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Converging on the orb: denser taxon sampling elucidates spider phylogeny and new analytical methods support repeated evolution of the orb web
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.
... However, palpimanoids were seemingly at their zenith in the Mesozoic, when together with the Synspermiata, they were a dominant spider group until major faunal turnover in the Cenozoic (Magalhães et al. 2020). Using modern sequencing methods, palpimanoids consistently fall as the sister group to the Entelegynes (Fernández et al. 2018; Kulkarni et al. 2020;Kallal et al. 2021), which contains the bulk of modern spider species richness and contains the dominant Cenozoic groups (Magalhães et al. 2020). Using molecular clock methodology, studies have shown that palpimanoids likely emerged in the Permian or Triassic (Wood et al. 2013;Magalhães et al. 2020;Kallal et al. 2021). ...
... Using modern sequencing methods, palpimanoids consistently fall as the sister group to the Entelegynes (Fernández et al. 2018; Kulkarni et al. 2020;Kallal et al. 2021), which contains the bulk of modern spider species richness and contains the dominant Cenozoic groups (Magalhães et al. 2020). Using molecular clock methodology, studies have shown that palpimanoids likely emerged in the Permian or Triassic (Wood et al. 2013;Magalhães et al. 2020;Kallal et al. 2021). This body of research suggests palpimanoids existed prior to the breakup of Pangea-a necessary precondition to be a useful group for examining vicariance. ...
... S1-S10 for all additional results. Our preference is for the Likelihood TE 70% results for the following reasons: 1) the Parsimony TE results overall had less resolution than the Likelihood, probably because the Likelihood analyses used models of molecular and morphological evolution; 2) the 70% molecular data is reduced in bp size compared to the 50% data set and so, is less likely to overwhelm the signal from the morphological data; and 3) the TE results with the 70% sequence occupancy data set, compared to the 50%, are more in agreement with results from other independent, yet more comprehensive studies that more thoroughly sample across spiders and that support a monophyletic Palpimanoidea (e.g., Kallal et al. 2021). ...
Burmese amber is a significant source of fossils that documents the mid-Cretaceous biota. This deposit was formed around 99 Ma on the Burma Terrane, which broke away from Gondwana and later collided with Asia, although the timing is disputed. Palpimanoidea is a dispersal-limited group that was a dominant element of the Mesozoic spider fauna, and has an extensive fossil record, particularly from Burmese amber. Using morphological and molecular data, evolutionary relationships of living and fossil Palpimanoidea are examined. Divergence dating with fossils as terminal tips, followed by ancestral range estimations, shows timing of diversification is contemporaneous with continental break-up and that widespread ancestral ranges divide into lineages that inherit different Pangean fragments, consistent with vicariance. Our results suggest that the Burmese amber fauna has ties to Gondwana due to a historical connection in the Early Cretaceous, and that the Burma Terrane facilitated biotic exchange by transporting lineages from Gondwana into the Holarctic in the Cretaceous.
... An entire large group of spiders, the RTA clade (e.g. jumping spiders, wolf spiders, wandering spiders), abandoned the construction of trap webs, likely as a consequence of adapting their feeding habits to the proliferation of ground-walking insects, particularly ants (Coddington et al., 2019;Garrison et al., 2016;Kallal et al., 2021). ...
... A clear case is the web constructed by spiders in the genus Wendilgarda (Theridiosomatidae) and their link with a novel hunting behaviour (Eberhard, 2001). Spiders in this family construct orb webs, but Wendilgarda construct webs with 'gum-foot' lines that connect to the water surface of streams, giving these spiders access to a whole new kind of resource, for example, insects such as water striders that float on the water film (Coddington, 1986;Coddington & Valerio, 1980;Eberhard, 2001;Kallal et al., 2021). ...
... This novel web is built by a species in the pirate spider family (Mimetidae) that exploits the behaviour that other web spiders use to initiate web construction. Pirate spiders are closely related to orb weavers but have also lost capture web construction Fern andez et al., 2018;Garrison et al., 2016;Kallal et al., 2021;Kulkarni et al., 2020;Wheeler et al., 2017). Instead, they mostly specialize on invading orb webs and cob webs to prey on the webs' owners, although they occasionally feed on some insects (Jackson & Whitehouse, 1986;Kloock, 2001Kloock, , 2012. ...
... Spiders are an ancient clade of terrestrial predators with over 50,000 described species (World Spider Catalog, 2023), occupying most habitats globally as a result of a multitude of biogeographic events (such as Pangean breakup, founder events, dispersals). They date back to the Carboniferous era (359-299 million years ago; Fernandez et al., 2018;Kallal et al., 2021) after which, they have evolved into an enormous diversity of sizes, morphologies, behaviors, silk uses, and web architectures. The smallest known adult spider is the orb weaver Patu digua (Symphytognathidae), with a body length of 0.37 mm (Forster and Platnick, 1977). ...
... The monophyly of symphytognathoids has been supported by morphological and behavioral characters (Griswold et al., 1998;Schutt, 2003;Lopardo and Hormiga, 2008;Lopardo et al., 2011;Hormiga and Griswold, 2014), but they have appeared as either paraphyletic or polyphyletic in molecular phylogenies using the six Sanger-based markers Wheeler et al., 2017) or transcriptomes (Fernandez et al., 2018;Kallal et al., 2021). Dimitrov et al. (2017) obtained Anapidae as paraphyletic with "Anapidae I" (represented by Anapis, one micropholcommatine genus (Taphiassa) and Holarchaea) as sister to Theridiidae and "Anapidae II" (represented by Gertschanapis, Maxanapis and Chasmocephalon) as sister to Cyatholipidae. ...
... Lopardo et al.'s (2011) extensive Sanger-based dataset supported symphytognathoid monophyly only when the nucleotide data were analyzed in combination with phenotypic data. It is noteworthy that transcriptomic data, analyzed as amino acids in a maximum likelihood framework, recovered symphytognathoids as polyphyletic (Fernández et al., 2018;Kallal et al., 2021). In a parsimony analysis of transcriptomic data Kallal et al. (2021) recovered Theridiosomatidae as sister to Araneidae while the other "symphytognathoid'' families formed a monophyletic group. ...
The miniature orb weaving spiders (symphytognathoids) are a group of small spiders (< 2 mm), including the smallest adult spider Patu digua (0.37 mm in body length), that have been classified into five families. The species of one of its constituent lineages, the family Anapidae, build a remarkable diversity of webs (ranging from orbs to sheet webs and irregular tangles) and even include a webless kleptoparasitic species. Anapids are also exceptional because of the extraordinary diversity of their respiratory systems. The phylogenetic relationships of symphytognathoid families have been recalcitrant with different classes of data, such as, monophyletic with morphology and its concatenation with Sanger-based six markers, paraphyletic (including a paraphyletic Anapidae) with solely Sanger-based six markers, and polyphyletic with transcriptomes. In this study, we capitalized on a large taxonomic sampling of symphytognathoids, focusing on Anapidae, and using de novo sequenced ultraconserved elements (UCEs) combined with UCEs recovered from available transcriptomes and genomes. We evaluated the conflicting relationships using a variety of support metrics and topology tests. We found support for the phylogenetic hypothesis proposed using morphology to obtain the "symphytognathoids'' clade, Anterior Tracheal System (ANTS) Clade and monophyly of the family Anapidae. Anapidae can be divided into three major lineages, the Vichitra Clade (including Teutoniella, Holarchaea, Sofanapis and Acrobleps), the subfamily Micropholcommatinae and the Orb-weaving anapids (Owa) Clade. Biogeographic analyses reconstructed a hypothesis of multiple long-distance transoceanic dispersal events, potentially influenced by the Antarctic Circumpolar Current and West Wind Drift. In symphytognathoids, the ancestral anterior tracheal system transformed to book lungs four times and reduced book lungs five times. The posterior tracheal system was lost six times. The orb web structure was lost four times independently and transformed into sheet web once.
... The first attempt to reconstruct the "tree of life" for all spider families was carried out by Wheeler et al. (2017) and based on the usual low number of molecular markers available with Sanger sequencing datasets. Since then, phylogenomic dataset have been developed, thereby providing more data to disentangle the relationships between the major groups (Bond et al., 2014;Garrison et al., 2016;Fernandez et al., 2018;Kallal et al., 2020;Kulkarni et al., 2020). Though, the taxon sampling remains limited if compared to the study of Wheeler et al. (2017). ...
... Most of the marronoid families are characterized by a lack of distinctive morphological features; for this reason, they were in the past placed in a few big families, such as Agelenidae, Amaurobiidae, Desidae and Dictynidae, from which they were gradually moved to a larger selection of families (Wheeler et al., 2017). Few molecular phylogenetic studies have focused on these families (Miller et al., 2010;Spagna and Gillespie, 2008;Spagna et al., 2010;Crews et al., 2020) and recent phylogenomic datasets still present a limited taxon sampling for these groups (Garrison et al., 2016;Fernandez et al., 2018;Kallal et al., 2020;Kulkarni et al., 2020). Thus, the relationship between marronoid families remains mostly unresolved. ...
... Maximum likelihood (ML) phylogenetic inference was performed using IQ-TREE, nodal support was estimated using 1000 replicates of UltraFast bootstrap (Minh et al., 2013). A second ML analysis was performed using the same settings but adding some topological constraints based on nodes that resulted highly supported in the phylotranscriptomic work by Kallal et al. (2020). This was done to constrain some of the relationships between families given the known limited resolution power of classic Sanger markers at higher phylogenetic level in spiders (Garrison et al., 2016;Wheeler et al., 2017). ...
The palearctic spider genus Mastigusa Menge, 1854 is characterized by a remarkable morphology and wide ecological variability, with free-living, cave dwelling and myrmecophile populations known. This genus has a long and tangled taxonomic history and was placed in different families in the past, all belonging to the "marronoid clade" an informal grouping of families characterized by the lack of strong synapomorphies. Three species are currently recognized, but their identity and circumscription has been long debated. A molecular approach was never applied for trying to solve these uncertainties, and doubts still remain both about its phylogenetic placement and about the taxonomic status of the described species. For the first time the genus Mastigusa is included in a molecular phylogenetic analysis and strong support is found for its placement within the family Cybaeidae, in sister relationship with the genus Cryphoeca Thorell, 1870. An analysis of Mastigusa populations spanning across the distribution range of the genus identifies a high and previously overlooked genetic diversity, with six distinct genetic lineages showing a strong geographic pattern. Divergence times between Mastigusa and its sister genus and between the distinct Mastigusa lineages are estimated, and the groundwork is laid for a taxonomic revision of the species belonging to the genus.
