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Prof. Dr. Walter Salzburger

Department of Environmental Sciences
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The evolutionary and ecological context of adaptive radiation in cichlid and other fishes from Lake Tanganyika

Research Project  | 1 Project Members

Adaptive radiation - the rapid origination of a set of ecologically and morphologically highly distinct species within an organismal lineage resulting from their adaptation to different habitat and/or feeding niches - is arguably one of the most intriguing evolutionary processes and thought to be responsible for much of the diversity of life on Earth. In line with this, the investigation of exceptional instances of adaptive radiation, such as the 'Cambrian explosion', Darwin's finches on Galápagos, the Caribbean anole lizards, and the cichlid fishes in the African Great Lakes, has shaped our understanding of the patterns and processes of organismal diversification. However, such outbursts of diversity have typically been examined as stand-alone packages without taking into consideration other groups of organisms that co-occur with the radiating lineages in the same - in most cases insular - environments, yet have not diversified (much). Here I propose to put the massive adaptive radiation of cichlid fishes in Lake Tanganyika, which I have studied in detail over the past two decades, into the context of the ecology and evolution of the entire fish fauna of this oldest lake in Africa. More specifically, through the in-depth and comparative taxonomic, genealogical, phenotypic, and ecological investigation of all species of fishes living in Lake Tanganyika, we intend to test predictions derived from theoretical and empirical research related to the phenomenon of adaptive radiation, focusing, among others, on the 'stages-model', the 'hybrid-swarm' hypothesis, and the 'phenotype-environment correlation' criterion. In addition, I propose to intensify the genomic investigation of the cichlids in comparison to these other groups of fishes, with a particular emphasis on sensory-system and immune-related genes. Taking advantage of the unique natural experiment going on in Lake Tanganyika, where representatives of 23 families spanning the entire phylogenetic spectrum of fishes ended up together in a single insular ecosystem, we should thus be able to identify the causal factors responsible for the various evolutionary trajectories that these different evolutionary lineages of fishes took, ultimately leading to the vastly different numbers of species and the great differences in eco-morphological disparity among these clades. This, in turn, will bring us a good deal further in answering the question what is so special about the cichlids.

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DIFFER

Research Project  | 2 Project Members

Genetic diversity - that is, the genomic variation among individuals of a given species - is pivotal for adaptation to environmental alterations and an important factor for ecosystem resilience. Yet, the determinants of genetic diversity remain poorly understood. Population size is often used as a proxy for genetic diversity, but the amount of genetic variation within populations is not always reflected by their population size. Instead, factors such as linked selection, the recombination-, mutation-, and speciation rate, or life history and ecological traits may be more strongly connected to genetic diversity. So far, the interplay of all these parameters has not been empirically investigated, so that their relative contributions to genetic diversity are unknown. In DIFFER!, I propose to thoroughly examine the role of all these potential determinants of genetic diversity by means of combining cutting-edge genomic techniques with a highly suitable model system: the more than 200 endemic cichlid fish species of the East African Lake Tanganyika. Owing to their great morphological and behavioral variation, contrasting speciation rates, and their recent radiation, these fishes offer an ideal framework for comparative analyses. Availability of long-read reference assemblies, recombination maps, a massive dataset of underwater photographs for estimating census population sizes, together with population sequencing of selected species and family-based 'trio' sequencing will enable me to investigate specifically the interplay between genetic diversity and (i) life history and ecological traits, (ii) speciation and hybridization rates, and (iii) mutation rates, while at the same time controlling for variation in population size, selection, and recombination. The results of this project will contribute towards the understanding of organismal evolution and provide a new basis for the evaluation of genetic diversity in ecosystem management.

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Molecular evolution and ontogenetic development of dietary adaptations in vertebrates at the micro- and macro-evolutionary scale

