The origin of the Hox/ParaHox genes, the Ghost Locus hypothesis and the complexity of the first animal

A key aim in evolutionary biology is to deduce ancestral states in order to better understand the evolutionary origins of clades of interest and the diversification process(es) that have elaborated them. These ancestral deductions can hit difficulties when undetected loss events are misinterpreted as ancestral absences. With the ever-increasing amounts of animal genomic sequence data we are gaining a much clearer view of the preponderance of differential gene losses across animal lineages. This has become particularly clear with recent progress in our understanding of the origins of the Hox/ParaHox developmental control genes relative to the earliest branching lineages of the animal kingdom: the sponges (Porifera), comb jellies (Ctenophora) and placozoans (Placozoa). These reassessments of the diversity and complexity of developmental control genes in the earliest animal ancestors need to go hand-in-hand with complementary advances in comparative morphology, phylogenetics and palaeontology in order to clarify our understanding of the complexity of the last common ancestor of all animals. The field is currently undergoing a shift from the traditional consensus of a sponge-like animal ancestor from which morphological and molecular elaboration subsequently evolved, to a scenario of a more complex animal ancestor, with subsequent losses and simplifications in various lineages.Peer reviewe

Amphioxus SYCP1 : a case of retrogene replacement and co-option of regulatory elements adjacent to the ParaHox cluster

MGG was supported by the University of St Andrews School of Biology Biotechnology and Biological Sciences Research Council DTG and the Wellcome Trust ISSF. Work in the authors’ laboratory is also supported by the Leverhulme Trust.Retrogenes are formed when an mRNA is reverse transcribed and re-inserted into the genome in a location unrelated to the original locus. If this retrocopy inserts into a transcriptionally favourable locus and is able to carry out its original function, it can, in rare cases, lead to retrogene replacement. This involves the original, often multi-exonic, parental copy being lost whilst the newer single-exon retrogene copy ‘replaces’ the role of the ancestral parent gene. One example of this is amphioxus SYCP1, a gene that encodes a protein used in synaptonemal complex formation during meiosis, and which offers the opportunity to examine how a retrogene evolves after the retrogene replacement event. SYCP1 genes exist as large multi-exonic genes in most animals. AmphiSYCP1, however, contains a single coding exon of ~3200bp and has inserted next to the ParaHox cluster of amphioxus, whilst the multi-exonic ancestral parental copy has been lost. Here, we show that AmphiSYCP1 has not only replaced its parental copy, but has evolved additional regulatory function by co- opting a bidirectional promoter from the nearby AmphiCHIC gene. AmphiSYCP1 has also evolved a de novo, multi-exonic 5’untranslated region that displays distinct regulatory states, in the form of two different isoforms, and has evolved novel expression patterns during amphioxus embryogenesis in addition to its ancestral role in meiosis. Absence of ParaHox-like expression of AmphiSYCP1, despite its proximity to the ParaHox cluster, also suggests this gene is not influenced by any potential pan-cluster regulatory mechanisms, which are seemingly restricted to only the ParaHox genes themselves.Publisher PDFPeer reviewe

Horizons in evolutionary genomics : an interview with David Ferrier

Research in the author’s laboratory is funded by the Leverhulme Trust, BBSRC, EU Horizon2020 CORBEL and ASSEMBLE+, and the University of St Andrews, School of Biology.David Ferrier is a Reader at the University of St Andrews and Deputy Director of the Scottish Oceans Institute, where his lab studies how the diversity of form in the animal kingdom evolved, with an emphasis on using comparative genomics. In this interview, David shares his thoughts on how to escape the ‘straitjacket’ of traditional model systems, transparency in peer review, and the past and future of genome sequencing.Publisher PDFNon peer reviewe