... All spiders produce silk, and many species use it to build foraging webs for predation Kallal et al., 2021). The spider superfamily Araneoidea is the largest group of web-spinning taxa and accounts for approximately one-quarter of the entire spider tree of life (World Spider Catalog 2022). ...
... When assigning the NCBI-Nr protein sequences to the PS levels based on the NCBI taxonomy database, there was a lack of gene sets from some superfamilies of Arachnida, so we collected or de novo assembled the genome and transcript sets of 130 chelicerates (Supplementary Table 1). Then, we observed a conflicting taxonomic relationship in which the NCBI taxonomy database archived Trichonephila (basionym: Nephila) as a member of Araneoidea's Nephilidae, while previous studies assigned Trichonephila to Araneoidea's Araneidae (Kallal et al., 2021;Wheeler et al., 2017). Then, we reconstructed the phylogenetic relationships for Araneoidea spiders to avoid some unforeseen errors. ...
... The results showed that the phylogenetic positions of the two families (Theridiosomatidae and Synaphridae) were inconsistent between the two topologies. Synaphridae was the sister group of Theridiosomatidae in topology 1 but was the sister group of Araneidae in topology 2. Topology 2 supported the results of a recent study employing multiple methods and denser taxon sampling (Kallal et al., 2021). More importantly, both topologies support that T. clavata belongs to Araneoidea's Araneidae ( Fig. 1D; Supplementary Fig. 3), although we think topology 2 may be more reliable. ...
... The first attempt to reconstruct the "tree of life" for all spider families was carried out by Wheeler et al. (2017) and based on the usual low number of molecular markers available with Sanger sequencing datasets. Since then, phylogenomic dataset have been developed, thereby providing more data to disentangle the relationships between the major groups (Bond et al., 2014;Garrison et al., 2016;Fernandez et al., 2018;Kallal et al., 2020;Kulkarni et al., 2020). Though, the taxon sampling remains limited if compared to the study of Wheeler et al. (2017). ...
... Most of the marronoid families are characterized by a lack of distinctive morphological features; for this reason, they were in the past placed in a few big families, such as Agelenidae, Amaurobiidae, Desidae and Dictynidae, from which they were gradually moved to a larger selection of families (Wheeler et al., 2017). Few molecular phylogenetic studies have focused on these families (Miller et al., 2010;Spagna and Gillespie, 2008;Spagna et al., 2010;Crews et al., 2020) and recent phylogenomic datasets still present a limited taxon sampling for these groups (Garrison et al., 2016;Fernandez et al., 2018;Kallal et al., 2020;Kulkarni et al., 2020). Thus, the relationship between marronoid families remains mostly unresolved. ...
... Maximum likelihood (ML) phylogenetic inference was performed using IQ-TREE, nodal support was estimated using 1000 replicates of UltraFast bootstrap (Minh et al., 2013). A second ML analysis was performed using the same settings but adding some topological constraints based on nodes that resulted highly supported in the phylotranscriptomic work by Kallal et al. (2020). This was done to constrain some of the relationships between families given the known limited resolution power of classic Sanger markers at higher phylogenetic level in spiders (Garrison et al., 2016;Wheeler et al., 2017). ...
... Ctenids belong to the superfamily Lycosoidea, which comprises the families Lycosidae, Pisauridae, Ctenidae, Psechridae, Thomisidae, Oxyopidae, Senoculidae and Trechaleidae, and they are placed in the retrolateral tibial apophysis (RTA) clade, the most speciose lineage of spiders (Wheeler et al., 2017;Fern andez et al., 2018;Kallal et al., 2021). The majority of RTA clade spiders have eight eyes, arranged roughly in two rows (but not Ctenidae, see below), where the anterior row contains the anteromedian (AME) and anterolateral eyes (ALE), and the posterior contains the posteromedian (PME) and the posterolateral eyes (PLE; Griswold, 1993;Ram ırez, 2014). ...
... This study presents the first densely sampled molecular phylogeny of Ctenidae that includes representatives of all of its subfamilies worldwide. The phylogenetic relationships of the main RTA clade lineages (Lycosoidea, Marronoidea, Dionycha and the oval calamistrum clade) are congruent with previous molecular hypotheses Fern andez et al., 2018;Kallal et al., 2021;Kulkarni et al., 2021). None of our phylogenetic analyses recovered Psechridae and Ctenidae as sister groups as hypothesized in previous studies based on transcriptomes and UCE data (Cheng and Piel, 2018;Kallal et al., 2021). ...
... The phylogenetic relationships of the main RTA clade lineages (Lycosoidea, Marronoidea, Dionycha and the oval calamistrum clade) are congruent with previous molecular hypotheses Fern andez et al., 2018;Kallal et al., 2021;Kulkarni et al., 2021). None of our phylogenetic analyses recovered Psechridae and Ctenidae as sister groups as hypothesized in previous studies based on transcriptomes and UCE data (Cheng and Piel, 2018;Kallal et al., 2021). Our analyses indicated that neither Ctenidae nor the subfamily Acantheinae are monophyletic. ...
Tropical wandering spiders (Ctenidae) are a diverse group of cursorial predators with its greatest species richness in the tropics. Traditionally, Ctenidae are diagnosed based on the presence of eight eyes arranged in three rows (a 2–4–2 pattern). We present a molecular phylogeny of Ctenidae, including for the first time representatives of all of its subfamilies. The molecular phylogeny was inferred using five nuclear (histone H3, 28S, 18S, Actin and ITS‐2) and four mitochondrial (NADH, COI, 12S and 16S) markers. The final matrix includes 259 terminals, 103 of which belong to Ctenidae and represent 28 of the current 49 described genera. We estimated divergence times by including fossils as calibration points and biogeographic events, and used the phylogenetic hypothesis obtained to reconstruct the evolution of the eye conformation in the retrolateral tibial apophysis (RTA) clade. Ctenidae and its main lineages originated during the Paleocene–Eocene and have diversified in the tropics since then. However, in some analyses Ctenidae was recovered as polyphyletic as the genus Ancylometes Bertkau, 1880 was placed as sister to Oxyopidae. Except for Acantheinae, in which the type genus Acantheis Thorell, 1891 is placed inside Cteninae, the four recognized subfamilies of Ctenidae are monophyletic in most analyses. The ancestral reconstruction of the ocular conformation in the retrolateral tibial apophysis clade suggests that the ocular pattern of Ctenidae has evolved convergently seven times and that it has originated from ocular conformations of two rows of four eyes (4–4) and the ocular pattern of lycosids (4–2–2). We also synonymize the monotypic genus Parabatinga Polotov & Brescovit, 2009 with Centroctenus Mello‐Leitão, 1929. We discuss some of the putative morphological synapomorphies of the main ctenid lineages within the phylogenetic framework offered by the molecular phylogenetic results of the study.
... Early analyses used morphological and behavioural traits to support different phylogenetic hypotheses (summarized in Coddington, 1986a), but recently emphasis has been on molecules, including target genes, whole genomes, transcribed gene regions, introns, ultraconserved elements (UCEs), transcriptomic data and fast/ slow evolving loci (e.g. Bond et al., 2014;Fernández et al., 2014;Dimitrov et al., 2016;Garrison et al., 2016;Wheeler, 2017;Coddington et al., 2019;Kallal et al., 2020;Kulkarni et al., 2021). Historically, most discussions of orb monophyly focused on whether orbs evolved once or twice, converging in Uloboridae (linked in some analyses with the derived, net-casting Deinopidae) and Araneoidea (seven different families). ...
... Historically, most discussions of orb monophyly focused on whether orbs evolved once or twice, converging in Uloboridae (linked in some analyses with the derived, net-casting Deinopidae) and Araneoidea (seven different families). Some molecular studies, however, have indicated three to six (Fernández et al., 2018) or, more recently, three to five independent derivations of orbs (Kallal et al., 2020): uloborids; deinopids; and three groups of araneoids: Tetragnathidae; Araneidae + Nephilidae ( o r N e p h i l i n a e ) + T h e r i d i o s o m a t i d a e ; a n d Anapidae + Mysmenidae + Symphytognathidae. Here I focus mostly on the two-group convergence hypothesis (uloborids and araneoids). ...
... Those cases in which similarity is not due to fabricational constraints or to symplesiomorphies were judged to constitute stronger evidence of monophyly. I present the data separately in Table 1 for all five groups (except Deinopidae) that Kallal et al. (2020) mentioned as possibly representing independent derivations of orbs, but focus on possible convergence between uloborids and araneoids (in effect, I compared the uloborid column b with the sum of the three columns c-e). Although there are good reasons to consider deinopid webs as derived from orbs (Coddington, 1986b), I omitted deinopids from this analysis because of uncertainties regarding the homologies of some traits; resolution of the deinopid question is not crucial to resolution of the single vs. double or multiple derivation of orb webs. ...
This first-ever extensive review of the construction behaviour of orb webs, of webs secondarily derived from orbs, and of non-orbs shows that the evidence favouring monophyly over convergent evolution of orbs is stronger than previously appreciated. The two major orb-weaving groups, Uloboridae and Araneoidea, share 31 construction behaviour traits, 20 of which are likely to be both derived and to have feasible alternatives, making convergence an unlikely explanation. Convergence in two lineages seems unlikely, and convergence in five different lineages, as proposed in some recent molecular studies of phylogeny, is even less credible. A further set of seven shared responses in orb design to experimentally constrained spaces also supports orb monophyly. Finally, a ‘control’ case of confirmed convergence on similar ‘pseudo-orbs’ in a taxonomically distant group also supports this argument, as it shows a low frequency of behavioural similarities. I argue that the omission of behavioural data from recent molecular studies of orb web evolution represents a failure of the analytic techniques, not the data, and increases the risk of making mistakes. In general, phylogenetic studies that aim to understand the evolution of particular phenotypes can benefit from including careful study of the phenotypes themselves.
