The origin of bmp16, a novel Bmp2/4 relative, retained in teleost fish genomes

<p>Abstract</p> <p>Background</p> <p>Whole genome sequences have allowed us to have an overview of the evolution of gene repertoires. The target of the present study, the TGFβ superfamily, contains many genes involved in vertebrate development, and provides an ideal system to explore the relationships between evolution of gene repertoires and that of developmental programs.</p> <p>Results</p> <p>As a result of a bioinformatic survey of sequenced vertebrate genomes, we identified an uncharacterized member of the TGFβ superfamily, designated <it>bmp16</it>, which is confined to teleost fish species. Our molecular phylogenetic study revealed a high affinity of <it>bmp16 </it>to the <it>Bmp2/4 </it>subfamily. Importantly, further analyses based on the maximum-likelihood method unambiguously ruled out the possibility that this teleost-specific gene is a product of teleost-specific genome duplication. This suggests that the absence of a <it>bmp16 </it>ortholog in tetrapods is due to a secondary loss. <it>In situ </it>hybridization showed embryonic expression of the zebrafish <it>bmp16 </it>in the developing swim bladder, heart, tail bud, and ectoderm of pectoral and median fin folds in pharyngula stages, as well as gut-associated expression in 5-day embryos.</p> <p>Conclusion</p> <p>Comparisons of expression patterns revealed (1) the redundancy of <it>bmp16 </it>expression with its homologs in presumably plesiomorphic expression domains, such as the fin fold, heart, and tail bud, which might have permitted its loss in the tetrapod lineage, and (2) the loss of craniofacial expression and gain of swim bladder expression of <it>bmp16 </it>after the gene duplication between <it>Bmp2</it>, <it>-4 </it>and <it>-16</it>. Our findings highlight the importance of documenting secondary changes of gene repertoires and expression patterns in other gene families.</p

Environmentally induced DNA methylation is inherited across generations in an aquatic keystone species

Transgenerational inheritance of environmentally induced epigenetic marks can have significant impacts on eco-evolutionary dynamics, but the phenomenon remains controversial in ecological model systems. We used whole-genome bisulfite sequencing of individual water fleas (Daphnia magna) to assess whether environmentally induced DNA methylation is transgenerationally inherited. Genetically identical females were exposed to one of three natural stressors, or a de-methylating drug, and their offspring were propagated clonally for four generations under control conditions. We identified between 70 and 225 differentially methylated CpG positions (DMPs) in F1 individuals whose mothers were exposed to a natural stressor. Roughly half of these environmentally induced DMPs persisted until generation F4. In contrast, treatment with the drug demonstrated that pervasive hypomethylation upon exposure is reset almost completely after one generation. These results suggest that environmentally induced DNA methylation is non-random and stably inherited across generations in Daphnia, making epigenetic inheritance a putative factor in the eco-evolutionary dynamics of freshwater communities

Chromosome-scale genome assembly of the brown anole (Anolis sagrei), an emerging model species

Rapid technological improvements are democratizing access to high quality, chromosome-scale genome assemblies. No longer the domain of only the most highly studied model organisms, now non-traditional and emerging model species can be genome-enabled using a combination of sequencing technologies and assembly software. Consequently, old ideas built on sparse sampling across the tree of life have recently been amended in the face of genomic data drawn from a growing number of high-quality reference genomes. Arguably the most valuable are those long-studied species for which much is already known about their biology; what many term emerging model species. Here, we report a highly complete chromosome-scale genome assembly for the brown anole, Anolis sagrei – a lizard species widely studied across a variety of disciplines and for which a high-quality reference genome was long overdue. This assembly exceeds the vast majority of existing reptile and snake genomes in contiguity (N50 = 253.6 Mb) and annotation completeness. Through the analysis of this genome and population resequence data, we examine the history of repetitive element accumulation, identify the X chromosome, and propose a hypothesis for the evolutionary history of fusions between autosomes and the X that led to the sex chromosomes of A. sagrei

Chromosome-level genome assembly of Lilford's wall lizard, Podarcis lilfordi (Günther, 1874) from the Balearic Islands (Spain)

