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ABSTRACT Evolutionary theory suggests that critical cellular structures should be subject to strong purifying selection as protein changes would result in inviability. However, how this evolutionary principle relates to multi-subunit complexes remains incompletely explored. For example, the macromolecular kinetochore complex, which mediates the faithful segregation of DNA during cell division, violates the expectation of purifying selection as subsets of kinetochore proteins exhibit rapid evolution despite its critical role. Here, we developed a multi-level approach to investigate the evolutionary dynamics of the kinetochore as a model for understanding how an essential multi-protein structure can experience high rates of diversifying selection while maintaining function. Our comprehensive approach analyzed 57 kinetochore genes for signatures of purifying and diversifying selection across 70 mammalian species. Intraspecies comparisons of kinetochore gene evolution showed that members of the order Afrotheria experience higher rates of diversifying selection than other mammalian orders. Among individual loci, genes that serve regulatory functions, such as the mitotic checkpoint genes, are conserved under strong purifying selection. In contrast, the proteins that serve as the structural base of the kinetochore, including the inner and outer kinetochore, evolve rapidly across species. We also demonstrated that diversifying selection is targeted to protein regions that lack clear structural predictions. Finally, we identified sites that exhibit corresponding trends in evolution across different genes, potentially providing evidence of compensatory evolution in this complex. Together, our study of the kinetochore reveals a potential avenue by which selection can alter the genes that comprise an essential cellular complex without compromising its function. 

Hagfishes are deep-sea animals, and they represent one of the oldest living relatives of animals with backbones. To defend themselves against predators, they produce a remarkable slime that is reinforced with fibers and can clog a predator’s gills, thwarting the attack. The slime deploys in less than half a second, exuding from specialized glands on the hagfish’s body and expanding up to 10,000 times its ejected volume. The defensive slime is highly dilute, consisting mostly of sea water, with low concentrations of mucus and strong, silk-like threads that are approximately 20 centimeters long. Where and how hagfish slime evolved remains a mystery. Zeng et al. set out to answer where on the hagfish’s body the slime glands originated, and how they may have evolved. First, Zeng et al. examined hagfishes and found that cells in the surface layer of their skin (the epidermis) produce threads roughly two millimeters in length that are released when the hagfish’s skin is damaged. These threads mix with the mucus that is produced by ruptured skin cells to form a slime that likely adheres to predators’ mouths. This slime could be a precursor of the slime produced by the specialized glands. To test this hypothesis, Zeng et al. analyzed which genes are turned on and off both in the hagfishes’ skin and in their slime glands. The patterns they found are consistent with the slime glands originating from the epidermis. Based on these results, Zeng et al. propose that ancient hagfishes first evolved the ability to produce slime with anti-predator effects when their skin was damaged in attacks. Over time, hagfishes that could produce and store more slime and eject it actively into a predator’s mouth likely had a better chance of surviving. This advantage may have led to the appearance of increasingly specialized glands that could carry out these functions. The findings of Zeng et al. will be of interest to evolutionary biologists, marine biologists, and those studying the ecology of predator-prey interactions. Because of its unique material properties, hagfish slime is also of interest to biophysicists, bioengineers and those engaged in biomimetic research. The origin of hagfish slime glands is an interesting example of how a new trait evolved, and may provide insight into the evolution of other adaptive traits. 

Abstract Background Phylogenomic approaches have great power to reconstruct evolutionary histories, however they rely on multi-step processes in which each stage has the potential to affect the accuracy of the final result. Many studies have empirically tested and established methodology for resolving robust phylogenies, including selecting appropriate evolutionary models, identifying orthologs, or isolating partitions with strong phylogenetic signal. However, few have investigated errors that may be initiated at earlier stages of the analysis. Biases introduced during the generation of the phylogenomic dataset itself could produce downstream effects on analyses of evolutionary history. Transcriptomes are widely used in phylogenomics studies, though there is little understanding of how a poor-quality assembly of these datasets could impact the accuracy of phylogenomic hypotheses. Here we examined how transcriptome assembly quality affects phylogenomic inferences by creating independent datasets from the same input data representing high-quality and low-quality transcriptome assembly outcomes. Results By studying the performance of phylogenomic datasets derived from alternative high- and low-quality assembly inputs in a controlled experiment, we show that high-quality transcriptomes produce richer phylogenomic datasets with a greater number of unique partitions than low-quality assemblies. High-quality assemblies also give rise to partitions that have lower alignment ambiguity and less compositional bias. In addition, high-quality partitions hold stronger phylogenetic signal than their low-quality transcriptome assembly counterparts in both concatenation- and coalescent-based analyses. Conclusions Our findings demonstrate the importance of transcriptome assembly quality in phylogenomic analyses and suggest that a portion of the uncertainty observed in such studies could be alleviated at the assembly stage. 

