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Salzburger, W.

Publications and source records attributed to Salzburger, W..

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Hemoglobin gene repertoire in teleost and cichlid fishes shaped by gene duplications and genome rearrangements

Hemoglobin is a crucial element of the oxygen transport system in vertebrates. It exhibits remarkable gene diversity across teleost fishes, reflecting their evolutionary adaptations for thriving in various aquatic environments. In this study, we present the dynamic evolution of hemoglobin subunit genes based on a comparison of high quality long-read genome assemblies of 24 vertebrate species, including 16 teleosts (of which six are cichlids). Our findings indicate that teleost genomes contain between five (fugu) and 43 (salmon) hemoglobin genes, representing the largest hemoglobin gene repertoire among vertebrates. We find evidence that the ancestor of teleosts had at least four Hb and three or four Hb{beta} subunit genes, and that the current gene diversity emerged during subsequent teleost radiation, driven primarily by (tandem) gene duplications, genome compaction, and rearrangement dynamics. We provide insights into the genomic organization of hemoglobin clusters, revealing the parallel origin of multiple clusters in tetrapods and in teleosts. Importantly, we show that the presence of paralogous rhbdf1 genes flanking both teleost hemoglobin clusters (LA and MN) supports the hypothesis for the origin of the LA cluster by rearrangement within teleosts, rather than by the teleost specific whole-genome duplication. We specifically focus on cichlid fishes, where adaptation to low oxygen environments has been shown to play roles in species diversification. Our analysis of six cichlid genomes, including the Pungu maclareni from crater lake Barombi Mbo, for which we sequenced the representative genome, reveals 18 to 31 copies of the Hb genes, and elevated rates of non- synonymous substitutions compared to other teleosts. Overall, this work facilitates a deeper understanding of how hemoglobin genes contribute to the adaptive and diversification potential of teleosts.

evolutionary biology↗

Frequent transitions from night-to-day activity after mass extinctions

Why certain species survive large-scale extinction events while others do not is poorly understood. While the fossil record can provide insights into morphological adaptations that increase survival probabilities, it provides limited information regarding behavioural traits. Here we integrate behavioural data with phylogenetic comparative models to study the evolution of day-night activity patterns (nocturnality and diurnality) in bony fishes, which have persisted through the last four mass extinction events. Our findings in fish, combined with data across all other clades of vertebrates, provide four lines of evidence that nocturnality conferred an evolutionary advantage during mass extinctions, and that frequent nocturnal-to-diurnal transitions facilitated post-extinction diversification: First, phylogenetic reconstruction indicates that the last common ancestors of all vertebrates and of clades of bony vertebrates were nocturnal. Second, in the lineage of bony fishes, which contains over half of all vertebrate species, twice as many transitions between nocturnal and diurnal activity patterns have occurred compared to tetrapods. Third, within a specific ecological niche, different species exhibit distinct temporal activity patterns, suggesting widespread temporal niche partitioning. Fourth, independent bursts in night-to-day transitions followed large-scale extinction events during the last two geological eras in all four major bony vertebrate groups. These observations suggest that ancestral nocturnality and frequent transitions to diurnality helped vertebrates survive and diversify in the face of extinction events, such as those expected during the current "6th mass extinction" event caused by anthropogenic climate change.

evolutionary biology↗

Host adaptive radiation is associated with rapid virus diversification and cross-species transmission in African cichlid fishes

Adaptive radiations are generated through a complex interplay of biotic and abiotic factors. Although adaptive radiations have been widely studied in the context of animal and plant evolution, little is known about how they impact the evolution of the viruses that infect these hosts, which in turn may provide insights into the drivers of disease emergence. We examined how the rapid adaptive radiation of the African cichlid fishes of Lake Tanganyika over the last 10 million years has shaped the diversity and evolution of the viruses they carry. Through metatranscriptomic analysis we identified 121 vertebrate-associated viruses among various tissue types that fell into 13 RNA and 4 DNA virus groups. Host-switching was commonplace, particularly within the Astroviridae, Metahepadnavirus, Nackednavirus, Picornaviridae, and Hepacivirus groups, occurring more frequently than in other fish communities. A time-calibrated phylogeny revealed that hepacivirus evolution was not constant throughout the cichlid radiation, but accelerated 2-3 million years ago, coinciding with a period of rapid cichlid diversification and niche packing in Lake Tanganyika, thereby providing more closely related hosts for viral infection. These data show that African cichlids contain a complex interacting pool of virus diversity, likely reflecting their close genetic relationships that lowers the barriers to cross-species virus transmission.