The Mediterranean lizard Podarcis lilfordi is an emblematic species of the Balearic Islands. The extensive phenotypic diversity among extant isolated populations makes the species a great insular model system for eco-evolutionary studies, as well as a challenging target for conservation management plans. Here we report the first high-quality chromosome-level assembly and annotation of the P. lilfordi genome, along with its mitogenome, based on a mixed sequencing strategy (10X Genomics linked reads, Oxford Nanopore Technologies long reads and Hi-C scaffolding) coupled with extensive transcriptomic data (Illumina and PacBio). The genome assembly (1.5 Gb) is highly contiguous (N50 = 90 Mb) and complete, with 99% of the sequence assigned to candidate chromosomal sequences and >97% gene completeness. We annotated a total of 25,663 protein-coding genes translating into 38,615 proteins. Comparison to the genome of the related species Podarcis muralis revealed substantial similarity in genome size, annotation metrics, repeat content, and a strong collinearity, despite their evolutionary distance (~18-20 MYA). This genome expands the repertoire of available reptilian genomes and will facilitate the exploration of the molecular and evolutionary processes underlying the extraordinary phenotypic diversity of this insular species, while providing a critical resource for conservation genomics.This study was supported by the Institut d’Estudis Catalans under the Catalan Initiative for the Earth Biogenome Project (PRO2020-S02 to L.B.), the Swedish Research Council (VR 2017-03846 and VR-2021-04656 to T.U. and VR-2020-03650 to N.F.) and Starting Grant from the European Research Council (no. 948126 to N.F.). We also acknowledge the support of the Spanish Ministry of Science and Innovation to the EMBL partnership, the Centro de Excelencia Severo Ochoa, the CERCA Programme/Generalitat de Catalunya, the Spanish Ministry of Science and Innovation through the Instituto de Salud Carlos III and the Generalitat de Catalunya through Departament de Salut and Departament d’Empresa i Coneixement. Co-financing funds were obtained from the European Regional Development Fund by the Spanish Ministry of Science and Innovation corresponding to the Programa Operativo FEDER Plurirregional de España (POPE) 2014-2020 and by the Secretaria d’Universitats i Recerca, Departament d’Empresa i Coneixement of the Generalitat de Catalunya corresponding to the Programa Operatiu FEDER de Catalunya 2014-2020.Peer reviewe

Analysis of the African coelacanth genome sheds light on tetrapod evolution

It was a zoological sensation when a living specimen of the coelacanth was first discovered in 1938, as this lineage of lobe-finned fish was thought to have gone extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods. Coelacanth protein-coding genes are significantly more slowly evolving than those of tetrapods, unlike other genomic features . Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion and the development of fins, tail, ear, eye, brain, and olfaction. Functional assays of enhancers involved in the fin-to-limb transition and in the emergence of extra-embryonic tissues demonstrate the importance of the coelacanth genome as a blueprint for understanding tetrapod evolution

Charakterisierung von verborgenen Komponenten im Genom des Urwirbeltiers

My thesis entitled ‘Characterization of cryptic components of the ancestral vertebrate genome’ aims at reconstructing the changes in DNA that parallel the evolution of vertebrates. The central question is which changes on the genomic level accompany, and maybe even account for, the emergence of phenotypic novelties. This approach is also key to a deeper understanding of the evolution of the human genome. Vertebrates are distinguished from invertebrates by numerous characteristics. Vertebrates are phenotypically characterized, for example, by a complex tripartite brain with integrative centers such as the telencephalon and an embryonic neural crest that contributes to elaborate craniofacial features that enable a predatory lifestyle. On the genomic level, vertebrates are distinguished from other chordates by two rounds of whole genome duplication (2R-WGD) that occurred in the last common ancestor of vertebrates around 525 million years ago. Initially, the ancestral vertebrate possessed four copies of each gene. Some of this redundant genetic material was subsequently deleted from the genome, or genes accumulated mutations and eventually became nonfunctional pseudogenes. A differential gene loss between vertebrate lineages might partly explain the phenotypic differences across vertebrates. My approach focuses on key developmental gene families (Bmp, Pax, Hox and ENC gene families) whose members are not present in all vertebrate lineages.A subproject of this thesis focused on the famous Hox gene family that specifies positional identity along the primary body axis in the early embryo across metazoans. The Hox14 gene was hitherto identified only in a handful of basal vertebrates (shark, lamprey and coelacanth), and I revealed the existence of a Hox14 gene in the Australian lungfish. In addition, I showed that its expression in lungfish, similar to shark and lamprey, is decoupled from the typical ‘Hox-code’.Another subproject involved the Pax6 gene that is considered to be the ‘master control gene’ for eye development throughout bilaterians. My research revealed that its sister gene Pax4, that was hitherto only identified in mammals, also exists in the genomes of teleosts, the coelacanth and some reptiles (turtles and crocodiles). Interestingly, I identified a previously unknown gene, Pax10, that is most likely the third gene of the original gene quartet, including Pax4 and -6, derived from the 2R-WGD. A comparative study including phylogenetic, syntenic and expression analyses of Pax4, -6 and -10 genes in diverse vertebrates shed light on the asymmetric evolution of the Pax4/6/10 class of genes. Based on these results I reconstructed a likely evolutionary scenario that describes the secondary modifications in this gene family.The ectodermal neural cortex (ENC) gene family, whose members are implicated in neurogenesis, is part of the kelch repeat superfamily. My analyses revealed that most vertebrates possess three distinct ENC genes derived from the 2R-WGD suggesting the loss of the forth subtype early in vertebrate evolution. Only eutherians secondarily lost ENC3. A comparison of the ENC1 expression patterns I obtained in shark with ENC1 expression profiles in tetrapods suggests a high level of conservation of developmental roles of this gene. Compared with many other gene families including key developmental regulators, the ENC gene family is unique in that conventional molecular phylogenetic inferences could not identify any obvious invertebrate ortholog. This suggests that the ENC gene family might have been too rapidly evolving to provide sufficient phylogenetic signals marking orthology to their invertebrate counterparts. Such gene families that experienced saltatory evolution likely remain unexplored, and might also have contributed to phenotypic evolution of vertebrates.One aspect of my thesis focused on a recently identified sister gene of the key developmental genes Bmp2 and -4, designated Bmp16. This gene greatly differs from its well-investigated sister genes in two aspects. Firstly, the absence of Bmp16 in many vertebrate lineages (mammals, amphibians and archosaurs) is in stark contrast to the universal presence of Bmp2 and -4 in vertebrate genomes. Secondly, gene expression analyses of Bmp16 in teleosts (zebrafish), chondrichthyans (sharks) and reptiles (anoles) revealed a high degree of evolutionary plasticity that has never been documented for any Bmp2 or -4 gene. By using morpholino-induced knockdown techniques, I investigated to what extent sister genes are capable of compensating for the loss of a functional Bmp16 gene. This approach might allude to why this gene independently got lost at least three times during vertebrate evolution.My thesis reveals recurrent patterns of gene family evolution in vertebrates. My detailed studies of selected gene families describe the dynamics that shaped the gene repertoires of extant vertebrates and thus contributed to phenotypic evolution leading to the biodiversity of vertebrates

