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BMC Evolutionary Biology
The latest research articles published by BMC Evolutionary Biology
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September 29, 2014
Background: Myxozoa are a diverse group of metazoan parasites with a very simple organization, which has for decades eluded their evolutionary origin. Their most prominent and characteristic feature is the polar capsule: a complex intracellular structure of the myxozoan spore, which plays a role in host infection. Striking morphological similarities have been found between myxozoan polar capsules and nematocysts, the stinging structures of cnidarians (corals, sea anemones and jellyfish) leading to the suggestion that Myxozoa and Cnidaria share a more recent common ancestry. This hypothesis has recently been supported by phylogenomic evidence and by the identification of a nematocyst specific minicollagen gene in the myxozoan Tetracapsuloides bryosalmonae. Here we searched genomes and transcriptomes of several myxozoan taxa for the presence of additional cnidarian specific genes and characterized these genes within a phylogenetic context. Results: Illumina assemblies of transcriptome or genome data of three myxozoan species (Enteromyxum leei, Kudoa iwatai, and Sphaeromyxa zaharoni) and of the enigmatic cnidarian parasite Polypodium hydriforme (Polypodiozoa) were mined using tBlastn searches with nematocyst-specific proteins as queries. Several orthologs of nematogalectins and minicollagens were identified. Our phylogenetic analyses indicate that myxozoans possess three distinct minicollagens. We found that the cnidarian repertoire of nematogalectins is more complex than previously thought and we identified additional members of the nematogalectin family. Cnidarians were found to possess four nematogalectin / nematogalectin-related genes, while in myxozoans only three genes could be identified. Conclusions: Our results demonstrate that myxozoans possess a diverse array of genes that are taxonomically restricted to Cnidaria. Characterization of these genes provide compelling evidence that polar capsules and nematocysts are homologous structures and that myxozoans are highly degenerate cnidarians. The diversity of minicollagens was higher than previously thought, with the presence of three minicollagen genes in myxozoans. Our phylogenetic results suggest that the different myxozoan sequences are the results of ancient divergences within Cnidaria and not of recent specializations of the polar capsule. For both minicollagen and nematogalectin, our results show that myxozoans possess less gene copies than their cnidarian counter parts, suggesting that the polar capsule gene repertoire was simplified with their reduced body plan.
September 27, 2014
Background: Nicrophorus vespilloides eggs are deposited into the soil in close proximity to the decomposing vertebrate carcasses that these insects use as an obligate resource to rear their offspring. Eggs in this environment potentially face significant risks from the bacteria that proliferate in the grave-soil environment following nutrient influx from the decomposing carcass. Our aims in this paper are twofold: first, to examine the fitness effects of grave-soil bacteria to eggs, and second, to quantify egg immunocompetence as a defence against these bacteria. Results: Our results provide strong evidence that grave-soil microbes significantly reduce the survival of Nicrophorus eggs. Females provided with microbe rich carcasses to rear broods laid fewer eggs that were less likely to hatch than females given uncontaminated carcasses. Furthermore, we show that egg hatch success is significantly reduced by bacterial exposure. Using a split-brood design, which controlled for intrinsic differences in eggs produced by different females, we found that eggs washed free of surface-associated bacteria show increased survival compared to unwashed eggs. By contrast, eggs exposed to the entomopathogen Serratia marcescens show decreased survival compared to unexposed eggs. We next tested the immune competence of eggs under challenge from bacterial infection, and found that eggs lacked endogenous production of antimicrobial peptides, despite well-developed responses in larvae. Finally, we found that despite lacking immunity, N. vespilloides eggs produce an extraembryonic serosa, indicating that the serosa has lost its immune inducing capacity in this species. Conclusions: The dependency on ephemeral resources might strongly select for fast developing animals. Our results suggest that Nicrophorus carrion beetles, and other species developing on ephemeral resources, face a fundamental trade-off between egg immunity and development time.
