Article

Converging on the orb: denser taxon sampling elucidates spider phylogeny and new analytical methods support repeated evolution of the orb web

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Abstract

High throughput sequencing and phylogenomic analyses focusing on relationships among spiders have both reinforced and upturned long‐standing hypotheses. Likewise, the evolution of spider webs—perhaps their most emblematic attribute—is being understood in new ways. With a matrix including 272 spider species and close arachnid relatives, we analyze and evaluate the relationships among these lineages using a variety of orthology assessment methods, occupancy thresholds, tree inference methods and support metrics. Our analyses include families not previously sampled in transcriptomic analyses, such as Symphytognathidae, the only araneoid family absent in such prior works. We find support for the major established spider lineages, including Mygalomorphae, Araneomorphae, Synspermiata, Palpimanoidea, Araneoidea and the Retrolateral Tibial Apophysis Clade, as well as the uloborids, deinopids, oecobiids and hersiliids Grade. Resulting trees are evaluated using bootstrapping, Shimodaira–Hasegawa approximate likelihood ratio test, local posterior probabilities and concordance factors. Using structured Markov models to assess the evolution of spider webs while accounting for hierarchically nested traits, we find multiple convergent occurrences of the orb web across the spider tree‐of‐life. Overall, we provide the most comprehensive spider tree‐of‐life to date using transcriptomic data and use new methods to explore controversial issues of web evolution, including the origins and multiple losses of the orb web.

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... As a consequence, inquiry into the evolutionary chronicle of symphytognathoids is inextricably linked to the Araneoidea problem. Transcriptomic analyses of extensive taxonomic samples of araneoids and thousands of loci (Fernández et al., 2018;Kallal et al., 2021) have also refuted symphytognathoid monophyly with high nodal support values. Surprisingly, the most recent phylogenomic analyses (Kulkarni et al., 2020, using ultraconserved elements (UCEs) and up to 26 symphytognathoid representatives, suggest (and paradoxically also with high nodal support values) that when the sequence data are analyzed as nucleotides, rather than as amino acids, and when about a hundred or more loci are used, symphytognathoids are indeed monophyletic. ...
... In addition, the robustness of our results (like any phylogenetic analysis) is clearly taxonand topology-dependent. Alternative hypotheses of symphytognathoid non-monophyly based on molecular data (e.g., Dimitrov et al., 2012Dimitrov et al., , 2017Wheeler et al., 2017;Fernández et al., 2018;Kallal et al., 2021), where symphytognathoid families are mostly unrelated to each other, might provide a different hypothesis where the anterior book lungs are mostly the symplesiomorphic condition, with tracheae evolving independently in or within each family. An interesting exception might occur in the topologies in which Anapidae and Symphytognathidae are closely related (e.g., in the hypotheses of Dimitrov et al., 2012Dimitrov et al., , 2017Wheeler et al., 2017), the regain of book lungs could result, as is the case in our study, in a distal clade within Anapidae. ...
... However, it is not evident whether this is a direct consequence of body size, nor how the process of miniaturization affects this correlation (Schütt, 2003;Dunlop, 2019). For example, a link between smaller body size and further reduction of the book lungs (i.e., in number of leaves) is unclear for symphytognathoids, in particular given that the current phylogenetic hypotheses (e.g., Kallal et al., 2021;Kulkarni et al., 2021) imply that "reduced" book lungs have originated from anterior tracheae. Also, given their inherent minute size, any correlation between symphytognathoid body size and anterior book lung leaf number might be expected to be susceptible to the decimals of millimeters. ...
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Spiders are unique in having a dual respiratory system with book lungs and tracheae, and most araneomorph spiders breathe simultaneously via book lungs and tracheae, or tracheae alone. The respiratory organs of spiders are diverse but relatively conserved within families. The small araneoid spiders of the symphytognathoid clade exhibit a remarkably high diversity of respiratory organs and arrangements, unparalleled by any other group of ecribellate orb weavers. In the present study, we explore and review the diversity of symphytognathoid respiratory organs. Using a phylogenetic comparative approach, we reconstruct the evolution of the respiratory system of symphytognathoids based on the most comprehensive phylogenetic frameworks to date. There are no less than 22 different respiratory system configurations in symphytognathoids. The phylogenetic reconstructions suggest that the anterior tracheal system evolved from fully developed book lungs and, conversely, reduced book lungs have originated independently at least twice from its homologous tracheal conformation. Our hypothesis suggests that structurally similar book lungs might have originated through different processes of tracheal transformation in different families. In symphytognathoids, the posterior tracheal system has either evolved into a highly branched and complex system or it is completely lost. No evident morphological or behavioral features satisfactorily explains the exceptional variation of the symphytognathoid respiratory organs.
... Oecobiidae (wall spiders) have historically been considered to be closely related to Hersiliidae (long-spinneret spiders) on the basis of both morphological and behavioral characters, such as the capture behavior in which the spider circles rapidly around the prey while placing threads on it, which attaches the prey to the substrate (details in Glatz 1967), and molecular data (Coddington & Levi 1991;Hormiga & Griswold 2014). However, some recent studies have suggested that Oecobiidae is more closely allied to orb-weaver spiders (Garrison et al. 2016;Wheeler et al. 2016;Fernández et al. 2018;Coddington et al. 2019;Kallal et al. 2020;Kulkarni et al. 2021), either maintaining a close relationship with Hersiliidae (Wheeler et al. 2016;Fernández et al. 2018;Kallal et al. 2020;Kulkarni et al. 2021) or placing it closer to the cribellate orb weavers Uloboridae (Garrison et al. 2016), though in this case Hersiliidae was not included in the analysis (Fig. 1). These phylogenetic hypotheses raise questions about the homology of web structures and web building behaviors in these families. ...
... Oecobiidae (wall spiders) have historically been considered to be closely related to Hersiliidae (long-spinneret spiders) on the basis of both morphological and behavioral characters, such as the capture behavior in which the spider circles rapidly around the prey while placing threads on it, which attaches the prey to the substrate (details in Glatz 1967), and molecular data (Coddington & Levi 1991;Hormiga & Griswold 2014). However, some recent studies have suggested that Oecobiidae is more closely allied to orb-weaver spiders (Garrison et al. 2016;Wheeler et al. 2016;Fernández et al. 2018;Coddington et al. 2019;Kallal et al. 2020;Kulkarni et al. 2021), either maintaining a close relationship with Hersiliidae (Wheeler et al. 2016;Fernández et al. 2018;Kallal et al. 2020;Kulkarni et al. 2021) or placing it closer to the cribellate orb weavers Uloboridae (Garrison et al. 2016), though in this case Hersiliidae was not included in the analysis (Fig. 1). These phylogenetic hypotheses raise questions about the homology of web structures and web building behaviors in these families. ...
... The tent is attached to the substrate at several pillars, forming arched structures between each pair of pillars, which the spiders use to move in and out of the tent. The web of Oecobius annulipes also has long radial threads that extend beyond the carpet, and cribellate silk threads Kallal et al. (2020) and Kulkarni et al. (2021); (B) shows a close phylogenetic relationship between Oecobiidae and Hersiliidae, following Wheeler et al. (2016); (C) shows a close relationship between Oecobiidae and Uloboridae, following Garrison et al. (2016). The asterisk indicates groups with orb webs, and the dashed lines indicate other lineages not included. ...
... Phylogenomic and transcriptomic methods have (Ramírez, 2014); (b) Sanger molecular data (Wheeler et al., 2017); (c) Sanger molecular (Moradmand et al., 2014); (d) total evidence ; (e) genomic (UCE) data . also recently been applied in higher-level systematics and evolutionary studies of spiders (Fernández et al., 2018;Garrison et al., 2016;Kallal et al., 2020;Kulkarni et al., 2020;Opatova et al., 2020;Ramírez et al., 2021;Xu et al., 2020). Although some spider clades have been studied using a combined analysis of morphology and traditional molecular markers (Blackledge et al., 2009;Bond et al., 2012;Polotow et al., 2015), none have yet been explored using the combination of genomic, transcriptomic, traditional loci and morphological data. ...
... Outgroup sampling was designed to include a broad representation of the Retrolateral Tibial Apophysis clade (which includes Dionycha), including most families in the "marronoid" and Oval Calamistrum clade (OCC; Wheeler et al., 2017). A zodariid spider was used to root the tree based on most recent phylogenetic results (Kallal et al., 2020;Wheeler et al., 2017). Representatives of all families currently and formerly placed in Dionycha were sampled for at least two datasets (phenotypic, genomic, or legacy markers). ...
... One of the key families to understanding dionychan evolution is Sparassidae. This family has been phylogenetically placed in Dionycha (Ramírez, 2014), as sister to the RTA clade (Moradmand et al., 2014), as sister to Dionycha + OCC (Wheeler et al., 2017) and as sister to marronoids (Fernández et al., 2018;Kallal et al., 2020;Kulkarni et al., 2020). Here we corroborated the latter hypothesis with strong support. ...
Article
The importance of morphology in the phylogenomic era has recently gained attention, but relatively few studies have combined both types of information when inferring phylogenetic relationships. Sanger sequencing legacy data can also be important for understanding evolutionary relationships. The possibility of combining genomic, morphological and Sanger data in one analysis seems compelling, permitting a more complete sampling and yielding a comprehensive view of the evolution of a group. Here we used these three data types to elucidate the systematics and evolution of the Dionycha, a highly diverse group of spiders relatively underrepresented in phylogenetic studies. The datasets were analyzed separately and combined under different inference methods, including a novel approach for analyzing morphological matrices with commonly used evolutionary models. We tested alternative hypotheses of relationships and performed simulations to investigate the accuracy of our findings. We provide a comprehensive and thorough phylogenetic hypothesis for Dionycha that can serve as a robust framework to test hypotheses about the evolution of key characters. We also show that morphological data might have a phylogenetic impact, even when massively outweighed by molecular data. Our approach to analyze morphological data may serve as an alternative to the proposed practice of arbitrarily partitioning, weighting, and choosing between parsimony and stochastic models. As a result of our findings, we propose Trachycosmidae new rank for a group of Australian genera formerly included in Trochanteriidae and Gallieniellidae, and consider Ammoxenidae as a junior synonym of Gnaphosidae. We restore the family rank for Prodidomidae, but transfer the subfamily Molycriinae to Gnaphosidae. Drassinella is transferred to Liocranidae, Donuea to Corinnidae, and Mahafalytenus to Viridasiidae.
... Spiders (order Araneae), the largest group within Arachnida, with at least ~49,000 known species (World Spider Catalog, 2021), is a highly diverse group of predators that can be found in nearly all terrestrial ecosystems (Figure 1). Recent studies have greatly helped to elucidate their phylogeny and delimitate its main evolutionary lineages (Wheeler et al., 2017;Kallal et al., 2020). ...
... Tree of life of the order Araneae. Relationships and divergence time estimates followed(Kallal et al., 2020). Main evolutionary lineages and taxonomic groups within spiders indicated as grey clades; the number in brackets indicates the estimated number of included families.Phylogenetic relationships of species with genomic information are highlighted (orange lines).Species used for the annotation and homology-based searches of D. silvatica genome are denoted with an asterisk. ...
