BMC Evolutionary Biology

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January 21, 2015

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Background: Chimpanzees (Pan troglodytes) can be divided into four subspecies. Substantial phylogenetic evidence suggests that these subspecies can be grouped into two distinct lineages: a western African group that includes P. t. verus and P. t. ellioti and a central/eastern African group that includes P. t. troglodytes and P. t. schweinfurthii. The geographic division of these two lineages occurs in Cameroon, where the rages of P. t. ellioti and P. t. troglodytes appear to converge at the Sanaga River. Remarkably, few population genetic studies have included wild chimpanzees from this region. Results: We analyzed microsatellite genotypes of 187 wild, unrelated chimpanzees, and mitochondrial control region sequencing data from 604 chimpanzees. We found that chimpanzees in Cameroon and eastern Nigeria comprise at least two, and likely three populations. Both the mtDNA and microsatellite data suggest that there is a primary separation of P. t. troglodytes in southern Cameroon from P. t. ellioti north and west of the Sanaga River. These two populations split ~200-250 thousand years ago (kya), but have exchanged one migrant per generation since separating. In addition, P. t. ellioti consists of two populations that split from one another ~4 kya. One population is located in the rainforests of western Cameroon and eastern Nigeria, whereas the second population appears to be confined to a savannah-woodland mosaic in central Cameroon. Conclusions: Our findings suggest that there are as many as three genetically distinct populations of chimpanzees in Cameroon and eastern Nigeria. P. t. troglodytes in southern Cameroon comprises one population that is separated from two populations of P. t. ellioti in western and central Cameroon, respectively. P. t. ellioti and P. t. troglodytes appear to be characterized by a pattern of isolation-with-migration, and thus, we propose that neutral processes alone can not explain the differentiation of P. t. ellioti and P. t. troglodytes.
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Background: The Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti) is found in the Gulf of Guinea biodiversity hotspot located in western equatorial Africa. This subspecies is threatened by habitat fragmentation due to logging and agricultural development, hunting for the bushmeat trade, and possibly climate change. Although P. t. ellioti appears to be geographically separated from the neighboring central chimpanzee (P. t. troglodytes) by the Sanaga River, recent population genetics studies of chimpanzees from across this region suggest that additional factors may also be important in their separation. The main aims of this study were: 1) to model the distribution of suitable habitat for P. t. ellioti across Cameroon and Nigeria, and P. t. troglodytes in southern Cameroon, 2) to determine which environmental factors best predict their optimal habitats, and 3) to compare modeled niches and test for their levels of divergence from one another. A final aim of this study was to examine the ways that climate change might impact suitable chimpanzee habitat across the region under various scenarios. Results: Ecological niche models (ENMs) were created using the software package Maxent for the three populations of chimpanzees that have been inferred to exist in Cameroon and eastern Nigeria: (i) P. t. troglodytes in southern Cameroon, (ii) P. t. ellioti in northwestern Cameroon, and (iii) P. t. ellioti in central Cameroon. ENMs for each population were compared using the niche comparison test in ENMtools, which revealed complete niche divergence with very little geographic overlap of suitable habitat between populations. Conclusions: These findings suggest that a positive relationship may exist between environmental variation and the partitioning of genetic variation found in chimpanzees across this region. ENMs for each population were also projected under three different climate change scenarios for years 2020, 2050, and 2080. Suitable habitat of P. t. ellioti in northwest Cameroon / eastern Nigeria is expected to remain largely unchanged through 2080 in all considered scenarios. In contrast, P. t. ellioti in central Cameroon, which represents half of the population of this subspecies, is expected to experience drastic reductions in its ecotone habitat over the coming century.
