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1.  Cophylogenetic interactions between marine viruses and eukaryotic picophytoplankton 
Background
Numerous studies have investigated cospeciation (or cophylogeny) in various host-symbiont systems, and different patterns were inferred, from strict cospeciation where symbiont phylogeny mirrors host phylogeny, to complete absence of correspondence between trees. The degree of cospeciation is generally linked to the level of host specificity in the symbiont species and the opportunity they have to switch hosts. In this study, we investigated cophylogeny for the first time in a microalgae-virus association in the open sea, where symbionts are believed to be highly host-specific but have wide opportunities to switch hosts. We studied prasinovirus-Mamiellales associations using 51 different viral strains infecting 22 host strains, selected from the characterisation and experimental testing of the specificities of 313 virus strains on 26 host strains.
Results
All virus strains were restricted to their host genus, and most were species-specific, but some of them were able to infect different host species within a genus. Phylogenetic trees were reconstructed for viruses and their hosts, and their congruence was assessed based on these trees and the specificity data using different cophylogenetic methods, a topology-based approach, Jane, and a global congruence method, ParaFit. We found significant congruence between virus and host trees, but with a putatively complex evolutionary history.
Conclusions
Mechanisms other than true cospeciation, such as host-switching, might explain a part of the data. It has been observed in a previous study on the same taxa that the genomic divergence between host pairs is larger than between their viruses. It implies that if cospeciation predominates in this algae-virus system, this would support the hypothesis that prasinoviruses evolve more slowly than their microalgal hosts, whereas host switching would imply that these viruses speciated more recently than the divergence of their host genera.
doi:10.1186/1471-2148-14-59
PMCID: PMC3983898  PMID: 24669847
Cophylogeny; Prasinovirus; Phycodnaviridae; Mamiellale; Chlorophyta; Specificity
2.  A comparative study of genome organization and inferences for the systematics of two large bushcricket genera of the tribe Barbitistini (Orthoptera: Tettigoniidae: Phaneropterinae) 
Background
Poecilimon and Isophya are the largest genera of the tribe Barbitistini and among the most systematically complicated and evolutionarily intriguing groups of Palearctic tettigoniids. We examined the genomic organization of 79 taxa with a stable chromosome number using classical (C–banding, silver and fluorochrome staining) and molecular (fluorescence in situ hybridization with 18S rDNA and (TTAGG) n telomeric probes) cytogenetic techniques. These tools were employed to establish genetic organization and differences or similarities between genera or species within the same genus and determine if cytogenetic markers can be used for identifying some taxonomic groups of species.
Results
Differences between the karyotypes of the studied genera include some general changes in the morphology of the X chromosome in Isophya (in contrast to Poecilimon). The number of major rDNA clusters per haploid genome divided Poecilimon into two main almost equal groups (with either one or two clusters), while two rDNA clusters predominated in Isophya. In both genera, rDNA loci were preferentially located in the paracentromeric region of the autosomes and rarely in the sex chromosomes. Our results demonstrate a coincidence between the location of rDNA loci and active NORs and GC-rich heterochromatin regions. The C/DAPI/CMA3 bands observed in most Poecilimon chromosomes suggest the presence of more families of repetitive DNA sequences as compared to the heterochromatin patterns in Isophya.
Conclusions
The results show both differences and similarities in genome organization among species of the same genus and between genera. Previous views on the systematics and phylogenetic grouping of certain lineages are discussed in light of the present cytogenetic results. In some cases, variation of chromosome markers was observed to correspond with variation in other evolutionary traits, which is related to the processes of ongoing speciation and hybridization in zones of secondary contact. It was concluded that the physical mapping of rDNA sequences and heterochromatin may be used as an additional marker for understanding interspecific relationships in these groups and their routes of speciation.
doi:10.1186/1471-2148-14-48
PMCID: PMC3975230  PMID: 24625118
FISH; rDNA; Heterochromatin; Evolution; Orthoptera; Poecilimon; Isophya
3.  Females tend to prefer genetically similar mates in an island population of house sparrows 
Background
It is often proposed that females should select genetically dissimilar mates to maximize offspring genetic diversity and avoid inbreeding. Several recent studies have provided mixed evidence, however, and in some instances females seem to prefer genetically similar males. A preference for genetically similar mates can be adaptive if outbreeding depression is more harmful than inbreeding depression or if females gain inclusive fitness benefits by mating with close kin. Here, we investigated genetic compatibility and mating patterns in an insular population of house sparrow (Passer domesticus), over a three-year period, using 12 microsatellite markers and one major histocompability complex (MHC) class I gene. Given the small population size and the distance from the mainland, we expected a reduced gene flow in this insular population and we predicted that females would show mating preferences for genetically dissimilar mates.
Results
Contrary to our expectation, we found that offspring were less genetically diverse (multi-locus heterozygosity) than expected under a random mating, suggesting that females tended to mate with genetically similar males. We found high levels of extra-pair paternity, and offspring sired by extra-pair males had a better fledging success than those sired by the social male. Again, unexpectedly, females tended to be more closely related to extra-pair mates than to their social mates. Our results did not depend on the type of genetic marker used, since microsatellites and MHC genes provided similar results, and we found only little evidence for MHC-dependent mating patterns.