evolutionary biology↗

Distribution, diversity and diversification from a DNA barcoding perspective: the case of Gammarus radiation in Europe`s oldest inland waterbody - the ancient Lake Ohrid

AimA detailed, comparative DNA-barcoding and morphospecies based overview of the vertical and horizontal distribution of Lake Ohrid endemic Gammarus species-flock. Re-evaluation of the origin of the species-flock dating, identification of events that putatively influenced diversification patterns in the species-flock. LocationLake Ohrid: a deep and ancient lake of tectonic origin, biosphere reserve, UNESCO World Heritage Site, located on the Macedonia/Albania border. TaxonGammarus species-flock (Amphipoda, Crustacea) MethodsExtensive sampling and DNA barcoding of 600 individuals were carried out. DNA sequences were analysed using species delimitation methods, haplotype network reconstructions, Bayesian molecular dating and demographic analysis. The COI-based delimitation results were validated with nuclear 28S RNA data. ResultsThe species flock distribution has weak horizontal but clear vertical structure. The diversity across bathymetric gradients correlates with temperature and salinity; and the highest diversity with sublittoral and springs of lakes shore. Two new MOTUs representing putatively new species are revealed and supported also by the nuclear marker. The time of flock radiation overlaps with the time of lake formation. The COI gene shows signs of positive selection and an acceleration in substitution rate. The demographic changes of the flock happened during the last ky. Main conclusionsDistribution of the Gammarus species-flock is vertically structured, reflecting habitat zonation. Parapatric speciation as one of the mechanisms in flocks diversification is suggested. Detection of new MOTU suggests that the flocks diversity is still not fully revealed. Nevertheless, failure to recover three other MOTUs suggests the loss of gammarid diversity in the lake. This represents,together with the current threats to the lake ecosystem (i.e. climate changes, development of tourism), a clear call for conservation efforts. The speciation events and demographic changes within the flock relate presumably to glacial and postglacial water level changes and to colonisation of new depth ranges and the associated springs.

molecular biology↗

Genomics of cold adaptations in the Antarctic notothenioid fish radiation.

Numerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve understanding of the evolution of this iconic fish group, we generated and analysed new genome assemblies for 24 species covering all major subgroups of the radiation. We present a new estimate for the onset of the radiation at 10.7 million years ago, based on a time-calibrated phylogeny derived from genome-wide sequence data. We identify a two-fold variation in genome size, driven by expansion of multiple transposable element families, and use long-read sequencing data to reconstruct two evolutionarily important, highly repetitive gene family loci. First, we present the most complete reconstruction to date of the antifreeze glycoprotein gene family, whose emergence enabled survival in sub-zero temperatures, showing the expansion of the antifreeze gene locus from the ancestral to the derived state. Second, we trace the loss of haemoglobin genes in icefishes, the only vertebrates lacking functional haemoglobins, through complete reconstruction of the two haemoglobin gene clusters across notothenioid families. Finally, we show that both the haemoglobin and antifreeze genomic loci are characterised by multiple transposon expansions that may have driven the evolutionary history of these genes.

genomics↗

The history and organization of the Workshop on Population and Speciation Genomics

With the advent of high-throughput genome sequencing, bioinformatics training has become essential for research in evolutionary biology and related fields. However, individual research groups are often not in the position to teach students about the most up-to-date methodology in the field. To fill this gap, extended bioinformatics courses have been developed by various institutions and provide intense training over the course of two or more weeks. Here, we describe our experience with the organization of a course in one of the longest-running extended bioinformatics series of work-shops, the Evomics Workshop on Population and Speciation Genomics that takes place biennially in the UNESCO world heritage town of [C]esky Krumlov, Czech Republic. We list the key ingredients that make this workshop successful in our view, and describe the routine for workshop organization that we have optimized over the years. We report the results of a survey conducted among past workshop participants that quantifies measures of effective teaching and provide examples of how the workshop setting has led to the cross-fertilisation of ideas and ultimately scientific progress. We expect that our account may be useful for other groups aiming to set up their own extended bioinformatics courses.