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Background: The mechanisms that underlie the diversification of tropical animals remain poorly understood, but new approaches that combine geo-spatial modeling with spatially explicit genetic data are providing fresh insights on this topic. Data about the diversification of tropical mammals remain particularly sparse, and vanishingly few opportunities exist to study endangered large mammals that increasingly exist only in isolated pockets. The chimpanzees of Cameroon represent a unique opportunity to examine the mechanisms that promote genetic differentiation in tropical mammals because the region is home to two chimpanzee subspecies: Pan troglodytes ellioti and P. t. trogolodytes. Their ranges converge in central Cameroon, which is a geographically, climatically and environmentally complex region that presents an unparalleled opportunity to examine the roles of rivers and/or environmental variation in influencing the evolution of chimpanzee populations. Results: We analyzed microsatellite genotypes and mtDNA HVRI sequencing data from wild chimpanzees sampled at a fine geographic scale across Cameroon and eastern Nigeria using a spatially explicit approach based upon Generalized Dissimilarity Modeling. Both the Sanaga River and environmental variation were found to contribute to driving separation of the subspecies. The importance of environmental variation differed among subspecies. Gene-environment associations were weak in P. t. troglodytes, whereas environmental variation was found to play a much larger role in shaping patterns of genetic differentiation in P. t. ellioti. Conclusions: We found that both the Sanaga River and environmental variation likely play a role in shaping patterns of chimpanzee genetic diversity. Future studies using single nucleotide polymorphism (SNP) data are necessary to further understand how rivers and environmental variation contribute to shaping patterns of genetic variation in chimpanzees.

December 30, 2014

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Background: Analyzed individually, gene trees for a given taxon set tend to harbour incongruent or conflicting signals. One popular approach to deal with this circumstance is to use concatenated data. But especially in prokaryotes, where lateral gene transfer (LGT) is a natural mechanism of generating genetic diversity, there are open questions as to whether concatenation amplifies or averages phylogenetic signals residing in individual genes. Here we investigate concatenations of prokaryotic and eukaryotic datasets to investigate possible sources of incongruence in phylogenetic trees and to examine the level of overlap between individual and concatenated alignments. Results: We analyzed prokaryotic datasets comprising 248 invidual gene trees from 315 genomes at three taxonomic depths spanning gammaproteobacteria, proteobacteria, and prokaryotes (bacteria plus archaea), and eukaryotic datasets comprising 279 invidual gene trees from 85 genomes at two taxonomic depths: across plants-animals-fungi and within fungi. Consistent with previous findings, the branches in trees made from concatenated alignments are, in general, not supported by any of their underlying individual gene trees, even though the concatenation trees tend to possess high bootstrap proportions values. For the prokaryote data, this observation is independent of phylogenetic depth and sequence conservation. The eukaryotic data show much better agreement between concatenation and single gene trees. LGT frequencies in trees were estimated using established methods. Sequence length in individual alignments, but not sequence divergence, was found to correlate with the generation of branches that correspond to the concatenated tree. Conclusions: The weak correspondence of concatenation trees with single gene trees gives rise to the question where the phylogenetic signal in concatenated trees is coming from. The eukaryote data reveals a better correspondence between individual and concatenation trees than the prokaryote data. The question of whether the lack of correspondence between individual genes and the concatenation tree in the prokaryotic data is due to LGT or phylogenetic artefacts remains unanswered. If LGT is the cause of incongruence between concatenation and individual trees, we would have expected to see greater degrees of incongruence for more divergent prokaryotic data sets, which was not observed, although estimated rates of LGT suggest that LGT is responsible for at least some of the observed incongruence.
