Walter Salzburger

Sympatric speciation in Nicaraguan crater lake cichlid fish

Sympatric speciation, the formation of species in the absence of geographical barriers, remains one of the most contentious concepts in evolutionary biology. Although speciation under sympatric conditions seems theoretically possible, empirical studies are scarce and only a few credible examples of sympatric speciation exist. Here we present a convincing case of sympatric speciation in the Midas cichlid species complex (Amphilophus sp.) in a young and small volcanic crater lake in Nicaragua. Our study includes phylogeographic, population-genetic (based on mitochondrial DNA, microsatellites and amplified fragment length polymorphisms), morphometric and ecological analyses. We find, first, that crater Lake Apoyo was seeded only once by the ancestral high-bodied benthic species Amphilophus citrinellus, the most common cichlid species in the area; second, that a new elongated limnetic species (Amphilophus zaliosus) evolved in Lake Apoyo from the ancestral species (A. citrinellus) within less than ∼10,000u2009yr; third, that the two species in Lake Apoyo are reproductively isolated; and fourth, that the two species are eco-morphologically distinct.

Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes.

BackgroundThe adaptive radiations of cichlid fishes in East Africa are well known for their spectacular diversity and their astonishingly fast rates of speciation. About 80% of all 2,500 cichlid species in East Africa, and virtually all cichlid species from Lakes Victoria (~500 species) and Malawi (~1,000 species) are haplochromines. Here, we present the most extensive phylogenetic and phylogeographic analysis so far that includes about 100 species and is based on about 2,000 bp of the mitochondrial DNA.ResultsOur analyses revealed that all haplochromine lineages are ultimately derived from Lake Tanganyika endemics. We find that the three most ancestral lineages of the haplochromines sensu lato are relatively species poor, albeit widely distributed in Africa, whereas a fourth newly defined lineage – the modern haplochromines – contains an unparalleled diversity that makes up more than 7% of the worlds ~25,000 teleost species. The modern haplochromines ancestor, most likely a riverine generalist, repeatedly gave rise to similar ecomorphs now found in several of the species flocks. Also, the Tanganyikan Tropheini are derived from that riverine ancestor suggesting that they successfully re-colonized Lake Tanganyika and speciated in parallel to an already established cichlid adaptive radiation. In contrast to most other known examples of adaptive radiations, these generalist ancestors were derived from highly diverse and specialized endemics from Lake Tanganyika. A reconstruction of life-history traits revealed that in an ancestral lineage leading to the modern haplochromines the characteristic egg-spots on anal fins of male individuals evolved.ConclusionWe conclude that Lake Tanganyika is the geographic and genetic cradle of all haplochromine lineages. In the ancestors of the replicate adaptive radiations of the modern haplochromines, behavioral (maternal mouthbrooding), morphological (egg-spots) and sexually selected (color polymorphism) key-innovations arose. These might be – together with the ecological opportunity that the habitat diversity of the large lakes provides – responsible for their evolutionary success and their propensity for explosive speciation.

Phylogeny of the Lake Tanganyika Cichlid Species Flock and Its Relationship to the Central and East African Haplochromine Cichlid Fish Faunas

Lake Tanganyika, the oldest of the East African Great Lakes, harbors the ecologically, morphologically, and behaviorally most complex of all assemblages of cichlid fishes, consisting of about 200 described species. The evolutionary old age of the cichlid assemblage, its extreme degree of morphological differentiation, the lack of species with intermediate morphologies, and the rapidity of lineage formation have made evolutionary reconstruction difficult. The number and origin of seeding lineages, particularly the possible contribution of riverine haplochromine cichlids to endemic lacustrine lineages, remains unclear. Our phylogenetic analyses, based on mitochondrial DNA sequences of three gene segments of 49 species (25% of all described species, up to 2,400 bp each), yield robust phylogenies that provide new insights into the Lake Tanganyika adaptive radiation as well as into the origin of the Central- and East-African haplochromine faunas. Our data suggest that eight ancient African lineages may have seeded the Tanganyikan cichlid radiation. One of these seeding lineages, probably comprising substrate spawning Lamprologus-like species, diversified into six lineages that evolved mouthbrooding during the initial stage of the radiation. All analyzed haplochromines from surrounding rivers and lakes seem to have evolved within the radiating Tanganyikan lineages. Thus, our findings contradict the current hypothesis that ancestral riverine haplochromines colonized Lake Tanganyika to give rise to at least part of its spectacular endemic cichlid species assemblage. Instead, the early phases of the Tanganyikan radiation affected Central and East African rivers and lakes. The haplochromines may have evolved in the Tanganyikan basin before the lake became a hydrologically and ecologically closed system and then secondarily colonized surrounding rivers. Apparently, therefore, the current diversity of Central and East African haplochromines represents a relatively young and polyphyletic fauna that evolved from or in parallel to lineages now endemic to Lake Tanganyika.