... A robust phylogenetic hypothesis is fundamental for investigating phenotypic evolution. Thus, the advent of genomic-scale sequencing and phylogenomic studies has not only provided novel views into family-level relationships within spiders (Bond et al. 2014;Garrison et al. 2016;Hamilton et al. 2016;Kallal et al. 2021;Kulkarni et al. 2020) but also shed new light on macroevolution and its link to phenotype (Fernández et al. 2018;Ramírez et al. 2021). Transcriptomes also provide a variety of genetic information underlying different traits or behaviors (Fernández et al. 2018). ...
... Phylogenomics has contributed to the resolution of ancient and rapid divergences in spiders (Bond et al. 2014;Garrison et al. 2016;Hamilton et al. 2016;Fernández et al. 2018;Kulkarni et al. 2020;Kallal et al. 2021;Ramírez et al. 2021). Despite the use of transcriptomes or target enrichment methods that have provided thousands of loci for use in phylogenetic reconstruction, limitations of their acquisition remain, such as the requirement of fresh tissue or the expensive synthesis of taxon-specific probe sets. ...
... We considered the evolution of simple lines into complex structures, which requires the use of different silks and coordination of other parts of the body (Vollrath andSelden 2007, Dimitrov and. The current classification is mainly convenient for studying the impact of these capture devices on the evolution of phenotypes rather than the evolution of capture devices themselves, despite many research classifying web architectures into over ten types based on the pattern of the final web surface silk and the number of web surfaces (Dimitrov et al. 2012;Garrison et al. 2016;Dimitrov et al. 2017;Fernández et al. 2018;Coddington et al. 2019;Kallal et al. 2021). ...
What happens when organisms actively modify their environment? Clarifying the role of construction behavior on a macroevolutionary scale is crucial to interpreting phenotypic evolution. Spiders, an extremely successful group of animals exhibiting a wide variety of functional, morphological, and behavioral diversity, are ideal candidates to test whether animal behaviors are related to their phenotypic evolution. Herein, we reconstructed the phylogenomic relationships of 303 spiders covering 105 families with 99 newly developed molecular markers that universally apply across Araneae, and explicitly tested the potential link between construction behavior and somatic evolution based on extensive morphological data from 3,342 extant species and 682 fossil species. Our dated molecular phylogeny provides the backbone for analyses, revealing the behavioral and ecological processes behind these spiders' morphological adaptations. Evolutionary model analyses showed the artifacts constructed by spiders, especially the suspending webs, expand the spider's ability to inhabit different habitats. These artifacts have more substantial impacts on their somatic traits than habitats and promote different trajectories of morphological evolution. Specifically, for spiders, silk-lined burrowing produced larger bodies, relatively shorter legs, and longer patellae, while web-building produced smaller bodies, relatively long legs, and shorter patellae, and hunting promoted an intermediate morphological size. Molecular convergence analysis showed that genes related to morphogenesis or response to stimulus and stress are enriched in spiders with construction behavior. Our study demonstrated that the construction behavior of an animal plays a crucial role in determining the direction and intensity of the selection pressure imposed on it and provides strong evidence that construction behaviors are associated with phenotypic evolution on macroevolutionary timescales.
... The RTA clade exhibits a worldwide distribution and is assumed to have emerged in the Jurassic period (139-161 million years ago (Ma)) (Garrison et al., 2016;Fernandez et al., 2018;Shao and Li, 2018;Magalhaes et al., 2020). According to male palp, trichobothria on the tarsi and metatarsi, the RTA clade is divided into four groups: Zodarioidea, Dionycha, Marronoid clade, and Oval calamistrum clade (Wheeler et al., 2017;Kallal et al., 2020). Araneae phylogeny has been extensively studied at various taxonomic levels by using morphological data (Coddington, 2005;Haupt, 2008), multiple molecular markers (Blackledge et al., 2009;Dimitrov et al., 2012;Wheeler et al., 2017), mitogenomic data (Pons et al., 2019;Kumar et al., 2020;Tyagi et al., 2020), and transcriptomic data (Garrison et al., 2016;Fernandez et al., 2018). ...
... Araneae phylogeny has been extensively studied at various taxonomic levels by using morphological data (Coddington, 2005;Haupt, 2008), multiple molecular markers (Blackledge et al., 2009;Dimitrov et al., 2012;Wheeler et al., 2017), mitogenomic data (Pons et al., 2019;Kumar et al., 2020;Tyagi et al., 2020), and transcriptomic data (Garrison et al., 2016;Fernandez et al., 2018). These previous studies largely supported the monophyly of the RTA clade; however, the family relationships within the RTA clade remain controversial among previous studies (Wheeler et al., 2017;Fernandez et al., 2018;Kallal et al., 2020). ...
... The phylogenomic analyses presented in this paper represent the largest assessment of RTA phylogeny using mitogenome data in terms of the number of spider species. Consistent with the results of previous studies (Kallal et al., 2020;Kulkarni et al., 2021), all the six phylogenetic trees based on mitogenomic data covered the monophyly of two groups (Oval calamistrum clade and Marronoid clade) and families with more than two species excluding Pisauridae. The non-monophyletic Pisauridae has also been reported paraphyletic in previous phylogeny analyses (Garrison et al., 2016;Wheeler et al., 2017). ...
The retrolateral tibial apophysis (RTA) clade is the largest spider lineage within Araneae. To better understand the diversity and evolution, we newly determined mitogenomes of ten RTA species from six families and performed a comparative mitogenomics analysis by combining them with 40 sequenced RTA mitogenomes available on GenBank. The ten mitogenomes encoded 37 typical mitochondrial genes and included a large non-coding region (putative control region). Nucleotide composition and codon usage were well conserved within the RTA clade, whereas diversity in sequence length and structural features was observed in control region. A reversal of strand asymmetry in nucleotide composition, i.e., negative AT-skews and positive GC-skews, was observed in each RTA species, likely resulting from mitochondrial gene rearrangements. All protein-coding genes were evolving under purifying selection, except for atp8 whose Ka/Ks was larger than 1, possibly due to positive selection or selection relaxation. Both mutation pressure and natural selection might contribute to codon usage bias of 13 protein-coding genes in the RTA lineage. Phylogenetic analyses based on mitogenomic data recovered a family-level phylogeny within the RTA; {[(Oval calamistrum clade, Dionycha), Marronoid clade], Sparassidae}. This study characterized RTA mitogenomes and provided some new insights into the phylogeny and evolution of the RTA clade.
... We composed a dataset combining eight traditional target markers from the analysis of Dimitrov et al. (2017) (12s, 16s, 18s, two fragments of 28s, co1, H3, and wnt), the marker Actin 5c (act) from Ballarin and Li (2018), and protein transcriptomic data (AA) from the "all taxa, 67% occupancy" dataset from Kallal et al. (2020). Because the relationships of some families of Araneoidea are not robust to analytical conditions of the phylogenomic data, we also considered the alternative analysis of genomic ultraconserved elements (UCE) of Kulkarni et al. (2021, see their Fig. 1 and Fig. S1) representing their results as a backbone constraint. ...
... The remaining genera of nesticids are a monophyletic group with high support, that we propose as a narrowed re-limited Nesticidae. The transcriptomic data analyzed alone ( Fig. S8) resulted in groups coincident with the original analysis of Kallal et al. (2020). The DNA data analyzed with a transcriptomic backbone constraint produced similar results as above, in the analyses under maximum likelihood or parsimony (Figs. ...
... Our phylogenetic analysis of molecular data and the morphological characters confirm that Tekellina does not belong to Theridiidae, but is instead closely related to Hamus and Nescina, currently placed in Nesticidae. The DNA markers suggest a close relationship of those three genera with Gaucelmus, and also with Synotaxus, currently the only member of Synotaxidae as redefined by genomic analyses (Kallal et al., 2020). In particular, the sister group relationship of Synotaxus and Gaucelmus augustinus is strongly supported by five markers independently (16s, 18s, 28s1, 28s2 and H3, with bootstrap 98-100%), and marginally by one marker (co1, 47%); this result was originally obtained by Wheeler et al. (2017), which is the source of part of the data that we analyzed here, including Gaucelmus and Synotaxus. ...
A new species, Tekellina araucana sp. n., is described from from Chile and Argentina. Detailed morphological data from the spinnerets and male palp of T. araucana sp. n. and Tekellina sadamotoi Yoshida & Ogata, 2016 is provided. A new diagnostic character of Tekellina Levi, 1957, a row of bottle-like modified setae between the anal tubercle and the spinnerets was found. The absence of aggregate and cylindrical gland spigots may be a further diagnostic character for the genus. New molecular sequence data of T. araucana sp. n., Tekellina archboldi Levi, 1957 (generotype) and Nescina kohi Lin, Ballarin & Li, 2016, is provided and analyzed together with legacy genetic and transcriptomic data from a wide sampling of species representing all areaneoid families. Both molecular and morphological data suggest that Tekellina is closely related to Synotaxus Simon, 1895 together with three genera formerly placed in Nesticidae. From those results we broaden the limits of Synotaxidae to include the genera Synotaxus, Hamus Lin, Ballarin & Li, Nescina Lin, Ballarin & Li, Gaucelmus Keyserling, 1884, and Tekellina. The morphological data, especially of the male palps, is consistent with that re-limitation.
... This clade is relatively well-sampled phylogenetically, and includes the majority of orbweavers, which build round (orbicular) webs incorporating sticky silk, along with weavers of sheetwebs, cobwebs, and others. The most recent reconstructions of web evolution focusing on araneoids has suggested multiple gains and losses of orb-webs (Kallal et al., 2021b). Within the araneoids, several clades have secondarily reverted to a non-capture web, active-hunter lifestyle, including Arkyidae, Malkaridae, and Mimetidae at the family level and numerous lineages at more specific taxonomic scales within Araneidae and Tetragnathidae. ...
... The widely-sampled, time-calibrated phylogeny from Kallal et al. (2021b) was used for phylogeneticallyinformed analyses (Fig. 1). If a landmarked specimen was not present in the phylogeny, it was paired with its closest sequenced relative; other terminals were omitted. ...