September 25, 2014
Background: MicroRNAs (miRNAs) are small non-coding RNA molecules with an important role upon post-transcriptional regulation. These molecules have been shown essential for several cellular processes in vertebrates, including muscle biology. Many miRNAs were described as exclusively or highly expressed in skeletal and/or cardiac muscle. However, knowledge on the genomic organization and evolution of muscle miRNAs has been unveiled in a reduced number of vertebrates and mostly only reflects their organization in mammals, whereas fish genomes remain largely uncharted. The main goal of this study was to elucidate particular features in the genomic organization and the putative evolutionary history of muscle miRNAs through a genome-wide comparative analysis of cartilaginous and bony fish genomes. Results: As major outcomes we show that (1) miR-208 was unexpectedly absent in cartilaginous and ray-finned fish genomes whereas it still exist in other vertebrate groups; (2) miR-499 was intergenic in medaka and stickleback conversely to other vertebrates where this miRNA is intronic; (3) the zebrafish genome is the unique harboring two extra paralogous copies of miR-499 and their host gene (Myh7b); (4) a rare deletion event of the intergenic and bicistronic cluster miR-1-1/133a-2 took place only into Tetraodontiformes genomes (pufferfish and spotted green puffer); (5) the zebrafish genome experienced a duplication event of miR-206/-133b; and (6) miR-214 was specifically duplicated in species belonging to superorder Acanthopterygii. Conclusions: Despite of the aforementioned singularities in fish genomes, large syntenic blocks containing muscle-enriched miRNAs were found to persist, denoting colligated functionality between miRNAs and neighboring genes. Based on the genomic data here obtained, we envisioned a feasible scenario for explaining muscle miRNAs evolution in vertebrates.
September 24, 2014
Evolutionary history of a vanishing radiation: isolation-dependent persistence and diversification in Pacific Island partulid tree snails
Background: Partulid tree snails are endemic to Pacific high islands and have experienced extraordinary rates of extinction in recent decades. Although they collectively range across a 10,000?km swath of Oceania, half of the family?s total species diversity is endemic to a single Eastern Pacific hot spot archipelago (the Society Islands) and all three partulid genera display highly distinctive distributions. Our goal was to investigate broad scale (range wide) and fine scale (within?Society Islands) molecular phylogenetic relationships of the two widespread genera, Partula and Samoana. What can such data tell us regarding the genesis of such divergent generic distribution patterns, and nominal species diversity levels across Oceania? Results: Museum, captive (zoo) and contemporary field specimens enabled us to genotype 54 of the ~120 recognized species, including many extinct or extirpated taxa, from 14 archipelagoes. The genera Partula and Samoana are products of very distinct diversification processes. Originating at the western edge of the familial range, the derived genus Samoana is a relatively recent arrival in the far eastern archipelagoes (Society, Austral, Marquesas) where it exhibits a stepping?stone phylogenetic pattern and has proven adept at both intra?and inter? archipelago colonization. The pronounced east?west geographic disjunction exhibited by the genus Partula stems from a much older long-distance dispersal event and its high taxonomic diversity in the Society Islands is a product of a long history of within?archipelago diversification. Conclusions: The central importance of isolation for partulid lineage persistence and diversification is evident in time-calibrated phylogenetic trees that show that remote archipelagoes least impacted by continental biotas bear the oldest clades and/or the most speciose radiations. In contemporary Oceania, that isolation is being progressively undermined and these tree snails are now directly exposed to introduced continental predators throughout the family?s range. Persistence of partulids in the wild will require proactive exclusion of alien predators in at least some designated refuge islands.
September 23, 2014
Background: A central question for understanding the evolutionary responses of plant species to rapidly changing environments is the assessment of their potential for short-term (in one or a few generations) genetic change. In our study, we consider the case of Pinus pinaster Aiton (maritime pine), a widespread Mediterranean tree, and (i) test, under different experimental conditions (growth chamber and semi-natural), whether higher recruitment in the wild from the most successful mothers is due to better performance of their offspring; and (ii) evaluate genetic change in quantitative traits across generations at two different life stages (mature trees and seedlings) that are known to be under strong selection pressure in forest trees. Results: Genetic control was high for most traits (h 2 = 0.137-0.876) under the milder conditions of the growth chamber, but only for ontogenetic change (0.276), total height (0.415) and survival (0.719) under the more stressful semi-natural conditions. Significant phenotypic selection gradients were found in mature trees for traits related to seed quality (germination rate and number of empty seeds). Moreover, female relative reproductive success was significantly correlated with offspring performance for specific leaf area (SLA) in the growth chamber experiment, and stem mass fraction (SMF) in the experiment under semi-natural conditions, two adaptive traits related to abiotic stress-response in pines. Selection gradients based on genetic covariance of seedling traits and responses to selection at this stage involved traits related to biomass allocation (SMF) and growth (as decomposed by a Gompertz model) or delayed ontogenetic change, depending also on the testing environment. Conclusions: Despite the evidence of microevolutionary change in adaptive traits in maritime pine, directional or disruptive changes are difficult to predict due to variable selection at different life stages and environments. At mature-tree stages, higher female effective reproductive success can be explained by differences in their production of offspring (due to seed quality) and, to a lesser extent, by seemingly better adapted seedlings. Selection gradients and responses to selection for seedlings also differed across experimental conditions. The distinct processes involved at the two life stages (mature trees or seedlings) together with environment-specific responses advice caution when predicting likely evolutionary responses to environmental change in Mediterranean forest trees.