Article
We present the chromosome-level genome assembly of Dysdera silvatica Schmidt, 1981, a nocturnal ground-dwelling spider endemic from the Canary Islands. The genus Dysdera has undergone a remarkable diversification in this archipelago mostly associated with shifts in the level of trophic specialization, becoming an excellent model to study the genomic drivers of adaptive radiations. The new assembly (1.37 Gb; scaffold N50 of 174.2 Mb), was performed using the chromosome conformation capture scaffolding technique, represents a continuity improvement of more than 4,500 times with respect to the previous version. The seven largest scaffolds or pseudochromosomes, which cover 87% of the total assembly size, likely correspond with the seven chromosomes of the karyotype of this species, including a characteristic large X chromosome. To illustrate the value of this new resource we performed a comprehensive analysis of the two major arthropod chemoreceptor gene families (i.e., gustatory and ionotropic receptors). We identified 545 chemoreceptor sequences distributed across all pseudochromosomes, with a notable underrepresentation in the X chromosome. At least 54% of them localize in 83 genomic clusters with a significantly lower evolutionary distances between them than the average of the family, suggesting a recent origin of many of them. This chromosome-level assembly is the first high-quality genome representative of the Synspermiata clade, and just the third among spiders, representing a new valuable resource to gain insights into the structure and organization of chelicerate genomes, including the role that structural variants, repetitive elements and large gene families played in the extraordinary biology of spiders.
... Spiders (order Araneae), the largest group within Arachnida, with at least~49,000 known species (World Spider Catalog, 2021), is a highly diverse group of predators that can be found in nearly all terrestrial ecosystems ( Figure 1). Recent studies have greatly helped to elucidate their phylogeny and delimitate its main evolutionary lineages (Wheeler et al., 2017;Kallal et al., 2020). The nocturnal ground-dwelling genus Dysdera Latreille 1804, which contains 286 species (World Spider Catalog, 2021), mostly with a circum-Mediterranean distribution, represents nearly half of the diversity of the Dysderidae family. ...
... Tables Table 1. Genome assembly statistics Table 2. Genome annotation statistics Table 3. Chromosome level statistics (Kallal et al., 2020). Main evolutionary lineages and taxonomic groups within spiders indicated as grey clades; the number in brackets indicates the estimated number of included families. ...
Preprint
We present the chromosome-level genome assembly of Dysdera silvatica Schmidt, 1981, a nocturnal ground-dwelling spider endemic from the Canary Islands. The genus Dysdera has undergone a remarkable diversification in this archipelago mostly associated with shifts in the level of trophic specialization, becoming an excellent model to study the genomic drivers of adaptive radiations. The new assembly (1.37 Gb; and scaffold N50 of 174.2 Mb), was performed using the chromosome conformation capture scaffolding technique, represents a continuity improvement of more than 4,500 times with respect to the previous version. The seven largest scaffolds or pseudochromosomes cover 87% of the total assembly size and match consistently with the seven chromosomes of the karyotype of this species, including the characteristic large X chromosome. To illustrate the value of this new resource we performed a comprehensive analysis of the two major arthropod chemoreceptor gene families (i.e., gustatory and ionotropic receptors). We identified 545 chemoreceptor sequences distributed across all pseudochromosomes, with a notable underrepresentation in the X chromosome. At least 54% of them localize in 83 genomic clusters with a significantly lower evolutionary distances between them than the average of the family, suggesting a recent origin of many of them. This chromosome-level assembly is the first high-quality genome representative of the Synspermiata clade, and just the third among spiders, representing a new valuable resource to gain insights into the structure and organization of chelicerate genomes, including the role that structural variants, repetitive elements and large gene families played in the extraordinary biology of spiders.
... Ancestral state estimation (ASE), or ancestral state reconstruction, is the process of estimating the evolutionary history of a character on a phylogeny (Cunningham et al., 1998;Donoghue, 1989;Swofford & Maddison, 1987). This process has been used to reveal the evolution of key innovations across the tree of life, such as the evolution of the orb web in spiders (Kallal et al., 2020) and of reproductive mode in squamates (Pyron & Burbrink, 2014), and to explore the early history of major clades such as flowering plants (Sauquet et al., 2017) and eukaryotes (Skejo et al., 2021). In fact, much of what we know about the history and evolutionary dynamics of morphology, ecology and biogeography across deep time-scales rely on ASE algorithms. ...
Article
Modern methods of ancestral state estimation (ASE) incorporate branch length information, and it has been demonstrated that ASEs are more accurate when conducted on the branch lengths most correlated with a character’s evolution; however, a reliable method for choosing between alternate branch length sets for discrete characters has not yet been proposed. In this study, we simulate paired chronograms and phylograms, and generate binary characters that evolve in correlation with one of these. We then investigate (1) the effect of alternate branch lengths on ASE error, and (2) whether phylogenetic signal statistics and/or model‐fit statistic can be used to select the branch lengths most correlated with a binary character. In agreement with previous studies, we find that ASEs are more accurate when conducted on the branch lengths most correlated with the character. Phylogenetic signal statistics show limited utility for selecting the correct branch lengths, but model‐fit statistics are found to be more accurate, with the correct branch lengths generally returning greater model‐fit (lower AICc and BIC values). Using this method to choose between alternate branch length sets is more accurate when tree and character properties are more favorable for model optimization, and when shape differences between alternate phylogenies are greater. Our results indicate that researchers conducting ASEs on discrete characters should carefully consider which branch lengths are appropriate, and, in the absence of other evidence, we suggest estimating model‐fit values over alternate branch length sets and evolutionary models and choosing the branch length/model combination that returns better model fit.
... In addition to carrying out ASTRAL analyses, we used concordance factors (CF) to gain a deeper understanding of how well different genes support the different topologies. As has been demonstrated in other studies using concordance factors (Chan et al., 2020;Kallal et al., 2021;Minh et al., 2020;van Elst et al., 2021), many branches with perfect UFB and SH support have quite low CF values ( Figure S18). In the topology from the NT12_all dataset, these values are extremely low especially for the backbone nodes (average gCF = 7%). ...
Article
The field of molecular phylogenetics is being revolutionized with next‐generation sequencing technologies making it possible to sequence large numbers of genomes for non‐model organisms ushering us into the era of phylogenomics. The current challenge is no longer how to get enough data, but rather how to analyse the data and how to assess the support for the inferred phylogeny. Here, we focus on one of the largest animal groups on the planet – butterflies and moths (order Lepidoptera), whose phylogeny remains unresolved despite several recent phylogenomic studies. In this study, we assess the potential causes and consequences of the conflicting phylogenetic hypotheses. With a dataset consisting of 331 protein‐coding genes and the alignment length over 290,000 base pairs, including 200 taxa representing 83% of lepidopteran superfamilies, we compare phylogenetic hypotheses inferred from amino acid and nucleotide alignments. The resulting two phylogenies are discordant, especially with respect to the placement of the superfamily Gelechioidea, which is likely due to compositional bias and possible other model violations. Furthermore, we employed a series of analyses to dissect our dataset and demonstrate that there is sufficient phylogenetic signal to resolve much – but not all – of the lepidopteran tree of life. The relationships among superfamilies within Ditrysia, the most species rich lepidopteran clade containing 98% of the extant species, remain poorly resolved. We conclude that taxon sampling remains an issue even in phylogenomic analyses and recommend that poorly sampled highly diverse groups, such as Gelechioidea in Lepidoptera, should receive extra attention in the future. Phylogenomics has helped us resolve much of the Lepidoptera tree of life, but the relationships among the superfamilies within Ditrysia, containing 98% of the order's species richness, remain unresolved. One of the unresolved questions is the phylogenetic position of the large microlepidopteran superfamily Gelechioidea, whose placement depends on the type of data analysed, amino acids or nucleotides. The likely reason for this discordance is model violation in phylogenetic inference.
... In spiders, a low body mass may also facilitate long-range dispersal via ballooning or thread-based locomotion (bridging) (Corcobado et al. 2010). The smallest known spiders belong to the Symphytognathidae, Mysmenidae, and Anapidae, all of which build aerial webs (orbs or suspended sheets) (Cardoso and Scharff 2009); these three families are members of the "symphytognathoid" clade (Kulkarni et al. 2021; but see also Kallal et al. 2020). It has been suggested that miniaturization is constrained by minimal organ sizes, most prominently the size of the central nervous system and sensory organs (Eberhard 2007;Quesada et al. 2011). ...
Article
A prominent question in animal research is how the evolution of morphology and ecology interact in the generation of phenotypic diversity. Spiders are some of the most abundant arthropod predators in terrestrial ecosystems and exhibit a diversity of foraging styles. It remains unclear how spider body size and proportions relate to foraging style, and if the use of webs as prey capture devices correlates with changes in body characteristics. Here we present the most extensive dataset to date of morphometric and ecological traits in spiders. We used this dataset to estimate the change in spider body sizes and shapes over deep time and to test if and how spider phenotypes are correlated with their behavioural ecology. We found that phylogenetic variation of most traits best fitted an Ornstein-Uhlenbeck model, which is a model of stabilizing selection. A prominent exception was body length, whose evolutionary dynamics were best explained with a Brownian Motion (free trait diffusion) model. This was most expressed in the araneoid clade (ecribellate orb-weaving spiders and allies) that showed bimodal trends towards either miniaturization or gigantism. Only few traits differed significantly between ecological guilds, most prominently leg length and thickness, and although a multivariate framework found general differences in traits among ecological guilds, it was not possible to unequivocally associate a set of morphometric traits with the relative ecological mode. Long, thin legs have often evolved with aerial webs and a hanging (suspended) locomotion style, but this trend is not general. Eye size and fang length did not differ between ecological guilds, rejecting the hypothesis that webs reduce the need for visual cue recognition and prey immobilization. For the inference of the ecology of species with unknown behaviours, we propose not to use morphometric traits, but rather consult (micro-)morphological characters, such as the presence of certain podal structures. These results suggest that, in contrast to insects, the evolution of body proportions in spiders is unusually stabilized, and ecological adaptations are dominantly realized by behavioural traits and extended phenotypes in this group of predators. This work demonstrates the power of combining recent advances in phylogenomics with trait-based approaches to better understand global functional diversity patterns through space and time.
... We reconstructed the phylogenomic trees using two occupancies (50% and 75%) for the loci captured from the four probe sets, thereby resulting in eight data matrices. The resulting topologies were similar to previous findings (e.g., Kulkarni et al. [58]), and the supports (i.e., bootstrap, gCF, and sCF) of each node were similar between the results of these two datasets (shown in Figure 4B,C). (from 10% to 100%) occupancies (for data, see Table S6). ...
Article
Full-text available
Reduced-representation sequencing (RRS) has made it possible to identify hundreds to thousands of genetic markers for phylogenomic analysis for the testing of phylogenetic hypotheses in non-model taxa. The use of customized probes to capture genetic markers (i.e., ultraconserved element (UCE) approach) has further boosted the efficiency of collecting genetic markers. Three UCE probe sets pertaining to spiders (Araneae) have been published, including one for the suborder Mesothelae (an early diverged spider group), one for Araneae, and one for Arachnida. In the current study, we developed a probe set specifically for the superfamily Araneoidea in spiders. We then combined the three probe sets for Araneoidea, Araneae, and Arachnid into a fourth probe set. In testing the effectiveness of the 4 probe sets, we used the captured loci of the 15 spider genomes in silico (6 from Araneoidea). The combined probe set outperformed all other probe sets in terms of the number of captured loci. The Araneoidea probe set outperformed the Araneae and Arachnid probe sets in most of the included Araneoidea species. The reconstruction of phylogenomic trees using the loci captured from the four probe sets and the data matrices generated from 50% and 75% occupancies indicated that the node linked to the Stegodyphus + RTA (retrolateral tibial apophysis) clade has unstable nodal supports in the bootstrap values, gCFs, and sCFs. Our results strongly indicate that developing ad hoc probe sets for sub-lineages is important in the cases where the origins of a lineage are ancient (e.g., spiders ~380 MYA).