Conclusions
These results are in agreement with the idea that mating with genetically similar mates can either avoid the disruption of co-adapted genes or confer a benefit in terms of kin selection.
doi:10.1186/1471-2148-14-47
PMCID: PMC3984696  PMID: 24621140
Sexual selection; Mate choice; Passer domesticus; Major Histocompatibility Complex (MHC); Microsatellites; Extra-pair paternity
4.  The role of chromosome variation in the speciation of the red brocket deer complex: the study of reproductive isolation in females 
Background
The red brocket deer, Mazama americana, has at least six distinct karyotypes in different regions of South America that suggest the existence of various species that are today all referred to as M. americana. From an evolutionary perspective, the red brockets are a relatively recent clade that has gone through intense diversification. This study sought to prove the existence of post-zygotic reproductive isolation in deer offspring between distinct chromosome lineages. To achieve this, inter-cytotype and intra-cytotype crosses were performed, which resulted in both F1 hybrid (n = 5) and pure offspring (n = 3) in captivity.
Results
F1 females were analyzed in terms of their karyotypes, ovarian histology, estrous cycles and in vitro embryo production. Pure females presented parameters that were similar to those previously reported for M. Americana; however, the parameters for hybrid females were different. Two hybrids were determined to be sterile, while the remaining hybrids presented characteristics of subfertility.
Conclusions
The results support the existence of well-established reproductive isolation among the most distant karyotype lineages and elucidates the need to define all karyotype variants and their geographical ranges in order to define the number of species of red brocket.
doi:10.1186/1471-2148-14-40
PMCID: PMC3946183  PMID: 24593190
Cryptic species; Hybrids; Chromosomal polymorphism; Mazama americana
5.  Active hiding of social information from information-parasites 
Background
Coevolution between pairs of different kind of entities, such as providers and users of information, involves reciprocal selection pressures between them as a consequence of their ecological interaction. Pied flycatchers (Ficedula hypoleuca) have been shown to derive fitness benefits (larger clutches) when nesting in proximity to great tits (Parus major), presumably because they this way discover and obtain information about nesting sites. Tits suffer from the resulting association (smaller clutches). An arms race between the tits (information host) and the flycatchers (information parasite) could thus result. Great tits often cover eggs with nesting material before, but not during incubation. We hypothesized that one function of egg-covering could be a counter-adaptation to reduce information parasitism by pied flycatchers. We predicted that tits should bring more new hair to cover their exposed eggs when a pied flycatcher is present near to tit nest than when a neutral (non-competing) species is present. We conducted decoy and playback experiment in Oulu and Turku, Finland. First, we removed and collected all the hair covering the tit eggs. Then, we measured how the perceived presence of flycatcher or waxwing (Bombycilla garrulus) affects tits' egg-covering by collecting and weighing the hair brought on the eggs and photographing the nest 24 h after the playback.
Results
Tits brought more hair into the nest and covered the eggs more carefully after flycatcher treatment, compared to waxwing treatment. We also found that the tits in Oulu (over 600 km to north from Turku) had more hair on the top of their eggs in general.
Conclusions
Together, these results suggest that the counter-adaptation function of egg-covering against information parasites may be an extension of original function to protect eggs from low temperatures.
doi:10.1186/1471-2148-14-32
PMCID: PMC3939400  PMID: 24580842
6.  An evolutionary ratchet leading to loss of elongation factors in eukaryotes 
Background
The GTPase eEF1A is the eukaryotic factor responsible for the essential, universal function of aminoacyl-tRNA delivery to the ribosome. Surprisingly, eEF1A is not universally present in eukaryotes, being replaced by the paralog EFL independently in multiple lineages. The driving force behind this unusually frequent replacement is poorly understood.
Results
Through sequence searching of genomic and EST databases, we find a striking association of eEF1A replacement by EFL and loss of eEF1A’s guanine exchange factor, eEF1Bα, suggesting that EFL is able to spontaneously recharge with GTP. Sequence conservation and homology modeling analyses indicate several sequence regions that may be responsible for EFL’s lack of requirement for eEF1Bα.
Conclusions
We propose that the unusual pattern of eEF1A, eEF1Bα and EFL presence and absence can be explained by a ratchet-like process: if either eEF1A or eEF1Bα diverges beyond functionality in the presence of EFL, the system is unable to return to the ancestral, eEF1A:eEFBα-driven state.
doi:10.1186/1471-2148-14-35
PMCID: PMC3938643  PMID: 24564225
eEF1A; EFL; eEF1B; Ribosome; Elongation factor; GTPase; GEF; Molecular evolution; Eukaryotes
7.  Intragenic homogenization and multiple copies of prey-wrapping silk genes in Argiope garden spiders 
Background
Spider silks are spectacular examples of phenotypic diversity arising from adaptive molecular evolution. An individual spider can produce an array of specialized silks, with the majority of constituent silk proteins encoded by members of the spidroin gene family. Spidroins are dominated by tandem repeats flanked by short, non-repetitive N- and C-terminal coding regions. The remarkable mechanical properties of spider silks have been largely attributed to the repeat sequences. However, the molecular evolutionary processes acting on spidroin terminal and repetitive regions remain unclear due to a paucity of complete gene sequences and sampling of genetic variation among individuals. To better understand spider silk evolution, we characterize a complete aciniform spidroin gene from an Argiope orb-weaving spider and survey aciniform gene fragments from congeneric individuals.
Results
We present the complete aciniform spidroin (AcSp1) gene from the silver garden spider Argiope argentata (Aar_AcSp1), and document multiple AcSp1 loci in individual genomes of A. argentata and the congeneric A. trifasciata and A. aurantia. We find that Aar_AcSp1 repeats have >98% pairwise nucleotide identity. By comparing AcSp1 repeat amino acid sequences between Argiope species and with other genera, we identify regions of conservation over vast amounts of evolutionary time. Through a PCR survey of individual A. argentata, A. trifasciata, and A. aurantia genomes, we ascertain that AcSp1 repeats show limited variation between species whereas terminal regions are more divergent. We also find that average dN/dS across codons in the N-terminal, repetitive, and C-terminal encoding regions indicate purifying selection that is strongest in the N-terminal region.
