A world-wide perspective on crucifer speciation and evolution: phylogenetics,biogeography and trait evolution in tribe Arabideae

Background and Aims

Tribe Arabideae are the most species-rich monophyletic lineage in Brassicaceae. More than 500 species are distributed in the majority of mountain and alpine regions worldwide. This study provides the first comprehensive phylogenetic analysis for the species assemblage and tests for association of trait and characters, providing the first explanations for the enormous species radiation since the mid Miocene.

Methods

Phylogenetic analyses of DNA sequence variation of nuclear encoded loci and plastid DNA are used to unravel a reliable phylogenetic tree. Trait and ancestral area reconstructions were performed and lineage-specific diversification rates were calculated to explain various radiations in the last 15 Myr in space and time.

Key Results

A well-resolved phylogenetic tree demonstrates the paraphyly of the genus Arabis and a new systematic concept is established. Initially, multiple radiations involved a split between lowland annuals and mountain/alpine perennial sister species. Subsequently, increased speciation rates occur in the perennial lineages. The centre of origin of tribe Arabideae is most likely the Irano-Turanian region from which the various clades colonized the temperate mountain and alpine regions of the world.

Conclusions

Mid Miocene early diversification started with increased speciation rates due to the emergence of various annual lineages. Subsequent radiations were mostly driven by diversification within perennial species during the Pliocene, but increased speciation rates also occurred during that epoch. Taxonomic concepts in Arabis are still in need of a major taxonomic revision to define monophyletic groups.     

The Drosophila insulator proteins CTCF and CP190 link enhancer blocking to body patterning

Insulator sequences guide the function of distantly located enhancer elements to the appropriate target genes by blocking inappropriate interactions. In Drosophila, five different insulator binding proteins have been identified, Zw5, BEAF-32, GAGA factor, Su(Hw) and dCTCF. Only dCTCF has a known conserved counterpart in vertebrates. Here we find that the structurally related factors dCTCF and Su(Hw) have distinct binding targets. In contrast, the Su(Hw) interacting factor CP190 largely overlapped with dCTCF binding sites and interacts with dCTCF. Binding of dCTCF to targets requires CP190 in many cases, whereas others are independent of CP190. Analysis of the bithorax complex revealed that six of the borders between the parasegment specific regulatory domains are bound by dCTCF and by CP190 in vivo. dCTCF null mutations affect expression of Abdominal-B, cause pharate lethality and a homeotic phenotype. A short pulse of dCTCF expression during larval development rescues the dCTCF loss of function phenotype. Overall, we demonstrate the importance of dCTCF in fly development and in the regulation of abdominal segmentation.     

Lactobacillus delbrueckii ssp. lactis and ssp. bulgaricus: a chronicle of evolution in action

Background

Lactobacillus delbrueckii ssp. lactis and ssp. bulgaricus are lactic acid producing bacteria that are largely used in dairy industries, notably in cheese-making and yogurt production. An earlier in-depth study of the first completely sequenced ssp. bulgaricus genome revealed the characteristics of a genome in an active phase of rapid evolution, in what appears to be an adaptation to the milk environment. Here we examine for the first time if the same conclusions apply to the ssp. lactis, and discuss intra- and inter-subspecies genomic diversity in the context of evolutionary adaptation.

Results

Both L. delbrueckii ssp. show the signs of reductive evolution through the elimination of superfluous genes, thereby limiting their carbohydrate metabolic capacities and amino acid biosynthesis potential. In the ssp. lactis this reductive evolution has gone less far than in the ssp. bulgaricus. Consequently, the ssp. lactis retained more extended carbohydrate metabolizing capabilities than the ssp. bulgaricus but, due to high intra-subspecies diversity, very few carbohydrate substrates, if any, allow a reliable distinction of the two ssp. We further show that one of the most important traits, lactose fermentation, of one of the economically most important dairy bacteria, L. delbruecki ssp. bulgaricus, relies on horizontally acquired rather than deep ancestral genes. In this sense this bacterium may thus be regarded as a natural GMO avant la lettre.

