Project

adaptive radiation; cichlid fish; speciation; phylogenomics; population genomics

Lead
Bei weitem die schnellste Rate von Artbildung wurde bei Buntbarschen im afrikanischen Viktoriasee nachgewiesen. Sie ermöglichte die Entstehung eines der artenreichsten Ökosysteme der Welt in nur wenigen zehntausend Jahren. Die genomischen Grundlagen dieser jungen Artenvielfalt sind noch nie vergleichend untersucht worden. Unser Projekt leistet dazu einen Beitrag.
Lay summary
Grosse Artenradiationen sind Ikonen der Evolutionsbiologie, besonders dann wenn sie in geologisch junger Zeit entstanden sind. Ihr Studium kann uns über das Entstehen und Vergehen von Artenvielfalt lehren, und darüber warum einige Tier- und Pflanzengruppen viel artenreicher werden als andere. Seitdem die Vorfahren der Viktoriabuntbarsche vor nur 15'000 Jahren in den sich damals gerade füllenden Viktoriasee einwanderten, entstanden 500 neue Arten mit den verschiedensten Erscheinungsbildern, Verhaltensweisen und ökologischen Anpassungen. Das ist die schnellste Artbildungsrate, die je bei Tieren festgestellt wurde, und lies eines der artenreichsten Ökosysteme der Erde entstehen. Ziel unseres Projektes ist es, Veränderungen in den Genomen der Buntbarsche zu charakterisieren, die mit dieser Diversifizierung einhergingen. Wir sequenzieren die gesamten Genome von mehreren hundert Buntbarschen verschiedenster Arten. Wir sequenzieren aber auch die Arten, die wahrscheinlich die direkten Nachkommen der damaligen Einwanderer sind und heute noch unverändert in anderen Gewässern leben, sowie Buntbarsche anderer Evolutionslinien, die in sehr ähnlichen Lebensräumen leben ohne sich aber in neue Arten aufgespalten zu haben. Wir möchten herausfinden, welche Gene für die Artbildung, und welche für ökologische Anpassungen verantwortlich sind, und wie diese im Genom gekoppelt werden, eine Voraussetzung für die Entstehung und Koexistenz von Arten. Wir möchten auch wissen, was der Ursprung der grossen genetischen Vielfalt ist. Waren die Vorfahren vielleicht bereits ungewöhnlich genetisch variabel und wie kam das? Könnte das Fehlen entsprechender Variation das Ausbleiben von Artbildung bei anderen Gruppen erklären? Wir rekonstruieren auch die zeitliche Abfolge der Geschehnisse in der Radiation um die Interaktion ökologischer und evolutionärer Mechanismen zu verstehen. Letztlich wird unser Projekt zu einem besseren Verständnis eines global einmaligen Biodiversitätshotspots beitragen.

Direct link to Lay Summary

Last update: 19.08.2016

Data from: The ecological and genomic basis of explosive adaptive radiation

Author	McGee, Matt
Publication date	21.09.2020
Persistent Identifier (PID)	https://doi.org/10.5061/dryad.fn2z34tr0
Repository	Dryad
Abstract

Rates of speciation vary tremendously among evolutionary lineages, with our understanding of what fuels the rapid succession of speciation events within young adaptive radiations remaining particularly incomplete. The cichlid fish family provides the most notable example of such variation among extant metazoans. It includes many slowly speciating lineages as well as the several exceptionally large and rapid adaptive radiations. By reconstructing a large phylogeny of all described cichlid species, we show that explosive speciation is solely concentrated in several large yet young lake species flocks. Across the family, speciation rate increases are associated with absence of top predators, and speciation rate decreases are associated with arid climate, but these factors are not nearly sufficient to explain explosive speciation in lake radiations, in particular the Lake Victoria adaptive radiation. Across lake radiations we observe a positive relationship between speciation rate and enrichment with large indel polymorphisms. Assembly of one hundred Victorian cichlid genomes comprising all extant ecological guilds and taxonomic genera reveals this radiation contains exceptional ‘genomic potential’ - hundreds of ancient haplotypes bearing indel polymorphisms, many of which are strongly associated with specific ecologies and are shared with ecologically similar species from other older lake radiations elsewhere in Africa. Network analysis reveals fundamentally non-treelike evolution through recombining old haplotypes, with origins of ecological guilds concentrated early in the Victoria radiation. Our results suggest that the combination of ecological opportunity, sexual selection and exceptional genomic potential is the key to understanding explosive adaptive radiation.