Conclusions
Using the complete A. argentata AcSp1 gene and spidroin genetic variation between individuals, this study clarifies some of the molecular evolutionary processes underlying the spectacular mechanical attributes of aciniform silk. It is likely that intragenic concerted evolution and functional constraints on A. argentata AcSp1 repeats result in extreme repeat homogeneity. The maintenance of multiple AcSp1 encoding loci in Argiope genomes supports the hypothesis that Argiope spiders require rapid and efficient protein production to support their prolific use of aciniform silk for prey-wrapping and web-decorating. In addition, multiple gene copies may represent the early stages of spidroin diversification.
doi:10.1186/1471-2148-14-31
PMCID: PMC3933166  PMID: 24552485
AcSp1; Concerted evolution; Intragenic homogenization; Multiple loci; Silk; Spidroin; Spider
8.  From algae to angiosperms–inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes 
Background
Next-generation sequencing has provided a wealth of plastid genome sequence data from an increasingly diverse set of green plants (Viridiplantae). Although these data have helped resolve the phylogeny of numerous clades (e.g., green algae, angiosperms, and gymnosperms), their utility for inferring relationships across all green plants is uncertain. Viridiplantae originated 700-1500 million years ago and may comprise as many as 500,000 species. This clade represents a major source of photosynthetic carbon and contains an immense diversity of life forms, including some of the smallest and largest eukaryotes. Here we explore the limits and challenges of inferring a comprehensive green plant phylogeny from available complete or nearly complete plastid genome sequence data.
Results
We assembled protein-coding sequence data for 78 genes from 360 diverse green plant taxa with complete or nearly complete plastid genome sequences available from GenBank. Phylogenetic analyses of the plastid data recovered well-supported backbone relationships and strong support for relationships that were not observed in previous analyses of major subclades within Viridiplantae. However, there also is evidence of systematic error in some analyses. In several instances we obtained strongly supported but conflicting topologies from analyses of nucleotides versus amino acid characters, and the considerable variation in GC content among lineages and within single genomes affected the phylogenetic placement of several taxa.
Conclusions
Analyses of the plastid sequence data recovered a strongly supported framework of relationships for green plants. This framework includes: i) the placement of Zygnematophyceace as sister to land plants (Embryophyta), ii) a clade of extant gymnosperms (Acrogymnospermae) with cycads + Ginkgo sister to remaining extant gymnosperms and with gnetophytes (Gnetophyta) sister to non-Pinaceae conifers (Gnecup trees), and iii) within the monilophyte clade (Monilophyta), Equisetales + Psilotales are sister to Marattiales + leptosporangiate ferns. Our analyses also highlight the challenges of using plastid genome sequences in deep-level phylogenomic analyses, and we provide suggestions for future analyses that will likely incorporate plastid genome sequence data for thousands of species. We particularly emphasize the importance of exploring the effects of different partitioning and character coding strategies.
doi:10.1186/1471-2148-14-23
PMCID: PMC3933183  PMID: 24533922
Composition bias; Phylogenomics; Plastid genome sequences; Plastomes; RY-coding; Viridiplantae
9.  Population structure of guppies in north-eastern Venezuela, the area of putative incipient speciation 
Background
Geographic barriers to gene flow and divergence among populations in sexual traits are two important causes of genetic isolation which may lead to speciation. Genetic isolation may be facilitated if these two mechanisms act synergistically. The guppy from the Cumaná region (within the Cariaco drainage) of eastern Venezuela has been previously described as a case of incipient speciation driven by sexual selection, significantly differentiated in sexual colouration and body shape from the common guppy, Poecilia reticulata. The latter occurs widely in northern Venezuela, including the south-eastern side of Cordillera de la Costa, where it inhabits streams belonging to the San Juan drainage. Here, we present molecular and morphological analyses of differentiation among guppy populations in the Cariaco and San Juan drainages. Our analyses are based on a 953 bp long mtDNA fragment, a set of 15 microsatellites (519 fish from 20 populations), and four phenotypic traits.
Results
Both microsatellite and mtDNA data showed that guppies inhabiting the two drainages are characterised by a significant genetic differentiation, but a higher proportion of the genetic variance was distributed among populations within regions. Most guppies in the Cariaco drainage had mtDNA from a distinct lineage, but we also found evidence for widespread introgression of mtDNA from the San Juan drainage into the Cariaco drainage. Phenotypically, populations in the two regions differed significantly only in the number of black crescents. Phenotypic clustering did not support existence of two distinct groupings, but indicated a degree of distinctiveness of Central Cumaná (CC) population. However, CC population showed little differentiation at the neutral markers from the proximate populations within the Cariaco drainage.
