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.
The proliferation of genomic resources for Chelicerata in the past 10 years has revealed that the evolution of chelicerate genomes is more dynamic than previously thought, with multiple waves of ancient whole genome duplications affecting separate lineages. Such duplication events are fascinating from the perspective of evolutionary history because the burst of new gene copies associated with genome duplications facilitates the acquisition of new gene functions (neofunctionalization), which may in turn lead to morphological novelties and spur net diversification. While neofunctionalization has been invoked in several contexts with respect to the success and diversity of spiders, the overall impact of whole genome duplications on chelicerate evolution and development remains imperfectly understood. The purpose of this review is to examine critically the role of whole genome duplication on the diversification of the extant arachnid orders, as well as assess functional datasets for evidence of subfunctionalization or neofunctionalization in chelicerates. This examination focuses on functional data from two focal model taxa: the spider Parasteatoda tepidariorum, which exhibits evidence for an ancient duplication, and the harvestman Phalangium opilio, which exhibits an unduplicated genome. I show that there is no evidence that taxa with genome duplications are more successful than taxa with unduplicated genomes. I contend that evidence for sub- or neofunctionalization of duplicated developmental patterning genes in spiders is indirect or fragmentary at present, despite the appeal of this postulate for explaining the success of groups like spiders. Available expression data suggest that the condition of duplicated Hox modules may have played a role in promoting body plan disparity in the posterior tagma of some orders, such as spiders and scorpions, but functional data substantiating this postulate are critically missing. Spatiotemporal dynamics of duplicated transcription factors in spiders may represent cases of developmental system drift, rather than neofunctionalization. Developmental system drift may represent an important, but overlooked, null hypothesis for studies of paralogs in chelicerate developmental biology. To distinguish between subfunctionalization, neofunctionalization, and developmental system drift, concomitant establishment of comparative functional datasets from taxa exhibiting the genome duplication, as well as those that lack the paralogy, is sorely needed.
more » « less- Award ID(s):
- 2016141
- PAR ID:
- 10463141
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative And Comparative Biology
- Volume:
- 63
- Issue:
- 3
- ISSN:
- 1540-7063
- Format(s):
- Medium: X Size: p. 825-842
- Size(s):
- p. 825-842
- Sponsoring Org:
- National Science Foundation
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Abstract Gene duplications have long been recognized as a contributor to the evolution of genes with new functions. Multiple copies of genes can result from tandem duplication, from transposition to new chromosomes, or from whole-genome duplication (polyploidy). The most common fate is that one member of the pair is deleted to return the gene to the singleton state. Other paths involve the reduced expression of both copies (hypofunctionalization) that are held in duplicate to maintain sufficient quantity of function. The two copies can split functions (subfunctionalization) or can diverge to generate a new function (neofunctionalization). Retention of duplicates resulting from doubling of the whole genome occurs for genes involved with multicomponent interactions such as transcription factors and signal transduction components. In contrast, these classes of genes are underrepresented in small segmental duplications. This complementary pattern suggests that the balance of interactors affects the fate of the duplicate pair. We discuss the different mechanisms that maintain duplicated genes, which may change over time and intersect.
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null (Ed.)Chelicerate arthropods exhibit dynamic genome evolution, with ancient whole-genome duplication (WGD) events affecting several orders. Yet, genomes remain unavailable for a number of poorly studied orders, such as Opiliones (daddy-long-legs), which has hindered comparative study. We assembled the first harvestman draft genome for the species Phalangium opilio , which bears elongate, prehensile appendages, made possible by numerous distal articles called tarsomeres. Here, we show that the genome of P. opilio exhibits a single Hox cluster and no evidence of WGD. To investigate the developmental genetic basis for the quintessential trait of this group—the elongate legs—we interrogated the function of the Hox genes Deformed ( Dfd ) and Sex combs reduced ( Scr ), and a homologue of Epidermal growth factor receptor ( Egfr ). Knockdown of Dfd incurred homeotic transformation of two pairs of legs into pedipalps, with dramatic shortening of leg segments in the longest leg pair, whereas homeosis in L3 is only achieved upon double Dfd + Scr knockdown. Knockdown of Egfr incurred shortened appendages and the loss of tarsomeres. The similarity of Egfr loss-of-function phenotypic spectra in insects and this arachnid suggest that repeated cooption of EGFR signalling underlies the independent gains of supernumerary tarsomeres across the arthropod tree of life.more » « less
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Within the arachnids, chromosome-level genome assemblies have greatly accelerated the understanding of gene family evolution and developmental genomics in key groups, such as spiders (Araneae), mites and ticks (Acariformes and Parasitiformes). Among other poorly studied arachnid orders that lack genome assemblies altogether are the clade Pedipalpi, which is comprised of three orders that form the sister group of spiders, which diverged over 400 Mya. We close this gap by generating the first chromosome-level assembly from a single specimen of the vinegaroon Mastigoproctus giganteus (Uropygi). We show that this highly complete genome retains plesiomorphic conditions for many gene families that have undergone lineage-specific derivations within the more diverse spiders. Consistent with the phylogenetic position of Uropygi, macrosynteny in the M. giganteus genome substantiates the signature of an ancient whole genome duplication.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