Two more Posterior Hox genes and Hox cluster dispersal in echinoderms

Research in the Ferrier group is funded by the Leverhulme Trust, EU Horizon2020, BBSRC and School of Biology.Background: Hox genes are key elements in patterning animal development. They are renowned for their, often, clustered organisation in the genome, with supposed mechanistic links between the organisation of the genes and their expression. The widespread distribution and comparable functions of Hox genes across the animals has led to them being a major study system for comparing the molecular bases for construction and divergence of animal morphologies. Echinoderms (including sea urchins, sea stars, sea cucumbers, feather stars and brittle stars) possess one of the most unusual body plans in the animal kingdom with pronounced pentameral symmetry in the adults. Consequently, much interest has focused on their development, evolution and the role of the Hox genes in these processes. In this context, the organisation of echinoderm Hox gene clusters is distinctive. Within the classificatory system of Duboule, echinoderms constitute one of the clearest examples of Disorganized (D) clusters (i.e. intact clusters but with a gene order or orientation rearranged relative to the ancestral state). Results: Here we describe two Hox genes (Hox11/13d and e) that have been overlooked in most previous work and have not been considered in reconstructions of echinoderm Hox complements and cluster organisation. The two genes are related to Posterior Hox genes and are present in all classes of echinoderm. Importantly, they do not reside in the Hox cluster of any species for which genomic linkage data is available. Conclusion: Incorporating the two neglected Posterior Hox genes into assessments of echinoderm Hox gene complements and organisation shows that these animals in fact have Split (S) Hox clusters rather than simply Disorganized (D) clusters within the Duboule classification scheme. This then has implications for how these genes are likely regulated, with them no longer covered by any potential long-range Hox cluster-wide, or multigenic sub-cluster, regulatory mechanisms.Publisher PDFPeer reviewe

Genome biology : unconventional DNA repair in an extreme genome

DNA is under constant assault and needs to efficiently repair breaks. A tiny marine relative of vertebrates makes do with an alternative mechanism to the canonical repair system, which coincides with it possessing one of the most extreme animal genomes.PostprintNon peer reviewe

Impacts of jellyfish on marine cage aquaculture : an overview of existing knowledge and the challenges to finfish health

BBSRC Eastbio funded studentship (lead author).Gelatinous plankton present a challenge to marine fish aquaculture that remains to be addressed. Shifting plankton distributions, suggested by some to be a result of factors such as climate change and overfishing, appear to be exacerbated by anthropogenic factors linked directly to aquaculture. Fish health can be negatively influenced by exposure to the cnidarian hydrozoan and scyphozoan life stages commonly referred to as “jellyfish”. Impact is particularly pronounced in gill tissue, where three key outcomes of exposure are described; direct traumatic damage, impaired function, and initiation of secondary disease. Cnidarian jellyfish demonstrated to negatively impact fish include Cyanea capillata, Aurelia aurita, and Pelagia noctiluca. Further coelenterates have also been associated with harm to fish, including sessile polyps of species such as Ectopleura larynx. An accurate picture of inshore planktic exposure densities within the coastal environments of aquaculture would aid in understanding cnidarian species of concern, and their impact upon fish health, particularly in gill disease. This information is however presently lacking. This review summarises the available literature regarding the impact of gelatinous plankton on finfish aquaculture, with a focus on cnidarian impact on fish health. Present strategies in monitoring and mitigation are presented, alongside identified critical knowledge gaps.PostprintPeer reviewe

Gill transcriptomic responses to toxin-producing alga Prymnesium parvum in rainbow trout