... This resulted in a phylogeny with 39 terminals, as the female conspecific of Diplocephalus was not included (Fig. 1). The specimens were coded for their predation method in three hierarchically nested ways: whether they use their Kallal et al. (2021b). Major clades highlighted: Opisthothelae, grey; Mygalomorphae, brown; Synspermiata, blue; Palpimanoidea, green; UDOH Grade, orange; RTA Clade, violet; Araneoidea, red. ...
Understanding complex morphological shape differences has been revolutionized by the marriage of three-dimensional morphometric techniques and micro-computed tomography scanning. In animals, a major focus of this work has been the vertebrates, particularly the axial skeleton, while shape diversity in arthropods, by comparison, is less well explored. For example, the chelicerae (fanged, jaw-like mouthpart appendages) of spiders exhibit a wide degree of variation and may be expected to differ across the diversity of spider sizes and hunting strategies (e.g., active hunters versus relying on a web to intercept and capture prey) as well as in comparison to other structures on the same organism. We characterize and quantify the shapes of the carapace and chelicerae of 40 spiders across the spider tree of life and look for differences based on how those spiders attain their prey and whether their shapes coevolved or are modular. We found evidence for differences in cheliceral shape and related structures in spiders with different predation strategies as well as evidence for both integration and modularity in those structures. This suggests different pressures on the chelicerae including but not limited to predation mode. Furthermore, while differences in the structures were observed, they still must work in concert.
... These repeat modules are not unique to U. diversus, they are also present in CrSp orthologs from other cribellate spiders such as Octonoba, Tengella, Stegodyphus, and Badumna [49,50,59]. For example, repeat module 1 has a 79% amino acid (aa) identity within Uloboridae and a range of 28-34% aa identity between uloborids and other families, suggesting it has been conserved for at least ~ 250 Mya (Additional file 3: Figure S4) [17,62]. Repeat modules 2 and 3 do not align well outside of Uloboridae while having 75% and 69% identity within Uloboridae, respectively (Additional file 3: Figure S4). ...
... We also propose that the D. spinosa spidroin (ABD61590) described by Garb et al. [57] is likely to be expressed in pseudoflagelliform silk glands, but is neither a Pflag ortholog nor a Flag spidroin as previously thought. In terms of Flag and Pflag evolution, we posit that these two spidroin types are the results of a duplication event in the common ancestor of araneoids, uloborids, the RTA-clade, and eresids (Entelegynae), approximately 250 Mya [17,62]. Flag appears to have been lost in uloborids and eresids, but retained in at least two RTA-clade families, Zoropsidae and Desidae (Fig. 4). ...
... For each silk type, we analyzed associated spidroins and elucidated their role in the mechanical properties of cribellate silk. Furthermore, we showed that the molecular composition of the capture thread of cribellate spiders has a complex evolutionary history involving at least six duplication events dating back to ~ 250 mya [17,62]. While Pflag and Flag spidroins resulted from a more recent duplication and likely were co-expressed ancestrally, CrSp spidroins do not appear homologous to AgSp (do not share a recent gene duplication event) suggesting both punctuated and gradual evolution of the capture spiral. ...
Background
Spiders have evolved two types of sticky capture threads: one with wet adhesive spun by ecribellate orb-weavers and another with dry adhesive spun by cribellate spiders. The evolutionary history of cribellate capture threads is especially poorly understood. Here, we use genomic approaches to catalog the spider-specific silk gene family (spidroins) for the cribellate orb-weaver Uloborus diversus .
Results
We show that the cribellar spidroin, which forms the puffy fibrils of cribellate threads, has three distinct repeat units, one of which is conserved across cribellate taxa separated by ~ 250 Mya. We also propose candidates for a new silk type, paracribellar spidroins, which connect the puffy fibrils to pseudoflagelliform support lines. Moreover, we describe the complete repeat architecture for the pseudoflagelliform spidroin (Pflag), which contributes to extensibility of pseudoflagelliform axial fibers.
Conclusions
Our finding that Pflag is closely related to Flag, supports homology of the support lines of cribellate and ecribellate capture threads. It further suggests an evolutionary phase following gene duplication, in which both Flag and Pflag were incorporated into the axial lines, with subsequent loss of Flag in uloborids, and increase in expression of Flag in ecribellate orb-weavers, explaining the distinct mechanical properties of the axial lines of these two groups.
... 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. ...
Behavior is often phylogenetically informative and detailed descriptions of behavior have been used to support taxonomic relationships in several groups, such as birds, lizards, and arthropods. Web building behavior has provided informative traits to several spider families, but observations are lacking for other families, such as wall spiders Oecobiidae. Recent phylogenetic hypotheses based on molecular traits placed oecobiids either close to cribellate orb weavers (Uloboridae) or to long-spinneret spiders (Hersiliidae). Here, we describe for first time the web construction behavior and details of the web design in the oecobiid Oecobius concinnus Simon 1893 (Oecobiidae). We compare them with uloborid and araneoid orb weavers. If Oecobiidae and Uloboridae are closely related, we expect that O. concinnus share some web construction behaviors with these orb weavers. Video recordings and analyses of web structures suggest the sequence of web construction (radii, then sticky spiral construction) and the arrangement of cribellate threads are possible homologies between Oecobiidae and orb weavers, supporting a close relationship of Oecobiidae with Uloboridae. © 2022 Dipartimento di Biologia, Università di Firenze, Italia.
... 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. ...
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.
... behaviors (e.g., Kallal et al., 2020;Wolff et al., 2019). However, the influence of convergence on mygalomorph spiders has not previously been explored analytically. ...
... A final consideration is the ecological constraint of niche availability. Both the aerial web-building niche and active, cursorial niches were inhabited early in araneomorph evolution (Kallal et al., 2020), and therefore opportunity for mygalomorph ancestors to exploit these niches would have been limited by direct competition with their araneomorph relatives. The mygalomorph adaptive landscape is narrow, but they are well-adapted to their sedentary lifestyle. ...
Understanding the drivers of morphological convergence requires investigation into its relationship with behavior and niche space, and such investigations in turn provide insights into evolutionary dynamics, functional morphology, and life history. Mygalomorph spiders (trapdoor spiders and their kin) have long been associated with high levels of morphological homoplasy, and many convergent features can be intuitively associated with different behavioral niches. Using genus-level phylogenies based on recent genomic studies and a newly assembled matrix of discrete behavioral and somatic morphological characters, we reconstruct the evolution of burrowing behavior in the Mygalomorphae, compare the influence of behavior and evolutionary history on somatic morphology, and test hypotheses of correlated evolution between specific morphological features and behavior. Our results reveal the simplicity of the mygalomorph adaptive landscape, with opportunistic, web-building taxa at one end, and burrowing/nesting taxa with structurally modified burrow entrances (e.g., a trapdoor) at the other. Shifts in behavioral niche, in both directions, are common across the evolutionary history of the Mygalomorphae, and several major clades include taxa inhabiting both behavioral extremes. Somatic morphology is heavily influenced by behavior, with taxa inhabiting the same behavioral niche often more similar morphologically than more closely related but behaviorally divergent taxa, and we were able to identify a suite of 11 somatic features that show significant correlation with particular behaviors. We discuss these findings in light of the function of particular morphological features, niche dynamics within the Mygalomorphae, and constraints on the mygalomorph adaptive landscape relative to other spiders.
... uenoi (Yaginuma, 1972); Cyclocarcina floronoides Komatsu, 1942 andNesticus kyongkeomsanensis Namkung, 2002. Traditionally, Nesticidae were considered as a sister group to Theridiidae, however recent phylogenies place them as a sister group to other families, e.g.: Linyphiidae (Bond et al., 2014), Synotaxidae (Kallal et al., 2021) or Araneidae (Ramírez et al., 2021). Therefore, we have included a broad sample of araneoid families as outgroups. ...
... The split between Crete and Turkey has been used to date the divergence of Sulcia species (Leptonetidae) with analogous distribution . We applied this constraint as a uniform prior with min bound of 12Ma and max bound of 120 Ma that corresponds to recent estimates of the minimum age of Araneoidea (Kallal et al., 2021). Molecular dating analyses in BEAST2 were run for 400 million generations (for the dating without biogeographic constraints) and 280 million (generations for the dating implementing the biogeographic constraint). ...
Nesticidae is a small family of spiders with a worldwide distribution that includes 15 genera and 272 described species. Seven genera and 56 species are known from Europe, distributed from the Iberian Peninsula to the Caucasus and the Ural Mountains. Most of these European species are cave dwellers and many of them are troglobites. In this study we present the first molecular phylogeny of the family Nesticidae in Europe with a wide geographical sampling across the continent. In our analysis the European nesticid fauna is well represented, including six genera and 40 of the 56 currently accepted species including the type species of all sampled genera. We have included in the analysis representatives of the North American and Asian fauna to test the monophyly of the European species and the phylogenetic relationships of European lineages. Phylogenetic relationships were reconstructed using maximum likelihood and Bayesian inference. As part of our Bayesian analyses, we also dated the phylogeny using two approaches, one based only on fossil calibrations and one that included an additional biogeographical constraint.
Our results show paraphyly of the European nesticids with respect to the Asian and North American taxa. We recover four main lineages within Europe. These four European lineages and all European genera have 100% bootstrap support and high posterior probability support in the BEAST2 analysis. The Typhlonesticus lineage is the earliest branching clade present in Europe and includes seven species, the five currently accepted species plus T. parvus from Bosnia and Herzegovina and T. silvestrii from western North America. The Eastern lineage includes the genus Aituaria and is the sister group of the Asian genera Nesticella and Wraios. The Domitius lineage is likely the sister group of the Central European lineage and spreads over the Iberian and Italian peninsulas. Finally, the Central European lineage includes three genera: Kryptonesticus, distributed from the karstic massifs of the Balkan Peninsula to Turkey, Nesticus with a single synanthropic species N. cellulanus and Carpathonesticus, exclusive to the Carpathian Mountains. With the exception of the genus Typhlonesticus, all European genera show an allopatric distribution (except for the two European synanthropic species). The results obtained in this study together with the revision of the original descriptions, redescriptions, and illustrations, lead us to propose 11 nomenclatural changes (new combinations) concerning the genera Typhlonesticus, Nesticus and Carpathonesticus.