Research Project  | 3 Project Members

Die Erschliessung neuer Nahrungsquellen - etwa durch Anpassungen in der Nahrungsaufnahme und -verwertung - spielt eine wichtige Rolle bei der Entstehung neuer Arten und trägt somit zum Erhalt der biologischen Vielfalt auf unserem Planeten bei. Im Rahmen unseres Sinergia Projektes untersuchen wir die damit einhergehenden morphologischen, physiologischen und genomischen Veränderungen im Verdauungssystem zweier artenreicher Wirbeltiergruppierungen, den Buntbarschen und den Säugetieren. Wir setzen dabei auf modernste Technologien im Bereich der vergleichenden und funktionellen Genomik sowie auf 3D-bildgebende Verfahren. Unser experimenteller Ansatz wird es uns erlauben, die zugrundeliegenden molekularen Vorgänge auf der Ebene einzelner Zellen des Verdauungstraktes zu untersuchen; zu testen, inwiefern diese Vorgänge flexibel auf unterschiedliche Nahrung reagieren; und die Ergebnisse mit der in der Evolution entstandenen Ernährungsformen der Arten - die sich in Fleisch- oder Pflanzenfresser, Generalisten oder Spezialisten aufteilen - in Beziehung zu setzen.

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Molecular evolution and ontogenetic development of dietary adaptations in vertebrates at the micro- and macro-evolutionary scale

Research Project  | 2 Project Members

Dietary adaptations — that is, all adaptations related to how nutrients are acquired and processed — play a central role in the evolution and maintenance of organismal diversity on Earth in general and in adaptive radiations of species in particular. In vertebrates, the trophic process can be divided into two fundamental components: food uptake and digestion. Through a timely combination of state-of-the-art genomics technologies and broad phylogenetic sampling, it is now possible to elucidate the molecular and developmental underpinnings of both feeding-related structures (e.g., jaws or teeth) and the digestive system at unprecedented resolution, as well as to evaluate their contributions to adaptation and diversification.

In the framework of this Sinergia proposal, we put forward an interdisciplinary and integrative approach, focusing our efforts towards a comprehensive understanding of dietary adaptations in the digestive system. Our multi-faceted approach is only possible through the joint expertise, research infrastructure, methodological skill-set, and biological samples of the consortium labs, thereby allowing each lab to expand substantially beyond their previous lines of research. Specifically, we propose a systematic and large-scale survey of dietary adaptations and their underlying morphological, cellular and gene regulatory changes across feeding strategies, key digestive organs (intestine and liver) and developmental stages in two prominent evolutionary radiations in vertebrates — of cichlid fishes from Lake Tanganyika and eutherian mammals — that cover both short (<6-9 million years, cichlids) and long (=75 million years, mammals) evolutionary time scales.

Our work plan is guided by a number of specific hypotheses. First, we hypothesize that digestive organ adaptations typically arise late in development, facilitated by decreased selective constraints. Second, while all major mutational types likely contributed to dietary adaptations in both cichlids and mammals, we conjecture that the predominant mutational mechanism is cis-regulatory changes in old genes in cichlids, as the short radiation time in this clade likely limited the accumulation of less rapidly accumulating coding mutations. Third, we predict that dietary novelties involved evolutionary changes in gene expression programs and the cellular composition of the digestive organs, and that all mutational types contributed to cell compositional changes. However, we surmise that new gene origination was key for the emergence of novel cell types, and that new cell types played a more prominent role for intestine than liver adaptations. Fourth, we hypothesize that the mechanisms and degree of phenotypic plasticity, leading to differences in intestine/liver anatomy and function, vary across development (i.e., more plasticity later in development) and between the two radiations (i.e., higher morphological plasticity in cichlids, but similar contributions of gene expression changes to phenotypic plasticity in cichlids and mammals). Finally, we note that our analyses of the unique and novel datasets generated in the proposed project will allow us to assess various general questions in an exploratory fashion, which will result in novel hypotheses to be tested in the future.

Our current predictions, research questions, and anticipated novel hypotheses, will be evaluated in the framework of four complementary goals. First, we will scrutinize the morphological features of the digestive system across development of representative cichlids using computed tomography scans and histological methods, which will set the stage for all subsequent molecular/cellular comparisons among cichlids and between cichlids and mammals. Second, we will generate and analyze extensive bulk and single-cell transcriptome data for the intestine and liver across development and adult stages of representative cichlids and mammals. We will thus trace evolutionary changes of gene expression programs and cellular compositions that underlie digestive organ innovations. Third, we will generate matched single-cell epigenomic datasets to explore the gene regulatory foundations of digestive organ development and adaptation. Finally, we will carry out dedicated feeding experiments in selected cichlids and a mammal (rat) to assess the extent to which adaptations may rapidly occur through phenotypic plasticity (i.e., developmental plasticity at the morphological, cellular, and molecular levels) rather than "hard-wired" genetic changes in the two vertebrate groups, respectively.