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Background: The puzzle of the selective benefits of multiple mating and multiple paternity in social insects has been a major focus of research in evolutionary biology. We examine paternity in a clade of social insects, the vespine wasps (the yellowjackets and hornets), which contains species with high multiple paternity as well as species with single paternity. This group is particularly useful for comparative analyses given the wide interspecific variation in paternity traits despite similar sociobiology and ecology of the species in the genera Vespula, Dolichovespula and Vespa. We describe the paternity of 5 species of yellowjackets (Vespula spp.) and we perform a phylogenetically controlled comparative analysis of relatedness, paternity frequency, paternity skew, colony size, and nest site across 22 vespine taxa. Results: We found moderate multiple paternity in four small-colony Vespula rufa-group species (effective paternity 1.5 – 2.1), and higher multiple paternity in the large-colony Vespula flavopilosa (effective paternity ~3.1). Our comparative analysis shows that colony size, but not nest site, predicts average intracolony relatedness. Underlying this pattern, we found that greater colony size is associated with both higher paternity frequency and reduced paternity skew. Conclusions: Our results support hypotheses focusing on the enhancement of genetic diversity in species with large colonies, and run counter to the hypothesis that multiple paternity is adaptively maintained due to sperm limitation associated with large colonies. We confirm the patterns observed in taxonomically widespread analyses by comparing closely related species of wasps with similar ecology, behavior and social organization. The vespine wasps may be a useful group for experimental investigation of the benefits of multiple paternity in the future.
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Background: The puzzle of the selective benefits of multiple mating and multiple paternity in social insects has been a major focus of research in evolutionary biology. We examine paternity in a clade of social insects, the vespine wasps (the yellowjackets and hornets), which contains species with high multiple paternity as well as species with single paternity. This group is particularly useful for comparative analyses given the wide interspecific variation in paternity traits despite similar sociobiology and ecology of the species in the genera Vespula, Dolichovespula and Vespa. We describe the paternity of 5 species of yellowjackets (Vespula spp.) and we perform a phylogenetically controlled comparative analysis of relatedness, paternity frequency, paternity skew, colony size, and nest site across 22 vespine taxa. Results: We found moderate multiple paternity in four small-colony Vespula rufa-group species (effective paternity 1.5 – 2.1), and higher multiple paternity in the large-colony Vespula flavopilosa (effective paternity ~3.1). Our comparative analysis shows that colony size, but not nest site, predicts average intracolony relatedness. Underlying this pattern, we found that greater colony size is associated with both higher paternity frequency and reduced paternity skew. Conclusions: Our results support hypotheses focusing on the enhancement of genetic diversity in species with large colonies, and run counter to the hypothesis that multiple paternity is adaptively maintained due to sperm limitation associated with large colonies. We confirm the patterns observed in taxonomically widespread analyses by comparing closely related species of wasps with similar ecology, behavior and social organization. The vespine wasps may be a useful group for experimental investigation of the benefits of multiple paternity in the future.
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Background: Analyzed individually, gene trees for a given taxon set tend to harbour incongruent or conflicting signals. One popular approach to deal with this circumstance is to use concatenated data. But especially in prokaryotes, where lateral gene transfer (LGT) is a natural mechanism of generating genetic diversity, there are open questions as to whether concatenation amplifies or averages phylogenetic signals residing in individual genes. Here we investigate concatenations of prokaryotic and eukaryotic datasets to investigate possible sources of incongruence in phylogenetic trees and to examine the level of overlap between individual and concatenated alignments. Results: We analyzed prokaryotic datasets comprising 248 invidual gene trees from 315 genomes at three taxonomic depths spanning gammaproteobacteria, proteobacteria, and prokaryotes (bacteria plus archaea), and eukaryotic datasets comprising 279 invidual gene trees from 85 genomes at two taxonomic depths: across plants-animals-fungi and within fungi. Consistent with previous findings, the branches in trees made from concatenated alignments are, in general, not supported by any of their underlying individual gene trees, even though the concatenation trees tend to possess high bootstrap proportions values. For the prokaryote data, this observation is independent of phylogenetic depth and sequence conservation. The eukaryotic data show much better agreement between concatenation and single gene trees. LGT frequencies in trees were estimated using established methods. Sequence length in individual alignments, but not sequence divergence, was found to correlate with the generation of branches that correspond to the concatenated tree. Conclusions: The weak correspondence of concatenation trees with single gene trees gives rise to the question where the phylogenetic signal in concatenated trees is coming from. The eukaryote data reveals a better correspondence between individual and concatenation trees than the prokaryote data. The question of whether the lack of correspondence between individual genes and the concatenation tree in the prokaryotic data is due to LGT or phylogenetic artefacts is remains unanswered. If LGT is the cause of incongruence between concatenation and individual trees, we would have expected to see greater degrees of incongruence for more divergent prokaryotic data sets, which was not observed, although estimated rates of LGT suggest that LGT is responsible for at least some of the observed incongruence.