... Cobwebs spun by members of the family Theridiidae and Nesticidae appear less highly organized than orb-webs. However, as cobweb spiders descended from an orb-web weaving ancestor, their webs and their adhesives, can be considered more specialized (Blackledge et al. 2009;Coddington et al. 2019;Kallal et al. 2021). A notable feature of theridiid cobwebs is the placement of adhesive on only short regions at the lower ends of a few threads named gumfoot lines (Argintean et al. 2006;Eberhard et al. 2008). ...
Article
Full-text available
The origin of aggregate silk glands and their production of wet adhesive silks is considered a key innovation of the Araneoidea, a superfamily of spiders that build orb-webs and cobwebs. Orb-web weavers place aggregate glue on an extensible capture spiral, whereas cobweb weavers add it to the ends of strong, stiff fibers, called gumfoot lines. Here we describe the material behavior and quantitative proteomics of the aggregate glues of two cobweb weaving species, the Western black widow, Latrodectus hesperus, and the common house spider, Parasteatoda tepidariorum. For each species respectively, we identified 48 and 33 proteins that were significantly more abundant in the portion of the gumfoot line with glue than in its fibers. These proteins were more highly glycosylated and phosphorylated than proteins found in silk fibers without glue, which likely explains aggregate glue stickiness. Most glue-enriched proteins were of anterior aggregate gland origin, supporting the hypothesis that cobweb weavers' posterior aggregate glue is specialized for another function. We found that cobweb weaver glue droplets are stiffer and tougher than the adhesive of most orb-web weaving species. Attributes of gumfoot glue protein composition that likely contribute to this stiffness include the presence of multiple protein families with conserved cysteine residues, a bimodal distribution of isoelectric points, and families with conserved functions in protein aggregation, all of which should contribute to cohesive protein-protein interactions. House spider aggregate droplets were more responsive to humidity changes than black widow droplets, which could be mediated by differences in protein sequence, post-translational modifications, the non-protein components of the glue droplets, and/or the larger amount of aqueous material that surrounds the adhesive cores of their glue droplets.
... The monotypic genus Hickmania is currently placed in the superfamily Austrochiloidea. This group of spiders forms an early diverging lineage in the evolution of araneomorph spiders (Platnick 1977;Forster et al. 1987;Wheeler et al. 2017;Fernández et al. 2018;Kallal et al. 2021;Kulkarni et al. 2021;Ramírez et al. 2021). Austrochiloids consist of two families, Austrochilidae and Gradungulidae, and are distributed in the southern hemisphere. ...
Article
Hickmania troglodytes is an emblematic cave spider representing a monotypic cribellate spider genus. This is the only Australian lineage of Austrochilidae while the other members of the family are found in southern South America. In addition to being the largest spider in Tasmania, Hickmania is an oddity in Austrochilidae because this is the only lineage in the family bearing posterior book lungs, tarsal spines and an embolar process on male pedipalps. Six-gene Sanger sequences and genome scale data such as ultraconserved elements (UCEs) and transcriptomes have suggested that Hickmania troglodytes is not nested with the family of current classification, Austrochilidae. We studied the phylogenetic placement of Hickmania troglodytes using an increased taxon sample by combining publicly available UCE and UCEs recovered from transcriptomic data in a parsimony and maximum likelihood framework. Based on our phylogenetic results we formally transfer Hickmania troglodytes from Austrochilidae to the family Gradungulidae. The cladistic placement of Hickmania in the family Gradungulidae fits the geographic distribution of both gradungulids (restricted to Australia and New Zealand) and austrochilids (restricted to southern South America) more appropriately.
... Secondly, over the years, different studies about the morphology and relationships among different groups of spiders have accumulated (e.g. Platnick et al., 1991;Griswold et al., 2005;Ram ırez, 2014), and these are now complemented by extensive studies based on molecular data (Wheeler et al., 2017;Fern andez et al., 2018;Kallal et al., 2021;Ram ırez et al., 2021). In particular, the popularization of next-generation sequencing (NGS) during the last decade allowed the massive collection of molecular data, which to a large extent have corroborated the conclusions made based on morphological data, but have also revealed novel or unexpected relationships among spider families. ...
Article
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Filistatids, the crevice weavers, are an ancient family of cribellate spiders without extant close relatives. As one of the first lineages of araneomorph spiders, they present a complicated mixture of primitive and derived characters that make them a key taxon to elucidate the phylogeny of spiders, as well as the evolution of phenotypic characters in this group. Their moderate diversity (187 species in 19 genera) is distributed mainly in arid and semi‐arid subtropical zones of all continents, except Antarctica. The objective of this paper is to generate a comprehensive phylogenetic hypothesis for this family to advance the understanding of its morphological evolution and biogeography, as well as lay the basis for a natural classification scheme. By studying the morphology using optical and electronic microscopy techniques, we produced a matrix of 302 morphological characters coded for a sample of 103 species of filistatids chosen to represent the phylogenetic diversity of the family. In addition, we included sequences of four molecular markers (COI, 16S, H3 and 28S; 3787 aligned positions) of 70 filistatid species. The analysis of the data (morphological, molecular, and combined) consistently indicates the separation of the Filistatidae into two subfamilies, Prithinae and Filistatinae, in addition to supporting several groups of genera: Filistata, Zaitunia and an undescribed genus from Madagascar; Sahastata and Kukulcania; all Prithinae except Filistatinella and Microfilistata; Antilloides and Filistatoides; a large Old World group including Pritha, Tricalamus, Afrofilistata, Labahitha, Yardiella, Wandella and putative new genera; and a South American group formed by Lihuelistata, Pikelinia and Misionella. Pholcoides is transferred to Filistatinae and Microfilistata is transferred to Prithinae, and each represents the sister group to the remaining genera of its own subfamily. Most genera are valid, although Pikelinia is paraphyletic with respect to Misionella, so we consider the two genera as synonyms and propose a few new generic combinations. Considering the new phylogenetic hypothesis, we discuss the evolution of some morphological character systems and the biogeography of the family. The ages of divergence between clades were estimated using a total‐evidence tip‐dating approach by including fossils of Filistatidae and early spider clades; this approach resulted in younger age estimates than those obtained with traditional node‐dating. Filistatidae is an ancient family that started diversifying in the Mesozoic and most genera date to the Cretaceous. Clades displaying transcontinental distributions were most likely affected by continental drift, but at least one clade shows unequivocal signs of transoceanic long‐distance dispersal.
... Among arachnids, spiders have been the subject of particularly intense phylogenomic scrutiny in recent years. Most of these studies have focused on deep to intermediate levels of divergence and have helped to disentangle the evolution of spider webs Fern andez et al., 2014;Kallal et al., 2021) and that of their silk glands and respiratory systems (Ram ırez et al., 2021). In particular spider groups, phylogenomic studies have also led, for example, to unraveling the evolution of sexual dimorphism (Kuntner et al., 2019), coloration (Foley et al., 2020) and morphological traits (Wood et al., 2018), have allowed a better understanding of their biogeography (Xu et al., 2021), and have resulted in broad taxonomic reorganizations (Opatova et al., 2019). ...
Article
RAD sequencing yields large amounts of genome-wide data at a relatively low cost and without requiring previous taxon-specific information, making it ideal for evolutionary studies of highly diversified and neglected organisms. However, concerns about information decay with phylogenetic distance have discouraged its use for assessing supraspecific relationships. Here, using Double Digest Restriction Associated DNA (ddRAD) data, we perform the first deep-level approach to the phylogeny of Zodarion, a highly diversified spider genus. We explore the impact of loci and taxon filtering across concatenated and multispecies coalescent reconstruction methods and investigate the patterns of information dropout in reference to both the time of divergence and the mitochondrial divergence between taxa. We found that relaxed loci-filtering and nested taxon-filtering strategies maximized the amount of molecular information and improved phylogenetic inference. As expected, there was a clear pattern of allele dropout towards deeper time and mitochondrial divergences, but the phylogenetic signal remained strong throughout the phylogeny. Therefore, we inferred topologies that were almost fully resolved, highly supported, and noticeably congruent between setups and inference methods, which highlights overall inconsistency in the taxonomy of Zodarion. Because Zodarion appears to be among the oldest and most mitochondrially diversified spider genera, our results suggest that ddRAD data show high potential for inferring intra-generic relationships across spiders and probably also in other taxonomic groups.
... The program is intended for fast bootstrap calculations. Three papers published in Cladistics during 2019-2020 performed analyses using MPBoot; the MPBoot results in two of those (Kallal et al., 2020;Rasplus et al., 2020) seem unremarkable, but those in the third one (Inoue et al., 2019) are unusual in that they display a relatively strong cladistic structure within a group of over 50 virtually identical specimens of Lampsilis hydiana (for which the likelihood bootstrap tree exhibited virtually no resolution 1 ). As discussed below, this may have been an artefact produced by MPBoot's approximate algorithms, and it seems likely that proper parsimony results would have been more similar to those of maximum-likelihood. ...
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This paper examines the implementation of parsimony methods in the programs PAUP*, MEGA and MPBoot, and compares them with TNT. PAUP* implements standard, well-tested algorithms, and flexible search strategies and options for handling trees; its main drawback is the lack of advanced search algorithms, which makes it difficult to find most parsimonious trees for large and complex datasets. In addition, branch-swapping can be much slower than in TNT for datasets with large numbers of taxa, although this is only occasionally a problem for phylogenomic datasets given that they typically have small numbers of taxa. The parsimony implementation of MEGA has major drawbacks. MEGA often fails to find parsimonious trees because it does not perform all possible branch swapping subtree pruning regrafting (SPR)/tree bisection-reconnection (TBR) rearrangements. It furthermore fails to properly handle ambiguity or multiple equally parsimonious trees, and it uses the same addition sequence for all bootstrap replicates. The latter yields values of group support that depend on the order in which taxa are listed in the dataset. In addition, tree searches are very slow and do not facilitate the exploration of different starting points (as random seed is fixed). MPBoot searches for optimal trees using the ratchet, but it is based on SPR instead of TBR (and only evaluates by default a subset of the SPR rearrangements). MPBoot approximates bootstrap frequencies by first finding a sample of trees and then selecting from those trees for every replicate, without performing a tree-search. The approximation is too rough in many cases, producing serious under- or overestimations of the correct support values and, for most kinds of datasets, slower estimations than can be obtained with TNT. In addition, bootstrapping with PAUP*, MEGA or MPBoot can attribute strong supports to groups that have no support at all under any meaningful concept of support, such as likelihood ratios or Bremer supports. In TNT, this problem is decreased by using the strict consensus tree to represent each replicate, or eliminated entirely by using different approximations of the Bremer support.
... More recent studies based on phylogenomic data have also refuted Pimoidae as circumscribed by morphological data. The transcriptomic analyses of Fernández et al. (2018) and Kallal et al. (2021) support the monophyly of linyphioids but place Weintrauboa as a sister group to the linyphiid clade, rather than to Pimoa. Analyses of ultraconserved elements (Kulkarni et al. 2020 have also supported the monophyly of linyphioids, based on representation of a single pimoid genus (Pimoa). ...
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We address the phylogenetic relationships of pimoid spiders (Pimoidae) using a standard target-gene approach with an extensive taxonomic sample, which includes representatives of the four currently recognized pimoid genera, 26 linyphiid genera, a sample of Physoglenidae, Cyatholipidae and one Tetragnathidae species. We test the monophyly of Pimoidae and Linyphiidae and explore the biogeographic history of the group. Nanoa Hormiga, Buckle and Scharff, 2005 and Pimoa Chamberlin & Ivie, 1943 form a clade which is the sister group of a lineage that includes all Linyphiidae, Weintrauboa Hormiga, 2003 and Putaoa Hormiga and Tu, 2008. Weintrauboa, Putaoa, Pecado and Stemonyphantes form a clade (Stemonyphantinae) sister to all remaining linyphiids. We use the resulting optimal molecular phylogenetic tree to assess hypotheses on the male palp sclerite homologies of pimoids and linyphiids. Pimoidae is redelimited to only include Pimoa and Nanoa. We formalize the transfer from Pimoidae of the genera Weintrauboa and Putaoa to Linyphiidae, re-circumscribe the linyphiid subfamily Stemonyphantinae, and offer revised morphological diagnoses for Pimoidae and Linyphiidae.