Haplochromine cichlids: Lake Victoria cichlid ecological diversity

Author	McGee, Matt
Publication date	19.04.2020
Persistent Identifier (PID)	PRJNA626405 ID: 626405
Repository	NCBI
Abstract

This project contains short-read sequencing data from 100 species of cichlid from Lake Victoria and the nearby Kyoga Basin that together comprise the full range of extant ecological diversity for this classic example of adaptive radiation.

Data from: Genomics of parallel ecological speciation in Lake Victoria cichlids

Author	Meier, Joana
Publication date	19.03.2019
Persistent Identifier (PID)	https://doi.org/10.5061/dryad.8p6m07g
Repository	Dryad
Abstract

The genetic basis of parallel evolution of similar species is of great interest in evolutionary biology. In the adaptive radiation of Lake Victoria cichlid fishes, sister species with either blue or red-back male nuptial coloration have evolved repeatedly, often associated with shallower and deeper water, respectively. One such case are blue and red-backed Pundamilia species, for which we recently showed that a young species pair may have evolved through “hybrid parallel speciation”. Coalescent simulations suggested that the older species P. pundamilia (blue) and P. nyererei (red-back) admixed in the Mwanza Gulf and that new “nyererei-like” and “pundamilia-like” species evolved from the admixed population. Here, we use genome scans to study the genomic architecture of differentiation, and assess the influence of hybridization on the evolution of the younger species pair. For each of the two species pairs, we find over 300 genomic regions, widespread across the genome, which are highly differentiated. A subset of the most strongly differentiated regions of the older pair are also differentiated in the younger pair. These shared differentiated regions often show parallel allele frequency differences, consistent with the hypothesis that admixture-derived alleles were targeted by divergent selection in the hybrid population. However, two thirds of the genomic regions that are highly differentiated between the younger species are not highly differentiated between the older species, suggesting independent evolutionary responses to selection pressures. Our analyses reveal how divergent selection on admixture-derived genetic variation can facilitate new speciation events.

The coincidence of ecological opportunity with hybridization explains rapid adaptive radiation in Lake Mweru cichlids

Author	Meier, Joana
Publication date	17.09.2019
Persistent Identifier (PID)	https://zenodo.org/record/3435419#.YKbI66gzZPY
Repository	Zenodo
Abstract

This dataset contains all the underlying data and scripts used for the publication by Meier et al., 2019, in Nature Communications on "The coincidence of ecological opportunity with hybridization explains rapid adaptive radiation in Lake Mweru cichlids".This package contains the R scripts and all input files to produce Figures 2-4, Supplementary Figures 3, 6-8, and Supplementary Data 1. It contains the morphology data, the D statistics used for plotting, the genomic data files used for generating PCA plots, the fineRADstructure output files, the BEAST trees with all calibration sets, the RAD variant calls, the mitochondrial D-loop alignment, and the mitochondrial and RAD RAxML trees. For more information, see Meier et al., 2019, Nature Communications.

