Stephan Koblmüller | Karl-Franzens-University of Graz (original) (raw)

Papers by Stephan Koblmüller

Journal of Zoological Systematics and Evolutionary Research, 2015

Gene flow, population growth and a novel substitution rate estimate in a subtidal rock specialist... more Gene flow, population growth and a novel substitution rate estimate in a subtidal rock specialist, the black-faced blenny Tripterygion delaisi (Perciformes, Blennioidei, Tripterygiidae) from the Adriatic Sea Abstract Population histories depend on the interplay between exogeneous and endogeneous factors. In marine species, phylogeographic and demographic patterns are often shaped by sea level fluctuations, water currents and dispersal ability. Using mitochondrial control region sequences (n = 120), we infer phylogeographic structure and historic population size changes of a common littoral fish species, the black-faced blenny Tripterygion delaisi (Perciformes, Blennioidei, Tripterygiidae) from the north-eastern Adriatic Sea. We find that Adriatic T. delaisi are differentiated from conspecific populations in the remaining Mediterranean, but display little phylogeographic structure within the Adriatic basin. The pattern is consistent with passive dispersal of planktonic larvae along cyclonic currents within the Adriatic Sea, but limited active dispersal of adults. Demographic reconstructions are consistent with recent population expansion, probably triggered by rising sea levels after the last glacial maximum (LGM). Placing the onset of population growth between the LGM and the warming of surface waters (18 000-13 000 years BP) and employing a novel expansion dating approach, we inferred a substitution rate of 2.61-3.61% per site per MY. Our study is one of only few existing investigations of the genetic structure of animals within the Adriatic basin and is the first to provide an estimate for mitochondrial control region substitution rates in blennioid fishes.

Journal of Molecular Evolution, 2005

Lake Tanganyika harbors an enormous diversity of cichlid fish that stem from eight distinct ances... more Lake Tanganyika harbors an enormous diversity of cichlid fish that stem from eight distinct ancestral lineages, which colonized the lake after its formation 9 to 12 million years ago. Six of twelve currently described tribes are assigned to the “H-lineage,” an assemblage of exclusively mouthbrood-ing cichlids, all of which evolved during a short period of time during the course of

Cladistics : the international journal of the Willi Hennig Society, 2015

Large prosomal scent glands constitute a major synapomorphic character of the arachnid order Opil... more Large prosomal scent glands constitute a major synapomorphic character of the arachnid order Opiliones. These glands produce a variety of chemicals very specific to opilionid taxa of different taxonomic levels, and thus represent a model system to investigate the evolutionary traits in exocrine secretion chemistry across a phylogenetically old group of animals. The chemically best-studied opilionid group is certainly Laniatores, and currently available chemical data allow first hypotheses linking the phylogeny of this group to the evolution of major chemical classes of secretion chemistry. Such hypotheses are essential to decide upon a best-fitting explanation of the distribution of scent-gland secretion compounds across extant laniatorean taxa, and hence represent a key toward a well-founded opilionid chemosystematics.

Journal of molecular evolution, 2004

The cichlid species flock of Lake Tanganyika is comprised of seven seeding lineages that evolved ... more The cichlid species flock of Lake Tanganyika is comprised of seven seeding lineages that evolved in step with changes of the lake environment. One seeding lineage diversified into at least six lineages within a short period of time. Our study focuses on the diversification of one of these lineages, the Ectodini, comprising highly specialized, sand- and rock-dwelling species. They display two distinct breeding styles: maternal and biparental mouthbrooding. By analyzing three mtDNA gene segments in 30 species representing all 13 described genera, we show that the Ectodini rapidly diversified into four clades at the onset of their radiation. The monotypic genus Grammatotria is likely to represent the most ancestral split, followed by the almost contemporary origin of three additional clades, the first comprising the benthic genus Callochromis, the second comprising the benthic genera Asprotilapia, Xenotilapia, Enantiopus, and Microdontochromis, and the third comprising the semi-pelagic...

As one of the most important processes underlying biodiversity, (adaptive) radiation has since lo... more As one of the most important processes underlying biodiversity, (adaptive) radiation has since long enthralled evolutionary biologists. It provides an ideal setting for the study of speciation. Textbook cases are found in two of the most species-rich fish families, cichlids and gobies. We focus on a clade of each of them, the tropheine cichlids from Lake Tanganyika and the sand gobies from the Eastern Mediterranean. As such, we include an example of two major types of fish species flocks: a lacustrine, sympatric one (Tropheini), and a case of vicariant allopatry (sand gobies). There is also general recognition that parasitism is an important element of biodiversity and a prime model for species formation. Despite this potential in terms of species richness and research methodology, the countless studies on these fish radiations have never taken a parasitological approach. Comparing different host-parasite settings, our approach aims at generalizations about speciation in monogenean parasites. To assess the contribution of various speciation modes to parasite biodiversity, we compared host and parasite phylogenetic trees using co-phylogenetic analyses. Cases of significant congruence between host and parasite evolutionary history were observed in both ecosystems. For parasites belonging to Gyrodactylus, host-switching clearly plays a pivotal role, as expected based on their life history. While the availability of sympatric host species obviously is a prerequisite, in itself this opportunity does not suffice to allow extensive ecological transfer. We will highlight the importance of host and parasite characteristics in monogenean diversification. These elements will be considered in the light of the phenomenon of radiation, and of the alleged uniqueness of the systems under study.