Convergent Evolution within an Adaptive Radiation of Cichlid Fishes

The recurrent evolution of convergent forms is a widespread phenomenon in adaptive radiations (e.g., [1-9]). For example, similar ecotypes of anoles lizards have evolved on different islands of the Caribbean, benthic-limnetic species pairs of stickleback fish emerged repeatedly in postglacial lakes, equivalent sets of spider ecomorphs have arisen on Hawaiian islands, and a whole set of convergent species pairs of cichlid fishes evolved in East African Lakes Malawi and Tanganyika. In all these cases, convergent phenotypes originated in geographic isolation from each other. Recent theoretical models, however, predict that convergence should be common within species-rich communities, such as species assemblages resulting from adaptive radiations. Here, we present the most extensive quantitative analysis to date of an adaptive radiation of cichlid fishes, discovering multiple instances of convergence in body and trophic morphology. Moreover, we show that convergent morphologies are associated with adaptations to specific habitats and resources and that Lake Tanganyikas cichlid communities are characterized by the sympatric occurrence of convergent forms. This prevalent coexistence of distantly related yet ecomorphologically similar species offers an explanation for the greatly elevated species numbers in cichlid species flocks.

The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes

The question of how genetic variation translates into organismal diversity has puzzled biologists for decades. Despite recent advances in evolutionary and developmental genetics, the mechanisms that underlie adaptation, diversification and evolutionary innovation remain largely unknown. The exceptionally diverse species flocks of cichlid fishes are textbook examples of adaptive radiation and explosive speciation and emerge as powerful model systems to study the genetic basis of animal diversification. East Africas hundreds of endemic cichlid species are akin to a natural mutagenesis screen and differ greatly not only in ecologically relevant (hence naturally selected) characters such as mouth morphology and body shape, but also in sexually selected traits such as coloration. One of the most fascinating aspects of cichlid evolution is the frequent occurrence of evolutionary parallelisms, which has led to the question whether selection alone is sufficient to produce these parallel morphologies, or whether a developmental or genetic bias has influenced the direction of diversification. Here, I review fitness‐relevant traits that could be responsible for the cichlids’ evolutionary success and assess whether these were shaped by sexual or natural selection. I then focus on the interaction and the relative importance of sexual vs. natural selection in cichlid evolution. Finally, I discuss what is currently known about the genes underlying the morphogenesis of adaptively relevant traits and highlight the importance of the forthcoming cichlid genomes in the quest of the genetic basis of diversification in this group.

Genome divergence during evolutionary diversification as revealed in replicate lake-stream stickleback population pairs.

Evolutionary diversification is often initiated by adaptive divergence between populations occupying ecologically distinct environments while still exchanging genes. The genetic foundations of this divergence process are largely unknown and are here explored through genome scans in multiple independent lake-stream population pairs of threespine stickleback. We find that across the pairs, overall genomic divergence is associated with the magnitude of divergence in phenotypes known to be under divergent selection. Along this same axis of increasing diversification, genomic divergence becomes increasingly biased towards the centre of chromosomes as opposed to the peripheries. We explain this pattern by within-chromosome variation in the physical extent of hitchhiking, as recombination is greatly reduced in chromosome centres. Correcting for this effect suggests that a great number of genes distributed widely across the genome are involved in the divergence into lake vs. stream habitats. Analyzing additional allopatric population pairs, however, reveals that strong divergence in some genomic regions has been driven by selection unrelated to lake-stream ecology. Our study highlights a major contribution of large-scale variation in recombination rate to generating heterogeneous genomic divergence and indicates that elucidating the genetic basis of adaptive divergence might be more challenging than currently recognized.

TANDEM: integrating automated allele binning into genetics and genomics workflows

SUMMARYnComputer programs for the statistical analysis of microsatellite data use allele length variation to infer, e.g. population genetic parameters, to detect quantitative trait loci or selective sweeps. However, observed allele lengths are usually inaccurate and may deviate from the expected periodicity of repeats. The common practice of rounding to the nearest whole number frequently results in miscalls and underestimations of allelic richness. Manual sorting of allele lengths into discrete classes, a process called binning, is tedious and error-prone. Here, we present a new program for the automated binning of microsatellite allele lengths to overcome these problems and to facilitate high-throughput allele binning.nnnAVAILABILITYnwww.evolution.unibas.ch/salzburger/software.htm.nnnSUPPLEMENTARY INFORMATIONnSupplementary data are available at Bioinformatics online.