... Spiders represent a clade with many examples of rapid radiations that present a high diversity of morphological, behavioral, and ecological traits interesting for character evolution studies (Bond and Opell 1998, Vizueta et al. 2019, Crews et al. 2020, Berger et al. 2021, Dimitrov and Hormiga 2021. Although the capture web is one of the most striking features of spiders and a target of many evolutionary studies (Bond et al. 2014, Garrison et al. 2016, Fernández et al. 2018, Coddington et al. 2019, Kallal et al. 2020, about half of spider species do not use webs for catching prey. This alternative web-less hunting style might have led to several changes in the morphology and ecology of web-less species (Wolff et al. 2013(Wolff et al. , 2021. ...
... In fact, metanalyses suggest that specialized setae on spider feet (scopulae and claw tufts) could be seen as a 'great silk alternative' (Wolff et al. 2013). Although the association between claw tuft and/or loss of third claw with the web-less behavior seems very strong, the hypothesis of causal relationship between those characters is difficult to test for three reasons: (1) methods available can bias toward finding significant relationships when there are none (Maddison and Garrison et al. 2016, Fernández et al. 2018, Coddington et al. 2019, Kallal et al. 2020). Here we found another possible complication: the possibility that those characters represent hemiplasies in some parts of the tree. ...
Traits that independently evolve many times are important for testing hypotheses about correlated evolution and understanding the forces shaping biodiversity. However, population genetics processes can cause hemiplasies (traits determined by genes whose topologies do not match the species tree), leading to a false impression of convergence (homoplasy) and potentially misleading inferences of correlated evolution. Discerning between homoplasies and hemiplasies can be important in cases of rapid radiations and clades with many gene tree incongruences. Here, focusing on two-clawed spiders (Dionycha) and close relatives, we evaluate if the observed distribution of characters related to a web-less lifestyle could be better explained as synapomorphies, homoplasies, or hemiplasies. We find that, although there are several convergences, hemiplasies are also sometimes probable. We discuss how these hemiplasies could affect inferences about correlation and causal relationship of traits. Understanding when and where in the tree of life hemiplasy could have happened is important, preventing false inference of convergent evolution. Furthermore, this understanding can provide alternative hypotheses that can be tested with independent data. Using traits related to the climbing ability of spiders we show that, when hemiplasy is unlikely, adequate model testing can be used to better understand correlated evolution, and propose hypotheses to be tested using controlled behavioral and mechanical experiments.
... Finally, representatives of all the families within the Synespermiata clade, including members of the Superfamily Dysderoidea were considered to provide fossil information for calibration. All trees were rooted, assuming a sister group relationship of the families Hypochilidae and Filistatidae with the Synespermiata clade (Garrison et al. 2016;Wheeler et al. 2017;Fernández et al. 2018;Michalik et al. 2019;Kulkarni et al. 2020Kallal et al. 2021;Ramírez et al. 2021). ...
Natural selection plays a key role in deterministic evolution, as clearly illustrated by the multiple cases of repeated evolution of ecomorphological characters observed in adaptive radiations. Unlike most spiders, Dysdera species display a high variability of cheliceral morphologies, which has been suggested to reflect different levels of specialisation to feed on isopods. In this study, we integrate geometric morphometrics and experimental trials with a fully resolved phylogeny of the highly diverse endemic species from the Canary Islands to 1) quantitatively delimit the different cheliceral morphotypes present in the archipelago, 2) test their association with trophic specialisation, as reported for continental species, 3) reconstruct the evolution of these ecomorphs throughout the diversification of the group, 4) test the hypothesis of convergent evolution of the different morphotypes, and 5) examine whether specialisation constitutes a case of evolutionary irreversibility in this group. We show the existence of nine cheliceral morphotypes and uncovered their significance for trophic ecology. Further, we demonstrate that similar ecomorphs evolved multiple times in the archipelago, providing a novel study system to explain how convergent evolution and irreversibility due to specialization may be combined to shape phenotypic diversification in adaptive radiations.
... The inability of bootstrap support values to differentiate between the efficiency of partitioning schemes for our dataset in lower-level lineages made it necessary to analyse concordance factors. Previous studies demonstrate that concordance factors are generally lower than UFBoot2 and SH-aLRT support values, particularly for large datasets where sampling variance is low (Chan et al., 2020;Kallal et al., 2021;Minh et al., 2020a;Rota et al., 2022;van Elst et al., 2021), but these values also responded differently to the choice of partitioning strategy for our dataset. Bootstrap values increase with the addition of data blocks and are thus sensitive to overparameterization which means that well-supported nodes in geneXcodon-based phylogenies (PS6-PS8) were likely victims of inflated support values (Supplementary material S1, part 4) (Leavitt et al., 2013;Li et al., 2008;Sullivan and Joyce, 2005). ...
Complex evolutionary patterns in the mitochondrial genome (mitogenome) of the most species-rich order, the Carcharhiniforms (groundsharks) has yielded challenges in phylogenomic reconstruction of families and genera belonging to it, particularly in the family Triakidae (houndsharks), where there are arguments for both monophyly and paraphyly. We hypothesized that opposing resolutions are a product of the a priori partitioning scheme selected. Accordingly, we employed an extensive statistical framework to select our partitioning scheme for inference of the mitochondrial phylogenomic relationships within Carcharhiniforms and used the multi-species coalescent model to account for the influence of gene tree discordance on species tree inference. We included five new houndshark mitogenomes to increase resolution of Triakidae and uncovered a 714 bp-duplication in the assembly of Galeorhinus galeus. Phylogenetic reconstruction confirmed monophyly within Triakidae and the existence of two clades of the expanded Mustelus genus, alluding to the evolutionary reversal of reproductive mode from placental to aplacental.
... Although the phylogenetic analyses in this study have few exemplar taxa due to the limited number of well-characterized mitogenomes, especially for jumping spiders, they show the potential of mitochondrial sequences for resolving the phylogenetic relationships of spiders and providing insight into the placement of certain problematic taxa. Both analyses on the nucleotide and amino acid datasets recovered the same relationships among the Salticidae and the outgroup families, which are largely congruent with recent transcriptome-or UCE (ultra-conserved element)-based phylogenomic studies [80][81][82][83]. Within the Dionycha clade, Salticidae was suggested to be a sister to the clade of Cheiracanthiidae + Philodromidae (Figure 8) through mitogenomic PCGs, but the phylogenomic study on Dionycha combining genomic, morphological and Sanger data indicated a sister relationship between Salticidae and Philodromidae [83]. ...
Salticidae is the most species-rich family of spiders with diverse morphology, ecology and behavior. However, the characteristics of the mitogenomes within this group are poorly understood with relatively few well-characterized complete mitochondrial genomes. In this study, we provide completely annotated mitogenomes for Corythalia opima and Parabathippus shelfordi, which represent the first complete mitogenomes of the tribe Euophryini of Salticidae. The features and characteristics of the mitochondrial genomes are elucidated for Salticidae by thoroughly comparing the known well-characterized mitogenomes. The gene rearrangement between trnL2 and trnN was found in two jumping spider species, Corythalia opima and Heliophanus lineiventris Simon, 1868. Additionally, the rearrangement of nad1 to between trnE and trnF found in Asemonea sichuanensis Song & Chai, 1992 is the first protein-coding gene rearrangement in Salticidae, which may have an important phylogenetic implication for the family. Tandem repeats of various copy numbers and lengths were discovered in three jumping spider species. The codon usage analyses showed that the evolution of codon usage bias in salticid mitogenomes was affected by both selection and mutational pressure, but selection may have played a more important role. The phylogenetic analyses provided insight into the taxonomy of Colopsus longipalpis (Żabka, 1985). The data presented in this study will improve our understanding of the evolution of mitochondrial genomes within Salticidae.
... for at least one gene, even though all were preserved in 75% ethanol at room temperature for over a decade. To these, we added 15 samples of 12 outgroup species chosen after previous phylogenetic work by Wheeler et al. (2017) and Kallal et al. (2021). The outgroups included all genera of Porteriinae, plus representatives of other subfamilies of Desidae: Amphinecta Simon, 1898 (Amphinectinae), Badumna Thorell, 1890 (Matachiinae), Desis Walckenaer, 1837 (Desinae) and Metaltella Mello-Leitão, 1931 (Metaltellinae). ...
We revise the Chilean genus Porteria, including the type species, Porteria albopunctata, and 11 new species: Porteria ajimayo sp. nov., Porteria alopobre sp. nov., Porteria ariasbohartae sp. nov., Porteria bunnyana sp. nov., Porteria contulmo sp. nov., Porteria correcaminos sp. nov., Porteria eddardstarki sp. nov., Porteria faberi sp. nov., Porteria fiura sp. nov., Porteria misbianka sp. nov. and Porteria torobayo sp. nov. A phylogenetic analysis using six genetic markers confirms the monophyly of Porteriinae, including Baiami and the core porteriines, here defined to include the ecribellate genera Cambridgea, Corasoides, Nanocambridgea and Porteria. Core porteriines are diagnosed by a narrowed section of the piriform gland spigot field, the cymbium extended to a narrow tip and lack of a median apophysis. Porteria and Corasoides are sister taxa, united by the behaviour of running atop the sheet of a web and by spinning a regular square mesh in the web platform. According to our results, the diversification of Porteria started about 30 Mya (44–17 Mya). A biogeographic analysis infers that an ancestor of Porteria reached South America via a founder event from Australia or New Zealand, where their close relatives occur.
... Therefore, it is rather surprising that recent phylogenomic analyses did not obtain a monophyletic group of orb-weaving spiders (e.g., Fernández et al., 2018;Garrison et al., 2016;Kallal et al., 2021) suggesting that this complex and stereotyped web-building behavior evolved independently. ...