The largely endemic cichlid species flocks of the East African Great Lakes are among the prime ex... more The largely endemic cichlid species flocks of the East African Great Lakes are among the prime examples for explosive speciation and adaptive radiation. Speciation rates differ among cichlid lineages, and the propensity to radiate has been linked to intrinsic and extrinsic factors such as sexual selection and ecological opportunity. Remarkably, only one cichlid tribe-the Boulengerochromini-comprises just a single species, Boulengerochromis microlepis, a predominantly piscivorous endemic of Lake Tanganyika and the world's largest cichlid. While the lineage diverged from its closest relatives at the onset of the Lake Tanganyika radiation [8 MYA, mitochondrial control region sequences collected in this study dated the most recent common ancestor of B. microlepis to *60-110 KYA. There was no evidence of phylogeographic structure in the lake-wide sample. Patterns of genetic diversity and demographic analyses were consistent with slow and steady population growth throughout the reconstructed timescale. Additionally, the shallow divergence within the species may be related to a possibly large variance in reproductive success in this highly fecund species. Trophic niche space restriction by sympatric piscivores, lack of geographic structure, low potential for sexual selection arising from the monogamous mating system and extinction may have contributed to keeping the lineage monotypic.

Lake Tanganyika is not the most speciesrich of the Great East African Lakes, but comprises the gr... more Lake Tanganyika is not the most speciesrich of the Great East African Lakes, but comprises the greatest diversity of cichlid fishes in terms of morphology, ecology, and breeding styles. The lake contains a polyphyletic assemblage of cichlid lineages, which evolved from several ancient species that colonized the emerging lake some 9-12 million years ago. Based on morphological characteristics, the Tanganyikan cichlids have been classified into 12, or, more recently, 16 tribes, which are largely supported by molecular data. The radiations of East African cichlids are believed to be driven by complex interactions between extrinsic factors, such as climatic changes and geological processes, and intrinsic biological characteristics of the involved organisms. Diversification within different lineages occurred simultaneously in response to drastic habitat changes such as the establishment of lacustrine deep-water conditions 5-6 MYA and subsequent major lakelevel fluctuations. This seems particularly true for the mouthbrooding lineages whereas the substrate breeders underwent a more gradual process of diversification. This review presents an account of the taxonomy and phylogeny of the Lake Tanganyika cichlid species assemblage, its relationship to the African cichlid fauna, key factors leading to the astonishing diversity and discusses recently proposed alternative age estimates for the Lake Tanganyika cichlid species assemblage.

Molecular Ecology, 2009

An extensive debate concerning the origin and taxonomic status of wolf-like canids in the North A... more An extensive debate concerning the origin and taxonomic status of wolf-like canids in the North American Great Lakes region and the consequences for conservation politics regarding these enigmatic predators is ongoing. Using maternally, paternally and biparentally inherited molecular markers, we demonstrate that the Great Lakes wolves are a unique population or ecotype of gray wolves. Furthermore, we show that the Great Lakes wolves experienced high degrees of ancient and recent introgression of coyote and western gray wolf mtDNA and Y-chromosome haplotypes, and that the recent demographic bottleneck caused by persecution and habitat depletion in the early 1900s is not reflected in the genetic data.

Molecular Phylogenetics and Evolution, 2007

Colour pattern diversity can be due to random processes or to natural or sexual selection. Conseq... more Colour pattern diversity can be due to random processes or to natural or sexual selection. Consequently, similarities in colour patterns are not always correlated with common ancestry, but may result from convergent evolution under shared selection pressures or drift. Neolamprologus brichardi and Neolamprologus pulcher have been described as two distinct species based on differences in the arrangement of two dark bars on the operculum. Our study uses DNA sequences of the mitochondrial control region to show that relatedness of haplotypes disagrees with species assignment based on head colour pattern. This suggests repeated parallel evolution of particular stripe patterns. The complete lack of shared haplotypes between populations of the same or different phenotypes reflects strong philopatric behaviour, possibly induced by the cooperative breeding mode in which offspring remain in their natal territory and serve as helpers until they disperse to nearby territories or take over a breeding position. Concordant phylogeographic patterns between N. brichardi/N. pulcher populations and other rock-dwelling cichlids suggest that the same colonization routes have been taken by sympatric species and that these routes were affected by lake level fluctuations in the past.

Hydrobiologia, 2014

The basal haplochromine genus Pseudocrenilabrus comprises three valid species, although the curre... more The basal haplochromine genus Pseudocrenilabrus comprises three valid species, although the current taxonomy most probably underestimates species richness. Previous phylogeographic studies on the P. philander species complex revealed a clear structuring of populations, shaped by river capture events. Here we report the discovery of P. cf. philander in Lake Chila, a small lake south of Lake Tanganyika. We were interested whether discrete morphs, similar to what has been found in Lake Mweru and the Lunzua River, were present in Lake Chila. We evaluated the phenotypic variability of the population in relation to other lacustrine and riverine populations by quantifying colouration and body shape. To place the specimens in a phylogeographic framework, we inferred a phylogeny based on the most variable part of the mitochondrial control region. We found two divergent mtDNA lineages in Lake Chila and tested for population structure and admixture between the lineages using microsatellite data. Our study reveals a complex phylogeographic pattern and demonstrates admixture of distant mtDNA lineages in Lake Chila, producing a hybrid swarm with substantial phenotypic variability. Unlike in Lake Mweru, Pseudocrenilabrus has not diversified further into discrete morphs in Lake Chila, probably because of the long-term instability of the lake and the presumed recency of the admixture event.