... As some lineages spend almost all of their time in webs while others do not build webs, they provide a unique opportunity to directly compare the evolutionary pathways of closely related builders and nonbuilders. As multiple convergent events of web loss and regain are distributed across the spider tree of life (13), there are sufficient replicates to attempt to draw a general conclusion. While all spiders are able to produce silk, the extend of construction behavior differs enormously between builders and nonbuilders: builders construct and dwell in webs or silk-lined burrows, that are involved in foraging and provide a protective and "predictable" environment; nonbuilders, on the other hand, interact directly with variable habitats and use their body for prey capture. ...
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Do animals set the course for the evolution of their lineage when manipulating their environment? This heavily disputed question is empirically unexplored but critical to interpret phenotypic diversity. Here, we tested whether the macroevolutionary rates of body morphology correlate with the use of built artifacts in a megadiverse clade comprising builders and nonbuilders—spiders. By separating the inferred building-dependent rates from background effects, we found that variation in the evolution of morphology is poorly explained by artifact use. Thus natural selection acting directly on body morphology rather than indirectly via construction behavior is the dominant driver of phenotypic diversity.
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Natural silks crafted by spiders comprise some of the most versatile materials known. Artificial silks–based on the sequences of their natural brethren–replicate some desirable biophysical properties and are increasingly utilized in commercial and medical applications today. To characterize the repertoire of protein sequences giving silks their biophysical properties and to determine the set of expressed genes across each unique silk gland contributing to the formation of natural silks, we report here draft genomic and transcriptomic assemblies of Darwin’s bark spider, Caerostris darwini , an orb-weaving spider whose dragline is one of the toughest known biomaterials on Earth. We identify at least 31 putative spidroin genes, with expansion of multiple spidroin gene classes relative to the golden orb-weaver, Trichonephila clavipes . We observed substantial sharing of spidroin repetitive sequence motifs between species as well as new motifs unique to C . darwini . Comparative gene expression analyses across six silk gland isolates in females plus a composite isolate of all silk glands in males demonstrated gland and sex-specific expression of spidroins, facilitating putative assignment of novel spidroin genes to classes. Broad expression of spidroins across silk gland types suggests that silks emanating from a given gland represent composite materials to a greater extent than previously appreciated. We hypothesize that the extraordinary toughness of C . darwini major ampullate dragline silk may relate to the unique protein composition of major ampullate spidroins, combined with the relatively high expression of stretchy flagelliform spidroins whose union into a single fiber may be aided by novel motifs and cassettes that act as molecule-binding helices. Our assemblies extend the catalog of sequences and sets of expressed genes that confer the unique biophysical properties observed in natural silks.
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Synopsis To capture prey otherwise unattainable by muscle function alone, some animal lineages have evolved movements that are driven by stored elastic energy, producing movements of remarkable speed and force. One such example that has evolved multiple times is a trap-jaw mechanism, in which the mouthparts of an animal are loaded with energy as they open to a wide gape and then, when triggered to close, produce a terrific force. Within the spiders (Araneae), this type of attack has thus far solely been documented in the palpimanoid family Mecysmaucheniidae but a similar morphology has also been observed in the distantly related araneoid subfamily Pararchaeinae, leading to speculation of a trap-jaw attack in that lineage as well. Here, using high-speed videography, we test whether cheliceral strike power output suggests elastic-driven movements in the pararchaeine Pararchaea alba. The strike speed attained places P. alba as a moderately fast striker exceeding the slowest mecysmaucheniids, but failing to the reach the most extreme high-speed strikers that have elastic-driven mechanisms. Using microcomputed tomography, we compare the morphology of P. alba chelicerae in the resting and open positions, and their related musculature, and based on results propose a mechanism for cheliceral strike function that includes a torque reversal latching mechanism. Similar to the distantly related trap-jaw mecysmaucheniid spiders, the unusual prosoma morphology in P. alba seemingly allows for highly maneuverable chelicerae with a much wider gape than typical spiders, suggesting that increasingly maneuverable joints coupled with a latching mechanism may serve as a precursor to elastic-driven movements.
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The tetragnathid genus Leucauge includes some of the most common orb-weaving spiders in the tropics. Although some species in this genus have attained relevance as model systems for several aspects of spider biology, our understanding of the generic diversity and evolutionary relationships among the species is poor. In this study we present the first attempt to determine the phylogenetic structure within Leucauge and the relationship of this genus with other genera of Leucauginae. This is based on DNA sequences from the five loci commonly used and Histone H4, used for the first time in spider phylogenetics. We also assess the informativeness of the standard markers and test for base composition biases in the dataset. Our results suggest that Leucauge is not monophyletic since species of the genera Opas, Opadometa, Mecynometa and Alcimosphenus are included within the current circumscription of the genus. Based on a phylogenetic re-circumscription of the genus to fulfil the requirement for monophyly of taxa, Leucauge White, 1841 is deemed to be a senior synonym of the genera Opas Pickard-Cambridge, 1896 revalidated synonymy, Mecynometa Simon, 1894 revalidated synonymy, Opadometa Archer, 1951 new synonymy and Alcimosphenus Simon, 1895 new synonymy. We identify groups of taxa critical for resolving relationships within Leucauginae and describe the limitations of the standard loci for accomplishing these resolutions.
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The arachnid order Schizomida is a relatively understudied group of soil-dwelling predators found on all continents except Antarctica. While efforts to understand their biology are growing, there is still much to know about them. A curious aspect of their morphology is the male flagellum, a sexually dimorphic, tail-like structure which differs in shape across the order and functions in their courtship rituals. The flagellar shape is important for taxonomic classification, yet few efforts have been made to examine shape diversity across the group. Using elliptical Fourier analysis, a type of geometric morphometrics based on shape outline, we quantified shape differences across a combined nearly 550 outlines in the dorsal and lateral views, categorizing them based on genus, family, biogeographic realm, and habitat, with special emphasis on Caribbean and Cuban fauna. We tested for allometric relationships, differences in disparity based on locations and sizes in morphospace among these categories, and for clusters of shapes in morphospace. We found multiple differences in all categories despite apparent overlaps in morphospace, evolutionary allometry, and evidence for discrete clusters in some flagellum shapes. This study can serve as a foundation for further study on the evolution, diversification, and taxonomic utility of the male flagellum.
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Genome-scale data sets are converging on robust, stable phylogenetic hypotheses for many lineages; however, some nodes have shown disagreement across classes of data. We use spiders (Araneae) as a system to identify the causes of incongruence in phylogenetic signal between three classes of data: exons (as in phylotranscriptomics), non-coding regions (included in ultraconserved elements [UCE] analyses), and a combination of both (as in UCE analyses). Gene orthologs, coded as amino acids and nucleotides (with and without third codon positions), were generated by querying published transcriptomes for UCEs, recovering 1,931 UCE loci (codingUCEs). We expected that congeners represented in the codingUCE and UCEs data would form clades in the presence of phylogenetic signal. Non-coding regions derived from UCE sequences were recovered to test the stability of relationships. Phylogenetic relationships resulting from all analyses were largely congruent. All nucleotide data sets from transcriptomes, UCEs, or a combination of both recovered similar topologies in contrast with results from transcriptomes analyzed as amino acids. Most relationships inferred from low occupancy data sets, containing several hundreds of loci, were congruent across Araneae, as opposed to high occupancy data matrices with fewer loci, which showed more variation. Furthermore, we found that low occupancy data sets analyzed as nucleotides (as is typical of UCE data sets) can result in more congruent relationships than high occupancy data sets analyzed as amino acids (as in phylotranscriptomics). Thus, omitting data, through amino acid translation or via retention of only high occupancy loci, may have a deleterious effect in phylogenetic reconstruction.
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Genome-scale data sets are converging on robust, stable phylogenetic hypotheses for many lineages; however, some nodes have shown disagreement across classes of data. We use spiders (Araneae) as a system to identify the causes of incongruence in phylogenetic signal between three classes of data: exons (as in phylotranscriptomics), non-coding regions (included in ultraconserved elements [UCE] analyses), and a combination of both (as in UCE analyses). Gene orthologs, coded as amino acids and nucleotides (with and without third codon positions), were generated by querying published transcriptomes for UCEs, recovering 1,931 UCE loci (codingUCEs). We expected that congeners represented in the codingUCE and UCEs data would form clades in the presence of phylogenetic signal. Non-coding regions derived from UCE sequences were recovered to test the stability of relationships. Phylogenetic relationships resulting from all analyses were largely congruent. All nucleotide data sets from transcriptomes, UCEs, or a combination of both recovered similar topologies in contrast with results from transcriptomes analyzed as amino acids. Most relationships inferred from low occupancy data sets, containing several hundreds of loci, were congruent across Araneae, as opposed to high occupancy data matrices with fewer loci, which showed more variation. Furthermore, we found that low occupancy data sets analyzed as nucleotides (as is typical of UCE data sets) can result in more congruent relationships than high occupancy data sets analyzed as amino acids (as in phylotranscriptomics). Thus, omitting data, through amino acid translation or via retention of only high occupancy loci, may have a deleterious effect in phylogenetic reconstruction.
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The common ancestor of spiders likely used silk to line burrows or make simple webs, with specialized spinning organs and aerial webs originating with the evolution of the megadiverse "true spiders" (Araneomorphae). The base of the araneomorph tree also concentrates the greatest number of changes in respiratory structures, a character system whose evolution is still poorly understood, and that might be related to the evolution of silk glands. Emphasizing a dense sampling of multiple araneomorph lineages where tracheal systems likely originated, we gathered genomic-scale data and reconstructed a phylogeny of true spiders. This robust phylogenomic framework was used to conduct maximum likelihood and Bayesian character evolution analyses for respiratory systems, silk glands, and aerial webs, based on a combination of original and published data. Our results indicate that in true spiders, posterior book lungs were transformed into morphologically similar tracheal systems six times independently, after the evolution of novel silk gland systems and the origin of aerial webs. From these comparative data we put forth a novel hypothesis that early-diverging web building spiders were faced with new energetic demands for spinning, which prompted the evolution of similar tracheal systems via convergence; we also propose tests of predictions derived from this hypothesis.
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We implement two measures for quantifying genealogical concordance in phylogenomic datasets: the gene concordance factor (gCF) and the novel site concordance factor (sCF). For every branch of a reference tree, gCF is defined as the percentage of "decisive" gene trees containing that branch. This measure is already in wide usage, but here we introduce a package that calculates it while accounting for variable taxon coverage among gene trees. sCF is a new measure defined as the percentage of decisive sites supporting a branch in the reference tree. gCF and sCF complement classical measures of branch support in phylogenetics by providing a full description of underlying disagreement among loci and sites. An easy to use implementation and tutorial is freely available in the IQ-TREE software package (http://www.iqtree.org).