Geometric regularity of spider webs has been intensively studied in orb-weaving spiders, although it is not exclusive of orb weavers. Here, we document the geometrically regular, repetitive elements in the webs of the non-orb-weaving groups Leptonetidae and Telemidae for the first time. Similar to orb weavers, we found areas with regularly spaced parallel lines in the webs of Calileptoneta helferi, Sulcia sp., and cf. Pinelema sp. Furthermore, we provide a detailed account of the regular webs of Ochyrocera (Ochyroceratidae). The sections of the web with regularly disposed parallel lines are built as U-shaped modules reminiscent of orb webs. It has been suggested that the regularly spaced parallel lines in the webs of Ochyroceratidae and Psilodercidae may be produced in a single sweep of their posterior lateral spinnerets, which have regularly spaced aciniform gland spigots, perhaps involving expansion of the spinnerets. To test this hypothesis, we compared the spacing between parallel lines with the spacing between spigots, searched for expansible membranes in the spinnerets, and examined the junctions of regularly spaced lines. The distance between parallel lines was 10-20 times the distance between spigots, and we found no expansible membranes, and the intersection of parallel lines are cemented, which opposes the single sweep hypothesis. Furthermore, we found cues of viscid silk in the parallel lines of the psilodercid Althepus and broadened piriform gland spigots that may be responsible of its production. Finally, we evaluated the presence or absence of geometrically regular web elements across the spider tree of life. We found reports of regular webs in 31 spider families, including 20 families that are not orb weavers and hypothesize that the two basic aspects of regularity (parallel lines spaced at regular intervals, and radial lines spaced at regular angles) probably appeared many times in the evolution of spiders.
... Vertebrate and onychophoran time trees were obtained from the literature (Baker, Buckman-Young, Costa, & Giribet, 2021;Irisarri et al., 2017) and pruned to keep only a selection of 13 vertebrate species whose aquaporins have previously been studied (Finn et al., 2014) and the four onychophorans (or closely-related species) that were included in MATEdb , respectively. For the rest of the phyla, arthropods, molluscs and annelids, timescaled ultrametric trees were inferred independently by using a node-dating approach on species trees that followed the most recent topologies (Anderson & Lindgren, 2021;Ballesteros et al., 2022;Colgan, Ponder, Beacham, & Macaranas, 2007;Cunha & Giribet, 2019;Doğan, Schrödl, & Chen, 2020;Erséus et al., 2020;Fernández, Edgecombe, & Giribet, 2018;González et al., 2015;Johnson et al., 2018;Kallal et al., 2021;Kawahara et al., 2019;Kocot et al., 2011;Kocot, Halanych, & Krug, 2013;Kocot, Poustka, Stöger, Halanych, & Schrödl, 2020;Kocot et al., 2017;Kocot, Todt, Mikkelsen, & Halanych, 2019;Lee et al., 2019;Lindgren, 2010;Lozano-Fernandez et al., 2019;McKenna et al., 2019;Misof et al., 2014;Moles & Giribet, 2021;Ontano et al., 2021;Pabst & Kocot, 2018;Peters et al., 2017;Razkin et al., 2015;Richter, Richter, & Scholtz, 2001;Salvi & Mariottini, 2016;Schwentner, Richter, Rogers, & Giribet, 2018;Smith, 2021;Smith et al., 2011;Sun et al., 2020;Uribe, Colgan, Castro, Kano, & Zardoya, 2016;Uribe & Zardoya, 2017;Wang, Shi, Qiu, Che, & Lo, 2017;Wiegmann et al., 2011;Yang et al., 2018). In the case of annelids, we dated the species tree using the Aqp1-like gene sequences in MCMCtree (Yang, 2007). ...
One of the most important physiological challenges animals had to overcome during terrestrialization (i.e., the transition from sea to land) was water loss, which alters their osmotic and hydric homeostasis. Aquaporins are a superfamily of membrane water transporters heavily involved in osmoregulatory processes. Their diversity and evolutionary dynamics in most animal lineages remain unknown, hampering our understanding of their role in marine‐terrestrial transitions. Here, we interrogated aquaporin gene repertoire evolution across the main terrestrial animal lineages. We annotated aquaporin‐coding genes in genomic data from 458 species from seven animal phyla where terrestrialization episodes occurred. We then explored aquaporin gene evolutionary dynamics to assess differences between terrestrial and aquatic species through phylogenomics and phylogenetic comparative methods. Our results revealed parallel aquaporin‐coding gene duplications during the ecological transition from marine to non‐marine environments (e.g., brackish, freshwater and terrestrial), rather than from aquatic to terrestrial ones, with some notable duplications in ancient lineages. In contrast, we also recovered a significantly lower number of superaquaporin genes in terrestrial arthropods, suggesting that more efficient oxygen homeostasis in land arthropods might be linked to a reduction in this type of aquaporin. Our results thus indicate that aquaporin‐coding gene duplication and loss might have been one of the key steps towards the evolution of osmoregulation across animals, facilitating the ‘out of the sea’ transition and ultimately the colonisation of land.
... Spiders are the pre-eminent silk producers among arthropods . About 13000 species of spiders (Hormiga and Griswold 2014;Kallal et al. 2020Kallal et al. , 2021World Spider Catalog 2022) construct orb webs with diameter ranging from 1 cm (family Anapidae) to 2 m (Caerostris darwini) to mainly capture the flying insects (Gregorič et al. 2011). The webs have two-dimensional circular capture area, a spiral capture thread circling outwards from the hub (Soler and Zaera 2016) and evenly distributed radial threads spanning from the hub towards the web periphery (Foelix 2011;Gan et al. 2015). ...
Spiders are the pre-eminent silk producers and many species construct orb webs to capture the insect prey. The present study was focused on the design and the orientation patterns of Neoscona theisi orb webs, during the crop growing seasons of rice and wheat. Architectural design of webs constructed by the orb web spider was examined in the crop fields by walking through the fields to locate the spider webs. Results revealed that web height and diameter increased along with increase in the diversity and availability of insect pests of rice. The proportion of vertically oriented webs of N. theisi increased progressively with increase in the availability of highly active and large-sized, prey in the paddy fields. In the wheat agroecosystem, the proportion of spiders without webs increased in response to the availability of the most abundant, small sized (with very low mobility) aphid prey, Sitobion avenae. It is likely that the adaptive plasticity in web size and orientation patterns exhibited by N. theisi not only helps it to maximize its prey capture efficiency but also plays an important role in contributing towards its dominance among the orb web-making species.
... The past decade alone has witnessed the first molecular phylogenetic hypotheses for several orders, such as Scorpiones, Ricinulei (hooded tick-spiders), Palpigradi (microwhip scorpions), Thelyphonida (vinegaroons), Schizomida (short-tailed whip scorpions), and Amblypygi (whip spiders) (Murienne et al. 2013a; Giribet et al. 2014;Fernández and Giribet 2015;Sharma et al. 2015;Clouse et al. 2017). More diverse chelicerate groups, such as Acari (mites), Araneae (spiders), Opiliones (harvestmen), and Pseudoscorpiones, have witnessed a surge of evolutionary inquiry in the past ten years (Hedin et al. 2012;Bond et al. 2014;Fernández et al. 2014;Garrison et al. 2016;Fernández et al. 2017;Klimov et al. 2017;Santibáñez-López et al. 2019;Benavides et al. 2019a;Kulkarni et al. 2020;Ballesteros et al. 2021;Kallal et al. 2021;Santibáñez-López et al. 2022). This decade is also notable for the completion of the first genomes for several chelicerate orders (Sanggaard et al. 2014;Gulia-Nuss et al. 2016;Hoy et al. 2016;Kenny et al. 2016;Schwager et al. 2017;Gainett et al. 2021;Ontano et al. 2021). ...
Considerable progress has been achieved in resolving higher-level relationships of Arthropoda in the past two decades, largely precipitated by advances in sequencing technology. Yet, dark branches persist in the arthropod tree of life, principally among groups that are difficult to collect, occur in cryptic habitats, or are characterized by minute body size. Among chelicerates, the mesodiverse order Solifugae (commonly called camel spiders or sun spiders) is one of the last orders of Arachnida that lacks a higher-level phylogeny altogether and has long been characterized as one of the "neglected cousins", a lineage of arachnid orders that are comparatively poorly studied with respect to evolutionary relationships. Though renowned for their aggression, remarkable running speed, and adaptation to arid habitats, inferring solifuge relationships has been hindered by inaccessibility of diagnostic characters in most ontogenetic stages for morphological datasets, whereas molecular investigations to date have been limited to one of the 12 recognized families. In this study we generated a phylogenomic dataset via capture of ultraconserved elements (UCEs) and sampled all extant families. We recovered a well-resolved phylogeny of solifuge families, with two distinct groups of New World taxa nested within a broader Paleotropical radiation. To provide a temporal context to solifuge diversification, we estimated molecular divergence times using fossil calibrations within a Bayesian framework. Solifugae were inferred to have radiated by the Permian, with divergences of most families dating to the post Paleogene-Cretaceous extinction. These results accord with a diversification history largely driven by vicariance as a result of continental breakup.
... At the same time, this morphological diversity is potentially informative in phylogeny reconstruction. For example, the investigation of sperm structures across the spider tree of life by Michalik and Ramírez [22] recovered synapomorphies for a wide range of taxa, such as synspermia as the characteristic of the Synspermiata -a clade of haplogyne spiders that includes Pholcidae and that was also recovered by all consecutive phylogenomic studies [23][24][25]. ...
Background
Pholcidae represent one of the largest and most diverse spider families and have been subject to various studies regarding behavior and reproductive biology. In contrast to the solid knowledge on phylogeny and general reproductive morphology, the primary male reproductive system is strongly understudied, as it has been addressed only for few species. Those studies however suggested a high diversity of sperm and seminal secretions across the family. To address this disparity and reconstruct the evolution of sperm traits, we investigate the primary male reproductive system of pholcid spiders by means of light, X-ray, and transmission electron microscopy using a comprehensive taxon sampling with 46 species from 33 genera, representing all five subfamilies.