Proceedings of the National Academy of Sciences, 2005

Many examples of the appearance of similar traits in different lineages are known during the evol... more Many examples of the appearance of similar traits in different lineages are known during the evolution of organisms. However, the underlying genetic mechanisms have been elucidated in very few cases. Here, we provide a clear example of evolutionary parallelism, involving changes in the same genetic pathway, providing functional adaptation of RH1 pigments to deep-water habitats during the adaptive radiation of East African cichlid fishes. We determined the RH1 sequences from 233 individual cichlids. The reconstruction of cichlid RH1 pigments with 11-cis-retinal from 28 sequences showed that the absorption spectra of the pigments of nine species were shifted toward blue, tuned by two particular amino acid replacements. These blue-shifted RH1 pigments might have evolved as adaptations to the deep-water photic environment. Phylogenetic evidence indicates that one of the replacements, A292S, has evolved several times independently, inducing similar functional change. The parallel evolution of the same mutation at the same amino acid position suggests that the number of genetic changes underlying the appearance of similar traits in cichlid diversification may be fewer than previously expected.

PLoS ONE, 2013

The cichlid fishes of the East African Great Lakes represent a model especially suited to study a... more The cichlid fishes of the East African Great Lakes represent a model especially suited to study adaptive radiation and speciation. With several African cichlid genome projects being in progress, a promising set of closely related genomes is emerging, which is expected to serve as a valuable data base to solve questions on genotype-phenotype relations. The mitochondrial (mt) genomes presented here are the first results of the assembly and annotation process for two closely related but eco-morphologically highly distinct Lake Tanganyika cichlids, Petrochromis trewavasae and Tropheus moorii. The genomic sequences comprise 16,588 bp (P. trewavasae) and 16,590 bp (T. moorii), and exhibit the typical mitochondrial structure, with 13 protein-coding genes, 2 rRNA genes, 22 tRNA genes, and a non-coding control region. Analyses confirmed that the two species are very closely related with an overall sequence similarity of 96%. We analyzed the newly generated sequences in the phylogenetic context of 21 published labroid fish mitochondrial genomes. Consistent with other vertebrates, the D-loop region was found to evolve faster than protein-coding genes, which in turn are followed by the rRNAs; the tRNAs vary greatly in the rate of sequence evolution, but on average evolve the slowest. Within the group of coding genes, ND6 evolves most rapidly. Codon usage is similar among examined cichlid tribes and labroid families; although a slight shift in usage patterns down the gene tree could be observed. Despite having a clearly different nucleotide composition, ND6 showed a similar codon usage. C-terminal ends of Cox1 exhibit variations, where the varying number of amino acids is related to the structure of the obtained phylogenetic tree. This variation may be of functional relevance for Cox1 synthesis. Citation: Fischer C, Koblmü ller S, Gü lly C, Schlö tterer C, Sturmbauer C, et al. (2013) Complete Mitochondrial DNA Sequences of the Threadfin Cichlid (Petrochromis trewavasae) and the Blunthead Cichlid (Tropheus moorii) and Patterns of Mitochondrial Genome Evolution in Cichlid Fishes. PLoS ONE 8(6): e67048.

PLoS ONE, 2012

The factors promoting the evolution of parental care strategies have been extensively studied in ... more The factors promoting the evolution of parental care strategies have been extensively studied in experiment and theory. However, most attempts to examine parental care in an evolutionary context have evaluated broad taxonomic categories. The explosive and recent diversifications of East African cichlid fishes offer exceptional opportunities to study the evolution of various life history traits based on species-level phylogenies. The Xenotilapia lineage within the endemic Lake Tanganyika cichlid tribe Ectodini comprises species that display either biparental or maternal only brood care and hence offers a unique opportunity to study the evolution of distinct parental care strategies in a phylogenetic framework. In order to reconstruct the evolutionary relationships among 16 species of this lineage we scored 2,478 Amplified Fragment Length Polymorphisms (AFLPs) across the genome. We find that the Ectodini genus Enantiopus is embedded within the genus Xenotilapia and that during 2.5 to 3 million years of evolution within the Xenotilapia clade there have been 3-5 transitions from maternal only to biparental care. While most previous models suggest that uniparental care (maternal or paternal) arose from biparental care, we conclude from our species-level analysis that the evolution of parental care strategies is not only remarkably fast, but much more labile than previously expected.

Molecular Phylogenetics and Evolution, Jul 1, 2008

The Haplochromini are by far the most species-rich cichlid fish tribe that originated along with ... more The Haplochromini are by far the most species-rich cichlid fish tribe that originated along with the socalled primary radiation of the Lake Tanganyika cichlid species flock, i.e. at the same time during which the majority of the endemic Lake Tanganyika cichlid tribes emerged. Unlike the other tribes, the haplochromines are not restricted to Lake Tanganyika but distributed throughout Africa, except for the northwestern part of the continent. Haplochromine cichlids seeded the adaptive radiation of cichlid fishes in Lakes Malawi, Kivu, Victoria, Turkana, as well as in the now extinct paleo-Lake Makgadikgadi. Here we present a comprehensive phylogenetic and phylogeographic analysis of haplochromine cichlids that is based upon DNA sequences of two mitochondrial gene segments of riverine taxa covering all major African biogeographic regions where haplochromines are found. Our analysis revealed that six lineages of haplochromines originated within a short period of time, about 5.3-4.4 MYA. These haplochromine lineages show a highly complex phylogeographic pattern, probably severely influenced by climate-and/or geology-induced changes of the environment, with river capture events most likely playing an important role for species dispersal.

