Evolution of a cichlid fish in a Lake Malawi satellite lake

Allopatric divergence in peripheral habitats may lead to rapid evolution of populations with novel phenotypes. In this study we provide the first evidence that isolation in peripheral habitats may have played a critical role in generation of Lake Malawi's cichlid fish diversity. We show that Lake Chilingali, a satellite lake 11.5 km from the shore of Lake Malawi, contains a breeding population of Rhamphochromis, a predatory genus previously thought to be restricted to Lake Malawi and permanently connected water bodies. The Lake Chilingali population is the smallest known Rhamphochromis, has a unique male nuptial colour pattern and has significant differentiation in mitochondrial DNA from Lake Malawi species. In laboratory mate choice trials with a candidate sister population from Lake Malawi, females showed a strong tendency to mate assortatively indicating that they are incipient biological species. These data support the hypothesis that isolation and reconnection of peripheral habitats due to lake level changes have contributed to the generation of cichlid diversity within African lakes. Such cycles of habitat isolation and reconnection may also have been important in evolutionary diversification of numerous other abundant and wide-ranging aquatic organisms, such as marine fishes and invertebrates.     

Range expansion during the Pleistocene drove morphological radiation of the fir genus (Abies,Pinaceae) in the Qinghai‐Tibet Plateau and Himalayas

Range expansion caused by climate oscillations in the past probably promoted morphological radiation in a few plant groups. In this study, we aim to test this hypothesis through phylogeographical analysis of the cold‐tolerant fir genus (Abies) in the Qinghai‐Tibet Plateau (QTP) and Himalayas, where it comprises 12 described species. We examined sequence variation in two maternally inherited mitochondrial (mt) DNA fragments (nad5‐4 and nad7‐1) and two paternally inherited plastid DNA fragments (trnS‐G and trnL‐F) for 733 individuals from 75 populations of the species in a monophyletic group. Only six mtDNA haplotypes were recovered, but five were shared between multiple species and one occurred at a high frequency, providing strong evidence of range expansion. Forty‐three plastid DNA haplotypes were detected, 19 of which were shared between species and three occurred at high frequency. Network, mismatch and Bayesian skyline plot analyses of all plastid DNA haplotypes from this clade clearly suggested range expansion. This expansion was dated as having occurred during the longest and most extensive glaciation in the Pleistocene. Our results therefore supported the range expansion hypothesis for this clade of Abies during the Pleistocene; expansion probably drove the morphological radiation of the clade in the QTP and Himalayas, although it remains unclear whether the different morphotypes should be acknowledged as independent, reproductively isolated species. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 444–453.     

Sex and differentiation: population genetic divergence and sexual dimorphism in Mexican goodeid fish

Genetic differentiation arises due to the interaction between natural and sexual selection, migration and genetic drift. A potential role of sexual selection in speciation has received much interest, although comparative studies are inconsistent in finding supporting evidence. A poorly tested prediction is that species subject to a higher intensity of sexual selection should show greater genetic differentiation amongst populations because females from these populations should be more choosy in mate choice. The Goodeinae is a group of endemic Mexican fishes in which female choice has driven some species to be morphologically sexually dimorphic, whereas others are relatively monomorphic. Here, we measured population divergence, using microsatellite loci, within four goodeid species which show contrasting levels of sexual dimorphism. We found higher levels of differentiation between populations of the more dimorphic species, implying less gene flow between populations. We also found evidence of higher levels of genetic differences between the sexes within populations of the dimorphic species, consistent with greater dispersal in males. Adjusted for geographic distance, the mean F(ST) for the dimorphic species is 0.25 compared with 0.16 for the less dimorphic species. We conclude that population differentiation is accelerated in more sexually dimorphic species, and that comparative phylogeography may provide a more powerful approach to detecting processes, such as an influence of sexual selection on differentiation, than broad-scale comparative studies.     