September 22, 2014
Background: The release of radioactive materials due to the Fukushima nuclear accident has raised concern regarding the biological impacts of ingesting radioactively contaminated diets on organisms. We previously performed an internal exposure experiment in which contaminated leaves collected from polluted areas were fed to larvae of the pale grass blue butterfly, Zizeeria maha, from Okinawa, which is one of the least polluted localities in Japan. Using the same experimental system, in the present study, we further examined the effects of low-level-contaminated diets on this butterfly. Leaves were collected from two localities in Tohoku (Motomiya (161 Bq/kg) and Koriyama (117 Bq/kg)); two in Kanto (Kashiwa (47.6 Bq/kg) and Musashino (6.4 Bq/kg)); one in Tokai (Atami (2.5 Bq/kg)); and from Okinawa (0.2 Bq/kg). In addition to the effects on the first generation, we examined the possible transgenerational effects of the diets on the next generation. Results: In the first generation, the Tohoku groups showed higher rates of mortality and abnormalities and a smaller forewing size than the Okinawa group. The mortality rates were largely dependent on the ingested dose of caesium. The survival rates of the Kanto-Tokai groups were greater than 80%, but the rates in the Tohoku groups were much lower. In the next generation, the survival rates in the Tohoku groups were below 20%, whereas those of the Okinawa groups were above 70%. The survival rates in the second generation were independent of the locality of the leaves ingested by the first generation, indicating that the diet in the second generation was the determinant of their survival. Moreover, a smaller forewing size was observed in the Tohoku groups in the second generation. However, the forewing size was inversely correlated with the cumulative caesium dose ingested throughout the first and second generations, indicating that the diet in the first generation also influenced the forewing size of the second generation. Conclusions: Biological effects are detectable under a low ingested dose of radioactivity from a contaminated diet. The effects are transgenerational but can be overcome by ingesting a non-contaminated diet, suggesting that at least some of the observed effects are attributable to non-genetic physiological changes.
September 18, 2014
Molecular species delimitation of a symbiotic fig-pollinating wasp species complex reveals extreme deviation from reciprocal partner specificity
Background: Symbiotic relationships have contributed to major evolutionary innovations, the maintenance of fundamental ecosystem functions, and the generation and maintenance of biodiversity. However, the exact nature of host/symbiont associations, which has important consequences for their dynamics, is often poorly known due to limited understanding of symbiont taxonomy and species diversity. Among classical symbioses, figs and their pollinating wasps constitute a highly diverse keystone resource in tropical forest and savannah environments. Historically, they were considered to exemplify extreme reciprocal partner specificity (one-to-one host-symbiont species relationships), but recent work has revealed several more complex cases. However, there is a striking lack of studies with the specific aims of assessing symbiont diversity and how this varies across the geographic range of the host. Results: Here, we use molecular methods to investigate cryptic diversity in the pollinating wasps of a widespread Australian fig species. Standard barcoding genes and methods were not conclusive, but incorporation of phylogenetic analyses and a recently developed nuclear barcoding gene (ITS2), gave strong support for five pollinator species. Each pollinator species was most common in a different geographic region, emphasising the importance of wide geographic sampling to uncover diversity, and the scope for divergence in coevolutionary trajectories across the host plant range. In addition, most regions had multiple coexisting pollinators, raising the question of how they coexist in apparently similar or identical resource niches. Conclusion: Our study offers a striking example of extreme deviation from reciprocal partner specificity over the full geographical range of a fig-wasp system. It also suggests that superficially identical species may be able to co-exist in a mutualistic setting albeit at different frequencies in relation to their fig host’s range. We show that comprehensive sampling and molecular taxonomic techniques may be required to uncover the true structure of cryptic biodiversity underpinning intimate ecological interactions.