Conclusions
Our findings are consistent with only partial genetic isolation between the two geographic regions and indicate that the geographic barrier of Cordillera de la Costa has not played an important role in strengthening the incomplete pre-zygotic reproductive barrier between Cumaná and common guppy. Significant phenotypic differentiation between genetically similar (in terms of neutral variation) populations suggests that mate choice can maintain divergence at sexually selected traits despite gene flow. However, neither genetic nor phenotypic clustering supported delineation of two species within the region.
doi:10.1186/1471-2148-14-28
PMCID: PMC3942120  PMID: 24533965
Gene flow; Introgression; Reproductive barriers; Sexual selection; mtDNA; Microsatellites
10.  Erosive processes after tectonic uplift stimulate vicariant and adaptive speciation: evolution in an Afrotemperate-endemic paper daisy genus 
Background
The role of tectonic uplift in stimulating speciation in South Africa’s only alpine zone, the Drakensberg, has not been explicitly examined. Tectonic processes may influence speciation both through the creation of novel habitats and by physically isolating plant populations. We use the Afrotemperate endemic daisy genus Macowania to explore the timing and mode (geographic versus adaptive) of speciation in this region. Between sister species pairs we expect high morphological divergence where speciation has happened in sympatry (adaptive) while with geographic (vicariant) speciation we may expect to find less morphological divergence and a greater degree of allopatry. A dated molecular phylogenetic hypothesis for Macowania elucidates species’ relationships and is used to address the potential impact of uplift on diversification. Morphological divergence of a small sample of reproductive and vegetative characters, used as a proxy for adaptive divergence, is measured against species’ range distributions to estimate mode of speciation across two subclades in the genus.
Results
The Macowania crown age is consistent with the hypothesis of post-uplift diversification, and we find evidence for both vicariant and adaptive speciation between the two subclades within Macowania. Both subclades exhibit strong signals of range allopatry, suggesting that geographic isolation was important in speciation. One subclade, associated with dry, rocky environments at high altitudes, shows very little morphological and ecological differentiation but high range allopatry. The other subclade occupies a greater variety of habitats and exhibits far greater morphological differentiation, but contains species with overlapping distribution ranges.
Conclusions
Species in Macowania are likely to have diversified in response to tectonic uplift, and we invoke uplift and uplift-mediated erosion as the main drivers of speciation. The greater relative morphological divergence in sympatric species of Macowania indicates that speciation in the non-sympatric taxa may not have required obvious adaptive differences, implying that simple geographic isolation was the driving force for speciation (‘neutral speciation’).
doi:10.1186/1471-2148-14-27
PMCID: PMC3927823  PMID: 24524661
Afrotemperate; Drakensberg; Uplift; Adaptive speciation; Vicariance; Gnaphalieae
11.  Evolutionary insights about bacterial GlxRS from whole genome analyses: is GluRS2 a chimera? 
Background
Evolutionary histories of glutamyl-tRNA synthetase (GluRS) and glutaminyl-tRNA synthetase (GlnRS) in bacteria are convoluted. After the divergence of eubacteria and eukarya, bacterial GluRS glutamylated both tRNAGln and tRNAGlu until GlnRS appeared by horizontal gene transfer (HGT) from eukaryotes or a duplicate copy of GluRS (GluRS2) that only glutamylates tRNAGln appeared. The current understanding is based on limited sequence data and not always compatible with available experimental results. In particular, the origin of GluRS2 is poorly understood.
Results
A large database of bacterial GluRS, GlnRS, tRNAGln and the trimeric aminoacyl-tRNA-dependent amidotransferase (gatCAB), constructed from whole genomes by functionally annotating and classifying these enzymes according to their mutual presence and absence in the genome, was analyzed. Phylogenetic analyses showed that the catalytic and the anticodon-binding domains of functional GluRS2 (as in Helicobacter pylori) were independently acquired from evolutionarily distant hosts by HGT. Non-functional GluRS2 (as in Thermotoga maritima), on the other hand, was found to contain an anticodon-binding domain appended to a gene-duplicated catalytic domain. Several genomes were found to possess both GluRS2 and GlnRS, even though they share the common function of aminoacylating tRNAGln. GlnRS was widely distributed among bacterial phyla and although phylogenetic analyses confirmed the origin of most bacterial GlnRS to be through a single HGT from eukarya, many GlnRS sequences also appeared with evolutionarily distant phyla in phylogenetic tree. A GlnRS pseudogene could be identified in Sorangium cellulosum.
Conclusions
Our analysis broadens the current understanding of bacterial GlxRS evolution and highlights the idiosyncratic evolution of GluRS2. Specifically we show that: i) GluRS2 is a chimera of mismatching catalytic and anticodon-binding domains, ii) the appearance of GlnRS and GluRS2 in a single bacterial genome indicating that the evolutionary histories of the two enzymes are distinct, iii) GlnRS is more widespread in bacteria than is believed, iv) bacterial GlnRS appeared both by HGT from eukarya and intra-bacterial HGT, v) presence of GlnRS pseudogene shows that many bacteria could not retain the newly acquired eukaryal GlnRS. The functional annotation of GluRS, without recourse to experiments, performed in this work, demonstrates the inherent and unique advantages of using whole genome over isolated sequence databases.
doi:10.1186/1471-2148-14-26
PMCID: PMC3927822  PMID: 24521160
GluRS; GluRS2; GlnRS; HGT; tRNAGln; Gene duplication; Phylum-specificity; Whole-genome analysis
12.  The evolution of paralogous enzymes MAT and MATX within the Euglenida and beyond 
Background
Methionine adenosyltransferase (MAT) is a ubiquitous essential enzyme that, in eukaryotes, occurs in two relatively divergent paralogues: MAT and MATX. MATX has a punctate distribution across the tree of eukaryotes and, except for a few cases, is mutually exclusive with MAT. This phylogenetic pattern could have arisen by either differential loss of old paralogues or the spread of one of these paralogues by horizontal gene transfer. Our aim was to map the distribution of MAT/MATX genes within the Euglenida in order to more comprehensively characterize the evolutionary history of MATX.