Haplochromine cichlid fishes from Lake Mweru, Lake Bangweulu and adjacent rivers Raw sequence reads

Author	Meier, Joana
Publication date	10.07.2019
Persistent Identifier (PID)	PRJNA553794 ID: 553794
Repository	NCBI
Abstract

RAD tag reads of haplochromine cichlids from Lakes Mweru and Bangweulu and adjacent rivers associated with the study "The coincidence of ecological opportunity with hybridization explains the prevalence of rapid adaptive radiation"

Genetic architecture of a key reproductive isolation trait differs between sympatric and non-sympatric sister species of Lake Victoria cichlids

Author	Feller, Anna
Publication date	25.03.2020
Persistent Identifier (PID)	https://doi.org/10.5061/dryad.5tb2rbp1n
Repository	Dryad
Abstract

One hallmark of the East African cichlid radiations is the rapid evolution of reproductive isolation that is robust to full sympatry of many closely related species. Theory predicts that species persistence and speciation in sympatry with gene flow are facilitated if loci of large effect or physical linkage (or pleiotropy) underlie traits involved in reproductive isolation. Here we investigate the genetic architecture of a key trait involved in behavioural isolation, male nuptial coloration, by crossing two sister species pairs of Lake Victoria cichlids of the genus Pundamilia and mapping nuptial coloration in the F2 hybrids. One is a young sympatric species pair, representative of an axis of colour motif differentiation, red-dorsum vs blue, that is highly recurrent in closely related sympatric species. The other is a species pair representative of colour motifs, red-chest vs blue, that are common in allopatric but uncommon in sympatric closely related species. We find significant QTLs with moderate to large effects (some overlapping) for red and yellow in the sympatric red-dorsum x blue cross, whereas we find no significant QTLs in the non-sympatric red-chest x blue cross. These findings are consistent with theory predicting that large effect loci or linkage/pleiotropy underlying mating trait differentiation could facilitate speciation and species persistence with gene flow in sympatry.

Data from: Rapid generation of ecologically relevant behavioural novelty in experimental cichlid hybrids

Author	Feller, Anna
Publication date	13.08.2020
Persistent Identifier (PID)	https://doi.org/10.5061/dryad.280gb5mn7
Repository	Dryad
Abstract

The East African cichlid radiations are characterised by repeated and rapid diversification into many distinct species with different ecological specialisations and by a history of hybridization events between non-sister species. Such hybridization might provide important fuel for adaptive radiation. Interspecific hybrids can have extreme trait values or novel trait combinations and such transgressive phenotypes may allow some hybrids to explore ecological niches neither of the parental species could tap into. Here, we investigate the potential of second-generation (F2) hybrids between two generalist cichlid species from Lake Malawi to exploit a resource neither parental species is specialised on: feeding by sifting sand. Some of the F2 hybrids phenotypically resembled fish of species that are specialised on sand sifting. We combined experimental behavioural and morphometric approaches to test whether the F2 hybrids are transgressive in both morphology and behaviour related to sand sifting. We then performed a quantitative trait loci (QTL) analysis using RADseq markers to investigate the genetic architecture of morphological and behavioural traits. We show that transgression is present in several morphological traits, that novel trait combinations occur, and we observe transgressive trait values in sand sifting behaviour in some of the F2 hybrids. Moreover, we find QTLs for morphology and for sand sifting behaviour, suggesting the existence of some loci with moderate to large effects. We demonstrate that hybridization has the potential to rapidly generate novel and ecologically relevant phenotypes that may be suited to a niche neither of the parental species occupies. Interspecific hybridization may thereby contribute to the rapid generation of ecological diversity in cichlid radiations.

Data from: Interspecific hybridization can generate functional novelty in cichlid fish

Author	Selz, Oliver
Publication date	14.10.2019
Persistent Identifier (PID)	https://doi.org/10.5061/dryad.m25t886
Repository	Dryad
Abstract