By contextualizing our anticipated results within the frameworks of dietary ecology and comparative digestive physiology, our work will substantially advance our understanding of the molecular, cellular and morphological evolution of dietary adaptations across different timescales and thus provide a novel and unique perspective on the evolution of vertebrates, including our own species.

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The shaping of genetic diversity as prerequisite for ecosystem resilience

Research Project  | 1 Project Members

Die genetische Vielfalt - sprich die Variation der Erbanlagen zwischen Individuen einer bestimmten Art - ist entscheidend für das Anpassungspotential dieser Art an Umweltveränderungen, und damit ein wichtiger Faktor für die Widerstandsfähigkeit ganzer Ökosysteme. Eine grosse genetische Vielfalt erhöht die Wahrscheinlichkeit, dass Arten Individuen mit Erbanlagen beinhalten, die sich unter veränderten Umweltbedingungen als vorteilhaft erweisen, und somit das Überleben dieser Art ermöglichen. Dennoch wissen wir wenig über die Faktoren, welche die genetische Vielfalt beeinflussen. Häufig wird die Populationsgrösse - also die Individuenanzahl einer Art in einem bestimmten geografischen Gebiet - als Indikator für die genetische Vielfalt verwendet, aber die Höhe der genetischen Vielfalt spiegelt sich nicht immer in der Populationsgrösse wider. Stattdessen können andere Faktoren, wie das Ausmass an genetischer Selektion, die Rekombinations-, Mutations- oder Artbildungsraten, sowie biologische und ökologischen Artmerkmale die genetische Vielfalt massgeblich bestimmen. Das Zusammenspiel all dieser Parameter ist jedoch bisher nicht empirisch untersucht worden. Das Ziel dieses Projektes ist es daher, die Rolle dieser potenziellen Bestimmungsfaktoren der genetischen Vielfalt zu untersuchen. Hierfür werden modernste genomische Methoden auf ein besonders geeignetes Modellsystem, die mehr als 200 endemischen Buntbarschenarten des ostafrikanischen Tanganjikasees, angewendet. Durch ihre grosse Vielfalt und durch die relative junge Artenaufspaltung bieten diese Fische einen idealen Rahmen für die vorgesehenen vergleichenden Analysen. Die Ergebnisse dieses Projekts werden zum besseren Verständnis der Evolution beitragen und eine neue Grundlage für die Bewertung der genetischen Vielfalt im Ökosystem-Management liefern. Durch Kenntnis der grössten Bestimmungsfaktoren der genetischen Vielfalt lassen sich neue Managementleitlinien und Arterhaltungsstrategien entwickeln, welche zum Schutz gesunder Ökosysteme beitragen können.

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The genomic basis of divergence and convergence in fish species-flocks

Research Project  | 1 Project Members

Convergent evolution - i.e. , the recurrent evolution of similar morphological types on different branches in the tree of life - is a pervasive phenomenon, urging generations of evolutionary biologists since Darwin to address the question, Why and how evolution repeats itself? Here, I propose to investigate the molecular and ecological underpinnings of the recurrent evolution of convergent species pairs of cichlid fish in the East African Great Lakes Malawi and Tanganyika, representing some of the most iconic and striking examples of this phenomenon. The observation that the convergent cichlid species pairs in sister-lakes Malawi and Tanganyika resemble each other not only in overall body shape, but in minute details of their phenotype as well as in coloration, is in the center of the debate on whether natural selection is sufficient to explain such a degree of convergence, or whether some sort of developmental or genetic constraint is influencing the way that phenotypes are generated in nature. In a first step, we will make use of hundreds of already available whole-genome DNA sequences, conduct additional DNA and transcriptome sequencing from population samples of convergent species, and use cutting-edge computational tools to establish the molecular foundation of convergent evolution in East African cichlids. This will be accompanied by an in-depth morphological and ecological examination of the convergent forms. In addition, I plan to extend the examination of the causal factors of convergent evolution towards both ends of the phylogenetic spectrum. Specifically, I propose to also study convergence within the cichlid species-flocks of lakes Malawi and Tanganyika including species that repeatedly diverged along a lake-stream environmental gradient, as well as convergence between African lake cichlids and their eco-morphologically most comparable counterpart in the marine realm, a fish community inhabiting a coral reef. Thus, we will provide what is among the first integrative, well-powered, and genome-wide analysis of convergent evolution across both cichlids and related teleosts. Our experimental design will allow us to ( i ) evaluate the relative contribution of natural selection versus developmental constraints to convergent evolution; ( ii ) examine whether convergent (involving distantly related taxa) and parallel evolution (involving more closely related taxa) are fundamentally distinct processes; and ( iii ) assess whether or not there are common features in organismal diversification in fish species-flocks.