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Studies in evolutionary biology and biogeography increasingly rely on the estimation of dated phylogenetic trees using molecular clocks. In turn, the calibration of such clocks is critically dependent on external evidence (i.e. fossils) anchoring the ages of particular nodes to known absolute ages. In recent years, a plethora of new fossil spiders, especially from the Mesozoic, have been described, while the number of studies presenting dated spider phylogenies based on fossil calibrations increased sharply. We critically evaluate 44 of these studies, which collectively employed 67 unique fossils in 180 calibrations. Approximately 54% of these calibrations are problematic, particularly regarding unsupported assignment of fossils to extant clades (44%) and crown (rather than stem) dating (9%). Most of these cases result from an assumed equivalence between taxonomic placement of fossils and their phylogenetic position. To overcome this limitation, we extensively review the literature on fossil spiders, with a special focus on putative synapomorphies and the phylogenetic placement of fossil species with regard to their importance for calibrating higher taxa (families and above) in the spider tree of life. We provide a curated list including 41 key fossils intended to be a basis for future estimations of dated spider phylogenies. In a second step, we use a revised set of 23 calibrations to estimate a new dated spider tree of life based on transcriptomic data. The revised placement of key fossils and the new calibrated tree are used to resolve a long‐standing debate in spider evolution – we tested whether there has been a major turnover in the spider fauna between the Mesozoic and Cenozoic. At least 17 (out of 117) extant families have been recorded from the Cretaceous, implying that at least 41 spider lineages in the family level or above crossed the Cretaeous–Paleogene (K–Pg) boundary. The putative phylogenetic affinities of families known only from the Mesozoic suggest that at least seven Cretaceous families appear to have no close living relatives and might represent extinct lineages. There is no unambiguous fossil evidence of the retrolateral tibial apophysis clade (RTA‐clade) in the Mesozoic, although molecular clock analyses estimated the major lineages within this clade to be at least ∼100 million years old. Our review of the fossil record supports a major turnover showing that the spider faunas in the Mesozoic and the Cenozoic are very distinct at high taxonomic levels, with the Mesozoic dominated by Palpimanoidea and Synspermiata, while the Cenozoic is dominated by Araneoidea and RTA‐clade spiders.
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Modeling discrete phenotypic traits for either ancestral character state reconstruction or morphology-based phylogenetic inference suffers from ambiguities of character coding, homology assessment, dependencies, and selection of adequate models. These drawbacks occur because trait evolution is driven by two key processes-hierarchical and hidden-which are not accommodated simultaneously by the available phylogenetic methods. The hierarchical process refers to the dependencies between anatomical body parts, while the hidden process refers to the evolution of gene regulatory networks (GRNs) underlying trait development. Herein, I demonstrate that these processes can be efficiently modeled using structured Markov models (SMM) equipped with hidden states, which resolves the majority of the problems associated with discrete traits. Integration of SMM with anatomy ontologies can adequately incorporate the hierarchical dependencies, while the use of the hidden states accommodates hidden evolution of GRNs and substitution rate heterogeneity. I assess the new models using simulations and theoretical synthesis. The new approach solves the long-standing "tail color problem," in which the trait is scored for species with tails of different colors or no tails. It also presents a previously unknown issue called the "two-scientist paradox," in which the nature of coding the trait and the hidden processes driving the trait's evolution are confounded; failing to account for the hidden process may result in a bias, which can be avoided by using hidden state models. All this provides a clear guideline for coding traits into characters. This article gives practical examples of using the new framework for phylogenetic inference and comparative analysis.
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Physical structures built by animals challenge our understanding of biological processes and inspire the development of smart materials and green architecture. It is thus indispensable to understand the drivers, constraints and dynamics that lead to the emergence and modification of building behaviour. Here, we demonstrate that spider web diversification repeatedly followed strikingly similar evolutionary trajectories, guided by physical constraints. We found that the evolution of suspended webs that intercept flying prey coincided with small changes in silk anchoring behaviour with considerable effects on the robustness of web attachment. The use of nanofiber based capture threads (cribellate silk) conflicts with the behavioural enhancement of web attachment, and the repeated loss of this trait was frequently followed by physical improvements of web anchor structure. These findings suggest that the evolution of building behaviour may be constrained by major physical traits limiting its role in rapid adaptation to a changing environment. This article is protected by copyright. All rights reserved
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Proper biological interpretation of a phylogeny can sometimes hinge on the placement of key taxa-or fail when such key taxa are not sampled. In this light, we here present the first attempt to investigate (though not conclusively resolve) animal relationships using genome-scale data from all phyla. Results from the site-heterogeneous CAT + GTR model recapitulate many established major clades, and strongly confirm some recent discoveries, such as a monophyletic Lophophorata, and a sister group relationship between Gnathifera and Chaetognatha, raising continued questions on the nature of the spiralian ancestor. We also explore matrix construction with an eye towards testing specific relationships; this approach uniquely recovers support for Panarthropoda, and shows that Lophotrochozoa (a subclade of Spiralia) can be constructed in strongly conflicting ways using different taxon- and/or orthologue sets. Dayhoff-6 recoding sacrifices information, but can also reveal surprising outcomes, e.g. full support for a clade of Lophophorata and Entoprocta + Cycliophora, a clade of Placozoa + Cnidaria, and raising support for Ctenophora as sister group to the remaining Metazoa, in a manner dependent on the gene and/or taxon sampling of the matrix in question. Future work should test the hypothesis that the few remaining uncertainties in animal phylogeny might reflect violations of the various stationarity assumptions used in contemporary inference methods.
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Instances of sexual size dimorphism (SSD) provide the context for rigorous tests of biological rules of size evolution, such as Cope's rule (phyletic size increase), Rensch's rule (allometric patterns of male and female size), as well as male and female body size optima. In certain spider groups, such as the golden orbweavers (Nephilidae), extreme female-biased SSD (eSSD, female:male body length $\ge$2) is the norm. Nephilid genera construct webs of exaggerated proportions, which can be aerial, arboricolous, or intermediate (hybrid). First, we established the backbone phylogeny of Nephilidae using 367 anchored hybrid enrichment markers, then combined these data with classical markers for a reference species-level phylogeny. Second, we used the phylogeny to test Cope and Rensch's rules, sex specific size optima, and the coevolution of web size, type, and features with female and male body size and their ratio, SSD. Male, but not female, size increases significantly over time, and refutes Cope's rule. Allometric analyses reject the converse, Rensch's rule. Male and female body sizes are uncorrelated. Female size evolution is random, but males evolve toward an optimum size (3.2-4.9 mm). Overall, female body size correlates positively with absolute web size. However, intermediate sized females build the largest webs (of the hybrid type), giant female Nephila and Trichonephila build smaller webs (of the aerial type), and the smallest females build the smallest webs (of the arboricolous type). We propose taxonomic changes based on the criteria of clade age, monophyly and exclusivity, classification information content, and diagnosability. Spider families, as currently defined, tend to be between 37 million years old and 98 million years old, and Nephilidae is estimated at 133 Ma (97-146), thus deserving family status. We, therefore, resurrect the family Nephilidae Simon 1894 that contains Clitaetra Simon 1889, the Cretaceous GeratonephilaPoinar and Buckley (2012), Herennia Thorell 1877, IndoetraKuntner 2006, new rank, Nephila Leach 1815, Nephilengys L. Koch 1872, Nephilingis Kuntner 2013, Palaeonephila Wunderlich 2004 from Tertiary Baltic amber, and TrichonephilaDahl 1911, new rank. We propose the new clade Orbipurae to contain Araneidae Clerck 1757, Phonognathidae Simon 1894, new rank, and Nephilidae. Nephilid female gigantism is a phylogenetically ancient phenotype (over 100 Ma), as is eSSD, though their magnitudes vary by lineage.
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The new genus and species Myrmecicultor chihuahuensis Ramírez, Grismado, and Ubick is described and proposed as the type of the new family, Myrmecicultoridae Ramírez, Grismado, and Ubick. The species is ecribellate, with entelegyne genitalia, two tarsal claws, without claw tufts, and the males have a retrolateral palpal tibial apophysis. Some morphological characters suggest a possible relationship with Zodariidae or Prodidomidae, but the phylogenetic analysis of six markers from the mitochondrial (12S rDNA, 16S rDNA, cytochrome oxidase subunit I) and nuclear (histone H3, 18S rDNA, 28S rDNA) genomes indicate that M. chihuahuensis is a separate lineage emerging near the base of the Dionycha and the Oval Calamistrum clade. The same result is obtained when the molecular data are combined with a dataset of morphological characters. Specimens of M. chi-huahuensis were found associated with three species of harvester ants, Pogonomyrmex rugosus, Novomessor albisetosis, and Novomessor cockerelli, and were collected in pitfall traps when the ants are most active. The known distribution spans the Big Bend region of Texas (Presidio, Brewster, and Hudspeth counties), to Coahuila (Cuatro Ciénegas) and Aguascalientes (Tepezalá), Mexico.
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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.
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Much genomic-scale, especially transcriptomic, data on spider phylogeny has accumulated in the last few years. These data have recently been used to investigate the diverse architectures and the origin of spider webs, concluding that the ancestral spider spun no foraging web, that spider webs evolved de novo 10-14 times, and that the orb web evolved at least three times. These findings in fact result from a particular phylogenetic character coding strategy, specifically coding the absence of webs as logically equivalent, and homologous to, 10 other observable (i.e., not absent) web architectures. ''Absence'' of webs should be regarded as inapplicable data. To be analyzed properly by character optimization algorithms, it should be coded as ''?'' because these codes-or their equivalent-are handled differently by such algorithms. Additional problems include critical misspellings of taxon names from one analysis to the next (misspellings cause some optimization algorithms to drop terminals, which affects taxon sampling and results), and mistakes in spider natural history. In sum, the method causes character optimization algorithms to produce counter-intuitive results, and does not distinguish absence from secondary loss. Proper treatment of missing entries and corrected data instead imply that foraging webs are primitive for spiders and that webs have been lost ∼5-7 times, not gained 10-14 times. The orb web, specifically, may be homologous (originated only once) although lost 2-6 times.
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Microhabitat changes are thought to be among the main drivers of diversification. However, this conclusion is mostly based on studies on vertebrates. Here, we investigate the influence of microhabitat on diversification rates in pholcid spiders (Araneae, Pholcidae). Diversification analyses were conducted in the framework of the largest molecular phylogeny of pholcid spiders to date based on three nuclear and three mitochondrial loci from 600 species representing more than 85% of the currently described pholcid genera.
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Understanding the genealogical relationships among the arachnid orders is an onerous task, but fossils have aided in anchoring some branches of the arachnid tree of life. The discovery of Palaeozoic fossils with characters found in both extant spiders and other arachnids provided evidence for a series of extinctions of what was thought to be a grade, Uraraneida, that led to modern spiders. Here, we report two extraordinarily well-preserved Mesozoic members of Uraraneida with a segmented abdomen, multi-articulate spinnerets with well-defined spigots, modified male palps, spider-like chelicerae and a uropygid-like telson. The new fossils, belonging to the species Chimerarachne yingi, were analysed phylogenetically in a large data matrix of extant and extinct arachnids under a diverse regime of analytical conditions, most of which resulted in placing Uraraneida as the sister clade of Araneae (spiders). The phylogenetic placement of this arachnid fossil extends the presence of spinnerets and modified palps more basally in the arachnid tree than was previously thought. Ecologically, the new fossil extends the record of Uraraneida 170 million years towards the present, thus showing that uraraneids and spiders co-existed for a large fraction of their evolutionary history.
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Spiders (Araneae) are a hugely successful lineage with a long history. Details of their origins remain obscure, with little knowledge of their stem group and few insights into the sequence of character acquisition during spider evolution. Here, we describe Chimerarachne yingi gen. et sp. nov., a remarkable arachnid from the mid-Cretaceous (approximately 100 million years ago) Burmese amber of Myanmar, which documents a key transition stage in spider evolution. Like uraraneids, the two fossils available retain a segmented opisthosoma bearing a whip-like telson, but also preserve two traditional synapomorphies for Araneae: a male pedipalp modified for sperm transfer and well-defined spinnerets resembling those of modern mesothele spiders. This unique character combination resolves C. yingi within a clade including both Araneae and Uraraneida; however, its exact position relative to these orders is sensitive to different parameters of our phylogenetic analysis. Our new fossil most likely represents the earliest branch of the Araneae, and implies that there was a lineage of tailed spiders that presumably originated in the Palaeozoic and survived at least into the Cretaceous of Southeast Asia.