Axes of differentiation in the bower-building cichlids of Lake Malawi

The 500-1000 cichlid species endemic to Lake Malawi constitute one of the most rapid and extensive radiations of vertebrates known. There is a growing debate over the role natural and sexual selection have played in creating this remarkable assemblage of species. Phylogenetic analysis of the Lake Malawi species flock has been confounded by the lack of appropriate morphological characters and an exceptional rate of speciation, which has allowed ancestral molecular polymorphisms to persist within species. To overcome this problem we used amplified fragment length polymorphism (AFLP) to reconstruct the evolution of species within three genera of Lake Malawi sand-dwelling cichlids that construct elaborate male display platforms, or bowers. Sister taxa with distinct bower morphologies, and that exist in discrete leks separated by only 1-2 m of depth, are divergent in both sexually selected and ecological traits. Our phylogeny suggests that the forces of sexual and ecological selection are intertwined during the speciation of this group and that specific bower characteristics and trophic morphologies have evolved repeatedly. These results suggest that trophic morphology and bower form may be inappropriate characters for delineating taxonomic lineages. Specifically the morphological characters used to describe the genera Lethrinops and Tramitichromis do not define monophyletic clades. Using a combination of behavioural and genetic characters, we were able to identify several cryptic cichlid species on a single beach, which suggests that sand dweller species richness has been severely underestimated.     

Quantitative traits and mode of speciation in Martinique anoles

We investigate extensive quantitative trait variation (dewlap hue, colour pattern, dorsum hue, body proportions and scalation) in the Martinique anole across eight transects representing nascent parapatric ecological speciation, nascent allopatric speciation and allopatric divergence without sufficient genetic structure to suggest speciation. Quantitative trait divergence can be extremely large between adjacent sets of populations, but with one exception that this is associated with difference in habitat rather than past allopatry. Nascent ecological speciation shows the greatest level of quantitative trait divergence across all character sets including those implicated in natural, as well as sexual selection. The sole example of nascent allopatric speciation is associated with fairly strong quantitative trait divergence among most character sets, but not the set most implicated in natural (rather than sexual) selection. The role of sexual selection in ecological speciation is discussed, both in terms of female choice with assortative mating and male–male competition with condition‐dependant sexual signals.     

Signal and preference divergence among populations of the non‐endemic basal Lake Malawi cichlid fish Astatotilapia calliptera (Perciformes: Cichlidae)

In Lake Malawi and Lake Victoria, cichlid fishes have diversified into hundreds of species, many reproductively isolated by mate choice. Territorial males tend to be more aggressive to similar‐coloured males, facilitating coexistence of divergent colour morphs or species. Behavioural mate choice and aggression biases of species and allopatric populations of specialized rocky shore cichlids are influenced by divergent signals such as male colour. Believed to be basal to the Lake Malawi haplochromine radiation, and inhabiting shallow weedy areas of the lake and neighbouring water bodies, Astatotilapia calliptera also shows allopatric variation in colour. Here, it is demonstrated that such signal divergence is associated with tendencies of females to mate with males of their own population and also for males to preferentially attack males of their own population, indicating that preference divergence related to signal divergence in allopatry may have operated throughout the adaptive radiation of the Malawian cichlids. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 180–188.     

Variable phylogeographic histories of five forest birds with populations in Upper and Lower Guinea: implications for taxonomy and evolutionary conservation

