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(Amblypygi) Provide Insights Into Arachnid Genome Evolution and Antenniform Leg Patterning Guilherme Gainett* and Prashant P

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(Amblypygi) Provide Insights Into Arachnid Genome Evolution and Antenniform Leg Patterning Guilherme Gainett* and Prashant P Gainett and Sharma EvoDevo (2020) 11:18 https://doi.org/10.1186/s13227-020-00163-w EvoDevo RESEARCH Open Access Genomic resources and toolkits for developmental study of whip spiders (Amblypygi) provide insights into arachnid genome evolution and antenniform leg patterning Guilherme Gainett* and Prashant P. Sharma Abstract Background: The resurgence of interest in the comparative developmental study of chelicerates has led to important insights, such as the discovery of a genome duplication shared by spiders and scorpions, inferred to have occurred in the most recent common ancestor of Arachnopulmonata (a clade comprising the fve arachnid orders that bear book lungs). Nonetheless, several arachnid groups remain understudied in the context of develop- ment and genomics, such as the order Amblypygi (whip spiders). The phylogenetic position of Amblypygi in Arach- nopulmonata posits them as an interesting group to test the incidence of the proposed genome duplication in the common ancestor of Arachnopulmonata, as well as the degree of retention of duplicates over 450 Myr. Moreover, whip spiders have their frst pair of walking legs elongated and modifed into sensory appendages (a conver- gence with the antennae of mandibulates), but the genetic patterning of these antenniform legs has never been investigated. Results: We established genomic resources and protocols for cultivation of embryos and gene expression assays by in situ hybridization to study the development of the whip spider Phrynus marginemaculatus. Using embryonic tran- scriptomes from three species of Amblypygi, we show that the ancestral whip spider exhibited duplications of all ten Hox genes. We deploy these resources to show that paralogs of the leg gap genes dachshund and homothorax retain arachnopulmonate-specifc expression patterns in P. marginemaculatus. We characterize the expression of leg gap genes Distal-less, dachshund-1/2 and homothorax-1/2 in the embryonic antenniform leg and other appendages, and provide evidence that allometry, and by extension the antenniform leg fate, is specifed early in embryogenesis. Conclusion: This study is the frst step in establishing P. marginemaculatus as a chelicerate model for modern evolu- tionary developmental study, and provides the frst resources sampling whip spiders for comparative genomics. Our results suggest that Amblypygi share a genome duplication with spiders and scorpions, and set up a framework to study the genetic specifcation of antenniform legs. Future eforts to study whip spider development must emphasize the development of tools for functional experiments in P. marginemaculatus. Keywords: Arachnida, Arachnopulmonata, Gene duplication, Paralogs, Leg gap genes, Sensory biology Background *Correspondence: [email protected] Department of Integrative Biology, University of Wisconsin-Madison, In the past 25 years, comparative developmental study Madison, WI 53706, USA of chelicerates has resurged with the integration of © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Gainett and Sharma EvoDevo (2020) 11:18 Page 2 of 18 molecular biology and genomics, spearheaded by devel- position of Amblypygi within Arachnopulmonata, a bet- opmental genetic investigations of the spiders Cupien- ter understanding of Amblypygi genomics is anticipated nius salei and Parasteatoda tepidariorum [1–6]. Such to facilitate exploration of the evolutionary outcomes works have investigated several important aspects of of the genome duplication in Arachnopulmonata, and chelicerate development, such as the molecular mecha- better characterizing the extent to which arachnopul- nism of dorso-ventral axis patterning [3, 7–9], segmen- monate orders retained and specialized the ensuing tation of the prosoma [1, 10–13] and opisthosoma [2, paralogous genes. Unfortunately, the embryology of 13], and specifcation of prosomal versus opisthosomal the order Amblypygi is known only from the works of fate [14, 15]. A few non-spider chelicerate models have Pereyaslawzewa [46], a brief mention in Strubell [47] also emerged in recent years and provided new perspec- (“Phrynidae”), Gough [48], and the comprehensive study tives on chelicerate development, such as the horseshoe of Weygoldt [49] in Phrynus marginemaculatus (formerly crab Limulus polyphemus (Xiphosura) [16, 17], the mites Tarantula marginemaculata). Archegozetes longisetosus [18–21] and Tetranychus urti- Beyond the interest in their genomic architecture, whip cae (Acariformes) [22–24], the tick Rhipicephalus micro- spiders possess a fascinating biology and natural history. plus (Parasitiformes) [25], the Arizona bark scorpion Whip spiders are emerging as model systems in behav- Centruroides sculpturatus (Scorpiones) [26] and the har- ioral ecology, learning, and neurophysiology in arachnids vestmen Phalangium opilio (Opiliones) [27–30]. Studies [50, 51]. Teir pedipalps, the second pair of append- in A. longisetosus and C. sculpturatus have suggested that ages, are robust raptorial devices used for striking prey, changes in Hox gene number and spatial expression are including mostly arthropods, and even small vertebrates responsible for such phenomena as the reduced segmen- [41, 50, 52]. However, their most conspicuous charac- tation of mites and the supernumerary posterior append- teristic and namesake is their “whip”, a modifed anten- age identities of scorpions [18, 26]. niform frst walking leg that is not used for locomotion, In addition to the insights into chelicerate develop- but instead as a sensory appendage. Te antenniform legs ment, one of the major recent outcomes of increasing are extremely elongated relative to the other leg pairs, availability of genomic resources in the group was the and the tibia and tarsus are pseudo-segmented into hun- discovery of a shared whole (or partial) genome duplica- dreds of articles that harbor an array of chemo-, thermo-, tion in spiders and scorpions. Tis genome duplication is hygro- and mechanoreceptive sensilla [53–55]. Te inferred to trace back to the most recent common ances- peripheral circuitry of the antenniform legs is complex, tor of the recently proposed clade Arachnopulmonata, exhibiting peripheral synapses and giant neurons which which includes spiders, scorpions, and three other arach- are possibly involved in fast sensory responses [55–57]. nid orders with book lungs [6, 26, 31–33]. Tis duplica- Te antenniform legs also have been shown to be impor- tion event is also inferred to be independent from the tant for foraging, mating, and intrasexual contests [58, multiple rounds of whole genome duplication undergone 59]. Notably, concentration of sensory structures, elonga- by horseshoe crabs (Xiphosura) [34, 35]. Te duplication tion and pseudo-segmentation of these legs constitute a in spiders and scorpions encompasses several important striking convergence with the antennae of mandibulate developmental genes, such as those in the homeobox arthropods (Pancrustacea and Myriapoda). Evidence family [6, 32]. Excitingly, there is increasing evidence of from Hox gene expression and functional experiments divergent expression and function of paralogs, such as in support the view that the antenna of mandibulates is the case of Hox genes, leg gap genes and retinal determi- positionally homologous to the chelicera of chelicerates nation gene network (RDGN) homologs [6, 26, 36–40]. (deutocerebral appendage) [21, 30]. Despite their difer- Nevertheless, knowledge on the development of sev- ent positions along the antero-posterior axis of the body, eral arachnid orders still remains scarce or entirely the serial homology of both antennae (mandibulates) and unexplored in the contexts of embryological study and antenniform legs (whip spiders) to walking legs consti- genomic architecture. One particularly interesting arach- tutes a potentially useful comparison to address whether nid order whose genomic evolution and developmental a striking morphological convergence is associated with biology remains largely unexplored is Amblypygi. Com- convergence in mechanisms of genetic patterning. monly known as whip spiders, Amblypygi comprise Much of our knowledge about the genetic basis for approximately 220 described species of nocturnal pred- appendage fate specifcation in arthropods was dis- ators that are distributed primarily in the tropics and covered in the fruit fy Drosophila melanogaster and subtropics worldwide [41, 42]. Amblypygi is part of the involves regulation by leg gap genes and Hox genes. clade Pedipalpi (together with
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