Abstract Multisensory integration (MSI) combines information from more than one sensory modality to elicit behaviours distinct from unisensory behaviours. MSI is best understood in animals with complex brains and specialized centres for parsing different modes of sensory information, but dispersive larvae of sessile marine invertebrates utilize multimodal environmental sensory stimuli to base irreversible settlement decisions on, and most lack complex brains. Here, we examined the sensory determinants of settlement in actinula larvae of the hydrozoanEctopleura crocea(Cnidaria), which possess a diffuse nerve net. A factorial settlement study revealed that photo‐, chemo‐ and mechanosensory cues each influenced the settlement response in a complex and hierarchical manner that was dependent on specific combinations of cues, an indication of MSI. Additionally, sensory gene expression over development peaked with developmental competence to settle, which in actinulae, requires cnidocyte discharge. Transcriptome analyses also highlighted several deep homological links between cnidarian and bilaterian mechano‐, chemo‐, and photosensory pathways. Fluorescent in situ hybridization studies of candidate transcripts suggested cellular partitioning of sensory function among the few cell types that comprise the actinula nervous system, where ubiquitous polymodal sensory neurons expressing putative chemo‐ and photosensitivity interface with mechanoreceptive cnidocytes. We propose a simple multisensory processing circuit, involving polymodal chemo/photosensory neurons and mechanoreceptive cnidocytes, that is sufficient to explain MSI in actinulae settlement. Our study demonstrates that MSI is not exclusive to complex brains, but likely predated and contextualized their evolution. 

Abstract Apoptosis is a fundamental feature of multicellular animals and is best understood in mammals, flies, and nematodes, with the invertebrate models being thought to represent a condition of ancestral simplicity. However, the existence of a leukemia-like cancer in the softshell clam Mya arenaria provides an opportunity to re-evaluate the evolution of the genetic machinery of apoptosis. Here, we report the whole-genome sequence for M. arenaria which we leverage with existing data to test evolutionary hypotheses on the origins of apoptosis in animals. We show that the ancestral bilaterian p53 locus, a master regulator of apoptosis, possessed a complex domain structure, in contrast to that of extant ecdysozoan p53s. Further, ecdysozoan taxa, but not chordates or lophotrochozoans like M. arenaria, show a widespread reduction in apoptosis gene copy number. Finally, phylogenetic exploration of apoptosis gene copy number reveals a striking linkage with p53 domain complexity across species. Our results challenge the current understanding of the evolution of apoptosis and highlight the ancestral complexity of the bilaterian apoptotic tool kit and its subsequent dismantlement during the ecdysozoan radiation. 

A fundamental question in evolutionary biology is how developmental processes are modified to produce morphological innovations while abiding by functional constraints. Here we address this question by investigating the cellular mechanism responsible for the transition between fused and open rhabdoms in ommatidia of apposition compound eyes; a critical step required for the development of visual systems based on neural superposition. Utilizing Drosophila and Tribolium as representatives of fused and open rhabdom morphology in holometabolous insects respectively, we identified three changes required for this innovation to occur. First, the expression pattern of the extracellular matrix protein Eyes Shut (EYS) was co-opted and expanded from mechanosensory neurons to photoreceptor cells in taxa with open rhabdoms. Second, EYS homologs obtained a novel extension of the amino terminus leading to the internalization of a cleaved signal sequence. This amino terminus extension does not interfere with cleavage or function in mechanosensory neurons, but it does permit specific targeting of the EYS protein to the apical photoreceptor membrane. Finally, a specific interaction evolved between EYS and a subset of Prominin homologs that is required for the development of open, but not fused, rhabdoms. Together, our findings portray a case study wherein the evolution of a set of molecular novelties has precipitated the origin of an adaptive photoreceptor cell arrangement.