This study evaluates phylogeographic structure in selected forest bird species distributed on either side of the Dahomey Gap in West Africa to extend analyses of avian diversification across the Guineo-Congolean forest. Mitochondrial DNA sequence data were collected for five species, including four with a break in distribution across the Dahomey Gap and one with a more continuous distribution. Data for the five focal species were included in a single analysis along with appropriate outgroup taxa, allowing estimates of divergence time on a common timescale. Both phylogeographic patterns and estimated divergence times were highly variable. In two cases (Green Hylia Hylia prasina and Yellow-whiskered Greenbul Eurillas latirostris), samples from east and west of the Dahomey Gap belong to divergent mitochondrial lineages, but with substantially older divergence in Eurillas (～4.1 MY). In Western Bluebill Spermophaga haematina, relatively divergent eastern and western lineages (～1.1 MY) were sampled in the same locality in eastern Ghana, suggesting east to west gene flow across the gap following earlier vicariance. In Forest Robin Stiphrornis erythrothorax, birds sampled within Ghana were from two highly divergent lineages (～1.9 MY), one of which is more closely related to birds from Cameroon and Equatorial Guinea, such that divergence across the Dahomey Gap was comparatively recent (～0.36 MY). For both Hylia and Stiphrornis, we corroborate recent studies documenting multiple divergent lineages within each genus, some of which may represent distinct species. Consistent with previous studies, our analysis shows that the Dahomey Gap can be a significant barrier to gene flow for species restricted to forest habitats. At the same time, individual species exhibit a broad range of divergence times and phylogeographic histories of variable complexity. We discuss the taxonomic implications of our results for each focal species.     

The genetic architecture of male colour differences between a sympatric Lake Malawi cichlid species pair

The genetic basis of traits involved in reproductive isolation is a key parameter in models of sympatric speciation by sexual selection, a potential mechanism driving the explosive radiation of East African cichlids. Analysis of hybrid crosses between two sympatric Lake Malawi cichlid species, representing the extremes of the extant colour distribution, generated Castle-Wright estimates of four to seven loci controlling colour differences. Segregation patterns deviated from a purely additive model with a significant contribution from dominance, and possibly also epistasis. Evidence was found for a strong influence of autosomal loci. As departures from simple additive variation could effect the operation of models of sympatric speciation, dominance and epistasis should not be neglected.     

Color patterns and species recognition in four closely related species of Lake Malawi cichlid

We examined interspecific female mating preferences in fourclosely related species of cichlid belonging to the Pseudotropheuszebra species complex of Lake Malawi. These species differin coloration but are similar in other respects, suggestingthat male color patterns may be important to female mate choicein species recognition. To test this hypothesis, we presented females from each species with a choice of four males, one ofher own species and three others that were each of a differentspecies. We also gave each female a choice between the threeheterospecific males only. In all four species, females showeda significant preference for conspecific males in the four-waychoice and chose the male with the most similar color patternto the conspecific male in the three-way choice. These resultsare discussed with reference to the theory of sexual selectionon color patterns as a means of sympatric speciation in cichlids.     

Fitness correlates of male coloration in a Lake Victoria cichlid fish

Sexual selection by female choice has contributed to the rapidevolution of phenotypic diversity in the cichlid fish speciesflocks of East Africa. Yet, very little is known about the ecologicalmechanisms that drive the evolution of female mating preferences.We studied fitness correlates of male nuptial coloration ina member of a diverse Lake Victoria cichlid lineage, Pundamilianyererei. In this species, male red coloration is subject tointraspecific sexual selection by female mate choice. Male nuptialcoloration plays a critical role also in reproductive isolationbetween this species and the closely related sympatric speciesP. pundamilia. Here, we show that P. nyererei male colorationis carotenoid based, illustrating the potential for honest signalingof individual quality. In a wild population, we found that variationin male coloration was not associated with variation in a setof strongly intercorrelated indicators of male dominance: malesize, territory size, and territory location. Instead, the 2male characters that predominantly determine female choice,territory size and red coloration, may be independent predictorsof male quality: males with bright red coloration and largeterritories had lower parasite infestation rates. As a result,female preferences tended to select against heavily parasitizedmales. Consistent with parasite-mediated sexual selection, maleshad higher and more variable parasite loads than females.     

