Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika

Ancient lakes are often collectively viewed as evolutionary hot spots of diversification. East Africa's Lake Tanganyika has long been the subject of scientific interest owing to dramatic levels of endemism in species as diverse as cichlid fishes, paludomid gastropods, decapod and ostracod crustaceans and poriferans. It is the largest and deepest of the African rift lakes, and its endemic fauna has been presented with a stable inland environment for over 10 Myr, offering unique opportunities for within-lake diversification. Although astonishing diversification has been documented in the endemic cichlid fauna of the lake, similar patterns of rapid diversification have long been assumed for other groups. In contrast to this hypothesis of rapid speciation, we show here that there has been no acceleration in the rate of speciation in the thalassoid gastropods of the lake following lake colonization. While limited within-lake speciation has occurred, the dramatic conchological diversity of gastropods presently found within the lake has evolved from at least four major lineages that pre-date its formation by as much as 40 Myr. At the same time, a widespread group of African gastropods appears to have evolved from taxa presently found in the lake. While Lake Tanganyika has been a cradle of speciation for cichlid fishes, it has also been an important evolutionary reservoir of gastropod lineages that have been extirpated outside the basin.     

Escalation and trophic specialization drive adaptive radiation of freshwater gastropods in ancient lakes on Sulawesi, Indonesia

Species flocks in ancient lakes have long been appreciated as ideal model systems for the study of speciation and adaptive processes. We here present data from a new invertebrate model system with intrinsic parameters distinct from those of other documented radiations. The ancient lakes on Sulawesi harbour an endemic species flock of at least 33 species of viviparous snails. Molecular data reveal multiple independent colonizations of the lakes by riverine ancestors. In each colonizing clade, parallel evolution of conspicuous shell morphologies, followed by a differentiation of trophic morphology and the development of habitat specificity can be observed. Extensive shell crushing experiments and strong dentition of the chelae observed in some lacustrine crab species suggest that coevolution with crabs, i.e. escalation, is the most likely cause of initial shell divergence. By contrast, repeated parallel evolution in radula morphology indicates that speciation within lineages is driven by divergent adaptation to different resources among sympatric taxa. The inclusion of coevolutionary processes is unique in this system compared with diversification models developed for vertebrate radiations.     

Role of ancient lakes in genetic and phenotypic diversification of freshwater snails

Endemic organisms of ancient lakes have been studied as models to understand processes of speciation and adaptive radiation. However, it remains unclear how ancient lakes play roles in genetic and phenotypic diversity of freshwater mollusks. In the present study, we focus on viviparid freshwater snails in the ancient lakes of East and Southeast Asia (Japan and China) to address this question. Using molecular phylogenetic analyses based on mitochondrial (COI, 16S) and nuclear genes (18S, 28S, H3), we show that patterns of species diversification in viviparid lineages. Colonization to ancient lakes occurred independently in China and Japan at least four times, with subsequent diversification into more than two species within each lake group. Morphological analyses of fossil related viviparids suggest parallel phenotypic evolution occurred in the different lakes and ages. Each lake contained a single lineage which was phenotypically diversified relative to those from other sites. Using genome‐wide SNPs obtained by MIG‐seq, we also examined the genetic structure of three Japanese viviparids, including two endemic species of ancient Lake Biwa. The results suggest that these two species diversified from the population of the third species living in wetlands surrounding the lake. These findings suggest that rapid diversification of lineages and phenotypic divergence can occur in ancient lakes compared to other habitats. Formation of large lakes probably promotes speciation and phenotypic divergence as a result of adaptation into different microhabitats. High numbers of ancient lakes could be a driver of species diversity in Asian viviparid snails.     