scientific communication and education↗

Diversification dynamics and (non-)parallel evolution along an ecological gradient in African cichlid fishes

Understanding the drivers and dynamics of diversification is a central topic in evolutionary biology. Here, we investigated the dynamics of diversification in the cichlid fish Astatotilapia burtoni that diverged along a lake-stream environmental gradient. Whole-genome and morphometric analyses revealed that divergent selection was essential at the early stages of diversification, but that periods in allopatry were likely involved towards the completion of speciation. While morphological differentiation was continuous, genomic differentiation was not, as shown by two clearly separated categories of genomic differentiation. Reproductive isolation increased along a continuum of genomic divergence, with a "grey zone" of speciation at [~]0.1% net nucleotide divergence. The quantification of the extent of (non-)parallelism in nine lake-stream population pairs from four cichlid species by means of multivariate analyses revealed one parallel axis of genomic and morphological differentiation among seven lake-stream systems. Finally, we found that parallelism was higher when ancestral lake populations were more similar.

evolutionary biology↗

Dynamics of sex chromosome evolution in a rapid radiation of cichlid fishes

Sex is a fundamental trait that is determined, depending on the species, by different environmental and/or genetic factors, including various types of sex chromosomes. While the functioning and emergence of sex chromosomes have been explored in species scattered across the eukaryotic tree of life, little is known about tempo and mode of sex chromosome evolution in closely related species. Here, we examine the dynamics of sex chromosome evolution in an archetypical example of adaptive radiation, the cichlid fishes of African Lake Tanganyika. Through inspection of male and female genomes from 244 cichlid taxa and the analysis of transcriptomes from 66 taxa, we identify signatures of sex chromosomes in 79 taxa, involving 12 different linkage groups. We estimate that Tanganyikan cichlids have the highest rates of sex chromosome turnover and heterogamety transitions known to date. We further show that the recruitment of chromosomes as sex chromosomes is not at random and that some chromosomes have convergently emerged as sex chromosomes in cichlids, which provides empirical support to the "limited options" hypothesis of sex chromosome evolution.

evolutionary biology↗

Structural manipulations of a shelter resource reveal underlying preference functions in a shell-dwelling cichlid fish

Many animals can modify the environments in which they live, thereby changing the selection pressures they experience. A common example of such niche-construction is the use, creation, or modification of environmental resources for use as nests or shelters. Because these resources often have correlated structural elements, it can be difficult to disentangle the relative contribution of these elements to resource choice, and the preference functions underlying niche-construction behaviour remain hidden. Here, we present an experimental paradigm that uses 3D-scanning, -modelling, and -printing to create replicas of structures that differ with respect to key structural attributes. We show that a niche-constructing, shelldwelling cichlid fish, Neolamprologus multifasciatus, has strong open-ended preference functions for exaggerated shell replicas. Fish preferred shells that were fully intact and either enlarged, lengthened, or had widened apertures. Shell intactness was the most important structural attribute, followed by shell length, then aperture width. We disentangle the relative roles of different shell attributes, which are tightly correlated in the wild, but nevertheless differentially influence shelter choice and therefore niche construction in this species. We highlight the broad utility of our approach when compared to more traditional methods (e.g. two-choice tasks) for studying animal decision-making in a range of contexts.

evolutionary biology↗

Ancestral hybridisation facilitated species diversification in the Lake Malawi cichlid fish adaptive radiation

The adaptive radiation of cichlid fishes in East Afrian Lake Malawi encompasses over 500 species that are believed to have evolved within the last 800 thousand years from a common founder population. It has been proposed that hybridisation between ancestral lineages can provide the genetic raw material to fuel such exceptionally high diversification rates, and evidence for this has recently been presented for the Lake Victoria Region cichlid superflock. Here we report that Lake Malawi cichlid genomes also show evidence of hybridisation between two lineages that split 3-4 million years ago, today represented by Lake Victoria cichlids and the riverine Astatotilapia sp. ruaha blue. The two ancestries in Malawi cichlid genomes are present in large blocks of several kilobases, but there is little variation in this pattern between Malawi cichlid species, suggesting that the large-scale mosaic structure of the genomes was largely established prior to the radiation. Nevertheless, tens of thousands of polymorphic variants apparently derived from the hybridisation are interspersed in the genomes. These loci show a striking excess of differentiation across ecological subgroups in the Lake Malawi cichlid assemblage, and parental alleles sort differentially into benthic and pelagic Malawi cichlid lineages, consistent with strong differential selection on these loci during species divergence. Furthermore, these loci are enriched for genes involved in immune response and vision, including opsin genes previously identified as important for speciation. Our results reinforce the role of ancestral hybridisation in explosive diversification by demonstrating its significance in one of the largest recent vertebrate adaptive radiations.