Podarcis muralis (Common Wall Lizard). Parasite load

International audienceHerein we present the first record of the tapeworm Mesocestoides litteratus in Podarcis muralis in its native range in Western Europe. The life cycle of this parasite comprises presumably two intermediate hosts and one definite host, although details remain unresolved. Most likely, the first intermediate host is a coprophagous arthropod that transmits the tapeworm parasite to its predators, usually a rodent, amphibian, lizard, or bird

Evolvability and evolutionary rescue

The survival prospects of threatened species or populations can sometimes be improved by adaptive change. Such evolutionary rescue is particularly relevant when the threat comes from changing environments, or when long-term population persistence requires range expansion into new habitats. Conservation biologists are therefore often interested in whether or not populations or lineages show a disposition for adaptive evolution, that is, if they are evolvable. Here, we discuss four alternative perspectives that target different causes of evolvability and outline some of the key challenges those perspectives are designed to address. Standing genetic variation provides one familiar estimate of evolvability. Yet, the mere presence of genetic variation is often insufficient to predict if a population will adapt, or how it will adapt. The reason is that adaptive change not only depends on genetic variation, but also on the extent to which this genetic variation can be realized as adaptive phenotypic variation. This requires attention to developmental systems and how plasticity influences evolutionary potential. Finally, we discuss how a better understanding of the different factors that contribute to evolvability can be exploited in conservation practice

Asymmetric paralog evolution between the “cryptic” gene Bmp16 and its well-studied sister genes Bmp2 and Bmp4

The vertebrate gene repertoire is characterized by “cryptic” genes whose identification has been hampered by their absence from the genomes of well-studied species. One example is the Bmp16 gene, a paralog of the developmental key genes Bmp2 and -4. We focus on the Bmp2/4/16 group of genes to study the evolutionary dynamics following gen(om)e duplications with special emphasis on the poorly studied Bmp16 gene. We reveal the presence of Bmp16 in chondrichthyans in addition to previously reported teleost fishes and reptiles. Using comprehensive, vertebrate-wide gene sampling, our phylogenetic analysis complemented with synteny analyses suggests that Bmp2, -4 and -16 are remnants of a gene quartet that originated during the two rounds of whole-genome duplication (2R-WGD) early in vertebrate evolution. We confirm that Bmp16 genes were lost independently in at least three lineages (mammals, archelosaurs and amphibians) and report that they have elevated rates of sequence evolution. This finding agrees with their more “flexible” deployment during development; while Bmp16 has limited embryonic expression domains in the cloudy catshark, it is broadly expressed in the green anole lizard. Our study illustrates the dynamics of gene family evolution by integrating insights from sequence diversification, gene repertoire changes, and shuffling of expression domains

Developmental plasticity in reptiles: Insights from temperature-dependent gene expression in wall lizard embryos : Insights from temperature-dependent gene expression in wall lizard embryos

Many features of the development of reptiles are affected by temperature, but very little is known about how incubation temperature affects gene expression. Here, we provide a detailed case study of gene expression profiles in common wall lizard (Podarcis muralis) embryos developing at stressfully low (15°C) versus benign (24°C) temperature. For maximum comparability between the two temperature regimes, we selected a precise developmental stage early in embryogenesis defined by the number of somites. We used a split-clutch design and lizards from four different populations to evaluate the robustness of temperature-responsive gene expression profiles. Embryos incubated at stressfully low incubation temperature expressed on average 20% less total RNA than those incubated at benign temperatures, presumably reflecting lower rates of transcription at cool temperature. After normalizing for differences in total amounts of input RNA, we find that approximately 50% of all transcripts show significant expression differences between the two incubation temperatures. Transcripts with the most extreme changes in expression profiles are associated with transcriptional and translational regulation and chromatin remodeling, suggesting possible epigenetic mechanisms underlying acclimation of early embryos to cool temperature. We discuss our findings in light of current advances in the use of transcriptomic data to study how individuals acclimatize and populations adapt to thermal stress