Phylogeography and demographic history of two widespread Indo-Pacific mudskippers (Gobiidae: Periophthalmus).

This study provides a first description of the phylogeographic patterns and evolutionary history of two species of the mudskipper genus Periophthalmus. These amphibious gobies are distributed throughout the whole Indo-Pacific region and Atlantic coast of Africa, in peritidal habitats of soft-bottom coastal ecosystems. Three sequence datasets of two widely distributed species, Periophthalmus argentilineatus and P. kalolo, were obtained by amplifying and sequencing two mtDNA markers (D-loop and 16S rDNA) and the nDNA rag1 region. The three datasets were then used to perform phylogeographic, demographic and population genetic analyses. Our results indicate that tectonic events and past climatic oscillations strongly contributed to shape present genetic differentiation, phylogeographic and demographic patterns. We found support for the monophyly of P. kalolo, and only shallow genetic differentiation between East-African and Indo-Malayan populations of this species. However, our collections of the morphospecies P. argentilineatus include three molecularly distinct lineages, one of them more closely related to P. kalolo. The presence of Miocenic timings for the most recent common ancestors of some of these morphologically similar clades, suggests the presence of strong stabilising selection in mudskippers' habitats. At population level, demographic analyses and palaeoecological records of mangrove ecosystems suggest that Pleistocene bottlenecks and expansion plus secondary contact events of the studied species were associated with recurrent sea transgressions during interglacials, and sea regressions or stable regimes during glacials, respectively.

Evidence for divergent natural selection of a Lake Tanganyika cichlid inferred from repeated radiations in body size.

Divergent natural selection is thought to play a vital role in speciation, but clear, measurable examples from nature are still few. Among the many possible sources of divergent natural selection, predation pressure may be important because predators are ubiquitous in food webs. Here, we show evidence for divergent natural selection in a Lake Tanganyika cichlid, Telmatochromis temporalis, which uses burrows under stones or empty snail shells as shelters. This species contains normal and dwarf morphs at several localities. The normal morph inhabits rocky shorelines, whereas the dwarf morph invariably inhabits shell beds, where empty snail shells densely cover the lake bottom. Genetic evidence suggested that the dwarf morph evolved independently from the normal morph at two areas, and morphological analysis and evaluation of habitat structure revealed that the body sizes of morphs closely matched the available shelter sizes in their habitats. These findings suggest that the two morphs repeatedly evolved through divergent natural selection associated with the strategy for sheltering from predators.

Microsatellites reveal high levels of population substructuring in the species-poor Eretmodine cichlid lineage from Lake Tanganyika.

This study investigated fine-scale population substructuring in an apparently monogamous, biparental mouth-brooding cichlid. Microsatellite allele frequencies were determined at four polymorphic loci for nine populations of Eretmodus cyanostictus. We provide empirical support for the hypothesis that a species employing this breeding strategy should exhibit high levels of population substructuring. Stretches of sand represent considerable barriers to dispersal and, in contrast to the rock-dwelling cichlids of Lake Malawi, distance alone, along a continuous rocky shoreline, is sufficient to reduce gene flow significantly There was a significant pattern of isolation by distance both along the whole study area and over the stretch of continuous shoreline, suggesting that this species has poor dispersal capabilities and that juveniles establish territories close to their natal site. Despite limited dispersal, E. cyanostictus populations are not significantly more inbred than a more-widely dispersing rock-dwelling cichlid from Lake Malawi. This finding may cast doubt on the hypothesis that polyandry has evolved as a mechanism for maintaining genetic diversity in Lake Malawi cichlids. High levels of substructuring may not always promote high levels of speciation, and other factors, such as the intensity of sexual selection, may be more important in determining the speciation potential of a lineage.

Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika.

The current phylogenetic hypothesis for the endemic Lake Tanganyika cichlid fishes of the tribe Eretmodini is based solely on morphology and suggests that more complex trophic morphologies derived only once from a less specialized ancestral condition. A molecular phylogeny of eretmodine cichlids based on partial mitochondrial DNA cytochrome b and control-region sequences was used to reconstruct the evolutionary sequence of trophic adaptations and to test alternative models of morphological divergence. The six mitochondrial lineages found disagree with the current taxonomy and the morphology-based phylogeny. Mitochondrial lineages with similar trophic morphologies are not grouped monophyletically but are typically more closely related to lineages with different trophic phenotypes currently assigned to other genera. Our results indicate multiple independent origins of similar trophic specializations in these cichlids. A pattern of repeated divergent morphological evolution becomes apparent when the phylogeography of the mitochondrial haplotypes is analyzed in the context of the geological and paleoclimatological history of Lake Tanganyika. In more than one instance within Lake Tanganyika, similar morphological divergence of dentitional traits occurred in sympatric species pairs. Possibly, resource-based divergent selective regimes led to resource partitioning and brought about similar trophic morphologies independently and repeatedly.

Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: evidence for introgression.