September 15, 2014
Causes of endemic radiation in the Caribbean: evidence from the historical biogeography and diversification of the butterfly genus Calisto (Nymphalidae: Satyrinae: Satyrini)
Background: Calisto is the largest butterfly genus in the West Indies but its systematics, historical biogeography and the causes of its diversification have not been previously rigorously evaluated. Several studies attempting to explain the wide-ranging diversity of Calisto gave different weights to vicariance, dispersal and adaptive radiation. We utilized molecular phylogenetic approaches and secondary calibrations points to estimate lineage ages. In addition, we used the dispersal-extinction-cladogenesis model and Caribbean paleogeographical information to reconstruct ancestral geographical distributions. We also evaluated different models of diversification to estimate the dynamics of lineage radiation within Calisto. By understanding the evolution of Calisto butterflies, we attempt to identify the main processes acting on insular insect diversity and the causes of its origin and its maintenance. Results: The crown age of Calisto was estimated to the early Oligocene (31 ± 5 Ma), and a single shift in diversification rate following a diversity-dependent speciation process was the best explanation for the present-day diversity found within the genus. A major increase in diversification rate was recovered at 14 Ma, following geological arrangements that favoured the availability of empty niches. Inferred ancestral distributional ranges suggested that the origin of extant Calisto is in agreement with a vicariant model and the origin of the Cuban lineage was likely the result of vicariance caused by the Cuba-Hispaniola split. A long-distance dispersal was the best explanation for the colonization of Jamaica and the Bahamas. Conclusions: The ancestral geographical distribution of Calisto is in line with the paleogeographical model of Caribbean colonization, which favours island-to-island vicariance. Because the sister lineage of Calisto remains ambiguous, its arrival to the West Indies remains to be explained, although, given its age and historical biogeography, the hypothesized GAARlandia land bridge might have been a plausible introduction route from continental America. Intra-island radiation caused by ecological innovation and the abiotic creation of niche spaces was found to be the main force shaping Calisto diversity and island endemism in Hispaniola and Cuba.
September 13, 2014
Background: The Metabolic Theory of Ecology (MTE) predicts that gestation duration, lactation duration, and their sum, total development time, are constrained by mass-specific basal metabolic rate such that they should scale with body mass with an exponent of 0.25. However, tests of the MTE’s predictions have yielded mixed results. In an effort to resolve this uncertainty, we used phylogenetically-controlled regression to investigate the allometries of gestation duration, lactation duration, and total development time in four well-studied mammalian orders, Artiodactyla, Carnivora, Primates, and Rodentia. Results: The results we obtained are not consistent with the predictions of the MTE. Gestation duration scaling exponents are below 0.25 in all four orders. The scaling exponent for lactation duration is below 0.25 in Carnivora and Rodentia, indistinguishable from 0.25 in Artiodactyls, and steeper than 0.25 in Primates. Total development time scales with body mass as predicted by the MTE in Primates, but not in artiodactyls, carnivores, and rodents. In the latter three orders, the exponent is 0.15. Conclusions: Together, these results indicate that the influence of basal metabolic rate on mammalian maternal investment durations must be more complicated than the MTE envisages, and that other factors must play an important role. Future research needs to allow for the possibility that different factors drive gestation duration and lactation duration, and that the drivers of the two durations may differ among orders.
September 12, 2014
Background: Stripes and other high contrast patterns found on animals have been hypothesised to cause “motion dazzle”, a type of defensive coloration that operates when in motion, causing predators to misjudge the speed and direction of object movement. Several recent studies have found some support for this idea, but little is currently understood about the mechanisms underlying this effect. Using humans as model ‘predators’ in a touch screen experiment we investigated further the effectiveness of striped targets in preventing capture, and considered how stripes compare to other types of patterning in order to understand what aspects of target patterning are important in making a target difficult to capture. Results: We find that striped targets are among the most difficult to capture, but that other patterning types are also highly effective at preventing capture in this task. Several target types, including background sampled targets and targets with a ‘spot’ on were significantly easier to capture than striped targets. We also show differences in capture attempt rates between different target types, but we find no differences in learning rates between target types. Conclusions: We conclude that striped targets are effective in preventing capture, but are not uniquely difficult to catch, with luminance matched grey targets also showing a similar capture rate. We show that key factors in making capture easier are a lack of average background luminance matching and having trackable ‘features’ on the target body. We also find that striped patterns are attempted relatively quickly, despite being difficult to catch. We discuss these findings in relation to the motion dazzle hypothesis and how capture rates may be affected more generally by pattern type.