Results
We generated 26 new sequences from 23 different lineages of euglenids and one prasinophyte alga Pyramimonas parkeae. MATX was present only in photoautotrophic euglenids. The mixotroph Rapaza viridis and the prasinophyte alga Pyramimonas parkeae, which harbors chloroplasts that are most closely related to the chloroplasts in photoautotrophic euglenids, both possessed only the MAT paralogue. We found both the MAT and MATX paralogues in two photoautotrophic species (Phacus orbicularis and Monomorphina pyrum). The significant conflict between eukaryotic phylogenies inferred from MATX and SSU rDNA data represents strong evidence that MATX paralogues have undergone horizontal gene transfer across the tree of eukaryotes.
Conclusions
Our results suggest that MATX entered the euglenid lineage in a single horizontal gene transfer event that took place after the secondary endosymbiotic origin of the euglenid chloroplast. The origin of the MATX paralogue is unclear, and it cannot be excluded that it arose by a gene duplication event before the most recent common ancestor of eukaryotes.
doi:10.1186/1471-2148-14-25
PMCID: PMC3923989  PMID: 24517416
Methionine adenosyltransferase; Horizontal gene transfer; Deep paralogy; Gene evolution; Euglenozoa
13.  Development of the ultrastructure of sonic muscles: a kind of neoteny? 
Background
Drumming muscles of some sound-producing fish are ‘champions’ of contraction speed, their rate setting the fundamental frequency. In the piranha, contraction of these muscles at 150 Hz drives a sound at the same frequency. Drumming muscles of different not closely related species show evolutionary convergences. Interestingly, some characters of sonic muscles can also be found in the trunk muscles of newly hatched larvae that are able to maintain tail beat frequencies up to 100 Hz. The aim of this work was to study the development of sound production and sonic and epaxial muscles simultaneously in the red bellied piranhas (Pygocentrus nattereri) to seek for possible common characteristics.
Results
Call, pulse and period durations increased significantly with the fish size, but the call dominant frequencies decreased, and the number of pulses and the call amplitude formed a bell curve. In epaxial muscles, the fibre diameters of younger fish are first positioned in the graphical slope corresponding to sonic muscles, before diverging. The fibre diameter of older fish trunk muscles was bigger, and the area of the myofibrils was larger than in sonic muscles. Moreover, in two of the biggest fish, the sonic muscles were invaded by fat cells and the sonic muscle ultrastructure was similar to the epaxial one. These two fish were also unable to produce any sound, meaning they lost their ability to contract quickly.
Conclusions
The volume occupied by myofibrils determines the force of contraction, the volume of sarcoplasmic reticulum sets the contraction frequency, and the volume of mitochondria sets the level of sustained performance. The functional outcomes in muscles are all attributable to shifts in the proportions of those structures. A single delay in the development restricts the quantity of myofibrils, maintains a high proportion of space in the sarcoplasm and develops sarcoplasmic reticulum. High-speed sonic muscles could thus be skeletal muscles with delayed development. This hypothesis has the advantage that it could easily explain why high-speed sonic muscles have evolved so many times in different lineages.
doi:10.1186/1471-2148-14-24
PMCID: PMC3924398  PMID: 24507247
Piranha; Call; Development; Pygocentrus; Sonic muscle
14.  Cannibalism in invasive, native and biocontrol populations of the harlequin ladybird 
Background
Cannibalism is widespread in both vertebrates and invertebrates but its extent is variable between and within species. Cannibalism depends on population density and nutritional conditions, and could be beneficial during colonisation of new environments. Empirical studies are needed to determine whether this trait might facilitate invasion of a new area in natural systems. We investigated whether the propensity for cannibalism in H. axyridis differs both between native and invasive populations and between invasive populations from the core and from the front of the invasive area in Western Europe. We also compared the propensity for cannibalism of these natural populations with that of laboratory-reared biocontrol populations. We measured the cannibalism rates of eggs by first instar larvae and adult females at two different individual densities of ladybirds from three types of population (invasive, native and biocontrol), in laboratory-controlled conditions.
Results
Cannibalism was significantly greater in larvae from invasive populations compared to native or biocontrol populations, but there was no difference in cannibalism rates between populations from the core or front of the invaded range. Cannibalism was significantly lower in larvae from biocontrol populations compared to wild (invasive and native) populations. No differences in cannibalism rates of adult females were found between any populations. While high population density significantly increased cannibalism in both larvae and adults, the norm of reaction of cannibalism to individual density did not change significantly during the invasion and/or laboratory rearing processes.
Conclusion
This study is the first to provide evidence for a higher propensity for cannibalism in invasive populations compared to native ones. Our experiments also shed light on the difference in cannibalism evolution with respect to life stages. However, we are still at an early stage in understanding the underlying mechanisms and several different research perspectives are needed to determine whether the higher propensity for cannibalism is a general feature of the invasion process.
doi:10.1186/1471-2148-14-15
PMCID: PMC3913791  PMID: 24495338
Harmonia axyridis; Cannibalism; Evolution; Invasive; Native and biocontrol populations
15.  Environmental quality alters female costs and benefits of evolving under enforced monogamy 
Background
Currently many habitats suffer from quality loss due to environmental change. As a consequence, evolutionary trajectories might shift due to environmental effects and potentially increase extinction risk of resident populations. Nevertheless, environmental variation has rarely been incorporated in studies of sexual selection and sexual conflict, although local environments and individuals’ condition undoubtedly influence costs and benefits. Here, we utilise polyandrous and monogamous selection lines of flour beetles, which evolved in presence or absence of sexual selection for 39 generations. We specifically investigated effects of low vs. standard food quality (i.e. stressful vs. benign environments) on reproductive success of cross pairs between beetles from the contrasting female and male selection histories to assess gender effects driving fitness.