Evolutionary history of an adaptive radiation in species pairs of threespine sticklebacks (Gasterosteus): insights from mitochondrial DNA

Species pairs of threespine stickleback, Gasterosteus aculeatus, co-exist in several lakes in the Strait of Georgia, southwestern British Columbia. One species, ‘benthics’ is robust-bodied and is morphologically and behaviourally specialized for benthivory. The other species, ‘limnetics’ is specialized for planktivory in open-water habitats of the lakes. We examined mitochondrial DNA restriction site variation in benthic and limnetic sticklebacks as well as in solitary freshwater, anadromous (sea-run), and marine populations to test: (i) if benthic and limnetic pairs have evolved only once or multiple times (parallel evolution) and (ii) if the species have evolved sympatrically, or allopatrically from ‘double invasions’ of lakes by ancestral anadromous/marine sticklebacks. Stickleback mtDNA comprised a single clade with a low (mean = 0.40%) degree of sequence divergence among the 77 haplotypes resolved. Most nucleotide diversity (97%) was found within (rather than among) populations of anadromous/marine sticklebacks whereas most diversity (77%) was found among populations in freshwater sticklebacks. Significant differences in haplotype frequencies were found between benthics and limnetics in three of the four species pair lakes examined, but in all cases the pairs within lakes were characterized by unique assemblages of closely related haplotypes. Hierarchical clustering of divergence estimates suggested that comparable species from different lakes have originated independently in all lakes because in no case did comparable species from different lakes cluster together. Divergent species within lakes tended to be more closely related to one another than to species in other lakes and there were two cases were benthics and limnetics within a particular lake were monophyletic. In two of the four two-species lakes, limnetics were less divergent from putative ancestral anadromous/marine stickleback as predicted by the double invasion hypothesis, but in the two other lakes benthics were less divergent. Our data argue strongly that the species pairs have evolved independently in each lake were they now co-exist. Further, in two lakes our data are consistent with the species having evolved by sympatric divergence, but allopatric divergence followed by introgression of mtDNA that has obscured ancestral relationships cannot be discounted completely. Finally, despite remaining uncertainty about the geography of speciation, the species appear to have evolved in the face of gene flow arguing that natural selection acting on trophic ecology has been a major component of ecological speciation in sticklebacks.     

Mitochondrial and Allozyme Genetics of Incipient Speciation in a Landlocked Population of Galaxias Truttaceus (Pisces: Galaxiidae)

Galaxias truttaceus is found in coastal rivers and streams in south-eastern Australia. It spawns at the head of estuaries in autumn and the larvae spend 3 months of winter at sea before returning to fresh water. In Tasmania there are landlocked populations of G. truttaceus in a cluster of geologically young lakes on the recently glaciated Central Plateau. These populations have no marine larval stage and spawn in the lakes in spring. Speciation due to land locking is thought to be a frequent occurrence within Galaxias. To investigate the nature of the speciation event which may be occurring within lake populations of G. truttaceus we studied the mitochondrial DNA (mtDNA) and allozyme diversity of both lake and stream populations. Using the presence or absence of restriction sites recognized by 13 six-base restriction endonucleases, we found 58 mtDNA haplotypes among 150 fish collected from 13 Tasmanian and one south-east Australian mainland stream populations. The most parsimonious network relating the haplotypes by site loss or gain was starlike in shape. We argue that this arrangement is best explained by selection upon slightly beneficial mutations within the mitochondrial genome. Gene diversity analysis under Wright's island model showed that the populations in each drainage were not genetically subdivided. Only two of these stream haplotypes were found among the 66 fish analyzed from four lake populations. Despite the extreme lack of mtDNA diversity in lake populations, the observed nuclear DNA heterozygosity of 40 lake fish (0.10355) was only slightly less than that of 82 stream fish (0.11635). In the short time (3000-7000 years) that the lake fish have been landlocked, random genetic drift in a finite, stable-sized population was probably not responsible for the lack of mtDNA diversity in the lake populations. We infer the lake populations have probably experienced at least one, severe, but transitory bottleneck possibly induced by natural selection for life-history characters essential for survival in the lacustrine habitat. If speciation is occurring in the landlocked populations of G. truttaceus, then it may be driven by genetic transilience.     