Genetic variation in taste receptor pseudogenes provides evidence for a dynamic role in human evolution
Background: Human bitter taste receptors are encoded by a gene family consisting of 25 functional TAS2R loci. In addition, humans carry 11 TAS2R pseudogenes, some of which display evidence for substantial diversification among species, showing lineage-specific loss of function. Since bitter taste is thought to help prevent the intake of toxic substances, diversity at TAS2R genes could reflect the action of natural selection on the ability to recognize some bitter compounds rather than others. Whether species-specific variation in TAS2R pseudogenes is solely the result of genetic drift or whether it may have been influenced by selection due to different feeding behaviors has been an open question. Results: In this study, we analyzed patterns of variation at human TAS2R pseudogenes in both African and non-African populations, and compared them to those observable in nonhuman primates and archaic human species. Our results showed a similar worldwide distribution of allelic variation for most of the pseudogenes, with the exception of the TAS2R6P and TAS2R18P loci, both of which presented an unexpected higher frequency of derived alleles outside Africa. At the TAS2R6P locus, two SNPs were found in strong linkage disequilibrium (r2 > 0.9) with variants in the functional TAS2R5 gene, which showed signatures of selection. The human TAS2R18P carried a species-specific stop-codon upstream of four polymorphic insertions in the reading frame. SNPs at this locus showed significant positive values in a number of neutrality statistics, and age estimates indicated that they arose after the homo-chimp divergence. Conclusions: The similar distribution of variation of many human bitter receptor pseudogenes among human populations suggests that they arose from the ancestral forms by a unidirectional loss of function. However we explain the higher frequency of TAS2R6P derived alleles outside Africa as the effect of the balancing selection acting on the closely linked TAS2R5 gene. In contrast, TAS2R18P displayed a more complex history, suggesting an acquired function followed by a recent pseudogenization that predated the divergence of human modern and archaic species, which we hypothesize was associated with adaptions to dietary changes.
September 9, 2014
Background: Extant sloths present an evolutionary conundrum in that the two living genera are superficially similar (small-bodied, folivorous, arboreal) but diverged from one another approximately 30 million years ago and are phylogenetically separated by a radiation of medium to massive, mainly ground-dwelling, taxa. Indeed, the species in the two living genera are among the smallest, and perhaps most unusual, of the 50+ known sloth species, and must have independently and convergently evolved small size and arboreality. In order to accurately reconstruct sloth evolution, it is critical to incorporate their extinct diversity in analyses. Here, we used a dataset of 57 species of living and fossil sloths to examine changes in body mass mean and variance through their evolution, employing a general time-variable model that allows for analysis of evolutionary trends in continuous characters within clades lacking fully-resolved phylogenies, such as sloths. Results: Our analyses supported eight models, all of which partition sloths into multiple subgroups, suggesting distinct modes of body size evolution among the major sloth lineages. Model-averaged parameter values supported trended walks in most clades, with estimated rates of body mass change ranging as high as 126 kg/million years for the giant ground sloth clades Megatheriidae and Nothrotheriidae. Inclusion of living sloth species in the analyses weakened reconstructed rates for their respective groups, with estimated rates for Megalonychidae (large to giant ground sloths and the extant two-toed sloth) were four times higher when the extant genus Choloepus was excluded. Conclusions: Analyses based on extant taxa alone have the potential to oversimplify or misidentify macroevolutionary patterns. This study demonstrates the impact that integration of data from the fossil record can have on reconstructions of character evolution and establishes that body size evolution in sloths was complex, but dominated by trended walks towards the enormous sizes exhibited in some recently extinct forms.
September 5, 2014
Background: New Caledonia harbours a highly diverse and endemic flora, and 13 (out of the 19 worldwide) species of Araucaria are endemic to this territory. Their phylogenetic relationships remain largely unresolved. Using nuclear microsatellites and chloroplast DNA sequencing, we focused on five closely related Araucaria species to investigate among-species relationships and the distribution of within-species genetic diversity across New Caledonia. Results: The species could be clearly distinguished here, except A. montana and A. laubenfelsii that were not differentiated and, at most, form a genetic cline. Given their apparent morphological and ecological similarity, we suggested that these two species may be considered as a single evolutionary unit. We observed cases of nuclear admixture and incongruence between nuclear and chloroplast data, probably explained by introgression and shared ancestral polymorphism. Ancient hybridization was evidenced between A. biramulata and A. laubenfelsii in Mt Do, and is strongly suspected between A. biramulata and A. rulei in Mt Tonta. In both cases, extensive asymmetrical backcrossing eliminated the influence of one parent in the nuclear DNA composition. Shared ancestral polymorphism was also observed for cpDNA, suggesting that species diverged recently, have large effective sizes and/or that cpDNA experienced slow rates of molecular evolution. Within-species genetic structure was pronounced, probably because of low gene flow and significant inbreeding, and appeared clearly influenced by geography. This may be due to survival in distinct refugia during Quaternary climatic oscillations. Conclusions: The study species probably diverged recently and/or are characterized by a slow rate of cpDNA sequence evolution, and introgression is strongly suspected. Within-species genetic structure is tightly linked with geography. We underline the conservation implications of our results, and highlight several perspectives.
