Phylogenetic Systematics and Evolution of the Spider Infraorder Mygalomorphae Using Genomic Scale Data

Abstract

The infraorder Mygalomorphae is one of the three main lineages of spiders comprising over 3000 nominal species. This ancient group has a worldwide distribution that includes among its ranks large and charismatic taxa such as tarantulas, trapdoor spiders, and highly venomous funnel-web spiders. Based on past molecular studies using Sanger-sequencing approaches, numerous mygalomorph families (e.g., Hexathelidae, Ctenizidae, Cyrtaucheniidae, Dipluridae, and Nemesiidae) have been identified as non-monophyletic. However, these data were unable to sufficiently resolve the higher-level (intra- and interfamilial) relationships such that the necessary changes in classification could be made with confidence. Here, we present a comprehensive phylogenomic treatment of the spider infraorder Mygalomorphae. We employ 472 loci obtained through anchored hybrid enrichment to reconstruct relationships among all the mygalomorph spider families and estimate the timeframe of their diversification. We sampled nearly all currently recognized families, which has allowed us to assess their status, and as a result, propose a new classification scheme. Our generic-level sampling has also provided an evolutionary framework for revisiting questions regarding silk use in mygalomorph spiders. The first such analysis for the group within a strict phylogenetic framework shows that a sheet web is likely the plesiomorphic condition for mygalomorphs, as well as providing insights to the ancestral foraging behavior for all spiders. Our divergence time estimates, concomitant with detailed biogeographic analysis, suggest that both ancient continental-level vicariance and more recent dispersal events have played an important role in shaping modern day distributional patterns. Based on our results, we relimit the generic composition of the Ctenizidae, Cyrtaucheniidae, Dipluridae, and Nemesiidae. We also elevate five subfamilies to family rank: Anamidae (NEW RANK), Euagridae (NEW RANK), Ischnothelidae (NEW RANK), Pycnothelidae (NEW RANK), and Bemmeridae (NEW RANK). Three families Entypesidae (NEW FAMILY), Microhexuridae (NEW FAMILY), and Stasimopidae (NEW FAMILY), and one subfamily Australothelinae (NEW SUBFAMILY) are newly proposed. Such a major rearrangement in classification, recognizing nine newly established family-level rank taxa, is the largest the group has seen in over three decades. [Biogeography; molecular clocks; phylogenomics; spider web foraging; taxonomy.]

Total‐evidence analysis of an undescribed fauna: resolving the evolution and classification of Australia’s golden trapdoor spiders (Idiopidae: Arbanitinae: Euoplini)

“…This study revealed a suite of morphological characters (Appendix ), from both male and female spiders, which will be valuable in future taxonomic revisions within the tribe, and which should be considered during taxonomic or phylogenetic studies on other mygalomorph groups too, especially idiopids and their closest relatives within the Domiothelina (i.e. Ctenizidae, Euctenizidae, Migidae and Halonoproctidae; Opatova et al, 2020). The challenging morphology of mygalomorph spiders has frequently been lamented by arachnologists; shared plesiomorphic characters and frequent homoplasy in derived characters obfuscate phylogenetic signal (Raven, 1985; Goloboff, 1993; Bond, 2012; Opatova et al, 2020), whereas at lower phylogenetic levels, discrete morphological differences may not be present between taxa that display interspecific levels of genetic divergence (see, e.g., Satler et al, 2013; Leavitt et al, 2015; Montes de Oca et al, 2016).…”

“…Ctenizidae, Euctenizidae, Migidae and Halonoproctidae; Opatova et al, 2020). The challenging morphology of mygalomorph spiders has frequently been lamented by arachnologists; shared plesiomorphic characters and frequent homoplasy in derived characters obfuscate phylogenetic signal (Raven, 1985; Goloboff, 1993; Bond, 2012; Opatova et al, 2020), whereas at lower phylogenetic levels, discrete morphological differences may not be present between taxa that display interspecific levels of genetic divergence (see, e.g., Satler et al, 2013; Leavitt et al, 2015; Montes de Oca et al, 2016). Selection has been suggested as the potential cause of these issues; adaptation to the sedentary, fossorial lifestyle shared by most mygalomorph taxa may select against significant departures from the morphological “norm” which clearly fits their ecological niche (Bond and Hedin, 2006; Ortiz et al, 2018).…”

“…Resolving the higher-level systematics of the Australasian spiny trapdoor spiders (family Idiopidae, subfamily Arbanitinae) has been a gradual process over more than three decades, involving several large-scale "reshuffles" in which genera have been redefined and relimited (Main, 1985;Raven and Wishart, 2005;Rix et al, 2017d). Following the trend seen in mygalomorph systematics at all phylogenetic levels (see, e.g., Hedin and Bond, 2006;Bond et al, 2012;Godwin et al, 2018;Hedin et al, 2018Hedin et al, , 2019Opatova et al, 2020), classifications within the Arbanitinae based on morphological data (Main, 1985;Raven, 1985;Raven and Wishart, 2005) recently have been refined and extended using molecular phylogenetic approaches (Rix et al, 2017b, d). In 2017, a molecular phylogeny of the subfamily that included the type species of all genera recognized at the time, as well as a wide selection of described and undescribed species in each genus, facilitated a comprehensive generic relimitation (Rix et al, 2017b, d).…”

“…Combining multiple data types into a single total‐evidence analysis can allow a researcher to overcome issues associated with each individual datatype. In the case of the Euoplini, analyzing molecular data alone would mean leaving out taxa for which a molecular exemplar is not available, but using morphological data alone also would be challenging, as mygalomorph spiders are notorious for their relatively conservative body plans (see Raven, 1985; Hedin and Bond, 2006; Bond et al, 2012; Leavitt et al, 2015; Godwin et al, 2018; Opatova et al, 2020). By combining these data types in a total‐evidence framework, available characters from all taxa can be included, and the topology of the resulting phylogeny can be driven by both molecular and morphological phylogenetic signal—thereby mitigating the shortcomings of each individual datatype.…”

Shifting evolutionary sands: transcriptome characterization of the Aptostichus atomarius species complex

“…Trapdoor spiders belong to an ancient lineage of chelicerate arthropods, the spider infraorder Mygalomorphae, which includes charismatic fauna such as tarantulas and Australian funnel web spiders [1]. These spiders are sedentary, fossorial predators that build silk-lined burrows; females are non-vagile and mature males emerge seasonally to search for females.…”