Molecular Phylogenetics and Evolution, 2007

Zambian rivers belong to two major drainages: the Luapula-Congo and the Zambezi River system. Tec... more Zambian rivers belong to two major drainages: the Luapula-Congo and the Zambezi River system. Tectonic activity repeatedly altered drainage systems in Africa, so that current Wsh faunas can only be understood in the context of historic drainage capture events. We use phylogenetic relationships of one widespread lineage of haplochromine cichlids, the serranochromines, to trace their biogeographic expansion and diversiWcation in Zambia. The mitochondrial DNA phylogeny suggests Wve ancient clades, and their common ancestor was likely to have invaded from the Lower Congo River. The branching intervals in the linearized tree analysis suggest three major cladogenesis events and two periods of faunal exchange. The Wve clades originating in the Congo River drainage diversiWed further; one stayed in the Congo drainage, one diversiWed in the Zambezi system only, while the three clades of mixed distribution underwent diversiWcation in the Zambezi system, to reenter the Congo drainage very recently, as indicated by sometimes zero mutation diVerences among taxa from diVerent drainages. Our hypothesis is consistent with the suggested radiation in the extinct Lake palaeo-Makgadikgadi, so that we propose that the Zambian serranochromine fauna in part represents survivors of the extinct lacustrine Xock plus several novel species that originated in situ.

Molecular Phylogenetics and Evolution, 2010

Lake Tanganyika comprises a cichlid species flock with substrate-breeding and mouthbrooding linea... more Lake Tanganyika comprises a cichlid species flock with substrate-breeding and mouthbrooding lineages. While sexual selection via mate choice on male mating color is thought to boost speciation rates in mouthbrooding cichlids, this is not the case in substrate-breeding lamprologines, which mostly form stable pairs and lack sexual dichromatism. We present a comprehensive reconstruction of the evolution of the cichlid tribe Lamprologini, based upon mtDNA sequences and multilocus nuclear DNA (AFLP) markers. Twelve mtDNA clades were identified, seven of which were corroborated by the AFLP tree. The radiation is likely to have started about 5.3 MYA, contemporarily with that of the mouthbrooding C-lineage, and probably triggered by the onset of deep-water conditions in Lake Tanganyika. Neither the Congo-nor the Malagarazi River species form the most ancestral branch. Several conflicts in the mtDNA phylogeny with taxonomic assignments based upon color, eco-morphology and behavior could be resolved and complemented by the AFLP analysis. Introgressive hybridization upon secondary contact seems to be the most likely cause for paraphyly of taxa due to mtDNA capture in species involving brood-care helpers, while accidental hybridization best explains the para-or polyphyly of several gastropod shell breeders. Taxonomic error or paraphyly due to the survival of ancestral lineages appear responsible for inconsistencies in the genera Lamprologus and Neolamprologus.

Marine Biology, 2009

Pleurosicya are the most abundant genera of coral-associated gobies. These genera are adapted to ... more Pleurosicya are the most abundant genera of coral-associated gobies. These genera are adapted to live among coral, while other small reef gobies (e.g., the genus Eviota) show no obligate association with this living substrate. Thirteen coral-associated species and two Eviota species were sampled from diVerent regions of the Red Sea, along with four populations/species of Gobiodon from the Indian and western PaciWc Oceans. A molecular phylogenetic analysis was performed using partial sequences of 12S rRNA, 16S rRNA and cytochrome b mitochondrial genes, 1,199 base pairs in total. Several clades were consistently resolved in neighbor joining-, maximum parsimony-, maximum likelihood and Bayesian analyses. While each of the four genera Gobiodon, Paragobiodon, Bryaninops and Pleurosicya proved to be monophyletic, their relative position in the phylogeny did not support an emergence of coral-associated gobiids as a monophyletic assemblage. Instead, two separate monophyletic sub-groups were discovered, the Wrst comprising Gobiodon and Paragobiodon, and the second Bryaninops and Pleurosicya. Our molecular phylogenetic examinations also revealed one unassigned species of Gobiodon from the Maldives as a distinct species and conWrmed three putative and yet unassigned species from the Red Sea. Moreover, the uniformly black colored species of Gobiodon are not monophyletic but have evolved independently within two distinct species groups. Genetic distances were large in particular within Pleurosicya and Eviota. Estimated divergence times suggest that coral-associated gobies have diversiWed in parallel to their preferred host corals. In particular, divergence times of Gobiodon species closely match those estimated for their typical host coral genus Acropora.

Journal of Zoological Systematics and Evolutionary Research, 2007

With an age of 9-12 million years (Myr) Lake Tanganyika holds the oldest and most complex species... more With an age of 9-12 million years (Myr) Lake Tanganyika holds the oldest and most complex species flock of cichlid fishes. It is believed to be of polyphyletic origin and rooted in nine ancient African lineages, six of which underwent diversification, while three remained monotypic. Here, the evolutionary history, route and timing of colonization were analyzed, as well as intraspecific genetic diversity of Tylochromis polylepis, the single albeit endemic representative of the tribe Tylochromini in Lake Tanganyika. The role of Tylochromis in the radiation was uncertain and the species was suggested to be either an ancient colonizer or a recent addition to the fauna. With 2.8-4.2% sequence divergence to four congeners living in Lakes Bangweulu and Mweru (Upper Congo River) as well as from Luozi River and Lake Etsotso (Lower Congo River), the species appears to be a recent colonizer, which is likely to have diverged from its riverine allies less than 510 000 years ago. The ability to enter an adaptive radiation at a highly mature stage with its densely packed species community and fine-tuned niche segregation seems remarkable. So far it was assumed that all Tanganyikan endemics evolved within the lake ecosystem by intralacustrine speciation, and that complex competitive interactions among endemics tighten the system against intruders. The intruding species can be classified as a generalist living over muddy bottom in the lake and in river estuaries. Microgeographic substructuring is suggested, possibly because of geographic segregation of breeding sites. Concerning the route of colonization, a downstream movement via one of the inflowing rivers situated in the south of Lake Tanganyika is suggested.

Journal of Molecular Evolution, 2005

changes. The lack of geographic color morphs suggests that competition and resource partitioning,... more changes. The lack of geographic color morphs suggests that competition and resource partitioning, rather than allopatric speciation, promoted speciation within the genus Bathybates.

