Chelicerata constitutes an ancient, biodiverse, and ecologically significant group of Arthropoda. The study of chelicerate evolution has undergone a renaissance in the past decade, resulting in major changes to our understanding of the higher-level phylogeny and internal relationships of living orders. Included among these conceptual advances are the discoveries of multiple whole-genome duplication events in a subset of chelicerate orders, such as horseshoe crabs, spiders, and scorpions. As a result, longstanding hypotheses and textbook scenarios of chelicerate evolution, such as the monophyly of Arachnida and a single colonization of land by the common ancestor of arachnids, have come into contention. The retention of ancient, duplicated genes across this lineage also offers fertile ground for investigating the role of gene duplication in chelicerate macroevolution. This new frontier of investigation is paralleled by the timely establishment of the first gene editing protocols for arachnid models, facilitating a new generation of experimental approaches.
Comprehensive Species Sampling and Sophisticated Algorithmic Approaches Refute the Monophyly of Arachnida
Deciphering the evolutionary relationships of Chelicerata (arachnids, horseshoe crabs, and allied taxa) has proven notoriously difficult, due to their ancient rapid radiation and the incidence of elevated evolutionary rates in several lineages. Although conflicting hypotheses prevail in morphological and molecular data sets alike, the monophyly of Arachnida is nearly universally accepted, despite historical lack of support in molecular data sets. Some phylotranscriptomic analyses have recovered arachnid monophyly, but these did not sample all living orders, whereas analyses including all orders have failed to recover Arachnida. To understand this conflict, we assembled a data set of 506 high-quality genomes and transcriptomes, sampling all living orders of Chelicerata with high occupancy and rigorous approaches to orthology inference. Our analyses consistently recovered the nested placement of horseshoe crabs within a paraphyletic Arachnida. This result was insensitive to variation in evolutionary rates of genes, complexity of the substitution models, and alternative algorithmic approaches to species tree inference. Investigation of sources of systematic bias showed that genes and sites that recover arachnid monophyly are enriched in noise and exhibit low information content. To test the impact of morphological data, we generated a 514-taxon morphological data matrix of extant and fossil Chelicerata, analyzed in tandem with the molecular matrix. Combined analyses recovered the clade Merostomata (the marine orders Xiphosura, Eurypterida, and Chasmataspidida), but merostomates appeared nested within Arachnida. Our results suggest that morphological convergence resulting from adaptations to life in terrestrial habitats has driven the historical perception of arachnid monophyly, paralleling the history of numerous other invertebrate terrestrial groups.
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- PAR ID:
- 10421144
- Editor(s):
- Teeling, Emma
- Publisher / Repository:
- Molecular Biology and Evolution
- Date Published:
- Journal Name:
- Molecular Biology and Evolution
- Volume:
- 39
- Issue:
- 2
- ISSN:
- 0737-4038
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Horseshoe crabs (Chelicerata: Xiphosura) are generally considered to exhibit a highly conserved morphology throughout their evolutionary history and are one of the archetypal ‘living fossil’ groups. This narrative has been challenged in recent years, with numerous lines of evidence indicate that horseshoe crabs have been an evolutionarily dynamic lineage, exhibiting several shifts into non-marine environments and associated peaks in rates of evolutionary change. Nevertheless, marine forms are still characterized by a relatively limited morphological variability for most of their evolutionary history, as evidenced by a consistent developmental trajectory shared between species over 250million years. Attempts to ascertain when horseshoe crabs adopted this ontogenetic trajectory are hindered by the sparse early Paleozoic record of the group; only two species, both assigned to the genus Lunataspis, have been described from the Ordovician, and no Silurian species are known. A new, highly aberrant horseshoe crab from the Late Ordovician Big Hill Lagerstätte, Michigan, provides evidence of early morphological experimentation within the group, indicating that even marine lineages were variable early on in their evolutionary history. The new species represents a distinct genus characterized by a greatly elongated prosomal carapace and is represented by two available specimens (with a third held in a private collection), all of which preserve the same highly unusual