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Background: The quasispecies model refers to information carriers that undergo self-replication with errors. A quasispecies is a steady-state population of biopolymer sequence variants generated by mutations from a master sequence. A quasispecies error threshold is a minimal replication accuracy below which the population structure breaks down. Theory and experimentation of this model often refer to biopolymers, e.g. RNA molecules or viral genomes, while its prebiotic context is often associated with an RNA world scenario. Here, we study the possibility that compositional entities which code for compositional information, intrinsically different from biopolymers coding for sequential information, could show quasispecies dynamics. Results: We employed a chemistry-based model, graded autocatalysis replication domain (GARD), which simulates the network dynamics within compositional molecular assemblies. In GARD, a compotype represents a population of similar assemblies that constitute a quasi-stationary state in compositional space. A compotype's center-of-mass is found to be analogous to a master sequence for a sequential quasispecies. Using single-cycle GARD dynamics, we measured the quasispecies transition matrix (Q) for the probabilities of transition from one center-of-mass Euclidean distance to another. Similarly, the quasispecies? growth rate vector (A) was obtained. This allowed computing a steady state distribution of distances to the center of mass, as derived from the quasispecies equation. In parallel, a steady state distribution was obtained via the GARD equation kinetics. Rewardingly, a significant correlation was observed between the distributions obtained by these two methods. This was only seen for distances to the compotype center-of-mass, and not to randomly selected compositions. A similar correspondence was found when comparing the quasispecies time dependent dynamics towards steady state. Further, changing the error rate by modifying basal assembly joining rate of GARD kinetics was found to display an error catastrophe, similar to the standard quasispecies model. Additional augmentation of compositional mutations leads to the complete disappearance of the master-like composition. Conclusions: Our results show that compositional assemblies, as simulated by the GARD formalism, portray significant attributes of quasispecies dynamics. This expands the applicability of the quasispecies model beyond sequence-based entities, and potentially enhances validity of GARD as a model for prebiotic evolution.

December 24, 2014

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Background: X chromosome inactivation is the transcriptional silencing of one X chromosome in the somatic cells of female mammals. In eutherian mammals (e.g. humans) one of the two X chromosomes is randomly chosen for silencing, with about 15% (usually in younger evolutionary strata of the X chromosome) of genes escaping this silencing. In contrast, in the distantly related marsupial mammals the paternally derived X is silenced, although not as completely as the eutherian X. A chromosome wide examination of X inactivation, using RNA-seq, was recently undertaken in grey short-tailed opossum (Monodelphis domestica) brain and extraembryonic tissues. However, no such study has been conduced in Australian marsupials, which diverged from their American cousins ~80 million years ago, leaving a large gap in our understanding of marsupial X inactivation. Results: We used RNA-seq data from blood or liver of a family (mother, father and daughter) of tammar wallabies (Macropus eugenii), which in conjunction with available genome sequence from the mother and father, permitted genotyping of 42 expressed heterozygous SNPs on the daughter’s X. These 42 SNPs represented 34 X loci, of which 68% (23 of the 34) were confirmed as inactivated on the paternally derived X in the daughter’s liver; the remaining 11 X loci escaped inactivation. Seven of the wallaby loci sampled were part of the old X evolutionary stratum, of which three escaped inactivation. Three loci were classified as part of the newer X stratum, of which two escaped inactivation. A meta-analysis of previously published opossum X inactivation data revealed that 5 of 52 genes in the old X stratum escaped inactivation. Conclusions: We demonstrate that chromosome wide inactivation of the paternal X is common to an Australian marsupial representative, but that there is more escape from inactivation than reported for opossum (32% v 14%). We also provide evidence that, unlike the human X chromosome, the location of loci within the oldest evolutionary stratum on the marsupial X does not correlate with their probability of escape from inactivation.