Journal of Zoological Systematics and Evolutionary Research, 2015

Gene flow, population growth and a novel substitution rate estimate in a subtidal rock specialist... more Gene flow, population growth and a novel substitution rate estimate in a subtidal rock specialist, the black-faced blenny Tripterygion delaisi (Perciformes, Blennioidei, Tripterygiidae) from the Adriatic Sea Abstract Population histories depend on the interplay between exogeneous and endogeneous factors. In marine species, phylogeographic and demographic patterns are often shaped by sea level fluctuations, water currents and dispersal ability. Using mitochondrial control region sequences (n = 120), we infer phylogeographic structure and historic population size changes of a common littoral fish species, the black-faced blenny Tripterygion delaisi (Perciformes, Blennioidei, Tripterygiidae) from the north-eastern Adriatic Sea. We find that Adriatic T. delaisi are differentiated from conspecific populations in the remaining Mediterranean, but display little phylogeographic structure within the Adriatic basin. The pattern is consistent with passive dispersal of planktonic larvae along cyclonic currents within the Adriatic Sea, but limited active dispersal of adults. Demographic reconstructions are consistent with recent population expansion, probably triggered by rising sea levels after the last glacial maximum (LGM). Placing the onset of population growth between the LGM and the warming of surface waters (18 000-13 000 years BP) and employing a novel expansion dating approach, we inferred a substitution rate of 2.61-3.61% per site per MY. Our study is one of only few existing investigations of the genetic structure of animals within the Adriatic basin and is the first to provide an estimate for mitochondrial control region substitution rates in blennioid fishes.

Journal of Molecular Evolution, 2005

Lake Tanganyika harbors an enormous diversity of cichlid fish that stem from eight distinct ances... more Lake Tanganyika harbors an enormous diversity of cichlid fish that stem from eight distinct ancestral lineages, which colonized the lake after its formation 9 to 12 million years ago. Six of twelve currently described tribes are assigned to the “H-lineage,” an assemblage of exclusively mouthbrood-ing cichlids, all of which evolved during a short period of time during the course of

Cladistics : the international journal of the Willi Hennig Society, 2015

Large prosomal scent glands constitute a major synapomorphic character of the arachnid order Opil... more Large prosomal scent glands constitute a major synapomorphic character of the arachnid order Opiliones. These glands produce a variety of chemicals very specific to opilionid taxa of different taxonomic levels, and thus represent a model system to investigate the evolutionary traits in exocrine secretion chemistry across a phylogenetically old group of animals. The chemically best-studied opilionid group is certainly Laniatores, and currently available chemical data allow first hypotheses linking the phylogeny of this group to the evolution of major chemical classes of secretion chemistry. Such hypotheses are essential to decide upon a best-fitting explanation of the distribution of scent-gland secretion compounds across extant laniatorean taxa, and hence represent a key toward a well-founded opilionid chemosystematics.

Journal of molecular evolution, 2004

The cichlid species flock of Lake Tanganyika is comprised of seven seeding lineages that evolved ... more The cichlid species flock of Lake Tanganyika is comprised of seven seeding lineages that evolved in step with changes of the lake environment. One seeding lineage diversified into at least six lineages within a short period of time. Our study focuses on the diversification of one of these lineages, the Ectodini, comprising highly specialized, sand- and rock-dwelling species. They display two distinct breeding styles: maternal and biparental mouthbrooding. By analyzing three mtDNA gene segments in 30 species representing all 13 described genera, we show that the Ectodini rapidly diversified into four clades at the onset of their radiation. The monotypic genus Grammatotria is likely to represent the most ancestral split, followed by the almost contemporary origin of three additional clades, the first comprising the benthic genus Callochromis, the second comprising the benthic genera Asprotilapia, Xenotilapia, Enantiopus, and Microdontochromis, and the third comprising the semi-pelagic...

As one of the most important processes underlying biodiversity, (adaptive) radiation has since lo... more As one of the most important processes underlying biodiversity, (adaptive) radiation has since long enthralled evolutionary biologists. It provides an ideal setting for the study of speciation. Textbook cases are found in two of the most species-rich fish families, cichlids and gobies. We focus on a clade of each of them, the tropheine cichlids from Lake Tanganyika and the sand gobies from the Eastern Mediterranean. As such, we include an example of two major types of fish species flocks: a lacustrine, sympatric one (Tropheini), and a case of vicariant allopatry (sand gobies). There is also general recognition that parasitism is an important element of biodiversity and a prime model for species formation. Despite this potential in terms of species richness and research methodology, the countless studies on these fish radiations have never taken a parasitological approach. Comparing different host-parasite settings, our approach aims at generalizations about speciation in monogenean parasites. To assess the contribution of various speciation modes to parasite biodiversity, we compared host and parasite phylogenetic trees using co-phylogenetic analyses. Cases of significant congruence between host and parasite evolutionary history were observed in both ecosystems. For parasites belonging to Gyrodactylus, host-switching clearly plays a pivotal role, as expected based on their life history. While the availability of sympatric host species obviously is a prerequisite, in itself this opportunity does not suffice to allow extensive ecological transfer. We will highlight the importance of host and parasite characteristics in monogenean diversification. These elements will be considered in the light of the phenomenon of radiation, and of the alleged uniqueness of the systems under study.