Genetic consequences of population expansions and contractions in the common hippopotamus (Hippopotamus amphibius) since the Late Pleistocene

Over the past two decades, an increasing amount of phylogeographic work has substantially improved our understanding of African biogeography, in particular the role played by Pleistocene pluvial–drought cycles on terrestrial vertebrates. However, still little is known on the evolutionary history of semi‐aquatic animals, which faced tremendous challenges imposed by unpredictable availability of water resources. In this study, we investigate the Late Pleistocene history of the common hippopotamus (Hippopotamus amphibius), using mitochondrial and nuclear DNA sequence variation and range‐wide sampling. We documented a global demographic and spatial expansion approximately 0.1–0.3 Myr ago, most likely associated with an episode of massive drainage overflow. These events presumably enabled a historical continent‐wide gene flow among hippopotamus populations, and hence, no clear continental‐scale genetic structuring remains. Nevertheless, present‐day hippopotamus populations are genetically disconnected, probably as a result of the mid‐Holocene aridification and contemporary anthropogenic pressures. This unique pattern contrasts with the biogeographic paradigms established for savannah‐adapted ungulate mammals and should be further investigated in other water‐associated taxa. Our study has important consequences for the conservation of the hippo, an emblematic but threatened species that requires specific protection to curtail its long‐term decline.     

Late Pleistocene lineage divergence among populations of Neolitsea sericea (Lauraceae) across a deep sea‐barrier in the Ryukyu Islands

Aim Our goals were: (1) to assess the population genetic structure and demographic divergence history of a bird‐dispersed tree, Neolitsea sericea, endemic to East Asian land‐bridge islands; and (2) to interpret the results in the light of controversies over the dating and configurations of land bridges through the Japanese Ryukyu Island Arc. Location Japan–Ryukyu–Taiwan Island Arc and Chinese/Korean offshore islands. Methods We applied 10 nuclear microsatellites (nSSRs) and one chloroplast (cp) DNA sequence marker (psbA–trnH intergenic spacer) to 31 populations (397 and 326 individuals, respectively) from throughout the species’ range to infer current patterns of genetic diversity and structure, and pollen‐to‐seed migration ratios (r). A coalescent‐based isolation‐with‐migration (IM) model was applied to the combined nSSR/cpDNA data set to estimate lineage divergence times and population demographic parameters. Results The geographic structure of nSSRs and the distribution of most cpDNA haplotypes revealed two distinct lineages located in areas north and south of the ‘Tokara Gap’, a narrow (c. 37 km wide) but deep (> 1000 m) sea‐strait between the northern and central Ryukyus. Based on the IM analyses, we (1) dated the divergence of these northern and southern lineages to c. 0.07 Ma (90% highest posterior density interval: 0.02–0.38 Ma); (2) estimated a slightly smaller effective population size for the northern compared to the southern lineage; and (3) recovered only trivial signals of post‐divergence gene flow between them. Main conclusions The estimated divergence time for northern and southern lineages is consistent with geological evidence for the existence of land connections in the Tokara region during cold stages of the latest Pleistocene; it is thus incompatible with an ‘ancient sea‐barrier hypothesis’ for the Ryukyu Arc, where we would have expected much older divergences related to the initial formation of the Tokara and Kerama tectonic straits during the Pliocene. Multiple factors are likely to have had a role in the divergence of N. sericea, including not only land‐bridge submergence, but also island configuration, and/or constraints on adaptation along a latitudinal temperature gradient.     

Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish

Rapid speciation in Lake Victoria cichlid fish of the genus Pundamilia may be facilitated by sexual selection: female mate choice exerts sexual selection on male nuptial coloration within species and maintains reproductive isolation between species. However, declining water transparency coincides with increasingly dull coloration and increasing hybridization. In the present study, we investigated the mechanism underlying this pattern in Pundamilia nyererei, a species that interbreeds with a sister species in turbid but not in clear water. We compared measures of intraspecific sexual selection between two populations from locations that differ in water transparency. First, in laboratory mate‐choice experiments, conducted in clear water and under broad‐spectrum illumination, we found that females originating from turbid water have significantly weaker preferences for male coloration than females originating from clear water. Second, both the hue and body coverage of male coloration differ between populations, which is consistent with adaptation to different photic habitats. These findings suggest that the observed relationship between male coloration and water transparency is not mediated by environmental variation alone. Rather, female mating preferences are indicated to have changed in response to this variation, constituting the first evidence for intraspecific preference‐trait co‐evolution in cichlid fish. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 398–406.     