This work was supported by the BBSRC EastBio PhD studentship awarded to MC, the Danish Strategic Research Council grant No 060300449B HABFISH, and the European Maritime and Fisheries Fund and the Danish Fisheries Agency joint grant “Sundt Dambrug”. Molecular work at University of Aberdeen was funded by Scottish Aquaculture Innovation grant SL 2017 08. EK was supported by BBSRC grant BB/R018812/1.The gill of teleost fish is a multifunctional organ involved in many physiological processes, including protection of the mucosal gill surface against pathogens and other environmental antigens by the gill-associated lymphoid tissue (GIALT). Climate change associated phenomena, such as increasing frequency and magnitude of harmful algal blooms (HABs) put extra strain on gill function, contributing to enhanced fish mortality and fish kills. However, the molecular basis of the HAB-induced gill injury remains largely unknown due to the lack of high-throughput transcriptomic studies performed on teleost fish in laboratory conditions. We used juvenile rainbow trout (Oncorhynchus mykiss) to investigate the transcriptomic responses of the gill tissue to two (high and low) sublethal densities of the toxin-producing alga Prymnesium parvum, in relation to non-exposed control fish. The exposure time to P. parvum (4–5 h) was sufficient to identify three different phenotypic responses among the exposed fish, enabling us to focus on the common gill transcriptomic responses to P. parvum that were independent of dose and phenotype. The inspection of common differentially expressed genes (DEGs), canonical pathways, upstream regulators and downstream effects pointed towards P. parvum-induced inflammatory response and gill inflammation driven by alterations of Acute Phase Response Signalling, IL-6 Signalling, IL-10 Signalling, Role of PKR in Interferon Induction and Antiviral Response, IL-8 Signalling and IL-17 Signalling pathways. While we could not determine if the inferred gill inflammation was progressing or resolving, our study clearly suggests that P. parvum blooms may contribute to the serious gill disorders in fish. By providing insights into the gill transcriptomic responses to toxin-producing P. parvum in teleost fish, our research opens new avenues for investigating how to monitor and mitigate toxicity of HABs before they become lethal.Publisher PDFPeer reviewe

Light-sheet microscopy with attenuation-compensated propagation-invariant beams

Scattering and absorption limit the penetration of optical fields into tissue. We demonstrate a new approach for increased depth penetration in light-sheet microscopy: attenuation-compensation of the light field. This tailors an exponential intensity increase along the illuminating propagation-invariant field, enabling the redistribution of intensity strategically within a sample to maximize signal and minimize irradiation. A key attribute of this method is that only minimal knowledge of the specimen transmission properties is required. We numerically quantify the imaging capabilities of attenuation-compensated Airy and Bessel light sheets, showing that increased depth penetration is gained without compromising any other beam attributes. This powerful yet straightforward concept, combined with the self-healing properties of the propagation-invariant field, improves the contrast-to-noise ratio of light-sheet microscopy up to eightfold across the entire field of view in thick biological specimens. This improvement can significantly increase the imaging capabilities of light-sheet microscopy techniques using Airy, Bessel, and other propagation-invariant beam types, paving the way for widespread uptake by the biomedical community.</p

Acromegaly, Mr Punch and caricature.

The origin of Mr Punch from the Italian Pulcinella of the Commedia dell'arte is well known but his feature, large hooked nose, protruding chin, kyphosis and sternal protrusion all in an exaggerated form also suggest the caricature of an acromegalic. This paper looks at the physical characteristics of acromegaly, the origin of Mr Punch and the development of caricature linking them together in the acromegalic caricature that now has a life of its own

Genes for de novo biosynthesis of omega-3 polyunsaturated fatty acids are widespread in animals

This work received funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) funded by the Scottish Funding Council (grant reference HR09011), and their support is gratefully acknowledged. Access to the Institute of Aquaculture laboratories was funded by the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement no. 262336 (AQUAEXCEL), Transnational Access Project Number 0095/06/03/13.Marine ecosystems are responsible for virtually all production of omega-3 (ω3) long- chain polyunsaturated fatty acids (PUFA), essential nutrients for vertebrates. Current consensus is that marine microbes account for this production, given they have key enzymes including methyl-end (or “ωx”) desaturases. ωx desaturases have also been described in a small number of animals, but their precise distribution has not been systematically explored. This study identifies 121 ωx desaturase sequences from 80 species within the Cnidaria, Rotifera, Mollusca, Annelida and Arthropoda. Horizontal Gene Transfer contributed to this hitherto unknown widespread distribution. Functional characterization of animal ωx desaturases provides evidence that multiple invertebrates have the ability to produce ω3 PUFA de novo and further biosynthesize ω3 long-chain PUFA. This represents a fundamental revision in our understanding of ω3 long- chain PUFA production in global food webs, as numerous widespread and abundant invertebrates have the endogenous capacity to make significant contributions beyond that coming from marine microbes.Publisher PDFPeer reviewe