carapace shape, indicating the unusual morphology to be a genuine characteristic of the species. Geometric morphometric analysis places the new species in an unoccupied region of morphospace distinct to that of other horseshoe crabs, confirming early morphological experimentation within the clade. Interestingly, while the prosoma is markedly different to any other horseshoe crab species known, the thoracetron is similar to that of Lunataspis. Taken in combination with the known ontogeny of Lunataspis borealis, which exhibits the characteristic xiphosurid development of the thoracetron but a more eurypterid-like ontogenetic trajectory of the prosoma, the new species indicates that developmental canalization occurred within the horseshoe crab lineage, with the thoracetron canalizing prior to the prosoma.more » « less
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Abstract Horseshoe crabs as a group are renowned for their morphological conservatism punctuated by marked shifts in morphology associated with the occupation of non-marine environments and have been suggested to exhibit a consistent developmental trajectory throughout their evolutionary history. Here, we report a new species of horseshoe crab from the Ordovician (Late Sandbian) of Kingston, Ontario, Canada, from juvenile and adult material. This new species provides critical insight into the ontogeny and morphology of the earliest horseshoe crabs, indicating that at least some Palaeozoic forms had freely articulating tergites anterior to the fused thoracetron and an opisthosoma comprising 13 segments.more » « less
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A key aspect of geoscience education initiatives is creating engaging programs that inspire future generations to care about the past, present, and future of our planet. Here, we present a lesson plan designed for 6-12 grade students that uses horseshoe crab (Xiphosura) paleobiology as a tool to teach students about paleoecology, phylogenetics and the scientific process. Framed as a criminal investigation, students are placed in groups and briefed as “fossil detectives”, who are tasked with identifying horseshoe crabs and determining their evolutionary and ecological affinities. Students are provided with a guidebook, evidence bags, and a phylogenetic poster with missing blanks for five horseshoe crabs, ranging in age from Ordovician to modern. Students use the fossil evidence bags of associated biota and guidebooks to determine the locality, age, identity, and paleoenvironmental affinity of each xiphosuran suspect. With this newfound data, paired with morphological observations, students then place each of the five horseshoe crab suspects within a time-scaled phylogeny poster. Afterwards, students are prompted to use logical reasoning skills to determine the minimum number of times horseshoe crabs have explored non-marine environments and which common ancestors likely made this transition on the phylogenetic tree. A pre- and post-test are also being developed to measure the outcomes of this lesson plan.more » « less
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True, John (Ed.)Neofunctionalization of duplicated gene copies is thought to be an important process underlying the origin of evolutionary novelty and provides an elegant mechanism for the origin of new phenotypic traits. One putative case where a new gene copy has been linked to a novel morphological trait is the origin of the arachnid patella, a taxonomically restricted leg segment. In spiders, the origin of this segment has been linked to the origin of the paralog dachshund-2, suggesting that a new gene facilitated the expression of a new trait. However, various arachnid groups that possess patellae do not have a copy of dachshund-2, disfavoring the direct link between gene origin and trait origin. We investigated the developmental genetic basis for patellar patterning in the harvestman Phalangium opilio, which lacks dachshund-2. Here, we show that the harvestman patella is established by a novel expression domain of the transcription factor extradenticle. Leveraging this definition of patellar identity, we surveyed targeted groups across chelicerate phylogeny to assess when this trait evolved. We show that a patellar homolog is present in Pycnogonida (sea spiders) and various arachnid orders, suggesting a single origin of the patella in the ancestor of Chelicerata. A potential loss of the patella is observed in Ixodida. Our results suggest that the modification of an ancient gene, rather than the neofunctionalization of a new gene copy, underlies the origin of the patella. Broadly, this work underscores the value of comparative data and broad taxonomic sampling when testing hypotheses in evolutionary developmental biology.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/molbev/msac021