African cichlid fish: a model system in adaptive radiation research

The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.     

Global diversity of fish (Pisces) in freshwater

The precise number of extant fish species remains to be determined. About 28,900 species were listed in FishBase in 2005, but some experts feel that the final total may be considerably higher. Freshwater fishes comprise until now almost 13,000 species (and 2,513 genera) (including only freshwater and strictly peripheral species), or about 15,000 if all species occurring from fresh to brackishwaters are included. Noteworthy is the fact that the estimated 13,000 strictly freshwater fish species live in lakes and rivers that cover only 1% of the earth’s surface, while the remaining 16,000 species live in salt water covering a full 70%. While freshwater species belong to some 170 families (or 207 if peripheral species are also considered), the bulk of species occur in a relatively few groups: the Characiformes, Cypriniformes, Siluriformes, and Gymnotiformes, the Perciformes (noteably the family Cichlidae), and the Cyprinodontiformes. Biogeographically the distribution of strictly freshwater species and genera are, respectively 4,035 species (705 genera) in the Neotropical region, 2,938 (390 genera) in the Afrotropical, 2,345 (440 genera) in the Oriental, 1,844 (380 genera) in the Palaearctic, 1,411 (298 genera) in the Nearctic, and 261 (94 genera) in the Australian. For each continent, the main characteristics of the ichthyofauna are briefly outlined. At this continental scale, ichthyologists have also attempted to identify ichthyological ‘‘provinces’’ that are regions with a distinctive evolutionary history and hence more or less characteristic biota at the species level. Ichthyoregions are currently identified in each continent, except for Asia. An exceptionally high faunal diversity occurs in ancient lakes, where one of the most noteworthy features is the existence of radiations of species that apparently result from intra-lacustrine speciation. Numerous fish-species flocks have been identified in various ancient lakes that are exceptional natural sites for the study of speciation. The major threats to fish biodiversity are intense and have been relatively well documented: overexploitation, flow modification, destruction of habitats, invasion by exotic species, pollution including the worldwide phenomena of eutrophication and sedimentation, all of which are interacting. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. Guest editors: E. V. Balian, C. Lévêque, H. Segers & K. Martens Freshwater Animal Diversity Assessment     

A phylogenetic perspective on habitat shifts and diversity in the North American Enallagma damselflies

Community ecologists are increasingly aware that the regional history of taxon diversification can have an important influence on community structure. Likewise, systematists recognize that ecological context can have an important influence on the processes of speciation and extinction that create patterns of descent. We present a phylogenetic analysis of 33 species of a North American radiation of damselflies (Zygoptera: Coenagrionidae: Enallagma Selys), which have been well studied ecologically, to elucidate the evolutionary mechanisms that have contributed to differences in diversity between larval habitats (lakes with and without fish predators). Analysis of molecular variation in 842 bp of the mitochondrial cytochrome oxidase I and II subunit and of the intervening Leu-tRNA and 37 morphological characters resulted in three well-defined clades that are only partially congruent with previous phylogenetic hypotheses. Molecular and morphological data partitions were significantly incongruent (p < .01). Lack of haplotype monophyly within species and small amounts of sequence divergence (< 1%) between related species in three of the four clades suggest that recent, and parallel, speciation has been an important source of community diversity. Reconstruction of habitat preference over the phylogeny suggests that the greater species diversity in fish-containing lake habitats reflects the recency of shifts into the fishless lake habit, although a difference in speciation or extinction rates between the two habitats is difficult to exclude as an additional mechanism.     