December 23, 2014

17:00
Background: Influenza A/H3N2 has been circulating in humans since 1968, causing considerable morbidity and mortality. Although H3N2 incidence is highly seasonal, how such seasonality contributes to global phylogeographic migration dynamics has not yet been established. In this study, we incorporate time-varying migration rates in a Bayesian MCMC framework. We focus on migration within China and between China and North-America as case studies, then expand the analysis to global communities. Results: Incorporating seasonally varying migration rates improves the modeling of migration in our regional case studies, and also in a global context. In our global model, windows of increased immigration map to the seasonal timing of epidemic spread, while windows of increased emigration map to epidemic decline. Seasonal patterns also correlate with the probability that local lineages go extinct and fail to contribute to long term viral evolution, as measured through the trunk of the phylogeny. However, the fraction of the trunk in each community was found to be better determined by its overall human population size. Conclusions: Seasonal migration and rapid turnover within regions is sustained by the invasion of 'fertile epidemic grounds' at the end of older epidemics. Thus, the current emphasis on connectivity, including air-travel, should be complemented with a better understanding of the conditions and timing required for successful establishment. Models which account for migration seasonality will improve our understanding of the seasonal drivers of influenza, enhance epidemiological predictions, and ameliorate vaccine updating by identifying strains that not only escape immunity but also have the seasonal opportunity to establish and spread. Further work is also needed on additional conditions that contribute to the persistence and long term evolution of influenza within the human population, such as spatial heterogeneity with respect to climate and seasonality.
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Background: X chromosome inactivation is the transcriptional silencing of one X chromosome in the somatic cells of female mammals. In eutherian mammals (e.g. humans) one of the two X chromosomes is randomly chosen for silencing, with about 15% (usually in younger evolutionary strata of the X chromosome) of genes escaping this silencing. In contrast, in the distantly related marsupial mammals the paternally derived X is silenced, although not as completely as the eutherian X. A chromosome wide examination of X inactivation, using RNA-seq, was recently undertaken in grey short-tailed opossum (Monodelphis domestica) brain and extraembryonic tissues. However, no such study has been conduced in Australian marsupials, which diverged from their American cousins ~80 million years ago, leaving a large gap in our understanding of marsupial X inactivation. Results: We used RNA-seq data from blood or liver of a family (mother, father and daughter) of tammar wallabies (Macropus eugenii), which in conjunction with available genome sequence from the mother and father, permitted genotyping of 42 expressed heterozygous SNPs on the daughter?s X. These 42 SNPs represented 34 X loci, of which 68% (23 of the 34) were confirmed as inactivated on the paternally derived X in the daughter?s liver; the remaining 11 X loci escaped inactivation. Seven of the wallaby loci sampled were part of the old X evolutionary stratum, of which three escaped inactivation. Three loci were classified as part of the newer X stratum, of which two escaped inactivation. A meta-analysis of previously published opossum X inactivation data revealed that 5 of 52 genes in the old X stratum escaped inactivation. Conclusions: We demonstrate that chromosome wide inactivation of the paternal X is common to an Australian marsupial representative, but that there is more escape from inactivation than reported for opossum (32% v 14%). We also provide evidence that, unlike the human X chromosome, the location of loci within the oldest evolutionary stratum on the marsupial X does not correlate with their probability of escape from inactivation.
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Background: Although the plastid genome is highly conserved across most angiosperms, multiple lineages have increased rates of structural rearrangement and nucleotide substitution. These lineages exhibit an excess of nonsynonymous substitutions (i.e., elevated dN/dS ratios) in similar subsets of plastid genes, suggesting that similar mechanisms may be leading to relaxed and/or positive selection on these genes. However, little is known regarding whether these mechanisms continue to shape sequence diversity at the intraspecific level. Results: We examined patterns of interspecific divergence and intraspecific polymorphism in the plastid genome of Campanulastrum americanum, and across plastid genes found a significant correlation between dN/dS and pN/pS (i.e., the within-species equivalent of dN/dS). A number of genes including ycf1, ycf2, clpP, and ribosomal protein genes exhibited high dN/dS ratios. McDonald-Kreitman tests detected little evidence for positive selection acting on these genes, likely due to the presence of substantial intraspecific divergence. Conclusions: These results suggest that mechanisms leading to increased nucleotide substitution rates in the plastid genome are continuing to act at the intraspecific level. Accelerated plastid genome evolution may increase the likelihood of intraspecific cytonuclear genetic incompatibilities, and thereby contribute to the early stages of the speciation process.

