end (Figs 5–6), while Speleonychia has only a single SBT (Briggs 1974: fig. 2). Etymology. The generic name is composed of “Sino”, derived from the Latin word “Sinae” (from the Ancient Greek “Σῖναι”) which generally refers to China, and of the Latin noun “onyx” (from the Ancient Greek “ὄνῠχος”) meaning ‘claw’, a common name applied to many travunioid and triaenonychoid genera. The second part of the new genus name also indicates morphological similarity with the genus Speleonychia. The genus name is feminine. Description. Highly troglomorphic with unpigmented body (Figs 22–31). Ocularium greatly reduced in size, smooth, set back from anterior margin of carapace; eyes and retinae completely absent (Figs 1, 22–31). Dorsal scutum of the “eta” (η) category of Kury & Medrano (2016). Genital operculum nearly triangular (Fig. 9). Sternum elongate and narrowly triangular (Fig. 8). Pedipalps thin, elongate, lacking pigment, with thin SBTs (Figs 5–6). Legs extremely long, thin, and lacking pigment. Claws III–IV with peltonychium (Figs 10–13). Penis truncus thin and elongate, musculature restricted to its base (Fig. 16); glans articulated with truncus, with two pairs of setae, the more distal pair being smaller than the other pair; stylus elongate, arising apically from glans (Figs 17–19).Published as part of Zhang, Chao & Derkarabetian, Shahan, 2021, First record of Travunioidea (Arachnida: Opiliones: Laniatores) from China, with the description of a new monotypic genus from a cave, pp. 87-97 in Zootaxa 4984 (1) on page 88, DOI: 10.11646/zootaxa.4984.1.8, http://zenodo.org/record/492865

Sinonychia martensi Zhang & Derkarabetian 2021, sp. n.