Conclusions

The dairy lactic acid producing bacteria L. delbrueckii ssp. lactis and ssp. bulgaricus appear to represent different points on the same evolutionary track of adaptation to the milk environment through the loss of superfluous functions and the acquisition of functions that allow an optimized utilization of milk resources, where the ssp. bulgaricus has progressed further away from the common ancestor.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-407) contains supplementary material, which is available to authorized users.     

Sequence-specific interaction between ABD-B homeodomain and castor gene in Drosophila

We have examined the effect of bithorax complex genes on the expression of castor gene. During the embryonic stages 12-15, both Ultrabithorax and abdominal-A regulated the castor gene expression negatively, whereas Abdominal-B showed a positive correlation with the castor gene expression according to real-time PCR. To investigate whether ABD-B protein directly interacts with the castor gene, electrophoretic mobility shift assays were performed using the recombinant ABD-B homeodomain and oligonucleotides, which are located within the region 10 kb upstream of the castor gene. The results show that ABD-B protein directly binds to the castor gene specifically. ABD-B binds more strongly to oligonucleotides containing two 5''-TTAT-3'' canonical core motifs than the probe containing the 5''-TTAC-3'' motif. In addition, the sequences flanking the core motif are also involved in the protein-DNA interaction. The results demonstrate the importance of HD for direct binding to target sequences to regulate the expression level of the target genes. [BMB Reports 2014; 47(2): 92-97]     

Heritability and quantitative genetic divergence of serotiny,a fire-persistence plant trait

Background and Aims

Although it is well known that fire acts as a selective pressure shaping plant phenotypes, there are no quantitative estimates of the heritability of any trait related to plant persistence under recurrent fires, such as serotiny. In this study, the heritability of serotiny in Pinus halepensis is calculated, and an evaluation is made as to whether fire has left a selection signature on the level of serotiny among populations by comparing the genetic divergence of serotiny with the expected divergence of neutral molecular markers (Q_ST–F_ST comparison).

Methods

A common garden of P. halepensis was used, located in inland Spain and composed of 145 open-pollinated families from 29 provenances covering the entire natural range of P. halepensis in the Iberian Peninsula and Balearic Islands. Narrow-sense heritability (h²) and quantitative genetic differentiation among populations for serotiny (Q_ST) were estimated by means of an ‘animal model’ fitted by Bayesian inference. In order to determine whether genetic differentiation for serotiny is the result of differential natural selection, Q_ST estimates for serotiny were compared with F_ST estimates obtained from allozyme data. Finally, a test was made of whether levels of serotiny in the different provenances were related to different fire regimes, using summer rainfall as a proxy for fire regime in each provenance.

Key Results

Serotiny showed a significant narrow-sense heritability (h²) of 0·20 (credible interval 0·09–0·40). Quantitative genetic differentiation among provenances for serotiny (Q_ST = 0·44) was significantly higher than expected under a neutral process (F_ST = 0·12), suggesting adaptive differentiation. A significant negative relationship was found between the serotiny level of trees in the common garden and summer rainfall of their provenance sites.

Conclusions

Serotiny is a heritable trait in P. halepensis, and selection acts on it, giving rise to contrasting serotiny levels among populations depending on the fire regime, and supporting the role of fire in generating genetic divergence for adaptive traits.     

Interspecific symbiont transfection confers a novel ecological trait to the recipient insect

In Japan, pea aphids Acyrthosiphon pisum mainly feed on vetch and clover, and many aphid clones produce more progeny on vetch than on clover. In this context, particular genotypes of the facultative symbiont Regiella insecticola enhance reproduction of infected pea aphids specifically on clover, thereby broadening the suitable food plant range of the insect. A species that is sympatric to A. pisum, vetch aphids Megoura crassicauda, are commonly found on vetch but not on clover. Laboratory rearing of M. crassicauda strains revealed active reproduction on vetch but substantially no reproduction on clover. Experimental transfection of Regiella from A. pisum to M. crassicauda by haemolymph injection established stable and heritable infection in the recipients, although no Regiella infection has been detected in natural populations of M. crassicauda. Different strains of Regiella-transfected M. crassicauda grew and reproduced on vetch, but exhibited lower fitness in comparison with corresponding uninfected aphid strains. Strikingly, the Regiella-transfected M. crassicauda exhibited improved survival and some reproduction on clover. These results suggest that Regiella has the potential to confer an ecological trait, adaptation to clover, on novel insect hosts, and also account for why Regiella is able to infect M. crassicauda but is scarcely found in these aphid populations.     