A complex pattern of post‐divergence expansion,contraction, introgression,and asynchronous responses to Pleistocene climate changes in two Dipelta sister species from western China

The well‐known vicariance and dispersal models dominate in understanding the allopatric pattern for related species and presume the simultaneous occurrence of speciation and biogeographic events. However, the formation of allopatry could postdate the species divergence. We examined this hypothesis using DNA sequence data from three chloroplast fragments and five nuclear loci of Dipelta floribunda Maxim. and D. yunnanensis Franch, two shrub species with the circum Sichuan Basin distribution, combining the climatic niche modeling approach. The best‐fit model supported by the approximate Bayesian computation analysis indicated that D. floribunda and D. yunnanensis diverged during the mid‐Pleistocene period, consistent with the largest glacial period in the Qinghai–Tibet Plateau. The historically interspecific gene flow was identified, but seemed to have ceased after the last interglacial period, when the range of D. floribunda moved northward from the south of the Sichuan Basin. Furthermore, populations of D. floribunda had expanded obviously in the north of the Sichuan Basin after the last glacial maximum (LGM). Relatively, the range of D. yunnanensis expanded before the LGM, and reduced during the post‐LGM especially in the north of the Sichuan Basin, reflecting the asynchronous responses of related species to contemporary climate changes. Our results suggested that complex topography should be considered in understanding distributional patterns, even for closely related species and their demographic responses.     

Parallel evolution of an alpine type ecomorph in a scorpionfly: Independent adaptation to high‐altitude environments in multiple mountain locations

Elucidation of the diversification process of organisms is one of the important tasks of biology. From the viewpoint of species diversity, insects are the most successful group among the diverse organisms on earth and evolutionary adaptation is one of the important factors driving this pattern. Evolutionary adaptation is one of the important factors in the diversification of insects. One of the representative examples of environmental adaptation in insects is the shortening and loss of wings in subalpine and alpine zones. In this study, we focused on the Japanese scorpionfly, Panorpodes paradoxus. In this species, individuals that inhabit mountainous regions and subalpine zones have long wings (the “general type”), and individuals that inhabit higher altitudinal ranges have short wings (the “alpine type”). We collected samples of all Japanese Panorpodes species and one Korean Panorpodes species, and conducted molecular phylogenetic analyses of the mtDNA COI (610 bp), COII (688 bp), and 16S rRNA (888 bp) and nuDNA EF1‐α (658 bp) and 28S rRNA (524 bp) regions in order to reveal the evolutionary history of the alpine type of P. paradoxus. As a result of molecular phylogenetic analyses, it was revealed that the alpine type of P. paradoxus was polyphyletic, and had evolved to become the alpine type at least twice independently at separate mountain locations. In addition, the result of divergence time estimation suggested that the alpine type is an “ecomorph”, having recently adapted to low temperature habitats following mountain uplift within the Japanese Archipelago and subsequent glacial‐interglacial cycles.     