Sinonychia martensi sp. n. Figs 1–31, 33 ZooBank LSID: urn:lsid:zoobank.org:act: 1FD58240-64B2-4B4B-8679-718B8A65FAFB Type material. CHINA: Beijing : Holotype male (MHBU-Opi-18 ZC0604), Beijing City, Fangshan District, Beiyao Village, Tangren Cave, N 39°47’, E 115°52’, 70 m elevation, leg. Z.G. Feng 12.9.2018. Paratypes: 1 female allotype (MHBU-Opi-18 ZC0605), 14 females (MHBU-Opi-18 ZC0606–0619) with collecting data as for holotype except: leg. Z.Y. Li. 12 females (MHBU-Opi-20 ZC1201–1212) with collecting data as for holotype except: leg. C. Zhang, X.H. Ru & Q.W. Cui 20.12.2020. Diagnosis. As given for the genus. Etymology. The new species is dedicated to Prof. Dr Jochen Martens (Mainz, Germany), one of the top ten opilionologists who have described the most species (Machado et al. 2007); name in the genitive case. Description. Male (holotype). Habitus as in Figs 1, 7, 22–24. Colouration (Figs 22–24): entire body pale yellow. Body length 1.92, scute length 1.54, scute width 1.15, carapace width 0.95, LII/SL 9.65. Dorsum (Figs 7, 22). Scutum minutely granular, scutum outline of the “eta” (η) category; posterior region of scutum widest, posterior end of opisthosoma convex. Surface of carapace completely smooth, anterior margin unarmed. Ocularium low, slightly conical, unarmed, without eyes, set back from anterior margin of scutum by 0.08 mm. Grooves between scutal areas inconspicuous. Free tergites and anal operculum unarmed. Venter (Figs 8, 24). Genital operculum nearly triangular (Fig. 9). Coxae I–IV, genital operculum and free sternites finely granular and covered with scattered minute setae. Sternum elongate, narrowly triangular (Fig. 8). Spiracles clearly visible. Chelicerae (Figs 2–4). Basichelicerite slender, without distinct dorso-distal bulla, no prominent armament except for three small SBTs. Cheliceral hand unarmed, pro-dorsally with SBTs, the inner ones larger than the outer ones, some SBTs ectally, ventrally, and entally in sub-distal portion. Fingers relatively short, inner edges dentate (Fig. 4); movable finger with eight small, rounded teeth; fixed finger with five more distinctly pointed teeth. Pedipalps (Figs 5–6). Measurements given in Table 1. Coxae dorsally unarmed and ventrally with one large and one small SBT (Figs 6, 8). Trochanter dorsally with one very small SBT, ventrally with one large SBT and one small accessory SBT. Femur dorsally convex, with a row of reduced SBTs; ventrally with three enlarged SBTs basally, followed by three small SBTs, the most distal one of them located ectally, with two SBTs distally on ental side. Patella ventro-entally with two SBTs and ventro-ectally with one SBT. Tibia with three SBTs each ventro-entally and ventro-ectally. Tarsus ventro-entally with three and ventro-ectally with four SBTs. Tarsal claw 0.38 long, curved, shorter than tarsus. Legs. All elongated; measurements given in Table 1. All segments smooth, with only few short setae. Femur IV straight. Claws of legs III–IV developed as peltonychia with only one pair of distolateral prongs in both wings of the central shield and with pointed distal prong (Figs 10–11). Distitarsus I with two, distitarsus II with seven tarsomeres. Distitarsi III–IV without scopula. Tarsal formula (I–IV): 7,17,4,4. Penis (Figs 16–19). Penis 1.31 long, truncus slender, nearly parallel-sided. Joint between glans and truncus articulated. Truncus distally and basally inflated; musculature limited to base of truncus. Glans almost cylindrical, longer than wide, distally contracted (in lateral view), basally slightly inflated. Distal portion of glans dorsally with weak invagination from where stylus arises, and laterally with two pairs of thick recurved setae. Apical pair of setae smaller than other pair and nearly perpendicular to axis of stylus; subapical pair of setae larger than apical pair and more strongly inclined towards base of penis. Stylus thin, cylindrical, and tubular. Female (Figs 12–15, 20–21, 25–31, 33). In general appearance very similar to male. Allotype (MHBU-Opi- 18ZC0605): Body length 2.09, dorsal scute length 1.41, scute width 1.23, carapace width 0.85. Measurements of pedipalp and legs given in Table 1. Pedipalpal claw length 0.40. Midgut (Fig. 15) with triangular D1, elongate OD2 with two branches, and an elongate OD3 with two branches. Free ninth tergite and lateral sclerites present (Fig. 14). Ovipositor (Figs 20–21). Four distal lobes. Ventral and dorsal lobes without setae. Each lateral lobe with two pairs of setae on lateral surface, without distal setae. Variation. Size range of females (n = 27): body length 1.63–2.14, width 1.10–1.25. Colouration of the body varies from yellowish white to pale yellow (Figs 28–31). The outline of the dorsum varies from trapezoidal (Fig. 28) to elongate trapezoidal (Figs 29–31). The distal portion and prongs of claws III–IV vary in their degree of fusion with the central shield (Figs 12–13). Notes. Sexual dimorphism is not exhibited in this species. Only a single male specimen was found among a total of 28 specimens. To avoid damage to the male holotype, some characters of the male that are not easily observable were only examined in the females. For example, the ninth tergite and lateral sclerites were observed by placing specimens into 10% KOH for a few minutes to dissolve the tissue (Fig. 14), and midgut morphology was observed by dissecting specimens (Fig. 15). Distribution. Known only from the type locality. Habitat. Tangren Cave lies in the Majiagou Formation of the Middle Ordovician, formed about 440–500 million years ago. The main body of the cave is deep in the mountain, 40 to 60 metres below the surface, with a northeast to southwest course. The temperature in the cave is 15–18℃ and the relative humidity is 95%. The cave entrance on the hillside (Fig. 32) leads to a relatively narrow and small vertical shaft. The cave is divided into three sections. The first section is about 6 metres long, close to the cliff. The second section is about 39 metres long and vertical, nearly 30 metres of it requires a suspended descent. The third section is about 10 metres long and also requires a suspended descent. The Tangren cave extends downward along the limestone stratum in the southwest of the mountain, with a slope of 20–30 degrees. About 100 metres from the entrance there is a spacious hall, 3–20 metres high and 2–40 metres wide. All specimens were collected in this hall, most of them under stones by hand, a few on the cave walls. The cave was visited by the collectors twice.Published as part of Zhang, Chao & Derkarabetian, Shahan, 2021, First record of Travunioidea (Arachnida: Opiliones: Laniatores) from China, with the description of a new monotypic genus from a cave, pp. 87-97 in Zootaxa 4984 (1) on pages 88-93, DOI: 10.11646/zootaxa.4984.1.8, http://zenodo.org/record/492865

65/65 CORE 50% coverage matrix

Concatenated UCE matrix for the 65/65 CORE dataset with 50% taxon coverag

65/65 CORE 50% coverage UCE loci

All individual UCE loci included in the 65/65 CORE 50% coverage matri

65/65 CORE 50% coverage tree

Resulting RAxML phylogeny for the 65/65 CORE dataset with 50% taxon coverag