September 4, 2014
Background: The evolutionary history of the Old World monkey tribe Papionini comprising the genera Macaca, Mandrillus, Cercocebus, Lophocebus, Theropithecus, Rungwecebus and Papio is still matter of debate. Although the African Papionini (subtribe Papionina) are generally considered to be the sister lineage to the Asian Papionini (subtribe Macacina), previous studies based on morphological data, nuclear or mitochondrial sequences have shown contradictory phylogenetic relationships among and within both subtribes. To further elucidate the phylogenetic relationships among papionins and to estimate divergence ages we generated mitochondrial genome data and combined them with previously published sequences. Results: Our mitochondrial gene tree comprises 33 papionins representing all genera of the tribe except Rungwecebus. In contrast to most previous studies, the obtained phylogeny suggests a division of the Papionini into three main mitochondrial clades with similar ages: 1) Papio, Theropithecus, Lophocebus; 2) Mandrillus, Cercocebus; and 3) Macaca; the Mandrillus + Cercocebus clade appears to be more closely related to Macaca than to the other African Papionini. Further, we find paraphyletic relationships within the Mandrillus + Cercocebus clade as well as in Papio. Relationships among Theropithecus, Lophocebus and Papio remain unresolved. Divergence ages reveal initial splits within the three mitochondrial clades around the Miocene/Pliocene boundary and differentiation of Macaca species groups occurred on a similar time scale as those found between genera of the subtribe Papionina. Conclusion: Due to the largely well-resolved mitochondrial phylogeny, our study provides new insights into the evolutionary history of the Papionini. Results show some contradictory relationships in comparison to previous analyses, notably the paraphyly within the Cercocebus + Mandrillus clade and three instead of only two major mitochondrial clades. Divergence ages among species groups of macaques are similar to those among African Papionini genera, suggesting that diversification of the mitochondrial genome is of a similar magnitude in both subtribes. However, since our mitochondrial tree represents just a single gene tree that most likely does not reflect the true species tree, extensive nuclear sequence data is required to illuminate the true species phylogeny of papionins and to trace possible ancient hybridization events among lineages.
September 2, 2014
Identification of differentially expressed genes in female Drosophila antonietae and Drosophila meridionalis in response to host cactus odor
Background: Studies of insect-plant interactions have provided critical insights into the ecology and evolution of adaptive processes within and among species. Cactophilic Drosophila species have received much attention because larval development occurs in the necrotic tissues of cacti, and both larvae and adults feed on these tissues. Such Drosophila-cactus interactions include effects of the host plant on the physiology and behavior of the flies, especially so their nutritional status, mating condition and reproduction. The aim of this work was to compare the transcriptional responses of two species, Drosophila antonietae and Drosophila meridionalis, and identify genes potentially related to responses to odors released by their host cactus, Cereus hildmannianus. The two fly species are sympatric in most of their populations and use this same host cactus in nature. Results: We obtained 47 unique sequences (USs) for D. antonietae in a suppression subtractive hybridization screen, 30 of these USs had matches with genes predicted for other Drosophila species. For D. meridionalis we obtained 81 USs, 46 of which were orthologous with genes from other Drosophila species. Functional information (Gene Ontology) revealed that these differentially expressed genes are related to metabolic processes, detoxification mechanisms, signaling, response to stimuli, and reproduction. The expression of 13 genes from D. meridionalis and 12 from D. antonietae were further analyzed by quantitative real time-PCR, showing that four genes were significantly overexpressed in D. antonietae and six in D. meridionalis. Conclusions: Our results revealed the differential expression of genes related to responses to odor stimuli by a cactus, in two associated fly species. Although the majority of activated genes were similar between the two species, we also observed that certain metabolic pathways were specifically activated, especially those related to signaling pathways and detoxification mechanisms. The activation of these genes may reflect different metabolic pathways used by these flies in their interaction with this host cactus. Our findings provide insight into how the use of C. hildmannianus may have arisen independently in the two fly species, through genetic differentiation in metabolic pathways to effectively explore this cactus as a host.