Results
We found a clear interaction of food quality, male selection history and female selection history. Monogamous females generally performed more poorly than polyandrous counterparts, but reproductive success was shaped by selection history of their mates and environmental quality. When monogamous females were paired with polyandrous males in the standard benign environment, females seemed to incur costs, possibly due to sexual conflict. In contrast, in the novel stressful environment, monogamous females profited from mating with polyandrous males, indicating benefits of sexual selection outweigh costs.
Conclusions
Our findings suggest that costs and benefits of sexually selected adaptations in both sexes can be profoundly altered by environmental quality. With regard to understanding possible impacts of environmental change, our results further show that the ecology of mating systems and associated selection pressures should be considered in greater detail.
doi:10.1186/1471-2148-14-21
PMCID: PMC3922901  PMID: 24499414
Sexual conflict; Tribolium; Polyandry; Monogamy; Mating costs; Reproductive success
16.  Multiple hybridization events, polyploidy and low postmating isolation entangle the evolution of neotropical species of Epidendrum (Orchidaceae) 
Background
Hybridization and polyploidy are central processes in evolution and speciation. These mechanisms often lead to complex patterns of genetic variation and the creation of novel genotypes, which may establish if they become isolated from gene flow. However, in the absence of reproductive isolation, species boundaries might easily be disrupted. Here, we used a combination of AFLPs, chloroplast DNA markers and flow cytometry to investigate the evolutionary outcomes of hybridization between two endemic Ecuadorian species of Epidendrum (E. madsenii and E. rhopalostele) in three hybrid zones. Postmating isolation was also quantified to determine the role of this barrier in restraining gene flow between hybrids and the parental species. In addition, future ecological niche models were constructed to predict the outcomes of hybridization between these species.
Results
Our results confirmed the presence of hybrids in all hybrid zones, but revealed that a third parental species (E. falcisepalum) has contributed to one of the hybrid zones studied. Backcross genotypes were frequent in all hybrid zones, which was in accordance with the absence of strong reproductive barriers. The process of hybridization was highly asymmetric and followed in some cases by polyploidy. The projection of future niche models predicted a severe reduction in the area suitable for the occurrence of these species, although favorable conditions will still occur for the existence of the current hybrid zones.
Conclusions
The recurrent process of hybridization has compromised the genetic integrity of the parental species. Most individuals of the parental species can no longer be considered as pure-bred individuals because most were classified as backcrossed hybrids. Novel genetic lineages occur in all hybrid zones implying that hybrids are fertile and can compete with the parental species. These results, together with the prediction of suitable conditions for the future occurrence of these hybrid zones, highlight the importance of conserving these geographic areas as sources of novel taxonomic entities.
doi:10.1186/1471-2148-14-20
PMCID: PMC3927766  PMID: 24495351
AFLPs; Conservation; Genome size; Orchids; Reproduction; Reticulate evolution
17.  Integrated shotgun sequencing and bioinformatics pipeline allows ultra-fast mitogenome recovery and confirms substantial gene rearrangements in Australian freshwater crayfishes 
Background
Although it is possible to recover the complete mitogenome directly from shotgun sequencing data, currently reported methods and pipelines are still relatively time consuming and costly. Using a sample of the Australian freshwater crayfish Engaeus lengana, we demonstrate that it is possible to achieve three-day turnaround time (four hours hands-on time) from tissue sample to NCBI-ready submission file through the integration of MiSeq sequencing platform, Nextera sample preparation protocol, MITObim assembly algorithm and MITOS annotation pipeline.
Results
The complete mitochondrial genome of the parastacid freshwater crayfish, Engaeus lengana, was recovered by modest shotgun sequencing (1.2 giga bases) using the Illumina MiSeq benchtop sequencing platform. Genome assembly using the MITObim mitogenome assembler recovered the mitochondrial genome as a single contig with a 97-fold mean coverage (min. = 17; max. = 138). The mitogenome consists of 15,934 base pairs and contains the typical 37 mitochondrial genes and a non-coding AT-rich region. The genome arrangement is similar to the only other published parastacid mitogenome from the Australian genus Cherax.
Conclusions
We infer that the gene order arrangement found in Cherax destructor is common to Australian crayfish and may be a derived feature of the southern hemisphere family Parastacidae. Further, we report to our knowledge, the simplest and fastest protocol for the recovery and assembly of complete mitochondrial genomes using the MiSeq benchtop sequencer.
doi:10.1186/1471-2148-14-19
PMCID: PMC3915555  PMID: 24484414
Freshwater crayfish; Mitochondrial genome characterization; Bench top sequencing; Engaeus; Parastacidae
18.  The effect of host social system on parasite population genetic structure: comparative population genetics of two ectoparasitic mites and their bat hosts 
Background
The population genetic structure of a parasite, and consequently its ability to adapt to a given host, is strongly linked to its own life history as well as the life history of its host. While the effects of parasite life history on their population genetic structure have received some attention, the effect of host social system has remained largely unstudied. In this study, we investigated the population genetic structure of two closely related parasitic mite species (Spinturnix myoti and Spinturnix bechsteini) with very similar life histories. Their respective hosts, the greater mouse-eared bat (Myotis myotis) and the Bechstein’s bat (Myotis bechsteinii) have social systems that differ in several substantial features, such as group size, mating system and dispersal patterns.
Results
We found that the two mite species have strongly differing population genetic structures. In S. myoti we found high levels of genetic diversity and very little pairwise differentiation, whereas in S. bechsteini we observed much less diversity, strongly differentiated populations and strong temporal turnover. These differences are likely to be the result of the differences in genetic drift and dispersal opportunities afforded to the two parasites by the different social systems of their hosts.