Early Human Speciation,Brain Expansion and Dispersal Influenced by African Climate Pulses

Early human evolution is characterised by pulsed speciation and dispersal events that cannot be explained fully by global or continental paleoclimate records. We propose that the collated record of ephemeral East African Rift System (EARS) lakes could be a proxy for the regional paleoclimate conditions experienced by early hominins. Here we show that the presence of these lakes is associated with low levels of dust deposition in both West African and Mediterranean records, but is not associated with long-term global cooling and aridification of East Africa. Hominin expansion and diversification seem to be associated with climate pulses characterized by the precession-forced appearance and disappearance of deep EARS lakes. The most profound period for hominin evolution occurs at about 1.9 Ma; with the highest recorded diversity of hominin species, the appearance of Homo (sensu stricto) and major dispersal events out of East Africa into Eurasia. During this period, ephemeral deep-freshwater lakes appeared along the whole length of the EARS, fundamentally changing the local environment. The relationship between the local environment and hominin brain expansion is less clear. The major step-wise expansion in brain size around 1.9 Ma when Homo appeared was coeval with the occurrence of ephemeral deep lakes. Subsequent incremental increases in brain size are associated with dry periods with few if any lakes. Plio-Pleistocene East African climate pulses as evinced by the paleo-lake records seem, therefore, fundamental to hominin speciation, encephalisation and migration.     

Genetic variation over space and time: analyses of extinct and remnant lake trout populations in the Upper Great Lakes

Lake trout (Salvelinus namaycush) in the upper Laurentian Great Lakes of North America experienced striking reductions in abundance and distribution during the mid-twentieth century. Complete collapse of populations was documented for Lake Michigan, and a few remnant populations remained only in lakes Huron and Superior. Using DNA obtained from historical scale collections, we analysed patterns of genetic diversity at five microsatellite loci from archived historical samples representing 15 populations (range 1940-1959) and from three contemporary remnant populations across lakes Huron and Superior (total n = 893). Demographic declines in abundance and the extirpation of native lake trout populations during the past 40 years have resulted in the loss of genetic diversity between lakes owing to extirpation of Lake Michigan populations and a temporal trend for reduction in allelic richness in the populations of lakes Superior and Huron. Naturally reproducing populations in Lake Superior, which had been considered to be remnants of historical populations, and which were believed to be responsible for the resurgence of lake trout numbers and distribution, have probably been affected by hatchery supplementation.     

Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity

Many groups show higher species richness in tropical regions but the underlying causes remain unclear. Despite many competing hypotheses to explain latitudinal diversity gradients, only three processes can directly change species richness across regions: speciation, extinction and dispersal. These processes can be addressed most powerfully using large-scale phylogenetic approaches, but most previous studies have focused on small groups and recent time scales, or did not separate speciation and extinction rates. We investigate the origins of high tropical diversity in amphibians, applying new phylogenetic comparative methods to a tree of 2871 species. Our results show that high tropical diversity is explained by higher speciation in the tropics, higher extinction in temperate regions and limited dispersal out of the tropics compared with colonization of the tropics from temperate regions. These patterns are strongly associated with climate-related variables such as temperature, precipitation and ecosystem energy. Results from models of diversity dependence in speciation rate suggest that temperate clades may have lower carrying capacities and may be more saturated (closer to carrying capacity) than tropical clades. Furthermore, we estimate strikingly low tropical extinction rates over geological time scales, in stark contrast to the dramatic losses of diversity occurring in tropical regions presently.     

CRATER LAKE COLONIZATION BY NEOTROPICAL CICHLID FISHES

Volcanic crater lakes are isolated habitats that are particularly well suited to investigating ecological and evolutionary divergence and modes of speciation. However, the mode, frequency, and timing of colonization of crater lakes have been difficult to determine. We used a statistical comparative phylogeographic approach, based on a mitochondrialDNA dataset, to infer the colonization history of two Nicaraguan crater lakes by populations of genetically and ecologically divergent cichlid lineages: Midas (Amphilophus cf. citrinellus complex) and moga (Hypsophrys nematopus). We compared estimates of diversity among populations within the two cichlid lineages and found that Midas were the most genetically diverse. From an approximate Bayesian computation analysis, we inferred that the crater lakes were each founded by both cichlid lineages in single waves of colonization: Masaya 5800 ± 300 years ago and Xiloá 5400 ± 750 years ago. We conclude that natural events are likely to have a dominant role in colonization of the crater lakes. Further, our findings suggest that the higher species richness and more rapid evolution of the Midas species complex, relative to other lineages of fishes in the same crater lakes, cannot be explained by earlier or more numerous colonization events.     

