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Characterizing And Mitigating Coherent Errors In A Trapped Ion Quantum Processor Using Hidden Inverses
Center for Evolutionary and Theoretical Immunology, Department of Biology, Division of Parasites, Southwestern Biological Museum, University of New Mexico, Albuquerque, NM 87131, USA
Received: 20 April 2022 / Revised: 20 June 2022 / Accepted: 27 June 2022 / Published: 5 July 2022
Schistosomatidae Stiles and Hassall 1898 is a medically important family of digenetic flukes (Trematoda: Digenea) whose members infect mammals or birds as definitive hosts and aquatic or amphibians as intermediate hosts. There are currently 17 named genera, for many of which the evolutionary relationships remain unresolved. The lack of a resolved phylogeny hinders our understanding of schistosomatid evolution, particularly patterns of host use and the role of host switching in diversification. Here, we used targeted sequence capture of ultraconserved elements (UCEs) from members of 13 of 17 named genera and 11 undescribed lineages believed to represent either new genera or species to construct a phylogenetic dataset to assess schistosomatid relationships. This study represents the largest phylogenetic work in Schistosomatidae both in terms of number of loci and breadth of taxon sampling. We present a near-exhaustive family-level phylogeny that provides resolution of several clades of long-standing uncertainty within Schistosomatidae, including resolution of the placement of North American mammalian schistosomes, suggesting a second separate takeover of mammalian hosts. In addition, we present evidence for placing Macrobilharzia at the base of the Schistosoma + Bivitellobilharzia radiation. Definitive and transitional host patterns and the strong role of interhost switching are discussed in relation to schistosomatid diversification.
A good understanding of diversification is lacking in most multi-host helminth groups [ 1 , 2 ]. In fact, several such groups have been sampled in sufficient numbers to reconstruct the reliable, clear phylogeny necessary to understand parasite evolution. Elucidation of helminth diversification has practical implications for knowledge and management of human and wildlife helminths, issues related to host competence , potential for host switching [4, 5, 6, 7], host associations [8, 9, 10]. ], character development  and cladogenesis [12, 13]. Among digenetic trematodes, the Schistosomatidae Stiles and Hassall 1898 are a diverse family whose members infect birds or mammals (definitive hosts) and aquatic or amphibious gastropods (intermediate hosts). Schistosomatidae have attracted considerable interest among parasitologists because of the medical and veterinary importance of their representatives. Three species within the genus Schistosoma Weinland, 1858 are the main etiological agents of human schistosomiasis, one of the world’s most persistent neglected tropical diseases, which still infects more than 250 million people worldwide [ 14 , 15 ]. In addition, non-human schistosomiasis has been implicated in human cercarial dermatitis (swimming itch), a re-emerging zoonotic disease [ 16 , 17 ].
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Among digenes, schistosomatids have unusual characteristics, the most notable of which is that they are exclusively dioecious (usually with marked sexual dimorphism) parasites of endotherms (birds and mammals), common attributes shared by no other family of digenes [18, 19]. Schistosomatids have evolved heterogametic (ZW) sex chromosomes  that function in sex determination. Schistosomatids have other interesting reproductive strategies [20, 21] and are among the few digenic lineages in which adults live outside the alimentary canal of their definitive vertebrate hosts. They also lack a second intermediate host in their life cycle. Decades of DNA sequencing of schistosomatids from their definitive and intermediate hosts (e.g. see other articles in this volume) combined with the use of museum-quality specimens have shed light on the previously under-recognized diversity of schistosomatids, particularly in birds. – infectious species, including those responsible for human cercarial dermatitis. These efforts provided the basis for developing a robust evolutionary framework to address the diversity and diversification of schistosomatids worldwide.
Despite progress, our understanding of schistosomatid relationships, patterns of host use, and character evolution remains incomplete [ 20 , 22 , 23 , 24 ]. Progress has been limited by the lack of informative morphological characteristics and adequate material of adult parasites for description. The inclusion of molecular analysis [ 25 , 26 , 27 ] has greatly expanded efforts to explain schistosomatid diversity, particularly in bird-infecting genera that have been shown to harbor cryptic diversity [ 10 , 28 ]. Although these and other studies have made significant progress, deeper knots regarding the relationships between genera remain unresolved and often provide conflicting phylogenetic signals. This is probably because the molecular phylogeny is based on several loci, mainly markers in the ribosomal RNA operon (28S, 18S, ITS1 and 2) and one mitochondrial gene (cox1).
There are currently 17 named genera and over 130 named species in the Schistosomatidae . Based on the sampling of larval schistosomatids, this is probably an underestimation [8, 29, 30, 31, 32, 33, 34, 35] of both genera and species. Historically, Schistosomatidae have been divided into three subfamilies [24, 36], primarily based on the morphology of adult worms. Schistosomatinae Stiles and Hassall 1898 includes Austrobilharzia, Bivitellobilharzia, Heterobilharzia, Macrobilharzia Ornithobilharzia, Schistosomatium and Schistosoma. Gigantobilharziinae Mehra 1940 includes Gigantobilharzia and Dendritobilharzia. Bilharziellinae Cena 1929 includes Bilharziella, Trichobilharzia, Jilinobilharzia, Allobilharzia and Anserobilharzia. A fourth subfamily Griphobilharziinae Platt, Blair, Purdie & Melville, 1991 was recognized, containing a single species, Griphobilharzia amoena, but sequence data place this species in the Spirorchiidae . Molecular phylogeny does not support these subfamily designations [21, 25, 26, 27, 31, 34, 37, 38, 39], and the most appropriate subfamily classification remains unclear.
As indicated by the conflicting results of previous studies (Table 1), sequencing of 500–1500 bp markers has continued. it is unlikely to resolve the deeper schistosomatid connection. New methodologies are needed to identify the following key nodes and groups, and thus to better characterize diversification, host use evolution, host switching and divergence times in Schistosomatidae:
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The conflict between these key nodes (Table 1) can be explained by widespread incomplete lineage sorting (ILS) in Schistosomatidae, as suggested by previous authors [ 21 , 27 ]. Resolving relationships in this context requires an increase in the number of analyzed characters, ideally by increasing the number of independently evolving loci, as well as a more comprehensive selection of taxa [42, 43, 44]. Recent analyzes of whole mitogenomes for Schistosoma species  have provided increased resolution, but this approach is unlikely to yield similar results when applied to Schistosomatidae, as mitochondrial loci co-evolve. Moreover, among digeneans, whole mitochondrial genomes present evolutionary trajectories that are strikingly different from nuclear genomes at deeper levels [ 46 , 47 ], suggesting a need for caution. Recent developments in phylogenomic methods have proven effective in resolving clades where ILS is suspected [ 48 , 49 ]. One such method uses targeted sequence capture of ultraconserved elements (UCEs)  to obtain data from hundreds to thousands of independent nuclear loci for phylogenomic analysis. This method requires a panel of probes targeting UCE loci and less conserved flanking regions in the group of interest that are sequenced using next-generation methods, producing alignments of thousands to millions of bases that can resolve points of divergence on multiple time scales. 50]. ]. The use of UCEs as phylogenomic markers has been successful in resolving rapid radiations in vertebrates [51, 52, 53, 54] as well as relationships in a growing number of invertebrate groups [55, 56, 57, 58]. In Digenea, the only application of this approach was characterized by a relatively low number of loci (517