December 21, 2014

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Background: Snails species belonging to the genus Bulinus (Planorbidae) serve as intermediate host for flukes belonging to the genus Schistosoma (Digenea, Platyhelminthes). Despite its importance in the transmission of these parasites, the evolutionary history of this genus is still obscure. In the present study, we used the partial mitochondrial cytochrome oxidase subunit I (cox1) gene, and the nuclear ribosomal ITS, 18S and 28S genes to investigate the haplotype diversity and phylogeny of seven Bulinus species originating from three endemic countries in Africa (Cameroon, Senegal and Egypt). Results: The cox1 region showed much more variation than the ribosomal markers within Bulinus sequences. High levels of genetic diversity were detected at all loci in the seven studied species, with clear segregation between individuals and appearance of different haplotypes, even within same species from the same locality. Sequences clustered into two lineages; (A) groups Bulinus truncatus, B. tropicus, B. globosus and B. umbilicatus; while (B) groups B. forskalii, B. senegalensis and B. camerunensis. Interesting patterns emerge regarding schistosome susceptibility: Bulinus species with lower genetic diversity are predicted to have higher infection prevalence than those with greater diversity in host susceptibility. Conclusion: The results reported in this study are very important since a detailed understanding of the population genetic structure of Bulinus is essential to understand the epidemiology of many schistosome parasites.
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Background: G protein-coupled receptors (GPCRs) play a central role in eukaryotic signal transduction. However, the GPCR component of this signalling system, at the early origins of metazoans is not fully understood. Here we aim to identify and classify GPCRs in Amphimedon queenslandica (sponge), a member of an earliest diverging metazoan lineage (Porifera). Furthermore, phylogenetic comparisons of sponge GPCRs with eumetazoan and bilaterian GPCRs will be essential to our understanding of the GPCR system at the roots of metazoan evolution. Results: We present a curated list of 220 GPCRs in the sponge genome after excluding incomplete sequences and false positives from our initial dataset of 282 predicted GPCR sequences obtained using Pfam search. Phylogenetic analysis reveals that the sponge genome contains members belonging to four of the five major GRAFS families including Glutamate (33), Rhodopsin (126), Adhesion (40) and Frizzled (3). Interestingly, the sponge Rhodopsin family sequences lack orthologous relationships with those found in eumetazoan and bilaterian lineages, since they clustered separately to form sponge specific groups in the phylogenetic analysis. This suggests that sponge Rhodopsins diverged considerably from that found in other basal metazoans. A few sponge Adhesions clustered basal to Adhesion subfamilies commonly found in most vertebrates, suggesting some Adhesion subfamilies may have diverged prior to the emergence of Bilateria. Furthermore, at least eight of the sponge Adhesion members have a hormone binding motif (HRM domain) in their N-termini, although hormones have yet to be identified in sponges. We also phylogenetically clarified that sponge has homologs of metabotropic glutamate (mGluRs) and GABA receptors. Conclusion: Our phylogenetic comparisons of sponge GPCRs with other metazoan genomes suggest that sponge contains a significantly diversified set of GPCRs. This is evident at the family/subfamily level comparisons for most GPCR families, in particular for the Rhodopsin family of GPCRs. In summary, this study provides a framework to perform future experimental and comparative studies to further verify and understand the roles of GPCRs that predates the divergence of bilaterian and eumetazoan lineages.