Comparative aspects of adaptive radiation and speciation in Lake Baikal and the great rift lakes of Africa

Lakes Baikal, Tanganyika and Malawi have similar origins, are physiographically similar, and of similar size. The hydrological regime of Baikal is, however, very different from that which prevails in its African sisters. Apart from being much cooler, it differs fundamentally in being oxygenated to all depths while the two great African rift lakes possess only a relatively thin oxygenated surface layer and have vast oxygenless, and therefore azoic, abyssal regions. Nevertheless, like Baikal, they have rich endemic faunas.That these faunas originated largely by intralacustrine speciation and not by multiple invasion is now well established. They provide some of the world's most spectacular examples of species flocks, and some groups display what has been aptly described as explosive speciation. Certain features, and especially the adaptive radiation, of some of the groups involved, are noted. Comparisons between lakes are illuminating. Some species flocks, such as those of amphipods, sponges and turbellarians of Baikal and the atyid prawns and potamid crabs of Tanganyika, have no counterparts in the other lakes. Other groups, such as the prosobranch gastropods, ostracods and harpacticoid copepods of Baikal and Tanganyika, and the fishes of all three, involve representatives of the same major group, though often of different families or even higher taxonomic categories.That allopatric speciation has been involved is universally acknowledged but the problems posed by species multiplication in deep water in L. Baikal have led to suggestions that sympatric speciation could have played a part. Notwithstanding the difficulties, it is suggested that the process can be explained without invoking the assistance of the sympatric model.The faunas of these lakes provide immense fields for investigation and enormous intellectual challenges. While each is an entity in itself, comparative studies may be particularly enlightening.The substance of this paper was presented as a lecture at the First International Baikal Vereshchagin Conference held in Listvyanka, Irkutsk Region, U.S.S.R. in October 1989.     

Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times

The extensive phenotypic polymorphism in the European whitefish has triggered evolutionary research in order to disentangle mechanisms underlying diversification. To illuminate the ecological distinctiveness in polymorphic whitefish, and evaluate taxonomic designations, we studied nine Norwegian lakes in three watercourses, which each harboured pairs of divergent whitefish morphs. We compared the morphology and life history of these morphs, documented the extent of genetic differentiation between them, and contrasted the niche use of sympatric morphs along both the habitat and resource axes. In all cases, sympatric morphs differed in the number of gill rakers, a highly heritable trait related to trophic utilization. Individual growth rate, age and size at maturity, diet and habitat use also differed between morphs within lakes, but were remarkably similar across lakes within the same morph. Microsatellite analyses confirmed for all but one pair that sympatric morphs were significantly genetically different, and that similar morphs from different lakes likely have a polyphyletic origin. These results are most compatible with the process of parallel evolution through recurrent postglacial divergence into pelagic and benthic niches in each of these lakes. We propose that sparsely and densely rakered whitefish sympatric pairs may be a likely case of ecological speciation, mediated in oligotrophic lakes with few trophic competitors.     

Parasite burdens differ between sympatric three-spined stickleback species

The ecological theory of adaptive radiation states that differences in ecological circumstances among local populations are the cause of divergence that leads to speciation. The role of parasites in contributing to divergence has seldom been considered, despite their ubiquity and known selective effects. The potential for parasites to contribute to divergence between closely related taxa was examined by quantifying the variation in parasite burdens between sympatric three-spined stickleback species ( Gasterosteus aculeatus complex) in two lakes in coastal British Columbia, Canada. In doing so the relative importance of geographical differences between lakes and trophic or microhabitat differences between species within lakes were evaluated. The entire metazoan parasite burdens of a total of 255 limnetic and benthic sticklebacks in Paxton and Priest lakes were assayed over five time points between spring and autumn. Despite their sympatric distributions, there were large differences in parasite burdens between benthic and limnetic sticklebacks within lakes and these were consistent across both lakes. In particular, limnetics suffered greater burdens of the parasites Schistocephalus solidus and Diplostomum scudderi and benthics had much higher burdens of parasitic glochidia (mollusc larvae). Parasite burdens also differed quantitatively between lakes, but in general such differences were less pronounced than those between the stickleback species. The documented differences in parasite burdens between stickleback species have potential to contribute to divergent selection on life history, immunological and secondary sexual characters that could contribute to reproductive isolation between the species.     