Conclusions
Our results suggest that host social system can strongly influence parasite population structure. As a result, the evolutionary potential of these two parasites with very similar life histories also differs, thereby affecting the risk and evolutionary pressure exerted by each parasite on its host.
doi:10.1186/1471-2148-14-18
PMCID: PMC3925363  PMID: 24479530
Coevolution; Host-parasite interaction; Local adaptation; Social system; Myotis myotis; Spinturnix myoti; Myotis bechsteinii; Spinturnix bechsteini
19.  Annual acknowledgement of reviewers 
Contributing reviewers
The editors of BMC Evolutionary Biology would like to thank all our reviewers who have contributed to the journal in Volume 13 (2013).
doi:10.1186/1471-2148-14-22
PMCID: PMC3905664
20.  Large-scale mitochondrial DNA analysis in Southeast Asia reveals evolutionary effects of cultural isolation in the multi-ethnic population of Myanmar 
Background
Myanmar is the largest country in mainland Southeast Asia with a population of 55 million people subdivided into more than 100 ethnic groups. Ruled by changing kingdoms and dynasties and lying on the trade route between India and China, Myanmar was influenced by numerous cultures. Since its independence from British occupation, tensions between the ruling Bamar and ethnic minorities increased.
Results
Our aim was to search for genetic footprints of Myanmar’s geographic, historic and sociocultural characteristics and to contribute to the picture of human colonization by describing and dating of new mitochondrial DNA (mtDNA) haplogroups. Therefore, we sequenced the mtDNA control region of 327 unrelated donors and the complete mitochondrial genome of 44 selected individuals according to highest quality standards.
Conclusion
Phylogenetic analyses of the entire mtDNA genomes uncovered eight new haplogroups and three unclassified basal M-lineages. The multi-ethnic population and the complex history of Myanmar were reflected in its mtDNA heterogeneity. Population genetic analyses of Burmese control region sequences combined with population data from neighboring countries revealed that the Myanmar haplogroup distribution showed a typical Southeast Asian pattern, but also Northeast Asian and Indian influences. The population structure of the extraordinarily diverse Bamar differed from that of the Karen people who displayed signs of genetic isolation. Migration analyses indicated a considerable genetic exchange with an overall positive migration balance from Myanmar to neighboring countries. Age estimates of the newly described haplogroups point to the existence of evolutionary windows where climatic and cultural changes gave rise to mitochondrial haplogroup diversification in Asia.
doi:10.1186/1471-2148-14-17
PMCID: PMC3913319  PMID: 24467713
Haplogroup; Complete mtDNA genome; Control region; Population genetics; Migration; Gene flow; Burma; Southeast Asia; Karen; Bamar; Demographic history
21.  Reassortment patterns of avian influenza virus internal segments among different subtypes 
Background
The segmented RNA genome of avian Influenza viruses (AIV) allows genetic reassortment between co-infecting viruses, providing an evolutionary pathway to generate genetic innovation. The genetic diversity (16 haemagglutinin and 9 neuraminidase subtypes) of AIV indicates an extensive reservoir of influenza viruses exists in bird populations, but how frequently subtypes reassort with each other is still unknown. Here we quantify the reassortment patterns among subtypes in the Eurasian avian viral pool by reconstructing the ancestral states of the subtypes as discrete states on time-scaled phylogenies with respect to the internal protein coding segments. We further analyzed how host species, the inferred evolutionary rates and the dN/dS ratio varied among segments and between discrete subtypes, and whether these factors may be associated with inter-subtype reassortment rate.
Results
The general patterns of reassortment are similar among five internal segments with the exception of segment 8, encoding the Non-Structural genes, which has a more divergent phylogeny. However, significant variation in rates between subtypes was observed. In particular, hemagglutinin-encoding segments of subtypes H5 to H9 reassort at a lower rate compared to those of H1 to H4, and Neuraminidase-encoding segments of subtypes N1 and N2 reassort less frequently than N3 to N9. Both host species and dN/dS ratio were significantly associated with reassortment rate, while evolutionary rate was not associated. The dN/dS ratio was negatively correlated with reassortment rate, as was the number of negatively selected sites for all segments.
Conclusions
These results indicate that overall selective constraint and host species are both associated with reassortment rate. These results together identify the wild bird population as the major source of new reassortants, rather than domestic poultry. The lower reassortment rates observed for H5N1 and H9N2 may be explained by the large proportion of strains derived from domestic poultry populations. In contrast, the higher rates observed in the H1N1, H3N8 and H4N6 subtypes could be due to their primary origin as infections of wild birds with multiple low pathogenicity strains in the large avian reservoir.
doi:10.1186/1471-2148-14-16
PMCID: PMC3905155  PMID: 24456010
22.  Female partner preferences enhance offspring ability to survive an infection 
Background
It is often suggested that mate choice enhances offspring immune resistance to infectious diseases. To test this hypothesis, we conducted a study with wild-derived house mice (Mus musculus musculus) in which females were experimentally mated either with their preferred or non-preferred male, and their offspring were infected with a mouse pathogen, Salmonella enterica (serovar Typhimurium).
Results
We found that offspring sired by preferred males were significantly more likely to survive the experimental infection compared to those sired by non-preferred males. We found no significant differences in the pathogen clearance or infection dynamics between the infected mice, suggesting that offspring from preferred males were better able to cope with infection and had improved tolerance rather than immune resistance.