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Background: The nonparametric bootstrap is widely used to measure the branch support of phylogenetic trees. However, bootstrapping is computationally expensive and remains a bottleneck in phylogenetic analyses. Recently, an ultrafast bootstrap approximation (UFBoot) approach was proposed for maximum likelihood analyses. However, such an approach is still missing for maximum parsimony. Results: To close this gap we present MPBoot, an adaptation and extension of UFBoot to compute branch supports under the maximum parsimony principle. MPBoot works for both uniform and non-uniform cost matrices. Our analyses on biological DNA and protein showed that under uniform cost matrices, MPBoot runs on average 4.7 (DNA) to 7 times (protein data) (range: 1.2-20.7) faster than the standard parsimony bootstrap implemented in PAUP*; but 1.6 (DNA) to 4.1 times (protein data) slower than the standard bootstrap with a fast search routine in TNT (fast-TNT). However, for non-uniform cost matrices MPBoot is 5 (DNA) to 13 times (protein data) (range:0.3-63.9) faster than fast-TNT. We note that MPBoot achieves better scores more frequently than PAUP* and fast-TNT. However, this effect is less pronounced if an intensive but slower search in TNT is invoked. Moreover, experiments on large-scale simulated data show that while both PAUP* and TNT bootstrap estimates are too conservative, MPBoot bootstrap estimates appear more unbiased. Conclusions: MPBoot provides an efficient alternative to the standard maximum parsimony bootstrap procedure. It shows favorable performance in terms of run time, the capability of finding a maximum parsimony tree, and high bootstrap accuracy on simulated as well as empirical data sets. MPBoot is easy-to-use, open-source and available at http://www.cibiv.at/software/mpboot .
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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.
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Funnel webs are common and widespread taxonomically, but little is known about how they are built or details of their structure. Aglaoctenus castaneus (Mello-Leitão, 1942) (Lycosidae) builds horizontal, densely meshed funnel webs of non-adhesive silk, with a tangle of lines above. Web construction behavior was unique in that the spider frequently laid swaths of lines rather than simple drag lines, both to float bands of fine lines on the breeze as bridges to distant objects and to fill in the sheet. Spiders utilized special spinneret movements to widen the swaths of lines that they laid on sheets. These movements have not been seen in web construction by other araneomorphs, but are were similar to and perhaps evolutionarily derived from those used during prey wrapping by many other species. Observations, made with a compound microscope, of the construction behavior of the agelenid Melpomene sp. O.P. Cambridge 1898, and of lines and attachments in sheets of these species and another funnel web spider, the zoropsid Tengella radiata (Kulczyński, 1909) demonstrated the possibly general nature of including obstacles in the web. This probably disadvantageous behavior may be related to constraints in selecting web sites imposed by the need for sheltered retreats, or to the spider's inability to remove preliminary lines. The observation also showed the importance of further improvements in the discriminations made between "sheet" and "brushed" webs in recent discussions of spider web evolution.
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In the mid-2000s, molecular phylogenetics turned into phylogenomics, a development that improved the resolution of phylogenetic trees through a dramatic reduction in stochastic error. While some then predicted “the end of incongruence”, it soon appeared that analysing large amounts of sequence data without an adequate model of sequence evolution amplifies systematic error and leads to phylogenetic artefacts. With the increasing flood of (sometimes low-quality) genomic data resulting from the rise of high-throughput sequencing, a new type of error has emerged. Termed here “data errors”, it lumps together several kinds of issues affecting the construction of phylogenomic supermatrices (e.g., sequencing and annotation errors, contaminant sequences). While easy to deal with at a single-gene scale, such errors become very difficult to avoid at the genomic scale, both because hand curating thousands of sequences is prohibitively time-consuming and because the suitable automated bioinformatics tools are still in their infancy. In this paper, we first review the pitfalls affecting the construction of supermatrices and the strategies to limit their adverse effects on phylogenomic inference. Then, after discussing the relative non-issue of missing data in supermatrices, we briefly present the approaches commonly used to reduce systematic error.
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Nicodamoidea (Nicodamidae plus Megadictynidae) and Araneoidea composition and relationships are consistent with recent analyses. We did not obtain resolution for the titanoecoids (Titanoecidae and Phyxelididae), but the Retrolateral Tibial Apophysis clade is well supported. Penestomidae, and probably Homalonychidae, are part of Zodarioidea, although the latter family was set apart by recent transcriptomic analyses. Our data support a large group that we call the marronoid clade (including the families Amaurobiidae, Desidae, Dictynidae, Hahniidae, Stiphidiidae, Agelenidae and Toxopidae). The circumscription of most marronoid families is redefined here. Amaurobiidae include the Amaurobiinae and provisionally Macrobuninae. We transfer Malenellinae (Malenella, from Anyphaenidae), Chummidae (Chumma) (new syn.) and Tasmarubriinae (Tasmarubrius, Tasmabrochus and Teeatta, from Amphinectidae) to Macrobuninae. Cybaeidae are redefined to include Calymmaria, Cryphoeca, Ethobuella and Willisius (transferred from Hahniidae), and Blabomma and Yorima (transferred from Dictynidae). Cycloctenidae are redefined to include Orepukia (transferred from Agelenidae) and Pakeha and Paravoca (transferred from Amaurobiidae). Desidae are redefined to include five subfamilies: Amphinectinae, with Amphinecta, Mamoea, Maniho, Paramamoea and Rangitata (transferred from Amphinectidae); Ischaleinae, with Bakala and Manjala (transferred from Amaurobiidae) and Ischalea (transferred from Stiphidiidae); Metaltellinae, with Austmusia, Buyina, Calacadia, Cunnawarra, Jalkaraburra, Keera, Magua, Metaltella, Penaoola and Quemusia; Porteriinae (new rank), with Baiami, Cambridgea, Corasoides and Nanocambridgea (transferred from Stiphidiidae); and Desinae, with Desis, and provisionally Poaka (transferred from Amaurobiidae) and Barahna (transferred from Stiphidiidae). Argyroneta is transferred from Cybaeidae to Dictynidae. Cicurina is transferred from Dictynidae to Hahniidae. The genera Neoramia (from Agelenidae) and Aorangia, Marplesia and Neolana (from Amphinectidae) are transferred to Stiphidiidae. The family Toxopidae (restored status) includes two subfamilies: Myroinae, with Gasparia, Gohia, Hulua, Neomyro, Myro, Ommatauxesis and Otagoa (transferred from Desidae); and Toxopinae, with Midgee and Jamara, formerly Midgeeinae, new syn. (transferred from Amaurobiidae) and Hapona, Laestrygones, Lamina, Toxops and Toxopsoides (transferred from Desidae). We obtain a monophyletic Oval Calamistrum clade and Dionycha; Sparassidae, however, are not dionychans, but probably the sister group of those two clades. The composition of the Oval Calamistrum clade is confirmed (including Zoropsidae, Udubidae, Ctenidae, Oxyopidae, Senoculidae, Pisauridae, Trechaleidae, Lycosidae, Psechridae and Thomisidae), affirming previous findings on the uncertain relationships of the “ctenids” Ancylometes and Cupiennius, although a core group of Ctenidae are well supported. Our data were ambiguous as to the monophyly of Oxyopidae. In Dionycha, we found a first split of core Prodidomidae, excluding the Australian Molycriinae, which fall distantly from core prodidomids, among gnaphosoids. The rest of the dionychans form two main groups, Dionycha part A and part B. The former includes much of the Oblique Median Tapetum clade (Trochanteriidae, Gnaphosidae, Gallieniellidae, Phrurolithidae, Trachelidae, Gnaphosidae, Ammoxenidae, Lamponidae and the Molycriinae), and also Anyphaenidae and Clubionidae. Orthobula is transferred from Phrurolithidae to Trachelidae. Our data did not allow for complete resolution for the gnaphosoid families. Dionycha part B includes the families Salticidae, Eutichuridae, Miturgidae, Philodromidae, Viridasiidae, Selenopidae, Corinnidae and Xenoctenidae (new fam., including Xenoctenus, Paravulsor and Odo, transferred from Miturgidae, as well as Incasoctenus from Ctenidae). We confirm the inclusion of Zora (formerly Zoridae) within Miturgidae.
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Species tree reconstruction is complicated by effects of incomplete lineage sorting, commonly modeled by the multi-species coalescent model (MSC). While there has been substantial progress in developing methods that estimate a species tree given a collection of gene trees, less attention has been paid to fast and accurate methods of quantifying support. In this article, we propose a fast algorithm to compute quartet-based support for each branch of a given species tree with regard to a given set of gene trees. We then show how the quartet support can be used in the context of the MSC to compute (1) the local posterior probability (PP) that the branch is in the species tree and (2) the length of the branch in coalescent units. We evaluate the precision and recall of the local PP on a wide set of simulated and biological datasets, and show that it has very high precision and improved recall compared with multi-locus bootstrapping. The estimated branch lengths are highly accurate when gene tree estimation error is low, but are underestimated when gene tree estimation error increases. Computation of both the branch length and local PP is implemented as new features in ASTRAL.
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Spiders (Order Araneae) are massively abundant generalist arthropod predators that are found in nearly every ecosystem on the planet and have persisted for over 380 million years. Spiders have long served as evolutionary models for studying complex mating and web spinning behaviors, key innovation and adaptive radiation hypotheses, and have been inspiration for important theories like sexual selection by female choice. Unfortunately, past major attempts to reconstruct spider phylogeny typically employing the “usual suspect” genes have been unable to produce a well-supported phylogenetic framework for the entire order. To further resolve spider evolutionary relationships we have assembled a transcriptome-based data set comprising 70 ingroup spider taxa. Using maximum likelihood and shortcut coalescence-based approaches, we analyze eight data sets, the largest of which contains 3,398 gene regions and 696,652 amino acid sites forming the largest phylogenomic analysis of spider relationships produced to date. Contrary to long held beliefs that the orb web is the crowning achievement of spider evolution, ancestral state reconstructions of web type support a phylogenetically ancient origin of the orb web, and diversification analyses show that the mostly ground-dwelling, web-less RTA clade diversified faster than orb weavers. Consistent with molecular dating estimates we report herein, this may reflect a major increase in biomass of non-flying insects during the Cretaceous Terrestrial Revolution 125–90 million years ago favoring diversification of spiders that feed on cursorial rather than flying prey. Our results also have major implications for our understanding of spider systematics. Phylogenomic analyses corroborate several well-accepted high level groupings: Opisthothele, Mygalomorphae, Atypoidina, Avicularoidea, Theraphosoidina, Araneomorphae, Entelegynae, Araneoidea, the RTA clade, Dionycha and the Lycosoidea. Alternatively, our results challenge the monophyly of Eresoidea, Orbiculariae, and Deinopoidea. The composition of the major paleocribellate and neocribellate clades, the basal divisions of Araneomorphae, appear to be falsified. Traditional Haplogynae is in need of revision, as our findings appear to support the newly conceived concept of Synspermiata. The sister pairing of filistatids with hypochilids implies that some peculiar features of each family may in fact be synapomorphic for the pair. Leptonetids now are seen as a possible sister group to the Entelegynae, illustrating possible intermediates in the evolution of the more complex entelegyne genitalic condition, spinning organs and respiratory organs.