August 29, 2014
Background: Lysozyme g is an antibacterial enzyme that was first found in the eggs of some birds, but recently has been found in additional species, including non-vertebrates. Some previously characterized lysozyme g sequences are suggested to have altered secretion potential and enzymatic activity, however the distribution of these altered sequences is unknown. Duplicated copies of the lysozyme g gene exist in some species; however, the origins of the duplicates and their roles in altered function are unclear. Results: We identified 234 lysozyme g sequences from 118 vertebrate species, including 181 sequences that are full or near full length representing all vertebrate classes except cartilaginous fish. Phylogenetic analysis shows that most lysozyme g gene duplicates are recent or lineage specific events, however three amplification events are more ancient, those in an early amniote, an early mammal, and an early teleost. The older gene duplications are associated with changes in function, including changes in secretion potential and muramidase antibacterial enzymatic activity. Conclusions: Lysozyme g is an essential muramidase enzyme that is widespread in vertebrates. Duplication of the lysozyme g gene, and the retention of non-secreted isozymes that have lost enzymatic activity indicate that lysozyme g has an activity other than the muramidase activity associated with being an antibacterial enzyme.
August 28, 2014
Background: A compelling demonstration of adaptation by natural selection is the ability of parasites to manipulate host behavior. One dramatic example involves fungal species from the genus Ophiocordyceps that control their ant hosts by inducing a biting behavior. Intensive sampling across the globe of ants that died after being manipulated by Ophiocordyceps suggests that this phenomenon is highly species-specific. We advance our understanding of this system by reconstructing host manipulation by Ophiocordyceps parasites under controlled laboratory conditions and combining this with field observations of infection rates and a metabolomics survey. Results: We report on a newly discovered species of Ophiocordyceps unilateralis sensu lato from North America that we use to address the species-specificity of Ophiocordyceps-induced manipulation of ant behavior. We show that the fungus can kill all ant species tested, but only manipulates the behavior of those it infects in nature. To investigate if this could be explained at the molecular level, we used ex vivo culturing assays to measure the metabolites that are secreted by the fungus to mediate fungus-ant tissue interactions. We show the fungus reacts heterogeneously to brains of different ant species by secreting a different array of metabolites. By determining which ion peaks are significantly enriched when the fungus is grown alongside brains of its naturally occurring host, we discovered candidate compounds that could be involved in behavioral manipulation by O. unilateralis s.l.. Two of these candidates are known to be involved in neurological diseases and cancer. Conclusions: The integrative work presented here shows that ant brain manipulation by O. unilateralis s.l. is species-specific seemingly because the fungus produces a specific array of compounds as a reaction to the presence of the host brain it has evolved to manipulate. These studies have resulted in the discovery of candidate compounds involved in establishing behavioral manipulation by this specialized fungus and therefore represent a major advancement towards an understanding of the molecular mechanisms underlying this phenomenon.
Analysis of hypoxia-inducible factor alpha polyploidization reveals adaptation to Tibetan plateau in the evolution of schizothoracine fish
Background: Hypoxia-inducible factor (HIF) is a master regulator that mediates major changes in gene expression under hypoxic conditions. Though HIF family has been identified in many organisms, little is known about this family in schizothoracine fish. Results: Duplicated hif-α (hif-1αA, hif-1αB, hif-2αA, and hif-2αB) genes were identified in schizothoracine fish. All the deduced HIF-α proteins contain the main domains (bHLH-PAS, ODDD, and TAD), also found in humans. Evidence suggests a Cyprinidae-specific deletion, specifically, a conserved proline hydroxylation motif LxxLAP, in the NODD domain of schizothoracine fish HIF-1αA. In addition, a schizothoracine-specific mutation was observed in the CODD domain of the specialized and highly specialized schizothoracine fish HIF-1αB, which is the proline hydroxylation motif mutated into PxxLAP. Standard and stochastic branch-site codon model analysis indicated that only HIF-1αB has undergone positive selection, which may have led to changes in function. To confirm this hypothesis, HIF-αs tagged with Myc were transfected into HEK 293 T cells. Each HIF-1αB was found to significantly upregulate luciferase activity under normoxic and hypoxic conditions, which indicated that the HIF-1αB protein was more stable than other HIF-αs. Conclusions: All deduced HIF-α proteins of schizothoracine fish contain important domains, like their mammalian counterparts, and each HIF-α is shorter than that of human. Our experiments reveal that teleost-specific duplicated hif-α genes played different roles under hypoxic conditions, and HIF-1αB may be the most important regulator in the adaptation of schizothoracine fish to the environment of the Tibetan Plateau.