Ancient lakes revisited: from the ecology to the genetics of speciation

Explosive speciation in ancient lakes has fascinated biologists for centuries and has inspired classical work on the tempo and modes of speciation. Considerable attention has been directed towards the extrinsic forces of speciation—the geological, geographical and ecological peculiarities of ancient lakes. Recently, there has been a resurgence of interest in the intrinsic nature of these radiations, the biological characteristics conducive to speciation. While new species are thought to arise mainly by the gradual enhancement of reproductive isolation among geographically isolated populations, ancient lakes provide little evidence for a predominant role of geography in speciation. Recent phylogenetic work provides strong evidence that multiple colonization waves were followed by parallel intralacustrine radiations that proceeded at relatively rapid rates despite long‐term gene flow through hybridization and introgression. Several studies suggest that hybridization itself might act as a key evolutionary mechanism by triggering major genomic reorganization/revolution and enabling the colonization of new ecological niches in ancient lakes. These studies propose that hybridization is not only of little impediment to diversification but could act as an important force in facilitating habitat transitions, promoting postcolonization adaptations and accelerating diversification. Emerging ecological genomic approaches are beginning to shed light on the long‐standing evolutionary dilemma of speciation in the face of gene flow. We propose an integrative programme for future studies on speciation in ancient lakes.     

Sympatric and Allopatric Divergence of MHC Genes in Threespine Stickleback

Parasites can strongly affect the evolution of their hosts, but their effects on host diversification are less clear. In theory, contrasting parasite communities in different foraging habitats could generate divergent selection on hosts and promote ecological speciation. Immune systems are costly to maintain, adaptable, and an important component of individual fitness. As a result, immune system genes, such as those of the Major Histocompatability Complex (MHC), can change rapidly in response to parasite-mediated selection. In threespine stickleback (Gasterosteus aculeatus), as well as in other vertebrates, MHC genes have been linked with female mating preference, suggesting that divergent selection acting on MHC genes might influence speciation. Here, we examined genetic variation at MHC Class II loci of sticklebacks from two lakes with a limnetic and benthic species pair, and two lakes with a single species. In both lakes with species pairs, limnetics and benthics differed in their composition of MHC alleles, and limnetics had fewer MHC alleles per individual than benthics. Similar to the limnetics, the allopatric population with a pelagic phenotype had few MHC alleles per individual, suggesting a correlation between MHC genotype and foraging habitat. Using a simulation model we show that the diversity and composition of MHC alleles in a sympatric species pair depends on the amount of assortative mating and on the strength of parasite-mediated selection in adjacent foraging habitats. Our results indicate parallel divergence in the number of MHC alleles between sympatric stickleback species, possibly resulting from the contrasting parasite communities in littoral and pelagic habitats of lakes.     