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Spiders (Araneae) make up a remarkably diverse lineage of predators that have successfully colonized most terrestrial ecosystems. All spiders produce silk, and many species use it to build capture webs with an extraordinary diversity of forms. Spider diversity is distributed in a highly uneven fashion across lineages. This strong imbalance in species richness has led to several causal hypotheses, such as codiversification with insects, key innovations in silk structure and web architecture, and loss of foraging webs. Recent advances in spider phylogenetics have allowed testing some of these hypotheses, but results are often contradictory, highlighting the need to consider additional drivers of spider diversification. The spatial and historical patterns of diversity and diversification remain contentious. Comparative analyses of spider diversification will advance only if we continue to make progress with studies of species diversity, distribution, and phenotypic traits, together with finer-scale phylogenies and genomic data. Expected final online publication date for the Annual Review of Entomology, Volume 66 is January 11, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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This paper addresses the systematics of the New Zealand spiders of the family Malkaridae. Malkarids are small araneoid spiders that live primarily in the leaf litter and mosses of temperate and tropical wet forests in Australia and New Zealand, with the exception of a single species in southern South America and another in New Caledonia. We treat the New Zealand species of Malkaridae that are not members of the subfamily Pararchaeinae, a monophyletic group of 11 new species that we classify in 2 new genera (Tingotingo, gen. nov. and Whakamoke, gen. nov.) and a new subfamily (Tingotinginae, subfam. nov.). We describe, diagnose, illustrate and map the distribution of specimen records of these 11 new species of New Zealand Malkaridae: Tingotingo porotiti, sp. nov., T. pouaru, sp. nov., T. tokorera, sp. nov., T. aho, sp. nov., Whakamoke orongorongo, sp. nov.; W. tarakina, sp. nov.; W. guacamole, sp. nov.; W. hunahuna, sp. nov.; W. paoka, sp. nov.; W. heru, sp. nov.; and W. rakiura, sp. nov. We also treat the phylogenetic relationships of Malkaridae and use the results of our previous work on the molecular phylogeny of Araneoidea as the bases for the classification of the family. Tingotingo, gen. nov. and Whakamoke, gen. nov. are sister clades. Tingotinginae, subfam. nov. is the sister group of the Malkarinae plus Pararchaeinae clade. We further hypothesise and discuss the morphological synapomorphies of Malkaridae, Tingotinginae, subfam. nov. and the two new genera.
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The spider family Tetragnathidae Menge is a cosmopolitan, relatively well-studied spider clade with some members readily identifiable by their elongate chelicerae and/or their horizontal orb webs. It has four recognized subfamilies—Tetragnathinae, Metainae, Leucauginae, and the Australasian endemic Nanometinae—although many genera remain unassigned to subfamilial groups. Nanometinae alpha taxonomy is the least well understood of these lineages despite the inclusion of members of the subfamily in a number of phylogenetic analyses over the past decade. Here we describe 10 new species and revise seven additional tetragnathids from Australia, New Zealand, New Caledonia, and Papua New Guinea in the genera Nanometa, Taraire, gen. nov., Tawhai, gen. nov., Harlanethis, gen. nov., and Iamarra, gen. nov. These 17 species are: Nanometa gentilisSimon, 1908, N. trivittata (Keyserling, 1887), comb. nov., N. sarasini (Berland, 1924), comb. nov., N. lagenifera (Urquhart, 1888), comb. nov., N. purpurapunctata (Urquhart, 1889), comb. nov., N. fea, sp. nov., N. tasmaniensis, sp. nov., N. tetracaena, sp. nov., N. dimitrovi, sp. nov., N. dutrorum, sp. nov., N. forsteri, sp. nov., Taraire rufolineata (Urquhart, 1889), comb. nov., Taraire oculta, sp. nov., Tawhai arborea (Urquhart, 1891), comb. nov., Harlanethis lipscombae, sp. nov., H. weintrauborum, sp. nov., and Iamarra multitheca, sp. nov. We also synonymize NediphyaMarusik and Omelko, 2017, and the monotypic genus ErycinioliaStrand, 1912, with Nanometa, bringing the total number of species in the genus from one to 14. Using an expanded taxon sampling for prior studies based on six molecular markers—12S rRNA, 16S rRNA, 18S rRNA, 28S rRNA, cytochrome c oxidase subunit I, and histone H3—and both maximum likelihood and Bayesian methods, we place these taxa in the tetragnathid tree of life. Nanometinae and its constituent genera Nanometa and Pinkfloydia are reciprocally monophyletic. Harlanethis belongs to Leucauginae. The genera Taraire, Tawhai, and Iamarra defy robust phylogenetic placement and are not yet assigned to subfamily.
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The infraorder Mygalomorphae is one of the three main lineages of spiders comprising over 3000 nominal species. This ancient group has a worldwide distribution that includes among its ranks large and charismatic taxa such as tarantulas, trapdoor spiders, and highly venomous funnel-web spiders. Based on past molecular studies using Sanger-sequencing approaches, numerous mygalomorph families (e.g., Hexathelidae, Ctenizidae, Cyrtaucheniidae, Dipluridae, and Nemesiidae) have been identified as non-monophyletic. However, these data were unable to sufficiently resolve the higher-level (intra- and interfamilial) relationships such that the necessary changes in classification could be made with confidence. Here, we present a comprehensive phylogenomic treatment of the spider infraorder Mygalomorphae. We employ 472 loci obtained through anchored hybrid enrichment to reconstruct relationships among all the mygalomorph spider families and estimate the timeframe of their diversification. We sampled nearly all currently recognized families, which has allowed us to assess their status, and as a result, propose a new classification scheme. Our generic-level sampling has also provided an evolutionary framework for revisiting questions regarding silk use in mygalomorph spiders. The first such analysis for the group within a strict phylogenetic framework shows that a sheet web is likely the plesiomorphic condition for mygalomorphs, as well as providing insights to the ancestral foraging behavior for all spiders. Our divergence time estimates, concomitant with detailed biogeographic analysis, suggest that both ancient continental-level vicariance and more recent dispersal events have played an important role in shaping modern day distributional patterns. Based on our results, we relimit the generic composition of the Ctenizidae, Cyrtaucheniidae, Dipluridae, and Nemesiidae. We also elevate five subfamilies to family rank: Anamidae (NEW RANK), Euagridae (NEW RANK), Ischnothelidae (NEW RANK), Pycnothelidae (NEW RANK), and Bemmeridae (NEW RANK). Three families Entypesidae (NEW FAMILY), Microhexuridae (NEW FAMILY), and Stasimopidae (NEW FAMILY), and one subfamily Australothelinae (NEW SUBFAMILY) are newly proposed. Such a major rearrangement in classification, recognizing nine newly established family-level rank taxa, is the largest the group has seen in over three decades. [Biogeography; molecular clocks; phylogenomics; spider web foraging; taxonomy.].
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The information criteria AIC, AICc and BIC are widely used for model selection in phylogenetics, however their theoretical justification and performance have not been carefully examined in this setting. Here we investigate these methods under simple and complex phylogenetic models. We show that AIC can give a biased estimate of its intended target, the expected predictive log likelihood or, equivalently, expected Kullback-Leibler divergence between the estimated model and the true distribution for the data. Reasons for bias include commonly-occurring issues such as small edge-lengths or, in mixture models, small weights. The use of partitioned models is another issue that can cause problems with information criteria. We show that for partitioned models, a different BIC correction is required for it to be a valid approximation to a Bayes factor. The commonly used AICc correction is not clearly defined in partition models and can actually create a substantial bias when the number of parameters gets large as is the case with larger trees and partitioned models. Bias-corrected cross-validation corrections are shown to provide better approximations to expected predictive log likelihood than AIC. We also illustrate how expected predictive log likelihood, the estimation target of AIC, can sometimes favour an incorrect model and give reasons for why selection of incorrectly under-partitioned models might be desirable in partitioned model settings.
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Phylogenomic methods have proven useful for resolving deep nodes and recalcitrant groups in the spider tree of life. Across arachnids, transcriptomic approaches may generate thousands of loci, and target‐capture methods, using the previously designed arachnid‐specific probe‐set, can target a maximum of about 1,000 loci. Here, we develop a specialized target‐capture probe set for spiders that contains over 2,000 ultraconserved elements (UCEs) and then demonstrate the utility of this probe set through sequencing and phylogenetic analysis. We designed the “spider‐specific” probe set using three spider genomes (Loxosceles, Parasteatoda and Stegodyphus) and ensured that the newly designed probe‐set include UCEs from the previously designed Arachnida probe set. The new “spider‐specific” probes were used to sequence UCE loci in 51 specimens. The remaining samples included five spider genomes and taxa that were enriched using Arachnida probe set. The “spider‐specific” probes were also used to gather loci from a total of 84 representative taxa across Araneae. On mapping these 84 taxa to the Arachnida probe set, we captured at most 710 UCE loci, while the spider specific probe set captured up to 1,547 UCE loci from the same taxon sample. Phylogenetic analyses using Maximum Likelihood and coalescent methods corroborate most nodes resolved by recent transcriptomic analyses, but not all (e.g., UCE data suggests monophyly of “symphytognathoids”). Our preferred analysis based on topology tests, suggests monophyly of the “symphytognathoids” (the miniature orb‐weavers), which in previous studies has only been supported by a combination of morphological and behavioral characters.
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The monotypic family Trogloraptoridae was only recently described from caves and old‐growth forest of Oregon and California (Western USA). These enigmatic spiders are characterized by striking raptorial claws, and based on their spinneret morphology, a close relationship to dysderoid spiders, a large clade within Synspermiata, was suggested. Here, we used a phylogenomic framework using transcriptomes to test the phylogenetic position of Trogloraptor marchingtoni. Our analysis placed this taxon within Synspermiata, which is supported by the presence of synspermia. Furthermore, a sister group relationship with Dysderoidea is strongly supported. In a second step, we reinvestigated the female genitalia using a non‐destructive approach. Our data revealed that Trogloraptor has a flow‐through genital system (entelegyne condition) and is not haplogyne as previously described based on dissections. The Trogloraptor female genital system consists of paired large spermathecae, which connect by a fertilization duct to a wide bursa. The copulatory duct arises from the sclerotized anterior margin of the bursa, and its organization is likely related to the organization of the male intromittent organ. Based on our phylogenetic data, we show that the entelegyne condition evolved at least six times independently within spiders. Moreover, our results indicate that the peculiar organization of the dysderoid female genitalia with an additional posterior sperm storage site is a synapomorphy of this Synspermiata clade.
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After more than fifteen years of existence, the R package ape has continuously grown its contents, and has been used by a growing community of users. The release of version 5.0 has marked a leap towards a modern software for evolutionary analyses. Efforts have been put to improve efficiency, flexibility, support for 'big data' (R's long vectors), ease of use, and quality check before a new release. These changes will hopefully make ape a useful software for the study of biodiversity and evolution in a context of increasing data quantity. Availability: ape is distributed through the Comprehensive R Archive Network: http://cran.r-project.org/package=apeFurther information may be found athttp://ape-package.ird.fr/.
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Imperfect knowledge of ancestral behaviour often hampers tracing behavioural evolution. This limitation is reduced in orb weaving spiders, because spider orb web construction behaviour and the cues used by modern orb-weavers are well-studied and highly conserved. Several species in orb-weaving families build non-orb webs that are clearly derived from orbs, allowing transitions from ancestral to modern behaviours to be described with high confidence. Three major patterns of general evolutionary significance were found in 69 phylogenetically independent transitions in 15 groups in 8 families: ancestral traits were often maintained as units; the most frequent of the eight different types of ancestral trait change was transfer of an ancestral behaviour to a new context; and 'new' traits that had no clear homology with ancestral traits were also common. Changes occurred in all major stages of orb construction. This may be the most extensive summary of evolutionary transitions in behaviour yet compiled.