Patterns of genetic differentiation were analysed and compared in two sympatric species of the endemic Lake Tanganyika cichlid tribe Eretmodini by means of mitochondrial DNA (mtDNA) sequences of the control region and six microsatellite DNA loci. The sample area covers a total of 138 km of mostly uninterrupted rocky shoreline in the Democratic Republic of Congo and includes the entire distribution range of Tanganicodus cf. irsacae that stretches over a distance of 35 km. Both markers detected significant genetic differentiation within and between the two species. T. cf. irsacae contained lower overall genetic variation than Eretmoduscyanostictus, possibly due to its more restricted range of distribution and its smaller effective population sizes. Complete fixation of Tanganicodus mtDNA haplotypes was observed in Eretmodus at two localities, while at two other localities some Tanganicodus individuals possessed Eretmodus mtDNA haplotypes. Taking into account the relatively large average sequence divergence of 6.2% between the two species, as well as the geographical distribution of mtDNA haplotypes in the lake, the observed pattern is more likely to be a consequence of asymmetric introgression than of shared ancestral polymorphism. As there is significant population differentiation between sympatric Tanganicodus and Eretmodus populations, the events of introgressions may have happened after secondary contact, but our data provide no evidence for ongoing gene flow and suggest that both species are reproductively isolated at present time.

Mitochondrial phylogeography of rock-dwelling cichlid fishes reveals evolutionary influence of historical lake level fluctuations of Lake Tanganyika, Africa.

The East African Lakes Tanganyika, Malawi and Victoria each harbour hundreds of endemic invertebrate and vertebrate species. Inferences about the ecological and evolutionary processes responsible for the origin of these species flocks will only be possible when they are made within historical and comparative frameworks. Specifically, the relative importance of intrinsic characteristics and extrinsic factors may offer information about the processes that drive diversification and speciation in these species. We investigated the sequence variation of a segment of the mitochondrial DNA control region of 32 populations representing all four nominal species in the three genera of eretmodine cichlids from Lake Tanganyika. Based on a phylogenetic analysis of these data we attempted to evaluate the importance of major lake level fluctuations on patterns of intralacustrine speciation. The geography of genetic variation reveals a high degree of within-lake endemism among genetically well-separated lineages distributed along the inferred shore lines of three historically intermittent lake basins. Seismic data indicate that extreme lowering of water levels in the Pleistocene caused the single Lake Tanganyika basin to split into three isolated ones. The strong phylogeographic structure of the Eretmodini, and the observation that some closely related populations occur on opposite shores of the lake, agree with this geological scenario. The three-clade-three-basin phylogeographic pattern was repeated twice within this tribe of cichlids. The phylogeographic pattern of eretmodine cichlids suggests that major fluctuations in the level of the lake have been important in shaping their adaptive radiation and speciation. The mitochondrially defined clades are in conflict with the current taxonomy of the group and suggest that there has been convergent evolution in trophic morphology, particularly in the shapes of oral teeth, taxonomically the most diagnostic characters of the three genera.

Lake level fluctuations synchronize genetic divergences of cichlid fishes in African lakes.

Water level fluctuations are important modulators of speciation processes in tropical lakes, in that they temporarily form or break down barriers to gene flow among adjacent populations and/or incipient species. Time estimates of the most recent major lowstands of the three African Great Lakes are thus crucial to infer the relative timescales of explosive speciation events in cichlid species flocks. Our approach combines geological evidence with genetic divergence data of cichlid fishes from the three Great East African Lakes derived from the fastest-evolving mtDNA segment. Thereby, we show for each of the three lakes that individuals sampled from several populations which are currently isolated by long geographic distances and/or deep water form clusters of equally closely related haplotypes. The distribution of identical or equally closely related haplotypes in a lake basin allows delineation of the extent of lake level fluctuations. Our data suggest that the same climatic phenomenon synchronized the onset of genetic divergence of lineages in all three species flocks, such that their most recent evolutionary history seems to be linked to the same external modulators of adaptive radiation. A calibration of the molecular clock of the control region was elaborated by gauging the age of the Lake Malawi species flock through the divergence among the utaka-cichlid and the mbuna-cichlid lineages to minimally 570,000 years and maximally 1 Myr. This suggests that the low-lake-level period which established the observed patterns of genetic relatedness dates back less than 57,000 years, probably even to 17,000-12,400 years ago, when Lake Victoria dried up and Lakes Malawi and Tanganyika were also low. A rapid rise of all three lakes about 11,000 years ago established the large-scale population subdivisions observed today. Over that period of time, a multitude of species originated in Lakes Malawi and Victoria with an impressive degree of morphological and ecological differentiation, whereas the Tanganyikan taxa that were exposed to the same habitat changes hardly diverged ecologically and morphologically. Our findings also show that patterns of genetic divergences of stenotopic organisms provide valuable feedback on geological and sedimentological time estimates for lake level changes.