HOST‐ASSOCIATED GENETIC DIFFERENTIATION IN PHYTOPHAGOUS INSECTS: GENERAL PHENOMENON OR ISOLATED EXCEPTIONS? EVIDENCE FROM A GOLDENROD‐INSECT COMMUNITY

There is growing awareness of the importance of natural selection in driving genetic divergence and speciation, and several of the most apparent cases of this ecological speciation are provided by the existence of genetically distinct host forms in phytophagous insects. Such examples of host-associated differentiation (HAD) have become increasingly documented, and the implications of this phenomenon for the diversification of insects are becoming widely appreciated. However, instances of HAD remain rare relative to insect diversity and are sparsely distributed both ecologically and taxonomically. We sought to assess the frequency of HAD in a model herbivore community by examining genetic divergence in a variety of herbivores that feed on two closely related and broadly sympatric species of goldenrod (Solidago altissima and S. gigantea). Using mitochondrial DNA and allozyme data, in conjunction with previously published studies, we found that four of nine herbivores exhibited evidence of HAD, including possible host races or cryptic species. Using a range of reasonable substitution rate estimates for cytochrome oxidase I mitochondrial DNA, we found that HAD appears to have proceeded asynchronously across taxa. This pattern, along with the broadly sympatric distribution of host plants and the specialized life histories of the phytophagous insects, is consistent with sympatric divergence in some or all of these taxa. Although further behavioral and ecological study is needed, our survey of HAD in a community of herbivores indicates that ecological (perhaps sympatric) speciation may have been responsible for generating a significant fraction of the extant diversity of phytophagous insects.     

Population genomic tests of models of adaptive radiation in Lake Victoria region cichlid fish

Adaptive radiation is usually thought to be associated with speciation, but the evolution of intraspecific polymorphisms without speciation is also possible. The radiation of cichlid fish in Lake Victoria (LV) is perhaps the most impressive example of a recent rapid adaptive radiation, with 600+ very young species. Key questions about its origin remain poorly characterized, such as the importance of speciation versus polymorphism, whether species persist on evolutionary time scales, and if speciation happens more commonly in small isolated or in large connected populations. We used 320 individuals from 105 putative species from Lakes Victoria, Edward, Kivu, Albert, Nabugabo and Saka, in a radiation-wide amplified fragment length polymorphism (AFLP) genome scan to address some of these questions. We demonstrate pervasive signatures of speciation supporting the classical model of adaptive radiation associated with speciation. A positive relationship between the age of lakes and the average genomic differentiation of their species, and a significant fraction of molecular variance explained by above-species level taxonomy suggest the persistence of species on evolutionary time scales, with radiation through sequential speciation rather than a single starburst. Finally the large gene diversity retained from colonization to individual species in every radiation suggests large effective population sizes and makes speciation in small geographical isolates unlikely.     

Parallel evolution in Ugandan crater lakes: repeated evolution of limnetic body shapes in haplochromine cichlid fish

Background

The enormous diversity found in East African cichlid fishes in terms of morphology, coloration, and behavior have made them a model for the study of speciation and adaptive evolution. In particular, haplochromine cichlids, by far the most species-rich lineage of cichlids, are a well-known textbook example for parallel evolution. Southwestern Uganda is an area of high tectonic activity, and is home to numerous crater lakes. Many Ugandan crater lakes were colonized, apparently independently, by a single lineage of haplochromine cichlids. Thereby, this system could be considered a natural experiment in which one can study the interaction between geographical isolation and natural selection promoting phenotypic diversification.

Results

We sampled 13 crater lakes and six potentially-ancestral older lakes and, using both mitochondrial and microsatellite markers, discovered strong genetic and morphological differentiation whereby (a) geographically close lakes tend to be genetically more similar and (b) three different geographic areas seem to have been colonized by three independent waves of colonization from the same source population. Using a geometric morphometric approach, we found that body shape elongation (i.e. a limnetic morphology) evolved repeatedly from the ancestral deeper-bodied benthic morphology in the clear and deep crater lake habitats.

Conclusions

A pattern of strong genetic and morphological differentiation was observed in the Ugandan crater lakes. Our data suggest that body shape changes have repeatedly evolved into a more limnetic-like form in several Ugandan crater lakes after independent waves of colonization from the same source population. The observed morphological changes in crater lake cichlids are likely to result from a common selective regime.

Electronic supplementary material

The online version of this article (doi:10.1186/s12862-015-0287-3) contains supplementary material, which is available to authorized users.