August 27, 2014
Background: Myzostomids are marine annelids, nearly all of which live symbiotically on or inside echinoderms, chiefly crinoids, and to a lesser extent asteroids and ophiuroids. These symbionts possess a variety of adult body plans and lifestyles. Most described species live freely on the exterior of their hosts as adults (though starting life on the host inside cysts), while other taxa permanently reside in galls, cysts, or within the host’s mouth, digestive system, coelom, or gonads. Myzostomid lifestyles range from stealing incoming food from the host’s food grooves to consuming the host’s tissue directly. Previous molecular studies of myzostomids have had limited sampling with respect to assessing the evolutionary relationships within the group; therefore molecular data from 75 myzostomid taxa were analyzed using maximum likelihood and maximum parsimony methods. To compare relationships of myzostomids with their hosts, a phylogeny was inferred for 53 hosts and a tanglegram constructed with 88 associations. Results: Gall- and some cyst-dwellers were recovered as a clade, while cyst-to-free-living forms were found as a grade including two clades of internal host-eaters (one infecting crinoids and the other asteroids and ophiuroids), mouth/digestive system inhabitants, and other cyst-dwellers. Clades of myzostomids were recovered that associated with asteroids, ophiuroids, and stalked or feather star crinoids. Co-phylogenetic analyses rejected a null-hypothesis of random associations at the global level, but not for individual associations. Event-based analyses relied most upon host-switching and duplication events to reconcile the association history. Conclusion: Hypotheses were revised concerning the systematics and evolution of Myzostomida, as well their relationships to their hosts. We found two or three transitions between food-stealing and host-eating. Taxa that dwell within the mouth or digestive system and some cyst forms are arguably derived from cyst-to-free-living ancestors – possibly the result of a free-living form moving to the mouth and paedomorphic retention of the juvenile cyst. Phylogenetic conservatism in host use was observed among related myzostomid taxa. This finding suggests that myzostomids (which have a free-living planktonic stage) are limited to one or a few closely related hosts, despite most hosts co-occurring on the same reefs, many within physical contact of each other.
Background: Drosophila Dscam1 is a cell-surface protein that plays important roles in neural development and axon tiling of neurons. It is known that thousands of isoforms bind themselves through specific homophilic interactions, a process which provides the basis for cellular self-recognition. Detailed biochemical studies of specific isoforms strongly suggest that homophilic binding, i.e. the formation of homodimers by identical Dscam1 isomers, is of great importance for the self-avoidance of neurons. Due to experimental limitations, it is currently impossible to measure the homophilic binding affinities for all 19,000 potential isoforms. Results: Here we reconstructed the DNA sequences of an ancestral Dscam form (which likely existed approximately 40 ~ 50 million years ago) using a comparative genomic approach. On the basis of this sequence, we established a working model to predict the self-binding affinities of all isoforms in both the current and the ancestral genome, using machine-learning methods. Detailed computational analysis was performed to compare the self-binding affinities of all isoforms present in these two genomes. Our results revealed that 1) isoforms containing newly derived variable domains exhibit higher self-binding affinities than those with conserved domains, and 2) current isoforms display higher self-binding affinities than their counterparts in the ancient genome. As thousands of Dscam isoforms are needed for the self-avoidance of the neuron, we propose that an increase in self-binding affinity provides the basis for the successful evolution of the arthropod brain. Conclusions: Our data presented here provide an excellent model for future experimental studies of the binding behavior of Dscam isoforms. The results of our analysis indicate that evolution favored the rise of novel variable domains thanks to their higher self-binding affinities, rather than selection merely on the basis of simple expansion of isoform diversity, as that this particular selection process would have established the powerful mechanisms required for neuronal self-avoidance. Thus, we reveal here a new molecular mechanism for the successful evolution of arthropod brains.
The Genealogical World of Phylogenetic Networks
BMC Evolutionary Biology
Molecular Biology and Evolution