Results
Our data show a high disparity of sperm morphology and seminal secretions within pholcids. We document several sperm characters that are unique for pholcids, such as a helical band (Pholcinae) or a lamellate posterior centriolar adjunct material (Modisiminae). Character mapping revealed several putative synapomorphies for individual taxa. With regard to sperm transfer forms, we found that synspermia occur only in the subfamily Ninetinae, whereas the other subfamilies have cleistospermia. In several species with cleistospermia, we demonstrate that spermatids remain fused until late stages of spermiogenesis before ultimately separating shortly before the coiling process. Additionally, we explored the previously hypothesized correlation between sperm size and minimum diameter of the spermophor in the male palpal organ. We show that synspermia differ strongly in size whereas cleistospermia are rather uniform, but neither transfer form is positively correlated with the diameter of the spermophor.
Conclusions
Our data revealed a dynamic evolution of sperm characters, with convergences across all subfamilies and a high level of homoplasy. The present diversity can be related to subfamily level and allows for assignments of specific subtypes of spermatozoa. Our observations support the idea that Ninetinae are an ancestral clade within Pholcidae that have retained synspermia and that synspermia represent the ancestral sperm transfer form of Pholcidae.
... A final consideration is the ecological constraint of niche availability. Both the aerial web-building niche, and active, cursorial niches were inhabited early in araneomorph evolution (Kallal et al., 2020), and therefore opportunity for mygalomorph ancestors to exploit these niches would have been limited by direct competition with their araneomorph relatives. The mygalomorph adaptive landscape is narrow, but they are well-adapted to their sedentary lifestyle. ...
Understanding the drivers of morphological convergence requires investigation into its relationship with behavior and niche-space, and such investigations in turn provide insights into evolutionary dynamics, functional morphology, and life history. Mygalomorph spiders (trapdoor spiders and their kin) have long been associated with high levels of homoplasy, and many convergent features can be intuitively associated with different behavioral niches. Using genus-level phylogenies based on recent genomic studies and a newly assembled matrix of discrete behavioral and somatic morphological characters, we reconstruct the evolution of burrowing behavior in the Mygalomorphae, compare the influence of behavior and evolutionary history on somatic morphology, and test hypotheses of correlated evolution between specific morphological features and behavior. Our results reveal the simplicity of the mygalomorph adaptive landscape, with opportunistic, web-building taxa at one end, and burrowing/nesting taxa with structurally-modified burrow entrances (e.g., a trapdoor) at the other. Shifts in behavioral niche, in both directions, are common across the evolutionary history of the Mygalomorphae, and several major clades include taxa inhabiting both behavioral extremes. Somatic morphology is heavily influenced by behavior, with taxa inhabiting the same behavioral niche often more similar morphologically than more closely-related but behaviorally-divergent taxa, and we were able to identify a suite of 11 somatic features that show significant correlation with particular behaviors. We discuss these findings in light of the function of particular morphological features, niche dynamics within the Mygalomorphae, and constraints on the mygalomorph adaptive landscape relative to other spiders.
... 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. ...
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.
... 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. ...
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 (a) the effect of alternate branch lengths on ASE error and (b) 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 favourable 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%). ...
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.
... 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). ...
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). ...
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).
... 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. ...
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.
Advanced sequencing technologies have expedited resolving higher-level arthropod relationships. Yet, dark branches persist, principally among groups occurring in cryptic habitats. Among chelicerates, Solifugae (“camel spiders”) is the last order lacking a higher-level phylogeny and thus, historically characterized as “neglected [arachnid] cousins”. Though renowned for aggression, remarkable running speed, and xeric adaptation, inferring solifuge relationships has been hindered by inaccessibility of diagnostic morphological characters, whereas molecular investigations have been limited to one of 12 recognized families. Our phylogenomic dataset via capture of ultraconserved elements sampling all extant families recovered a well-resolved phylogeny, with two distinct groups of New World taxa nested within a broader Paleotropical radiation. Divergence times using fossil calibrations inferred Solifugae radiated by the Permian, and most families diverged pre-Paleogene-Cretaceous extinction, largely driven by continental breakup. We establish Boreosolifugae new suborder uniting five Laurasian families, and Australosolifugae new suborder uniting seven Gondwanan families using morphological and biogeographic signal.
Spiders are among the most diverse animals, which developed different morphological and behavioral traits for capturing prey. We studied the anatomy and functionality of the rare and apomorphic raptorial spider feet using 3D reconstruction modeling, among other imaging techniques. The evolutionary reconstruction of the raptorial feet (tarsus plus pretarsus) features using a composite tree of spiders, indicating that similar traits emerged three times independently in Trogloraptoridae, Gradungulinae, and Doryonychus raptor (Tetragnathidae). The characteristics defining the raptorial feet are an interlocked complex merging of the base of the elongated prolateral claw with the pretarsal sclerotized ring, with the former clasping against the tarsus. Raptorial feet even flex over robust raptorial macrosetae forming a reduced tarsal version of a catching basket to encase prey during hunting. Our results show that Celaeniini (Araneidae) and Heterogriffus berlandi (Thomisidae), taxa previously compared with raptorial spiders, lack the raptorial feet key characteristics and the tarsal-catching basket. We make predictions about the possible behavior of the abovementioned taxa that will need to be tested by observing living specimens. We conclude that multiple morphological tarsal and pretarsal micro-structures define the raptorial foot functional unit and recommend a comprehensive evaluation before assigning this configuration to any spider taxa.
Biodiversity catalogs are an invaluable resource for biological research. Efforts to scientifically document biodiversity have not been evenly applied, either because of charisma or because of ease of study. Spiders are among the most precisely cataloged and diverse invertebrates, having surpassed 50,000 described species globally. The World Spider Catalog presents a unique opportunity to assess the disproportionate documentation of spider diversity. In the present article, we develop a taxonomic ratio relating new species descriptions to other taxonomic activity as a proxy for taxonomic effort, using spiders as a case study. We use this taxonomic effort metric to examine biases along multiple axes: phylogeny, zoogeography, and socioeconomics. We also use this metric to estimate the number of species that remain to be described. This work informs arachnologists in identifying high-priority taxa and regions for species discovery and highlights the benefits of maintaining open-access taxonomic databases—a necessary step in overcoming bias and documenting the world's biodiversity.
The orb web is a remarkable example of animal architecture that is observed in families of spiders that diverged over 200 million years ago. While several genomes exist for araneid orb-weavers, none exist for other orb-weaving families, hampering efforts to investigate the genetic basis of this complex behavior. Here we present a chromosome-level genome assembly for the cribellate orb-weaving spider Uloborus diversus. The assembly reinforces evidence of an ancient arachnid genome duplication and identifies complete open reading frames for every class of spidroin gene, which encode the proteins that are the key structural components of spider silks. We identified the 2 X chromosomes for U. diversus and identify candidate sex-determining loci. This chromosome-level assembly will be a valuable resource for evolutionary research into the origins of orb-weaving, spidroin evolution, chromosomal rearrangement, and chromosomal sex determination in spiders.
Insights into the processes underpinning convergent evolution advance our understanding of the contributions of ancestral, introgressed, and novel genetic variation to phenotypic evolution. Phylogenomic analyses characterizing genome-wide gene tree heterogeneity can provide first clues about the extent of ILS and of introgression and thereby into the potential of these processes or (in their absence) the need to invoke novel mutations to underpin convergent evolution. Here, we were interested in understanding the processes involved in convergent evolution in open-habitat chats (wheatears of the genus Oenanthe and their relatives). To this end, based on whole-genome resequencing data from 50 taxa of 44 species, we established the species tree, characterized gene tree heterogeneity, and investigated the footprints of ILS and introgression within the latter. The species tree corroborates the pattern of abundant convergent evolution, especially in wheatears. The high levels of gene tree heterogeneity in wheatears are explained by ILS alone only for 30% of internal branches. For multiple branches with high gene tree heterogeneity, D-statistics and phylogenetic networks identified footprints of introgression. Finally, long branches without extensive ILS between clades sporting similar phenotypes provide suggestive evidence for a role of novel mutations in the evolution of these phenotypes. Together, our results suggest that convergent evolution in open-habitat chats involved diverse processes and highlight that phenotypic diversification is often complex and best depicted as a network of interacting lineages.
Describing patterns of biological diversity and understanding their origins is one of the major challenges of modern ecology. Tropical environments in particular are the most species-rich terrestrial ecosystems and among the least well-known. Spiders are a relevant model group in ecology, because they are abundant and diverse with high ecological importance, whose study should allow a better understanding of the processes responsible for diversity patterns. We investigated the patterns of diversity and the processes responsible for spider assemblages in Neotropical forests and the Hawaiian archipelago using a set of complementary approaches (based on taxa, traits, evolutionary units). Due to the lack of knowledge on sampling and diversity of tropical spiders, we tested and compared different sampling methods and standardized protocols by focusing on different vegetation strata. We developed a morpho-species database to overcome the lack of taxonomic knowledge. We studied a set of traits (body size, leg length and hunting guilds) to test their informative character in tropical assemblages. Finally, we determined evolutionary units to study diversity by applying a multilocus (mitochondrial and nuclear) approach on a large collection of tropical spiders, for which taxonomic knowledge is incomplete and problematic. We have shown that the taxon-, traits- and evolutionary units diversity patterns of tropical spiders are influenced by the habitat, and that consequently habitat filtering is crucial in determining the assemblages of these spiders. In addition, we have shown the context-dependent and scale-dependent nature of diversity patterns in tropical spiders with variations of tropical spider assemblages at a finer scale than that of habitats. Overall, this plaid for more case studies studying tropical diversity patterns at the scale of strata, vegetation sub-structures, and micro-habitat conditions, for which we are suggesting research axe.
In the last decade and a half, advances in genetic sequencing technologies have revolutionized systematics, transforming the field as studying morphological characters; a few genetic markers have given way to genomic data sets in the phylogenomic era. A plethora of molecular phylogenetic studies on many taxonomic groups have come about, converging on, or refuting prevailing morphology or legacy-marker-based hypotheses about evolutionary affinities. Spider systematics has been no exception to this transformation and the interrelationships of several groups have now been studied using genomic data. About 50,500 extant spider species have been described so far, all with a conservative body plan, but innumerable morphological and behavioral peculiarities. Inferring the spider tree of life using morphological data has been a challenging task. Molecular data have corroborated many hypotheses of higher-level relationships, but also resulted in new groups that refute previous hypotheses. In this review, we discuss recent advances in the reconstruction of the Spider Tree of Life and highlight areas where additional effort is needed with potential solutions. We base this review on the most comprehensive spider phylogeny to date, representing 131 of the currently known 132 (99%) spider families. To achieve this sampling, we combined a legacy data set of six Sanger-based markers with newly generated and publicly available genome-scale data sets. We find that some inferred relationships between major lineages of spiders (such as Austrochiloidea, Palpimanoidea, Synspermiata, etc.) are robust across different classes of data. However, several surprising new hypotheses have emerged with different classes of molecular data. We identify and discuss the robust and controversial hypotheses and compile this blueprint to design future studies targeting systematic revisions of these problematic groups. We offer an evolutionary framework to explore comparative questions such as evolution of venoms, silk, webs, morphological traits, and reproductive strategies.