The largely endemic cichlid species flocks of the East African Great Lakes are among the prime ex... more The largely endemic cichlid species flocks of the East African Great Lakes are among the prime examples for explosive speciation and adaptive radiation. Speciation rates differ among cichlid lineages, and the propensity to radiate has been linked to intrinsic and extrinsic factors such as sexual selection and ecological opportunity. Remarkably, only one cichlid tribe-the Boulengerochromini-comprises just a single species, Boulengerochromis microlepis, a predominantly piscivorous endemic of Lake Tanganyika and the world's largest cichlid. While the lineage diverged from its closest relatives at the onset of the Lake Tanganyika radiation [8 MYA, mitochondrial control region sequences collected in this study dated the most recent common ancestor of B. microlepis to *60-110 KYA. There was no evidence of phylogeographic structure in the lake-wide sample. Patterns of genetic diversity and demographic analyses were consistent with slow and steady population growth throughout the reconstructed timescale. Additionally, the shallow divergence within the species may be related to a possibly large variance in reproductive success in this highly fecund species. Trophic niche space restriction by sympatric piscivores, lack of geographic structure, low potential for sexual selection arising from the monogamous mating system and extinction may have contributed to keeping the lineage monotypic.

Lake Tanganyika is not the most speciesrich of the Great East African Lakes, but comprises the gr... more Lake Tanganyika is not the most speciesrich of the Great East African Lakes, but comprises the greatest diversity of cichlid fishes in terms of morphology, ecology, and breeding styles. The lake contains a polyphyletic assemblage of cichlid lineages, which evolved from several ancient species that colonized the emerging lake some 9-12 million years ago. Based on morphological characteristics, the Tanganyikan cichlids have been classified into 12, or, more recently, 16 tribes, which are largely supported by molecular data. The radiations of East African cichlids are believed to be driven by complex interactions between extrinsic factors, such as climatic changes and geological processes, and intrinsic biological characteristics of the involved organisms. Diversification within different lineages occurred simultaneously in response to drastic habitat changes such as the establishment of lacustrine deep-water conditions 5-6 MYA and subsequent major lakelevel fluctuations. This seems particularly true for the mouthbrooding lineages whereas the substrate breeders underwent a more gradual process of diversification. This review presents an account of the taxonomy and phylogeny of the Lake Tanganyika cichlid species assemblage, its relationship to the African cichlid fauna, key factors leading to the astonishing diversity and discusses recently proposed alternative age estimates for the Lake Tanganyika cichlid species assemblage.

Molecular Ecology, 2009

An extensive debate concerning the origin and taxonomic status of wolf-like canids in the North A... more An extensive debate concerning the origin and taxonomic status of wolf-like canids in the North American Great Lakes region and the consequences for conservation politics regarding these enigmatic predators is ongoing. Using maternally, paternally and biparentally inherited molecular markers, we demonstrate that the Great Lakes wolves are a unique population or ecotype of gray wolves. Furthermore, we show that the Great Lakes wolves experienced high degrees of ancient and recent introgression of coyote and western gray wolf mtDNA and Y-chromosome haplotypes, and that the recent demographic bottleneck caused by persecution and habitat depletion in the early 1900s is not reflected in the genetic data.

Molecular Phylogenetics and Evolution, 2007

Colour pattern diversity can be due to random processes or to natural or sexual selection. Conseq... more Colour pattern diversity can be due to random processes or to natural or sexual selection. Consequently, similarities in colour patterns are not always correlated with common ancestry, but may result from convergent evolution under shared selection pressures or drift. Neolamprologus brichardi and Neolamprologus pulcher have been described as two distinct species based on differences in the arrangement of two dark bars on the operculum. Our study uses DNA sequences of the mitochondrial control region to show that relatedness of haplotypes disagrees with species assignment based on head colour pattern. This suggests repeated parallel evolution of particular stripe patterns. The complete lack of shared haplotypes between populations of the same or different phenotypes reflects strong philopatric behaviour, possibly induced by the cooperative breeding mode in which offspring remain in their natal territory and serve as helpers until they disperse to nearby territories or take over a breeding position. Concordant phylogeographic patterns between N. brichardi/N. pulcher populations and other rock-dwelling cichlids suggest that the same colonization routes have been taken by sympatric species and that these routes were affected by lake level fluctuations in the past.

Hydrobiologia, 2014

The basal haplochromine genus Pseudocrenilabrus comprises three valid species, although the curre... more The basal haplochromine genus Pseudocrenilabrus comprises three valid species, although the current taxonomy most probably underestimates species richness. Previous phylogeographic studies on the P. philander species complex revealed a clear structuring of populations, shaped by river capture events. Here we report the discovery of P. cf. philander in Lake Chila, a small lake south of Lake Tanganyika. We were interested whether discrete morphs, similar to what has been found in Lake Mweru and the Lunzua River, were present in Lake Chila. We evaluated the phenotypic variability of the population in relation to other lacustrine and riverine populations by quantifying colouration and body shape. To place the specimens in a phylogeographic framework, we inferred a phylogeny based on the most variable part of the mitochondrial control region. We found two divergent mtDNA lineages in Lake Chila and tested for population structure and admixture between the lineages using microsatellite data. Our study reveals a complex phylogeographic pattern and demonstrates admixture of distant mtDNA lineages in Lake Chila, producing a hybrid swarm with substantial phenotypic variability. Unlike in Lake Mweru, Pseudocrenilabrus has not diversified further into discrete morphs in Lake Chila, probably because of the long-term instability of the lake and the presumed recency of the admixture event.