Speciation on a local geographic scale: the evolution of a rare rock outcrop specialist in Mimulus

Speciation can occur on both large and small geographical scales. In plants, local speciation, where small populations split off from a large-ranged progenitor species, is thought to be the dominant mode, yet there are still few examples to verify speciation has occurred in this manner. A recently described morphological species in the yellow monkey flowers, Mimulus filicifolius, is an excellent candidate for local speciation because of its highly restricted geographical range. Mimulus filicifolius was formerly identified as a population of M. laciniatus due to similar lobed leaf morphology and rocky outcrop habitat. To investigate whether M. filicifolius is genetically divergent and reproductively isolated from M. laciniatus, we examined patterns of genetic diversity in ten nuclear and eight microsatellite loci, and hybrid fertility in M. filicifolius and its purported close relatives: M. laciniatus, M. guttatus and M. nasutus. We found that M. filicifolius is genetically divergent from the other species and strongly reproductively isolated from M. laciniatus. We conclude that M. filicifolius is an independent rock outcrop specialist despite being morphologically and ecologically similar to M. laciniatus, and that its small geographical range nested within other wide-ranging members of the M. guttatus species complex is consistent with local speciation.     

The peppered moth and industrial melanism: evolution of a natural selection case study

From the outset multiple causes have been suggested for changes in melanic gene frequency in the peppered moth Biston betularia and other industrial melanic moths. These have included higher intrinsic fitness of melanic forms and selective predation for camouflage. The possible existence and origin of heterozygote advantage has been debated. From the 1950s, as a result of experimental evidence, selective predation became the favoured explanation and is undoubtedly the major factor driving the frequency change. However, modelling and monitoring of declining melanic frequencies since the 1970s indicate either that migration rates are much higher than existing direct estimates suggested or else, or in addition, non-visual selection has a role. Recent molecular work on genetics has revealed that the melanic (carbonaria) allele had a single origin in Britain, and that the locus is orthologous to a major wing patterning locus in Heliconius butterflies. New methods of analysis should supply further information on the melanic system and on migration that will complete our understanding of this important example of rapid evolution.     

Carpeloidy in flower evolution and diversification: a comparative study in Carica papaya and Arabidopsis thaliana

Background and Aims

Bisexual flowers of Carica papaya range from highly regular flowers to morphs with various fusions of stamens to the ovary. Arabidopsis thaliana sup1 mutants have carpels replaced by chimeric carpel–stamen structures. Comparative analysis of stamen to carpel conversions in the two different plant systems was used to understand the stage and origin of carpeloidy when derived from stamen tissues, and consequently to understand how carpeloidy contributes to innovations in flower evolution.

Methods

Floral development of bisexual flowers of Carica was studied by scanning electron microscopy and was compared with teratological sup mutants of A. thaliana.

Key Results

In Carica development of bisexual flowers was similar to wild (unisexual) forms up to locule initiation. Feminization ranges from fusion of stamen tissue to the gynoecium to complete carpeloidy of antepetalous stamens. In A. thaliana, partial stamen feminization occurs exclusively at the flower apex, with normal stamens forming at the periphery. Such transformations take place relatively late in development, indicating strong developmental plasticity of most stamen tissues. These results are compared with evo-devo theories on flower bisexuality, as derived from unisexual ancestors. The Arabidopsis data highlight possible early evolutionary events in the acquisition of bisexuality by a patchy transformation of stamen parts into female parts linked to a flower axis-position effect. The Carica results highlight tissue-fusion mechanisms in angiosperms leading to carpeloidy once bisexual flowers have evolved.

