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Brenneis, G.

Publications and source records attributed to Brenneis, G..

5 recordsLinked to original sources

Homoplastic evolution of proximal podomere patterning across Arthropoda

The jointed arthropod leg is often credited as a key innovation spurring the evolutionary success of the phylum. Across lineages, each territory of the appendage has served as the substrate for myriad adaptations and structural innovations. While much of the available data has supported a conserved suite of transcription factors responsible for the initiation and patterning of the arthropod appendage, recent works have begun to highlight instances of lineage-specific shifts in expression dynamics, particularly amongst the chelicerates, correlated both with the emergence of novel structures and developmental system drift in the specification of plesiomorphic structures. These works confound efforts to align or homologize the leg segments across arthropod lineages, an effort already challenged by ground plan differences in segment number between the subphyla. An even more unusual architecture of leg segments occurs in sea spiders (Pycnogonida), which alone among Arthropoda are considered by systematists to bear three coxae (proximal segments), in contrast to the single coxa of the remaining arthropods. Here, we examined proximal podomere patterning in the developing appendages of a sea spider and an arachnid. We find that a particular spatial arrangement of Lim1 and SoxNeuro characterizes the developing coxa and trochanter of the harvestman Phalangium opilio (Opiliones) throughout appendage formation, with RNAi depletions of Lim1 yielding deletions of coxa and trochanter. Comparison of expression patterns across taxa shows that Lim1 and SoxNeuro have a similar spatial arrangement in the harvestman and sea spider, but these suggest conflicting interpretations of leg segment homology. We show that this is attributable to homoplastic patterns of evolution in SoxNeuro across Arthropoda. Expanding our surveys of prominent PD axis-patterning transcription factors supports additional instances of homoplasy in the domains of Sp6-9 and Irx2. The pervasiveness of homoplasy in gene expression patterns demands measured skepticism of homology statements and careful comparisons of multiple patterning genes, toward achieving falsifiability in the homology of structures.

developmental biology↗

Developmental system drift in the patterning of the arthropod tarsus

The current understanding of proximodistal axis patterning in arthropod legs is grounded in insect models. The paradigm for appendage evolution in this phylum is that the gene regulatory network responsible for leg subdivision and patterning is broadly conserved. Recent surveys of these genes have suggested that chelicerate exemplars exhibit divergent appendage patterning dynamics, though functional data remain limited. One salient mismatch in expression occurs in homologs of the homeobox gene clawless. In insects, clawless is expressed in the distalmost leg territory, specifying the claw-bearing pretarsus. In the harvestman, Phalangium opilio, clawless occupies a broad tarsal domain early in development, localizing later to the metatarsus-tarsus boundary, suggestive of a tarsal patterning function. Here, we tested the function of harvestman clawless using RNAi. Unlike insects, we show that clawless knockdown results in disrupted tarsal growth and patterning of its proximal segmental boundary, with no effect on the claw. Truncation of the tarsus is associated with defective tarsomere formation. We additionally surveyed clawless homologs in exemplars of chelicerate diversity, which suggests that the tarsal-patterning function for clawless was likely present in the chelicerate common ancestor. These results, alongside available expression data, suggest panarthropod appendage patterning exhibits numerous cases of developmental system drift.

evolutionary biology↗

The genome of a sea spider corroborates a shared Hox cluster motif in arthropods with reduced posterior tagma

BackgroundChelicerate evolution is contentiously debated, with recent studies challenging traditional phylogenetic hypotheses and scenarios of major evolutionary events, like terrestrialization. Sea spiders (Pycnogonida) represent the uncontested marine sister group of all other chelicerates, featuring a - likely plesiomorphic - indirect development mode. Accordingly, pycnogonids hold the potential to provide crucial insight into early chelicerate genome evolution and ancestral principles of chelicerate body patterning. Leveraging this potential, however, has hitherto been hampered by the lack of high-quality genomic resources for pycnogonids. ResultsWe employed long-read sequencing and proximity ligation data to assemble the first near chromosome-level sea spider genome for Pycnogonum litorale, complemented by developmental transcriptomes and a high-fidelity Iso-Seq dataset. The assembly has a size of 471Mb in 57 pseudochromosomes, a repeat content of 61.05%, 15,497 predicted protein-coding genes, and is highly complete (95.8% BUSCO Arthropoda score, 95.7% of conserved microRNA families present). We identified a single, intact Hox gene cluster that lacks abdominal-A/Hox9, suggesting the loss of this Hox gene. ConclusionsOur high-quality genomic and transcriptomic resources establish P. litorale as a key research organism for modern studies on chelicerate genome evolution, development, and phylogeny. The presence of a single Hox cluster in the P. litorale genome further strengthens the inference that no whole-genome duplication occurred at the base of the chelicerate tree. The lack of abdA suggests that the combination of abdA loss and posterior tagmata reduction is a common theme in arthropod evolution, as it is shared with other, distantly related arthropod taxa with a vestigial opisthosoma/abdomen.

evolutionary biology↗

A novel expression domain of extradenticle underlies the evolutionary developmental origin of the chelicerate patella

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.

evolutionary biology↗

Phylogenomic resolution of sea spider diversification through integration of multiple data classes

Despite significant advances in invertebrate phylogenomics over the past decade, the higher-level phylogeny of Pycnogonida (sea spiders) remains elusive. Due to the inaccessibility of some small-bodied lineages, few phylogenetic studies have sampled all sea spider families. Previous efforts based on a handful of genes have yielded unstable tree topologies. Here, we inferred the relationships of 89 sea spider species using targeted capture of the mitochondrial genome, 56 conserved exons, 101 ultraconserved elements, and three nuclear ribosomal genes. We inferred molecular divergence times by integrating morphological data for fossil species to calibrate 15 nodes in the arthropod tree of life. This integration of data classes resolved the basal topology of sea spiders with high support. The enigmatic family Austrodecidae was resolved as the sister group to the remaining Pycnogonida and the small-bodied family Rhynchothoracidae as the sister group of the robust-bodied family Pycnogonidae. Molecular divergence time estimation recovered a basal divergence of crown group sea spiders in the Ordovician. Comparison of diversification dynamics with other marine invertebrate taxa that originated in the Paleozoic suggests that sea spiders and some crustacean groups exhibit resilience to mass extinction episodes, relative to mollusk and echinoderm lineages.

evolutionary biology↗