evolutionary biology↗

Vision using multiple distinct rod opsins in deep-sea fishes

Vertebrate vision is accomplished through a set of light-sensitive photopigments, which are located in the photoreceptors of the retina and consist of a visual opsin protein bound to a chromophore. In dim-light, vertebrates generally rely upon a single rod opsin (RH1) for obtaining visual information. By inspecting 101 fish genomes, we found that three deep-sea teleost lineages have independently expanded their RH1 gene repertoires. Amongst these, the silver spinyfin (Diretmus argenteus Johnson 1863) stands out as having the highest number of visual opsins known for animals to date (2 cone and 38 rod opsins). Spinyfins simultaneously express up to 14 RH1s encoding for photopigments with different peak spectral sensitivities ({lambda}max=448-513 nm) that cover the range of the residual daylight, as well as the bioluminescence spectrum present in the deep-sea. Our findings present novel molecular and functional evidence for the recurrent evolution of multiple rod opsin-based vision in vertebrates.\n\nSHORT ABSTRACTContrary to the single rod opsin used by most vertebrates, some fishes use multiple rod opsins for vision in the dimly lit deep-sea.

evolutionary biology↗

The most developmentally truncated fishes show extensive Hox gene loss and miniaturized genomes

Hox genes play a fundamental role in regulating the embryonic development of all animals. Manipulation of these transcription factors in model organisms has unraveled key aspects of evolution, like the transition from fin to limb. However, by virtue of their fundamental role and pleiotropic effects, simultaneous knockouts of several of these genes pose significant challenges. Here, we report on evolutionary simplification in two species of the dwarf minnow genus Paedocypris using whole genome sequencing. The two species feature unprecedented Hox gene loss and genome reduction in association with their massive developmental truncation. We also show how other genes involved in the development of musculature, nervous system, and skeleton have been lost in Paedocypris, mirroring its highly progenetic phenotype. Further, we identify two mechanisms responsible for genome streamlining: severe intron shortening and reduced repeat content. As a naturally simplified system closely related to zebrafish, Paedocypris provides novel insights into vertebrate development.

genomics↗

Bayesian divergence-time estimation with genome-wide SNP data of sea catfishes (Ariidae) supports Miocene closure of the Panamanian Isthmus

The closure of the Isthmus of Panama has long been considered to be one of the best defined biogeographic calibration points for molecular divergence-time estimation. However, geological and biological evidence has recently cast doubt on the presumed timing of the initial isthmus closure around 3 Ma but has instead suggested the existence of temporary land bridges as early as the Middle or Late Miocene. The biological evidence supporting these earlier land bridges was based either on only few molecular markers or on concatenation of genome-wide sequence data, an approach that is known to result in potentially misleading branch lengths and divergence times, which could compromise the reliability of this evidence. To allow divergence-time estimation with genomic data using the more appropriate multi-species coalescent model, we here develop a new method combining the SNP-based Bayesian species-tree inference of the software SNAPP with a molecular clock model that can be calibrated with fossil or biogeographic constraints. We validate our approach with simulations and use our method to reanalyze genomic data of Neotropical army ants (Dorylinae) that previously supported divergence times of Central and South American populations before the isthmus closure around 3 Ma. Our reanalysis with the multi-species coalescent model shifts all of these divergence times to ages younger than 3 Ma, suggesting that the older estimates supporting the earlier existence of temporary land bridges were artifacts resulting at least partially from the use of concatenation. We then apply our method to a new RAD-sequencing data set of Neotropical sea catfishes (Ariidae) and calibrate their species tree with extensive information from the fossil record. We identify a series of divergences between groups of Caribbean and Pacific sea catfishes around 10 Ma, indicating that processes related to the emergence of the isthmus led to vicariant speciation already in the Late Miocene, millions of years before the final isthmus closure.

evolutionary biology↗