Proceedings of the National Academy of Sciences, 2005

Many examples of the appearance of similar traits in different lineages are known during the evol... more Many examples of the appearance of similar traits in different lineages are known during the evolution of organisms. However, the underlying genetic mechanisms have been elucidated in very few cases. Here, we provide a clear example of evolutionary parallelism, involving changes in the same genetic pathway, providing functional adaptation of RH1 pigments to deep-water habitats during the adaptive radiation of East African cichlid fishes. We determined the RH1 sequences from 233 individual cichlids. The reconstruction of cichlid RH1 pigments with 11-cis-retinal from 28 sequences showed that the absorption spectra of the pigments of nine species were shifted toward blue, tuned by two particular amino acid replacements. These blue-shifted RH1 pigments might have evolved as adaptations to the deep-water photic environment. Phylogenetic evidence indicates that one of the replacements, A292S, has evolved several times independently, inducing similar functional change. The parallel evolution of the same mutation at the same amino acid position suggests that the number of genetic changes underlying the appearance of similar traits in cichlid diversification may be fewer than previously expected.

PLoS ONE, 2013

The cichlid fishes of the East African Great Lakes represent a model especially suited to study a... more The cichlid fishes of the East African Great Lakes represent a model especially suited to study adaptive radiation and speciation. With several African cichlid genome projects being in progress, a promising set of closely related genomes is emerging, which is expected to serve as a valuable data base to solve questions on genotype-phenotype relations. The mitochondrial (mt) genomes presented here are the first results of the assembly and annotation process for two closely related but eco-morphologically highly distinct Lake Tanganyika cichlids, Petrochromis trewavasae and Tropheus moorii. The genomic sequences comprise 16,588 bp (P. trewavasae) and 16,590 bp (T. moorii), and exhibit the typical mitochondrial structure, with 13 protein-coding genes, 2 rRNA genes, 22 tRNA genes, and a non-coding control region. Analyses confirmed that the two species are very closely related with an overall sequence similarity of 96%. We analyzed the newly generated sequences in the phylogenetic context of 21 published labroid fish mitochondrial genomes. Consistent with other vertebrates, the D-loop region was found to evolve faster than protein-coding genes, which in turn are followed by the rRNAs; the tRNAs vary greatly in the rate of sequence evolution, but on average evolve the slowest. Within the group of coding genes, ND6 evolves most rapidly. Codon usage is similar among examined cichlid tribes and labroid families; although a slight shift in usage patterns down the gene tree could be observed. Despite having a clearly different nucleotide composition, ND6 showed a similar codon usage. C-terminal ends of Cox1 exhibit variations, where the varying number of amino acids is related to the structure of the obtained phylogenetic tree. This variation may be of functional relevance for Cox1 synthesis. Citation: Fischer C, Koblmü ller S, Gü lly C, Schlö tterer C, Sturmbauer C, et al. (2013) Complete Mitochondrial DNA Sequences of the Threadfin Cichlid (Petrochromis trewavasae) and the Blunthead Cichlid (Tropheus moorii) and Patterns of Mitochondrial Genome Evolution in Cichlid Fishes. PLoS ONE 8(6): e67048.

PLoS ONE, 2012

The factors promoting the evolution of parental care strategies have been extensively studied in ... more The factors promoting the evolution of parental care strategies have been extensively studied in experiment and theory. However, most attempts to examine parental care in an evolutionary context have evaluated broad taxonomic categories. The explosive and recent diversifications of East African cichlid fishes offer exceptional opportunities to study the evolution of various life history traits based on species-level phylogenies. The Xenotilapia lineage within the endemic Lake Tanganyika cichlid tribe Ectodini comprises species that display either biparental or maternal only brood care and hence offers a unique opportunity to study the evolution of distinct parental care strategies in a phylogenetic framework. In order to reconstruct the evolutionary relationships among 16 species of this lineage we scored 2,478 Amplified Fragment Length Polymorphisms (AFLPs) across the genome. We find that the Ectodini genus Enantiopus is embedded within the genus Xenotilapia and that during 2.5 to 3 million years of evolution within the Xenotilapia clade there have been 3-5 transitions from maternal only to biparental care. While most previous models suggest that uniparental care (maternal or paternal) arose from biparental care, we conclude from our species-level analysis that the evolution of parental care strategies is not only remarkably fast, but much more labile than previously expected.

Molecular Phylogenetics and Evolution, Jul 1, 2008

The Haplochromini are by far the most species-rich cichlid fish tribe that originated along with ... more The Haplochromini are by far the most species-rich cichlid fish tribe that originated along with the socalled primary radiation of the Lake Tanganyika cichlid species flock, i.e. at the same time during which the majority of the endemic Lake Tanganyika cichlid tribes emerged. Unlike the other tribes, the haplochromines are not restricted to Lake Tanganyika but distributed throughout Africa, except for the northwestern part of the continent. Haplochromine cichlids seeded the adaptive radiation of cichlid fishes in Lakes Malawi, Kivu, Victoria, Turkana, as well as in the now extinct paleo-Lake Makgadikgadi. Here we present a comprehensive phylogenetic and phylogeographic analysis of haplochromine cichlids that is based upon DNA sequences of two mitochondrial gene segments of riverine taxa covering all major African biogeographic regions where haplochromines are found. Our analysis revealed that six lineages of haplochromines originated within a short period of time, about 5.3-4.4 MYA. These haplochromine lineages show a highly complex phylogeographic pattern, probably severely influenced by climate-and/or geology-induced changes of the environment, with river capture events most likely playing an important role for species dispersal.