Conclusions

We show two different developmental routes leading to stamen to carpel conversions by late re-specification. The process may be a fundamental aspect of flower development that is hidden in most instances by developmental homeostasis.     

Insulin signalling underlies both plasticity and divergence of a reproductive trait in Drosophila

Phenotypic plasticity is the ability of a single genotype to yield distinct phenotypes in different environments. The molecular mechanisms linking phenotypic plasticity to the evolution of heritable diversification, however, are largely unknown. Here, we show that insulin/insulin-like growth factor signalling (IIS) underlies both phenotypic plasticity and evolutionary diversification of ovariole number, a quantitative reproductive trait, in Drosophila. IIS activity levels and sensitivity have diverged between species, leading to both species-specific ovariole number and species-specific nutritional plasticity in ovariole number. Plastic range of ovariole number correlates with ecological niche, suggesting that the degree of nutritional plasticity may be an adaptive trait. This demonstrates that a plastic response conserved across animals can underlie the evolution of morphological diversity, underscoring the potential pervasiveness of plasticity as an evolutionary mechanism.     

Leaf trait co-ordination in relation to construction cost, carbon gain and resource-use efficiency in exotic invasive and native woody vine species

Background and Aims

Success of invasive plant species is thought to be linked with their higher leaf carbon fixation strategy, enabling them to capture and utilize resources better than native species, and thus pre-empt and maintain space. However, these traits are not well-defined for invasive woody vines.

Methods

In a glass house setting, experiments were conducted to examine how leaf carbon gain strategies differ between non-indigenous invasive and native woody vines of south-eastern Australia, by investigating their biomass gain, leaf structural, nutrient and physiological traits under changing light and moisture regimes.

Key Results

Leaf construction cost (CC), calorific value and carbon : nitrogen (C : N) ratio were lower in the invasive group, while ash content, N, maximum photosynthesis, light-use efficiency, photosynthetic energy-use efficiency (PEUE) and specific leaf area (SLA) were higher in this group relative to the native group. Trait plasticity, relative growth rate (RGR), photosynthetic nitrogen-use efficiency and water-use efficiency did not differ significantly between the groups. However, across light resource, regression analyses indicated that at a common (same) leaf CC and PEUE, a higher biomass RGR resulted for the invasive group; also at a common SLA, a lower CC but higher N resulted for the invasive group. Overall, trait co-ordination (using pair-wise correlation analyses) was better in the invasive group. Ordination using 16 leaf traits indicated that the major axis of invasive-native dichotomy is primarily driven by SLA and CC (including its components and/or derivative of PEUE) and was significantly linked with RGR.

Conclusions

These results demonstrated that while not all measures of leaf resource traits may differ between the two groups, the higher level of trait correlation and higher revenue returned (RGR) per unit of major resource need (CC) and use (PEUE) in the invasive group is in line with their rapid spread where introduced.     

The making of a pest: the evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species

Evolutionary innovation can allow a species access to a new ecological niche, potentially reducing competition with closely related species. While the vast majority of Drosophila flies feed on rotting fruit and other decaying matter, and are harmless to human activity, Drosophila suzukii, which has a morphologically modified ovipositor, is capable of colonizing live fruit that is still in the process of ripening, causing massive agricultural damage. Here, we conducted the first comparative analysis of this species and its close relatives, analysing both ovipositor structure and fruit susceptibility. We found that the ovipositor of the species most closely related to D. suzukii, Drosophila subpulchrella, has a similar number of enlarged, evolutionarily derived bristles, but a notably different overall shape. Like D. suzukii, D. subpulchrella flies are capable of puncturing the skin of raspberries and cherries, but we found no evidence that they could penetrate the thicker skin of two varieties of grapes. More distantly related species, one of which has previously been mistaken for D. suzukii, have blunt ovipositors with small bristles. While they did not penetrate fruit skin in any of the assays, they readily colonized fruit interiors where the skin was broken. Our results suggest that considering evolutionary context may be beneficial to the management of invasive species.     