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The Cretaceous experienced one of the most remarkable greenhouse periods in geological history. During this time, ecosystem reorganizations significantly impacted the diversification of many groups of organisms. The rise of angiosperms marked a major biome turnover. Notwithstanding, relatively little remains known about how the Cretaceous global ecosystem impacted the evolution of spiders, which constitute one of the most abundant groups of predators. Herein, we evaluate the transcriptomes of 91 taxa representing more than half of the spider families. We add 23 newly sequenced taxa to the existing database to obtain a robust phylogenomic assessment. Phylogenetic reconstructions using different datasets and methods obtain novel placements of some groups, especially in the Synspermiata and the group having a retrolateral tibial apophysis (RTA). Molecular analyses indicate an expansion of the RTA clade at the Early Cretaceous with a hunting predatory strategy shift. Fossil analyses show a 7-fold increase of diversification rate at the same period, but this likely owes to the first occurrences spider in amber deposits. Additional analyses of fossil abundance show an accumulation of spider lineages in the Early Cretaceous. We speculate that the establishment of a warm greenhouse climate pumped the diversification of spiders, in particular among webless forms tracking the abundance of insect prey. Our study offers a new pathway for future investigations of spider phylogeny and diversification.
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Dating back to almost 400 mya, spiders are among the most diverse terrestrial predators [1]. However, despite considerable effort [1-9], their phylogenetic relationships and diversification dynamics remain poorly understood. Here, we use a synergistic approach to study spider evolution through phylogenomics, comparative transcriptomics, and lineage diversification analyses. Our analyses, based on ca. 2,500 genes from 159 spider species, reject a single origin of the orb web (the "ancient orb-web hypothesis") and suggest that orb webs evolved multiple times since the late Triassic-Jurassic. We find no significant association between the loss of foraging webs and increases in diversification rates, suggesting that other factors (e.g., habitat heterogeneity or biotic interactions) potentially played a key role in spider diversification. Finally, we report notable genomic differences in the main spider lineages: while araneoids (ecribellate orb-weavers and their allies) reveal an enrichment in genes related to behavior and sensory reception, the retrolateral tibial apophysis (RTA) clade-the most diverse araneomorph spider lineage-shows enrichment in genes related to immune responses and polyphenic determination. This study, one of the largest invertebrate phylogenomic analyses to date, highlights the usefulness of transcriptomic data not only to build a robust backbone for the Spider Tree of Life, but also to address the genetic basis of diversification in the spider evolutionary chronicle.
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The orb-weaving spider family Araneidae is extremely diverse (> 3,100 spp.) and its members can be charismatic terrestrial arthropods, many of them recognizable by their iconic orbicular snare web, such as the common garden spiders. Despite considerable effort to better understand their backbone relationships based on multiple sources of data (morphological, behavioral and molecular), pervasive low support remains in recent studies. In addition, no overarching phylogeny of araneids is available to date, hampering further comparative work. In this study, we analyze the transcriptomes of 33 taxa, including 19 araneids - 12 of them new to this study - representing most of the core family lineages, to examine the relationships within the family using genomic-scale datasets resulting from various methodological treatments, namely ortholog selection and gene occupancy as a measure of matrix completion. Six matrices were constructed to assess these effects by varying orthology inference method and gene occupancy threshold. Orthology methods used are the benchmarking tool BUSCO and the tree-based method UPhO; three gene occupancy thresholds (45%, 65%, 85%) were used to assess the effect of missing data. Gene tree and species tree-based methods (including multi-species coalescent and concatenation approaches, as well as maximum likelihood and Bayesian inference) were used totalling 17 analytical treatments. The monophyly of Araneidae and the placement of core araneid lineages were supported, together with some previously unsound backbone divergences; these include high support for Zygiellinae as the earliest diverging subfamily (followed by Nephilinae), the placement of Gasteracanthinae as sister group to Cyclosa and close relatives, and close relationships between the Araneus + Neoscona clade and Cyrtophorinae + Argiopinae clade. Incongruences were relegated to short branches in the clade comprising Cyclosa and its close relatives. We found congruence between most of the completed analyses, with minimal topological effects from occupancy/missing data and orthology assessment. The resulting number of genes by certain combinations of orthology and occupancy thresholds being analyzed had the greatest effect on the resulting trees, with anomalous outcomes concluding from analysis of lower numbers of genes.
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Psechrids are an enigmatic family of S.E. Asian spiders. This small family builds sheet webs and even orb webs, yet unlike other orb weavers, its putative relatives are largely cursorial lycosoids - a superfamily of approximately seven spider families related to wolf spiders. The orb web was invented at least twice: first in a very ancient event, and then second, within this clade of wolf-like spiders that reinvented this ability. Exactly how the spiders modified their silks, anatomy, and behaviors to accomplish this transition requires that we identify their precise evolutionary origins -- yet, thus far, molecular phylogenies show poor support and considerable disagreement. Using phylogenomic methods based on whole body transcriptomes for psechrids and their putative relatives, we have recovered a well-supported phylogeny that places the Psechridae sister to the Ctenidae -- a family of mostly cursorial habits but that, as with all psechrids, retains some cribellate species. Although this position reinforces the prevailing view that orb weaving in psechrids is largely a consequence of convergence, it is still possible some components of this behavior are retained or resurrected in common with more distant true orb weaving ancestors.
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To survive, web-building spiders rely on their capture threads to restrain prey. Many species use special adhesives for this task, and again the majority of those species cover their threads with viscoelastic glue droplets. Cribellate spiders, by contrast, use a wool of nanofibres as adhesive. Previous studies hypothesized that prey is restrained by van der Waals' forces and entrapment in the nanofibres. A large discrepancy when comparing the adhesive force on artificial surfaces versus prey implied that the real mechanism was still elusive. We observed that insect prey's epicuticular waxes infiltrate the wool of nanofibres, probably induced by capillary forces. The fibre-reinforced composite thus formed led to an adhesion between prey and thread eight times stronger than that between thread and wax-free surfaces. Thus, cribellate spiders employ the originally protective coating of their insect prey as a fatal component of their adhesive and the insect promotes its own capture. We suggest an evolutionary arms race with prey changing the properties of their cuticular waxes to escape the cribellate capture threads that eventually favoured spider threads with viscous glue.%U http://rspb.royalsocietypublishing.org/content/royprsb/284/1855/20170363.full.pdf
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Model-based molecular phylogenetics plays an important role in comparisons of genomic data, and model selection is a key step in all such analyses. We present ModelFinder, a fast model-selection method that greatly improves the accuracy of phylogenetic estimates by incorporating a model of rate heterogeneity across sites not previously considered in this context and by allowing concurrent searches of model space and tree space.
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The formation and spread of the Australian arid zone during the Neogene was a profoundly transformative event in the biogeographic history of Australia, resulting in extinction or range contraction in lineages adapted to mesic habitats, as well as diversification and range expansion in arid-adapted taxa (most of which evolved from mesic ancestors). However, the geographic origins of the arid zone biota are still relatively poorly understood, especially among highly diverse invertebrate lineages, many of which are themselves poorly documented at the species level. Spiny trapdoor spiders (Idiopidae: Arbanitinae) are one such lineage, having mesic 'on-the-continent' Gondwanan origins, while also having experienced major arid zone radiations in select clades. In this study, we present new orthologous nuclear markers for the phylogenetic inference of mygalomorph spiders, and use them to infer the phylogeny of Australasian Idiopidae with a 12-gene parallel tagged amplicon next-generation sequencing approach. We use these data to test the mode and timing of diversification of arid-adapted idiopid lineages across mainland Australia, and employ a continent-wide sampling of the fauna's phylogenetic and geographic diversity to facilitate ancestral area inference. We further explore the evolution of phenotypic and behavioural characters associated with both arid and mesic environments, and test an 'out of south-western Australia' hypothesis for the origin of arid zone clades. Three lineages of Idiopidae are shown to have diversified in the arid zone during the Miocene, one (genus Euoplos) exclusively in Western Australia. Arid zone Blakistonia likely had their origins in South Australia, whereas in the most widespread genus Aganippe, a more complex scenario is evident, with likely range expansion from southern Western Australia to southern South Australia, from where the bulk of the arid zone fauna then originated. In Aganippe, remarkable adaptations to phragmotic burrow-plugging in transitional arid zone taxa have evolved twice independently in Western Australia, while in Misgolas and Cataxia, burrow door-building behaviours have likely been independently lost at least three times in the eastern Australian mesic zone. We also show that the presence of idiopids in New Zealand (Cantuaria) is likely to be the result of recent dispersal from Australia, rather than ancient continental vicariance. By providing the first comprehensive, continental synopsis of arid zone biogeography in an Australian arachnid lineage, we show that the diversification of arbanitine Idiopidae was intimately associated with climate shifts during the Neogene, resulting in multiple Mio-Pliocene radiations.
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We investigate the phylogeny of “pirate spiders” (Mimetidae), a family of araneophagic spiders known for their use of aggressive mimicry as a foraging strategy, but poorly understood phylogenetically. Relationships are inferred by including molecular data from six loci for 92 mimetid terminals spanning four genera, and 119 outgroups representing 12 families. Phylogenetic analyses based on parsimony, maximum-likelihood and Bayesian approaches, as well as static and dynamic homology, robustly support monophyly of Mimetidae and a sister-group relationship to a clade comprising Tetragnathidae + Arkyidae. Relationships among the mimetid genera are largely congruent across methods, as follows: (Gelanor (Ero (Anansi n. gen. (Australomimetus, Mimetus)))). Diversification of Mimetidae is estimated to be around 114 Ma, in the Early Cretaceous. In light of the results of our phylogenetic analyses, we erect Anansi n. gen. to include a clade of mimetids from West Africa that contains at least four species, including the newly described A. luki n. sp. We present the first report of maternal care in Mimetidae based on novel field observations.
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Version 1.5 of the computer program TNT completely integrates landmark data into phylogenetic analysis. Landmark data consist of coordinates (in two or three dimensions) for the terminal taxa; TNT reconstructs shapes for the internal nodes such that the difference between ancestor and descendant shapes for all tree branches sums up to a minimum; this sum is used as tree score. Landmark data can be analysed alone or in combination with standard characters; all the applicable commands and options in TNT can be used transparently after reading a landmark data set. The program continues implementing all the types of analyses in former versions, including discrete and continuous characters (which can now be read at any scale, and automatically rescaled by TNT). Using algorithms described in this paper, searches for landmark data can be made tens to hundreds of times faster than it was possible before (from T to 3T times faster, where T is the number of taxa), thus making phylogenetic analysis of landmarks feasible even on standard personal computers.
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Current sequencing technologies are making available unprecedented amounts of genetic data for a large variety of species including non-model organisms. Although many phylogenomic surveys spend considerable time finding orthologs from the wealth of sequence data, these results do not transcend the original study and after being processed for specific phylogenetic purposes these orthologs do not become stable orthology hypotheses. We describe a procedure to detect and document the phylogenetic distribution of orthologs allowing researchers to use this information to guide selection of loci best suited to test specific evolutionary questions. At the core of this pipeline is a new phylogenetic orthology method that is neither affected by the position of the root nor requires explicit assignment of outgroups. We discuss the properties of this new orthology assessment method and exemplify its utility for phylogenomics using a small insects dataset. Additionally we exemplify the pipeline to identify and document stable orthologs for the group of orb-weaving spiders (Araneoidea) using RNAseq data.The scripts used in this study, along with sample files and additional documentation, are available at https://github.com/ballesterus/UPhO.