Molecular Phylogenetics and Evolution, 2007

Zambian rivers belong to two major drainages: the Luapula-Congo and the Zambezi River system. Tec... more Zambian rivers belong to two major drainages: the Luapula-Congo and the Zambezi River system. Tectonic activity repeatedly altered drainage systems in Africa, so that current Wsh faunas can only be understood in the context of historic drainage capture events. We use phylogenetic relationships of one widespread lineage of haplochromine cichlids, the serranochromines, to trace their biogeographic expansion and diversiWcation in Zambia. The mitochondrial DNA phylogeny suggests Wve ancient clades, and their common ancestor was likely to have invaded from the Lower Congo River. The branching intervals in the linearized tree analysis suggest three major cladogenesis events and two periods of faunal exchange. The Wve clades originating in the Congo River drainage diversiWed further; one stayed in the Congo drainage, one diversiWed in the Zambezi system only, while the three clades of mixed distribution underwent diversiWcation in the Zambezi system, to reenter the Congo drainage very recently, as indicated by sometimes zero mutation diVerences among taxa from diVerent drainages. Our hypothesis is consistent with the suggested radiation in the extinct Lake palaeo-Makgadikgadi, so that we propose that the Zambian serranochromine fauna in part represents survivors of the extinct lacustrine Xock plus several novel species that originated in situ.

Molecular Phylogenetics and Evolution, 2010

Lake Tanganyika comprises a cichlid species flock with substrate-breeding and mouthbrooding linea... more Lake Tanganyika comprises a cichlid species flock with substrate-breeding and mouthbrooding lineages. While sexual selection via mate choice on male mating color is thought to boost speciation rates in mouthbrooding cichlids, this is not the case in substrate-breeding lamprologines, which mostly form stable pairs and lack sexual dichromatism. We present a comprehensive reconstruction of the evolution of the cichlid tribe Lamprologini, based upon mtDNA sequences and multilocus nuclear DNA (AFLP) markers. Twelve mtDNA clades were identified, seven of which were corroborated by the AFLP tree. The radiation is likely to have started about 5.3 MYA, contemporarily with that of the mouthbrooding C-lineage, and probably triggered by the onset of deep-water conditions in Lake Tanganyika. Neither the Congo-nor the Malagarazi River species form the most ancestral branch. Several conflicts in the mtDNA phylogeny with taxonomic assignments based upon color, eco-morphology and behavior could be resolved and complemented by the AFLP analysis. Introgressive hybridization upon secondary contact seems to be the most likely cause for paraphyly of taxa due to mtDNA capture in species involving brood-care helpers, while accidental hybridization best explains the para-or polyphyly of several gastropod shell breeders. Taxonomic error or paraphyly due to the survival of ancestral lineages appear responsible for inconsistencies in the genera Lamprologus and Neolamprologus.

Marine Biology, 2009

Pleurosicya are the most abundant genera of coral-associated gobies. These genera are adapted to ... more Pleurosicya are the most abundant genera of coral-associated gobies. These genera are adapted to live among coral, while other small reef gobies (e.g., the genus Eviota) show no obligate association with this living substrate. Thirteen coral-associated species and two Eviota species were sampled from diVerent regions of the Red Sea, along with four populations/species of Gobiodon from the Indian and western PaciWc Oceans. A molecular phylogenetic analysis was performed using partial sequences of 12S rRNA, 16S rRNA and cytochrome b mitochondrial genes, 1,199 base pairs in total. Several clades were consistently resolved in neighbor joining-, maximum parsimony-, maximum likelihood and Bayesian analyses. While each of the four genera Gobiodon, Paragobiodon, Bryaninops and Pleurosicya proved to be monophyletic, their relative position in the phylogeny did not support an emergence of coral-associated gobiids as a monophyletic assemblage. Instead, two separate monophyletic sub-groups were discovered, the Wrst comprising Gobiodon and Paragobiodon, and the second Bryaninops and Pleurosicya. Our molecular phylogenetic examinations also revealed one unassigned species of Gobiodon from the Maldives as a distinct species and conWrmed three putative and yet unassigned species from the Red Sea. Moreover, the uniformly black colored species of Gobiodon are not monophyletic but have evolved independently within two distinct species groups. Genetic distances were large in particular within Pleurosicya and Eviota. Estimated divergence times suggest that coral-associated gobies have diversiWed in parallel to their preferred host corals. In particular, divergence times of Gobiodon species closely match those estimated for their typical host coral genus Acropora.

Journal of Zoological Systematics and Evolutionary Research, 2007

With an age of 9-12 million years (Myr) Lake Tanganyika holds the oldest and most complex species... more With an age of 9-12 million years (Myr) Lake Tanganyika holds the oldest and most complex species flock of cichlid fishes. It is believed to be of polyphyletic origin and rooted in nine ancient African lineages, six of which underwent diversification, while three remained monotypic. Here, the evolutionary history, route and timing of colonization were analyzed, as well as intraspecific genetic diversity of Tylochromis polylepis, the single albeit endemic representative of the tribe Tylochromini in Lake Tanganyika. The role of Tylochromis in the radiation was uncertain and the species was suggested to be either an ancient colonizer or a recent addition to the fauna. With 2.8-4.2% sequence divergence to four congeners living in Lakes Bangweulu and Mweru (Upper Congo River) as well as from Luozi River and Lake Etsotso (Lower Congo River), the species appears to be a recent colonizer, which is likely to have diverged from its riverine allies less than 510 000 years ago. The ability to enter an adaptive radiation at a highly mature stage with its densely packed species community and fine-tuned niche segregation seems remarkable. So far it was assumed that all Tanganyikan endemics evolved within the lake ecosystem by intralacustrine speciation, and that complex competitive interactions among endemics tighten the system against intruders. The intruding species can be classified as a generalist living over muddy bottom in the lake and in river estuaries. Microgeographic substructuring is suggested, possibly because of geographic segregation of breeding sites. Concerning the route of colonization, a downstream movement via one of the inflowing rivers situated in the south of Lake Tanganyika is suggested.

Journal of Molecular Evolution, 2005

changes. The lack of geographic color morphs suggests that competition and resource partitioning,... more changes. The lack of geographic color morphs suggests that competition and resource partitioning, rather than allopatric speciation, promoted speciation within the genus Bathybates.