Amassing diversity in an ancient lake: evolution of a morphologically diverse parthenogenetic gastropod assemblage in Lake Malawi

Exceptional ecological niche diversity, clear waters and unique divergent selection pressures have often been invoked to explain high morphological and genetic diversity of taxa within ancient lakes. However, it is possible that in some ancient lake taxa high diversity has arisen because these historically stable environments have allowed accumulation of lineages over evolutionary timescales, a process impossible in neighbouring aquatic habitats undergoing desiccation and reflooding. Here we examined the evolution of a unique morphologically diverse assemblage of thiarid gastropods belonging to the Melanoides polymorpha'complex' in Lake Malawi. Using mitochondrial DNA sequences, we found this Lake Malawi complex was not monophyletic, instead sharing common ancestry with Melanoides anomala and Melanoides mweruensis from the Congo Basin. Fossil calibrations of molecular divergence placed the origins of this complex to within the last 4 million years. Nuclear amplified fragment length polymorphism markers revealed sympatric M. polymorpha morphs to be strongly genetically differentiated lineages, and males were absent from our samples indicating that reproduction is predominantly parthenogenetic. These results imply the presence of Lake Malawi as a standing water body over the last million years or more has facilitated accumulation of clonal morphological diversity, a process that has not taken place in more transient freshwater habitats. As such, the historical stability of aquatic environments may have been critical in determining present spatial distributions of biodiversity.     

Postglacial climate changes and rise of three ecotypes of harbour porpoises,Phocoena phocoena,in western Palearctic waters

Despite no obvious barriers to gene flow in the marine realm, environmental variation and ecological specializations can lead to genetic differentiation in highly mobile predators. Here, we investigated the genetic structure of the harbour porpoise over the entire species distribution range in western Palearctic waters. Combined analyses of 10 microsatellite loci and a 5085 base‐pair portion of the mitochondrial genome revealed the existence of three ecotypes, equally divergent at the mitochondrial genome, distributed in the Black Sea (BS), the European continental shelf waters, and a previously overlooked ecotype in the upwelling zones of Iberia and Mauritania. Historical demographic inferences using approximate Bayesian computation (ABC) suggest that these ecotypes diverged during the last glacial maximum (c. 23–19 kilo‐years ago, kyrbp ). ABC supports the hypothesis that the BS and upwelling ecotypes share a more recent common ancestor (c. 14 kyrbp ) than either does with the European continental shelf ecotype (c. 28 kyrbp ), suggesting they probably descended from the extinct populations that once inhabited the Mediterranean during the glacial and post‐glacial period. We showed that the two Atlantic ecotypes established a narrow admixture zone in the Bay of Biscay during the last millennium, with highly asymmetric gene flow. This study highlights the impacts that climate change may have on the distribution and speciation process in pelagic predators and shows that allopatric divergence can occur in these highly mobile species and be a source of genetic diversity.     

Phylogeographic and demographic effects of Pleistocene climatic fluctuations in a montane salamander, Plethodon fourchensis

Climatic changes associated with Pleistocene glacial cycles profoundly affected species distributions, patterns of interpopulation gene flow, and demography. In species restricted to montane habitats, ranges may expand and contract along an elevational gradients in response to environmental fluctuations and create high levels of genetic variation among populations on different mountains. The salamander Plethodon fourchensis is restricted to high-elevation, mesic forest on five montane isolates in the Ouachita Mountains. We used DNA sequence data along with ecological niche modelling and coalescent simulations to test several hypotheses related to the effects of Pleistocene climatic fluctuations on species in montane habitats. Our results revealed that P. fourchensis is composed of four well-supported, geographically structured lineages. Geographic breaks between lineages occurred in the vicinity of major valleys and a narrow high-elevation pass. Ecological niche modelling predicted that environmental conditions in valleys separating most mountains are suitable; however, interglacial periods like the present are predicted to be times of range expansion in P. fourchensis . Divergence dating and coalescent simulations indicated that lineage diversification occurred during the Middle Pleistocene via the fragmentation of a wide-ranging ancestor. Bayesian skyline plots showed gradual decreases in population size in three of four lineages over the most recent glacial period and a slight to moderate amount of population growth during the Holocene. Our results not only demonstrate that climatic changes during the Pleistocene had profound effects on species restricted to montane habitats, but comparison of our results for P. fourchensis with its parapatric, sister taxon, P. ouachitae , also emphasizes how responses can vary substantially even among closely related, similarly distributed taxa.