The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics

With more than 3,000 species, the fish family Cichlidae is one of the most species-rich families of vertebrates. Cichlids occur in southern and central America, Africa, Madagascar, and India. The hotspot of their biodiversity is East Africa, where they form adaptive radiations composed of hundreds of endemic species in several lakes of various sizes and ages. The unparalleled species richness of East African cichlids has been something of a conundrum for evolutionary biologists and ecologists, since it has been in doubt whether these hundreds of species arose by allopatric speciation or whether it is necessary to invoke somewhat less traditional models of speciation, such as micro-allopatric, peripatric, or even sympatric speciation or evolution through sexual selection mediated by female choice. Ernst Mayr’s analyses of these evolutionary uniquely diverse species assemblages have contributed to a more direct approach to this problem and have led to a deeper understanding of the patterns and processes that caused the formation of these huge groups of species. We review here recent molecular data on population differentiation and phylogenetics, which have helped to unravel, to some extent, the patterns and processes that led to the formation and ecological maintenance of cichlid species flocks. It is becoming apparent that sexually selected traits do play an important role in speciation in micro-allopatric or even sympatric settings. Species richness seems to be roughly correlated with the surface area, but not the age, of the lakes. We observe that the oldest lineages of a species flock of cichlids are often less species-rich and live in the open water or deepwater habitats. While the species flocks of the Lake Malawai and the Lake Victoria areas were shown to be monophyletic, the cichlid assemblage of Lake Tanganyika seems to consist of several independent species flocks. Cichlids emerge as an evolutionary model system in which many fundamental questions in evolution and ecology can be tested successfully, yet for other fish species flocks the relative importance of alternative mechanisms of speciation is likely to differ from that in cichlid fish.

Novel Relationships Among Ten Fish Model Species Revealed Based on a Phylogenomic Analysis Using ESTs

The power of comparative phylogenomic analyses also depends on the amount of data that are included in such studies. We used expressed sequence tags (ESTs) from fish model species as a proof of principle approach in order to test the reliability of using ESTs for phylogenetic inference. As expected, the robustness increases with the amount of sequences. Although some progress has been made in the elucidation of the phylogeny of teleosts, relationships among the main lineages of the derived fish (Euteleostei) remain poorly defined and are still debated. We performed a phylogenomic analysis of a set of 42 of orthologous genes from 10 available fish model systems from seven different orders (Salmoniformes, Siluriformes, Cypriniformes, Tetraodontiformes, Cyprinodontiformes, Beloniformes, and Perciformes) of euteleostean fish to estimate divergence times and evolutionary relationships among those lineages. All 10 fish species serve as models for developmental, aquaculture, genomic, and comparative genetic studies. The phylogenetic signal and the strength of the contribution of each of the 42 orthologous genes were estimated with randomly chosen data subsets. Our study revealed a molecular phylogeny of higher-level relationships of derived teleosts, which indicates that the use of multiple genes produces robust phylogenies, a finding that is expected to apply to other phylogenetic issues among distantly related taxa. Our phylogenomic analyses confirm that the euteleostean superorders Ostariophysi and Acanthopterygii are monophyletic and the Protacanthopterygii and Ostariophysi are sister clades. In addition, and contrary to the traditional phylogenetic hypothesis, our analyses determine that killifish (Cyprinodontiformes), medaka (Beloniformes), and cichlids (Perciformes) appear to be more closely related to each other than either of them is to pufferfish (Tetraodontiformes). All 10 lineages split before or during the fragmentation of the supercontinent Pangea in the Jurassic.

Case studies and mathematical models of ecological speciation. 1. Cichlids in a crater lake

A recent study of a pair of sympatric species of cichlids in Lake Apoyo in Nicaragua is viewed as providing probably one of the most convincing examples of sympatric speciation to date. Here, we describe and study a stochastic, individual‐based, explicit genetic model tailored for this cichlid system. Our results show that relatively rapid (< 20 000 generations) colonization of a new ecological niche and (sympatric or parapatric) speciation via local adaptation and divergence in habitat and mating preferences are theoretically plausible if: (i) the number of loci underlying the traits controlling local adaptation, and habitat and mating preferences is small; (ii) the strength of selection for local adaptation is intermediate; (iii) the carrying capacity of the population is intermediate; and (iv) the effects of the loci influencing nonrandom mating are strong. We discuss patterns and timescales of ecological speciation identified by our model, and we highlight important parameters and features that need to be studied empirically to provide information that can be used to improve the biological realism and power of mathematical models of ecological speciation.