Trap diversity and evolution in the family Droseraceae

We review trapping mechanisms in the carnivorous flowering plant family Droseraceae (order Caryophyllales). Its members are generally known to attract, capture, retain and digest prey animals (mainly arthropods) with active snap-traps (Aldrovanda, Dionaea) or with active sticky flypaper traps (Drosera) and to absorb the resulting nutrients. Recent investigations revealed how the snap-traps of Aldrovanda vesiculosa (waterwheel plant) and Dionaea muscipula (Venus’ flytrap) work mechanically and how these apparently similar devices differ as to their functional morphology and shutting mechanics. The Sundews (Drosera spp.) are generally known to possess leaves covered with glue-tentacles that both can bend toward and around stuck prey. Recently, it was shown that there exists in this genus a higher diversity of different tentacle types and trap configurations than previously known which presumably reflect adaptations to different prey spectra. Based on these recent findings, we finally comment on possible ways for intrafamiliar trap evolution.     

Exploring myriapod segmentation: the expression patterns of even-skipped,engrailed, and wingless in a centipede

Segment formation is critical to arthropod development, yet there is still relatively little known about this process in most arthropods. Here, we present the expression patterns of the genes even-skipped (eve), engrailed, and wingless in a centipede, Lithobius atkinsoni. Despite some differences when compared with the patterns in insects and crustaceans, the expression of these genes in the centipede suggests that their basic roles are conserved across the mandibulate arthropods. For example, unlike the seven pair-rule stripes of eve expression in the Drosophila embryonic germband, the centipede eve gene is expressed strongly in the posterior of the embryo, and in only a few stripes between newly formed segments. Nonetheless, this pattern likely reflects a conserved role for eve in the process of segment formation, within the different context of a short-germband mode of embryonic development. In the centipede, the genes wingless and engrailed are expressed in stripes along the middle and posterior of each segment, respectively, similar to their expression in Drosophila. The adjacent expression of the engrailed and wingless stripes suggests that the regulatory relationship between the two genes may be conserved in the centipede, and thus this pathway may be a fundamental mechanism of segmental development in most arthropods.     

Cabomba as a model for studies of early angiosperm evolution

BACKGROUND: The angiosperms, or flowering plants, diversified in the Cretaceous to dominate almost all terrestrial environments. Molecular phylogenetic studies indicate that the orders Amborellales, Nymphaeales and Austrobaileyales, collectively termed the ANA grade, diverged as separate lineages from a remaining angiosperm clade at a very early stage in flowering plant evolution. By comparing these early diverging lineages, it is possible to infer the possible morphology and ecology of the last common ancestor of the extant angiosperms, and this analysis can now be extended to try to deduce the developmental mechanisms that were present in early flowering plants. However, not all species in the ANA grade form convenient molecular-genetic models. SCOPE: The present study reviews the genus Cabomba (Nymphaeales), which shows a range of features that make it potentially useful as a genetic model. We focus on characters that have probably been conserved since the last common ancestor of the extant flowering plants. To facilitate the use of Cabomba as a molecular model, we describe methods for its cultivation to flowering in the laboratory, a novel Cabomba flower expressed sequence tag database, a well-adapted in situ hybridization protocol and a measurement of the nuclear genome size of C. caroliniana. We discuss the features required for species to become tractable models, and discuss the relative merits of Cabomba and other ANA-grade angiosperms in molecular-genetic studies aimed at understanding the origin of the flowering plants.     

Evidence in hand: recent discoveries and the early evolution of human manual manipulation

For several decades, it was largely assumed that stone tool use and production were abilities limited to the genus Homo. However, growing palaeontological and archaeological evidence, comparative extant primate studies, as well as results from methodological advancements in biomechanics and morphological analyses, have been gradually accumulating and now provide strong support for more advanced manual manipulative abilities and tool-related behaviours in pre-Homo hominins than has been traditionally recognized. Here, I review the fossil evidence related to early hominin dexterity, including the recent discoveries of relatively complete early hominin hand skeletons, and new methodologies that are providing a more holistic interpretation of hand function, and insight into how our early ancestors may have balanced the functional requirements of both arboreal locomotion and tool-related behaviours.