The role of interspecific hybridization in evolution is still being debated. Interspecific hybridization has on the one hand been suggested to facilitate the evolution of ecological novelty and hence the invasion of new niches and adaptive radiation when ecological opportunity is present beyond the parental species niches. On the other hand, hybrids between two ecologically divergent species may perform less well than parental species in their respective niches because hybrids would be intermediate in performance in both niches. The evolutionary consequences of hybridization may hence be context-dependent, depending on whether additional ecological opportunities do or do not exist. Surprisingly, these complementary predictions may never have been tested in the same experiment in animals. To do so, we investigate if hybrids between ecologically distinct cichlid species perform less well than the parental types when feeding on food either parental species are adapted to, and if the same hybrids perform better compared to their parents when feeding on food none of the species are adapted to. We generated two first-generation experimental hybrid crosses between species of African cichlids. In feeding efficiency experiments we measure the performance of hybrids and parental species on food types representing both parental species niches and additional ‘novel’ niches, not utilized by part of the parental species but by other species in the African cichlid radiations. We found that hybrids can have higher feeding efficiencies on the ‘novel’ food types but typically have lower efficiencies on parental food types when compared to parental species. This suggests that hybridization can generate functional variation that can be of ecological relevance allowing the access to resources outside of either parental species niche. Hence, we provide support for the hypothesis of ecological context-dependency of the evolutionary impact of interspecific hybridization.

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Number	Title	Start	Funding scheme

Large and rapid adaptive radiations are iconic textbook examples of evolution in action. When analyzed in an appropriate comparative context, they become powerful systems to investigate and identify causes of variation in rates and patterns of diversification among evolutionary lineages. When cichlid fishes colonized a newly refilled Lake Victoria 15,000 years ago, they diversified into more than 500 species. This is one of the fastest rates of speciation ever documented in animals. Learning how the genomes of these cichlids interacted with environmental and intrinsic drivers of evolution during this radiation will shed light on the evolution of species diversity in general. When compared to other taxa in similar environmental situations, it will also elucidate how constraints to diversification can be overcome. Together with colleagues, we have recently generated five fully annotated reference genomes of African cichlid fish, including one from Lake Victoria. We have also generated extensive population genomic data for several Lake Victoria cichlid species using reduced representation library sequencing methods, and most recently we have sequenced whole genomes of eight further species. In order to more fully understand both the evolutionary processes of species diversification and the genomic mechanisms underlying these processes, we now need whole genome sequence information from many species across the radiation. In this project we propose to reconstruct the evolutionary history of the Lake Victoria radiation by sequencing more than 120 of the 500 known species of Lake Victoria cichlids. We will also use genomic sequence data to reconstruct relationships for several small radiations in isolated lakes that were colonized either by populations descending from the same admixed ancestry as the Victoria radiation, or that descended from one of the lineages that admixed in the history of the Lake Victoria region superflock. Reconstructing the phylogenetic history of radiations in Lake Victoria and those in the smaller lakes will allow us to test important hypotheses about the dynamics of adaptive radiation, such as the temporal sequence in the origination of major ecotypic groups (the “stages of radiation” hypothesis), the extent of parallel speciation at different geographical and time scales, and will allow us, for the first time in a large recent cichlid radiation, to test for a slowdown in speciation and phenotypic evolution rates as would be predicted by ecological limits to evolving species richness. The comparison of radiations with different ancestries will then allow us to understand how a history of admixture has affected these dynamics and shaped the outcomes of cichlid radiation.Using population genomic analyses to infer species and clade-level demographic histories, we will infer demographic parameters for key phases in the radiations and for individual speciation events. We will use these inferences to test predictions made by alternative evolutionary models for speciation and adaptive radiation (speciation in sympatry versus intralacustrine allopatry, speciation in small populations with founder effects versus speciation in large populations, divergent selection, gene flow, hybrid speciation). We shall seek to characterize the genomic elements involved in speciation and post-speciation adaptive radiation in terms of genetic incompatibilities, adaptation-related and sexually selected genes. We will examine if the same elements are repeatedly involved in species differentiation, and at which level such parallelism occurs (SNP, gene, pathway). Finally, we will infer the sources of genetic variants from standing variation within one ancestral population, ancestral admixture between species, and de novo mutation within the radiation. We will use this data to test components of the hybrid swarm origin and syngameon hypotheses of adaptive radiation.