Conclusion
Our results provide the first direct experimental evidence within a single study that partner preferences enhance offspring resistance to infectious diseases.
doi:10.1186/1471-2148-14-14
PMCID: PMC3905909  PMID: 24450606
Partner preference; Sexual selection; Mus musculus musculus; Salmonella; Pathogen clearance; Disease resistance; Pathogen-mediated sexual selection; Tolerance
23.  Generation of divergent uroplakin tetraspanins and their partners during vertebrate evolution: identification of novel uroplakins 
Background
The recent availability of sequenced genomes from a broad array of chordates (cephalochordates, urochordates and vertebrates) has allowed us to systematically analyze the evolution of uroplakins: tetraspanins (UPK1a and UPK1b families) and their respective partner proteins (UPK2 and UPK3 families).
Results
We report here: (1) the origin of uroplakins in the common ancestor of vertebrates, (2) the appearance of several residues that have statistically significantly positive dN/dS ratios in the duplicated paralogs of uroplakin genes, and (3) the existence of strong coevolutionary relationships between UPK1a/1b tetraspanins and their respective UPK2/UPK3-related partner proteins. Moreover, we report the existence of three new UPK2/3 family members we named UPK2b, 3c and 3d, which will help clarify the evolutionary relationships between fish, amphibian and mammalian uroplakins that may perform divergent functions specific to these different and physiologically distinct groups of vertebrates.
Conclusions
Since our analyses cover species of all major chordate groups this work provides an extremely clear overall picture of how the uroplakin families and their partner proteins have evolved in parallel. We also highlight several novel features of uroplakin evolution including the appearance of UPK2b and 3d in fish and UPK3c in the common ancestor of reptiles and mammals. Additional studies of these novel uroplakins should lead to new insights into uroplakin structure and function.
doi:10.1186/1471-2148-14-13
PMCID: PMC3922775  PMID: 24450554
24.  Temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity 
Background
Temporal variation in the genetic structure of populations can be caused by multiple factors, including natural selection, stochastic environmental variation, migration, or genetic drift. In benthic marine species, the developmental mode of larvae may indicate a possibility for temporal genetic variation: species with dispersive planktonic larvae are expected to be more likely to show temporal genetic variation than species with benthic or brooded non-dispersive larvae, due to differences in larval mortality and dispersal ability. We examined temporal genetic structure in populations of Pygospio elegans, a poecilogonous polychaete with within-species variation in developmental mode. P. elegans produces either planktonic, benthic, or intermediate larvae, varying both among and within populations, providing a within-species test of the generality of a relationship between temporal genetic variation and larval developmental mode.
Results
In contrast to our expectations, our microsatellite analyses of P. elegans revealed temporal genetic stability in the UK population with planktonic larvae, whereas there was variation indicative of drift in temporal samples of the populations from the Baltic Sea, which have predominantly benthic and intermediate larvae. We also detected temporal variation in relatedness within these populations. A large temporal shift in genetic structure was detected in a population from the Netherlands, having multiple developmental modes. This shift could have been caused by local extiction due to extreme environmental conditions and (re)colonization by planktonic larvae from neighboring populations.
Conclusions
In our study of P. elegans, temporal genetic variation appears to be due to not only larval developmental mode, but also the stochastic environment of adults. Large temporal genetic shifts may be more likely in marine intertidal habitats (e.g. North Sea and Wadden Sea) which are more prone to environmental stochasticity than the sub-tidal Baltic habitats. Sub-tidal and/or brackish (less saline) habitats may support smaller P. elegans populations and these may be more susceptible to the effects of random genetic drift. Moreover, higher frequencies of asexual reproduction and the benthic larval developmental mode in these populations leads to higher relatedness and contributes to drift. Our results indicate that a general relationship between larval developmental mode and temporal genetic variation may not exist.
doi:10.1186/1471-2148-14-12
PMCID: PMC3905951  PMID: 24447386
Pygospio elegans; Poecilogony; Population genetics; Developmental mode; Genetic drift; Temporal; Sweepstakes reproductive success; Full-sibs
25.  Evolutionary classification of ammonium, nitrate, and peptide transporters in land plants 
Background
Nitrogen uptake, reallocation within the plant, and between subcellular compartments involves ammonium, nitrate and peptide transporters. Ammonium transporters are separated into two distinct families (AMT1 and AMT2), each comprised of five members on average in angiosperms. Nitrate transporters also form two discrete families (NRT1 and NRT2), with angiosperms having four NRT2s, on average. NRT1s share an evolutionary history with peptide transporters (PTRs). The NRT1/PTR family in land plants usually has more than 50 members and contains also members with distinct activities, such as glucosinolate and abscisic acid transport.
Results
Phylogenetic reconstructions of each family across 20 land plant species with available genome sequences were supplemented with subcellular localization and transmembrane topology predictions. This revealed that both AMT families diverged prior to the separation of bryophytes and vascular plants forming two distinct clans, designated as supergroups, each. Ten supergroups were identified for the NRT1/PTR family. It is apparent that nitrate and peptide transport within the NRT1/PTR family is polyphyletic, that is, nitrate and/or peptide transport likely evolved multiple times within land plants. The NRT2 family separated into two distinct clans early in vascular plant evolution. Subsequent duplications occurring prior to the eudicot/monocot separation led to the existence of two AMT1, six AMT2, 31 NRT1/PTR, and two NRT2 clans, designated as groups.
Conclusion
Phylogenetic separation of groups suggests functional divergence within the angiosperms for each family. Distinct groups within the NRT1/PTR family appear to separate peptide and nitrate transport activities as well as other activities contained within the family, for example nitrite transport. Conversely, distinct activities, such as abscisic acid and glucosinolate transport, appear to have recently evolved from nitrate transporters.
doi:10.1186/1471-2148-14-11
PMCID: PMC3922906  PMID: 24438197
Ammonium transporter (AMT1 and AMT2); Nitrate transporter (NRT1 and NRT2); Peptide transporter (PTR); Gene family evolution

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