The evolutionary diversification of orb-web weaving spiders is closely tied to the mechanical performance of dragline silk. This proteinaceous fiber provides the primary structural framework of orb web architecture, and its extraordinary toughness allows these structures to absorb the high energy of aerial prey impact. The dominant model of dragline silk molecular structure involves the combined function of two highly repetitive, spider-specific, silk genes (spidroins)—MaSp1 and MaSp2. Recent genomic studies, however, have suggested this framework is overly simplistic, and our understanding of how MaSp genes evolve is limited. Here we present a comprehensive analysis of MaSp structural and evolutionary diversity across species of Argiope (garden spiders). This genomic analysis reveals the largest catalog of MaSp genes found in any spider, driven largely by an expansion of MaSp2 genes. The rapid diversification of Argiope MaSp genes, located primarily in a single genomic cluster, is associated with profound changes in silk gene structure. MaSp2 genes, in particular, have evolved complex hierarchically organized repeat units (ensemble repeats) delineated by novel introns that exhibit remarkable evolutionary dynamics. These repetitive introns have arisen independently within the genus, are highly homogenized within a gene, but diverge rapidly between genes. In some cases, these iterated introns are organized in an alternating structure in which every other intron is nearly identical in sequence. We hypothesize that this intron structure has evolved to facilitate homogenization of the coding sequence. We also find evidence of intergenic gene conversion and identify a more diverse array of stereotypical amino acid repeats than previously recognized. Overall, the extreme diversification found among MaSp genes requires changes in the structure-function model of dragline silk performance that focuses on the differential use and interaction among various MaSp paralogs as well as the impact of ensemble repeat structure and different amino acid motifs on mechanical behavior.
Web designs have long been used to characterize spider taxa and to deduce the relations between them; but systematic documentation of the amount of variation in webs within and between taxonomic groups is rare. This study, based on previously published observations and new observations of 15 species in the family Uloboridae, including two genera, Octonoba Opell, 1979 and Siratoba Opell, 1979, whose webs were previously undocumented, reviews the taxonomic distribution and variation in 22 orb web traits in at least 43 species in 11 genera in uloborids. These traits appear to occur in all orb-weaving genera in which reasonable samples are available, though only small samples are available for many species. Larger samples of the webs of three species of Uloborus Latreille, 1806, two of Hyptiotes Walckenaer, 1837, and one each of Zosis Walckenaer, 1841, Siratoba, Octonoba, Waitkera Opell, 1979 and Philoponella Mello-Leito, 1917, revealed greater intra-specific consistencies in some traits than others. Hub traits were especially consistent. Variations in three traits may represent adjustments to the size of the space in which the orb is built. Primary webs, which combine orb and sheet-web traits, are built by spiderlings newly emerged from the egg sac and by adult males in at least five genera of orb-weaving uloborids and may be unique to this family. Preliminary comparisons between uloborid and araneoid orbs suggest that uloborid orbs may also differ from araneoid orbs in combining several other traits.
Background
A robust and stable phylogenetic framework is a fundamental goal of evolutionary biology. As the third largest insect order following by Diptera and Coleoptera in the world, lepidoptera (butterflies and moths) play a central role in almost every terrestrial ecosystem as the indicators of environmental change and serve as important models for biologists exploring questions related to ecology and evolutionary biology. However, for such charismatic insect group, the higher-level phylogenetic relationships among its superfamilies are still poorly unresolved.
Results
we increased taxon sampling among Lepidoptera (40 superfamilies and 76 families contained 286 taxa) and filtered the unqualified samples, then acquired a series of large amino-acid datasets from 69,680 to 400,330 for phylogenomic reconstructions. Using these datasets, we explored the effect of different taxon sampling on tree topology by considering a series of systematic errors using ML and BI methods. Moreover, we also tested the effectiveness in topology robustness among the three ML-based models. The results showed that taxon sampling is an important determinant in tree robustness of accurate lepidopteran phylogenetic estimation. Long-branch attraction (LBA) caused by site-wise heterogeneity is a significant source of bias given rise to topologies divergence of ditrysia in phylogenomic reconstruction. Phylogenetic inference showed a most comprehensive framework by far to reveal the relationships among lepidopteran superfamilies, but limited by taxon sampling, it could only represent the current understanding of the lepidopteran tree of life. The relationships within the species-rich and relatively rapid radiation Ditrysia and especially Apoditrysia remain poorly unresolved, which need to increase taxon sampling and adopt lineage-specific genes for further phylogenomic reconstruction.
Conclusions
The present study further expands the taxon sampling of lepidopteran phylogeny and provides a potential phylogenomic foundation for further understanding its current higher-level relationships.
The woodlouse hunter Dysdera spiders have colonized all Macaronesian archipelagos. We report here for the first time an evolutionary connection between the Iberian Peninsula, Madeira, and the remote archipelago of Azores. Based on museum specimens from the 1950s, we describe the first endemic Dysdera species from the Azores. Additionally, we report the recent collection of immature individuals related yet probably not conspecific to the new species, rejecting previous suggestions that the endemic lineage had gone extinct. A multi-locus target phylogeny revealed that an undescribed species from Madeira was the closest relative to the Azores lineage, and that both island taxa were in turn sister to an Iberian endemic species, within a mostly Iberian clade. Interestingly, the Madeiran relative was not closely related to the remaining endemic species reported in the archipelago, suggesting an independent colonization. A divergence time estimation analysis unravelled that Dysdera colonized both archipelagos early after their emergence. The colonization pathway remains ambiguous, but the Iberian Peninsula acted as the ultimate source of the ancestral colonizers. Finally, we describe the new species Dysdera cetophonorum Crespo & Arnedo sp. nov. from Pico and Dysdera citauca Crespo & Arnedo, sp. nov. from Ilhéu de Cima (Porto Santo) and redescribe and illustrate the female genitalia for the first time of their poorly known closest relative, Dysdera flavitarsis Simon, 1882 from the north-western Iberian Peninsula.
http://zoobank.org/urn:lsid:zoobank.org:pub:1E75CCEC-1632-4581-93A5-E61721970022
Spider webs in general and orb webs in particular are delicate, ephemeral structures that are frequently damaged in nature. Some orb weavers respond to damage by quickly shoring up their webs with non-sticky dragline silk. This study of how Micrathena duodecimspinosa (O. Pickard-Cambridge, 1890) shores up damaged frame lines shows that repairs were largely based on a single, repeated pattern of attachments. These movements are shared with the distantly related family Pholcidae, suggesting a possibly ancient origin. Spiders tended to initiate repairs at the lower edge of a damaged sector, probably to reduce the damage produced when the spider's own weight caused sticky lines in slack portions of the web to sag into and adhere to each other. Repairs of lateral frames recuperated capture area more successfully than did those of upper frames, probably because damage caused by the spider's own weight during repair was reduced.
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.
Spiders are among the most varied terrestrial predators, with highly diverse morphology, ecology, and behavior. Morphological and molecular data have greatly contributed to advances in the phylogeny and evolutionary dynamics of spiders. Here, we performed comprehensive mitochondrial phylogenomics analysis on 78 mitochondrial genomes (mitogenomes) representing 29 families; of these, 23 species from eight families were newly generated. Mesothelae retained the same gene arrangement as the arthropod ancestor ( Limulus polyphemus), while Opisthothelae showed extensive rearrangement, with 12 rearrangement types in transfer RNAs (tRNAs) and control region. Most spider tRNAs were extremely truncated and lacked typical dihydrouridine or TΨC arms, showing high tRNA structural diversity; in particular, trnS1 exhibited anticodon diversity across the phylogeny. The evolutionary rates of mitochondrial genes were potentially associated with gene rearrangement or truncated tRNAs. Both mitogenomic sequences and rearrangements possessed phylogenetic characteristics, providing a robust backbone for spider phylogeny, as previously reported. The monophyly of suborder, infraorder, retrolateral tibial apophysis clade, and families (except for Pisauridae) was separately supported, and high-level relationships were resolved as (Mesothelae, (Mygalomorphae, (Entelegynae, (Synspermiata, Hypochilidae)))). The phylogenetic positions of several families were also resolved (e.g., Eresidae, Oecobiidae and Titanoecidae). Two reconstructions of ancestral web type obtained almost identical results, indicating that the common ancestor of spiders likely foraged using a silk-lined burrow. This study, the largest mitochondrial phylogenomics analysis of spiders to date, highlights the usefulness of mitogenomic data not only for providing efficient phylogenetic signals for spider phylogeny, but also for characterizing trait diversification in spider evolution.
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.
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.
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.
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.
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).
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.
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.
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
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.
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.
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.
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.
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.
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.
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.
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.
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 .
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.
The standard bootstrap (SBS), despite being computationally intensive, is widely used in maximum likelihood phylogenetic analyses. We recently proposed the ultrafast bootstrap approximation (UFBoot) to reduce computing time while achieving more unbiased branch supports than SBS under mild model violations. UFBoot has been steadily adopted as an efficient alternative to SBS and other bootstrap approaches.
Here, we present UFBoot2, which substantially accelerates UFBoot and reduces the risk of overestimating branch supports due to polytomies or severe model violations. Additionally, UFBoot2 provides suitable bootstrap resampling strategies for phylogenomic data. UFBoot2 is 778 times (median) faster than SBS and 8.4 times (median) faster than RAxML rapid bootstrap on tested datasets. UFBoot2 is implemented in the IQ-TREE software package version 1.6 and freely available at http://www.iqtree.org.
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.
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