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Scientific Drilling at Lake Tanganyika, Africa: A Transformative Record for Understanding Evolution in Isolation and the Historical Biology of the African Continent

Research Project  | 1 Project Members

With this proposal we propose to hold a workshop at the University of Basel in June 2016 to develop a strategy for conducting evolutionary biology and paleobiology (including ancient genomics) research on sediment drill cores to be collected from Lake Tanganyika, Africa. The Lake Tanganyika ecosystem is a textbook example of evolution and biological diversification in isolation, a result of its great antiqui- ty (over 10 million years) and persistence as a freshwater body (Salzburger et al, 2014). Over its long history, a rich and continuous fossil record of this evolutionary system has accumulated on the lake's floor. In collaboration with a large interdisciplinary team of international scientists, we propose to tap this historical record to understand how the ecosystems of both Lake Tanganyika and its surrounding watershed has developed. Scientific drilling on the African Great Lakes has already yielded exciting scientific payoffs in the fields of paleoclimate and paleoecological research, by extending our detailed understanding of African environmental change over a million years (e.g. Cohen et al., 2007; Lyons et al., 2015). With a drilling project at the oldest African lake, Lake Tanganyika, we have the opportunity to vastly increase both the research scope and temporal duration of these records. Fish and invertebrate fossils from Lake Tanganyika drill cores promise to provide both skeletal body fossils and ancient DNA records of the extraordinary endemic organisms found in this lake. When coupled with the precise geochronology and paleoenvi- ronmental records obtained from the same cores we have the op- portunity to produce transformative breakthroughs in understand the dynamics of adaptive radiations. In addition, the vegetation (pollen and phytoliths) and charcoal records from the cores will vastly improve our understanding of terrestrial ecosystem evolution in trop- ical Africa over the late Neogene, which is critical for understanding the context of our own species. That is, deep scientific drilling into the lake floor of Tanganyika will provide a climatological and environmental record that covers - in unprecedented precision - the entire time span of human evolution, starting from the human-chimp split, and in the very ge- ographic region where this event has happened.

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On the periphery: Does peripatric speciation promote rainforest diversity in east africa?

Research Project  | 5 Project Members

Speciation, or the process by which new species arise, is a fundamental topic in biology. Despite over a century of study it still remains relatively poorly understood, particularly in terms of the main mechanisms that determine how populations become reproductively isolated. With the advent of phylogenomics and fine scale spatial tools, such as Geographic Information System (GIS) data, we can now conduct comparative analyses into the main causal factors that drive speciation. In order to understand whether specific speciation patterns are pervasive in a system, analyses of independently derived species are necessary to see whether common patterns can be observed. Amphibians have been used extensively to study the biogeographic and phylogenetic signals left by past speciation events and here we investigate whether the dispersal of a small number of peripheral individuals into a new habitat, has resulted in the origin of new species. The Eastern Arc Mountains (EAM) of Tanzania boast exceptional amphibian species richness, believed to be largely the result of repeated allopatric speciation through vicariance events. However, recent molecular studies have shown that some of the endemic montane rainforest taxa in this biodiversity hotspot are most closely related to widespread species in the adjacent lowlands and so whether these mountains act only as museums, harbouring refugial relicts of past habitat expansions and contractions, or whether they continue to promote speciation through colonization from surrounding lowland areas followed by adaptation and divergence is not yet clearly understood. By applying ecological niche modelling and next-generation sequencing to characterize the spatial and genomic makeup of East African amphibians, we wish to investigate whether a low number of founder individuals from lowland species dispersing onto the rainforests of the EAM and adapting to new habitats has repeatedly promoted the formation of new species. The results of this study will have important implications for our understanding of how dispersal and adaptation can lead to speciation without vicariance events and why certain areas such as the EAM are more species rich than others. In turn the findings might highlight the importance of non-EAM regions for promoting speciation, as has been outlined in other regions of Africa ( sensu Ecotones) and by implication that these areas also deserve attention in evolutionary and conservation studies for contributing to rainforest diversity.