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Background: Crop diversity managed by smallholder farmers in traditional agrosystems is the outcome of historical and current processes interacting at various spatial scales, and influenced by factors such as farming practices and environmental pressures. Only recently have studies started to consider the complexity of these processes instead of simply describing diversity for breeding purposes. A first step in that aim is to add multiple references to the collection of genetic data, including the farmers’ varietal taxonomy and practices and the historical background of the crop. Results: On the basis of interview data collected in a previous study, we sampled 166 populations of durum wheat varieties in two traditional Moroccan agrosystems, in the Pre-Rif and Atlas Mountains regions. Using a common garden experiment, we detected a high phenotypic variability on traits indicative of taxonomical position and breeding status, namely spike shape and plant height. Populations often combined modern (short) with traditional-like (tall) statures, and classical durum squared spike shape (5 flowers/spikelet) with flat spike shape (3 flowers/ spikelet) representative of primitive domesticated tetraploid wheat (ssp. dicoccum). By contrast, the genetic diversity assessed using 14 microsatellite markers was relatively limited. When compared to the genetic diversity found in a large collection of tetraploid wheat, it corresponded to free-threshing tetraploid wheat. Within Morocco, the two studied regions differed for both genetic diversity and variety names. Within regions, neither geography nor variety names nor even breeding status constituted strong barriers to gene exchange despite a few significant patterns. Conclusions: This first assessment of morphological and genetic diversity allowed pointing out some important factors that may have influenced the structure and evolutionary dynamics of durum wheat in Morocco: the significance of variety names, the occurrence of mixtures within populations, the relative strength of seed exchange between farmers and local adaptation, as well as the fate of modern varieties once they have been introduced. Further, multidisciplinary studies at different spatial scales are needed to better understand these complex agrosystems of invaluable importance for food security.
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Background: Allopatric divergence across lineages can lead to post-zygotic reproductive isolation upon secondary contact and disrupt coevolution between mitochondrial and nuclear genomes, promoting emergence of genetic incompatibilities. A previous F ST scan on the transcriptome of the Baltic clam Macoma balthica highlighted several genes potentially involved in mito-nuclear incompatibilities (MNIs). As proteins involved in the mitochondrial oxidative phosphorylation (OXPHO) chain are prone to MNIs and can contribute to the maintenance of genetic barriers, the mitochondrial genomes of six Ma. balthica individuals spanning two secondary contact zones were sequenced using the Illumina MiSeq plateform. Results: The mitogenome has an approximate length of 16,806 bp and encodes 13 protein-coding genes, 2 rRNAs and 22 tRNAs, all located on the same strand. atp8, a gene long reported as rare in bivalves, was detected. It encodes 42 amino acids and is putatively expressed and functional. A large unassigned region was identified between rrnS and tRNA Met and could likely correspond to the Control Region. Replacement and synonymous mutations were mapped on the inferred secondary structure of all protein-coding genes of the OXPHO chain. The atp6 and atp8 genes were characterized by background levels of replacement mutations, relative to synonymous mutations. However, most nad genes (notably nad2 and nad5) were characterized by an elevated proportion of replacement mutations. Conclusions: Six nearly complete mitochondrial genomes were successfully assembled and annotated, providing the necessary roadmap to study MNIs at OXPHO loci. Few replacement mutations were mapped on mitochondrial-encoded ATP synthase subunits, which is in contrast with previous data on nuclear-encoded subunits. Conversely, the high population divergence and the prevalence of non-synonymous mutations at nad genes are congruent with previous observations from the nuclear transcriptome. This further suggest that MNIs between subunits of Complex I of the OXPHO chain, coding for NADH dehydrogenase, may play a role in maintaining barriers to gene flow in Ma. balthica.

December 20, 2014

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Background: The genes of the major histocompatibility complex (MHC/MH) have attracted considerable scientific interest due to their exceptional levels of variability and important function as part of the adaptive immune system. Despite a large number of studies on MH class II diversity of both model and non-model organisms, most research has focused on patterns of genetic variability at individual loci, failing to capture the functional diversity of the biologically active dimeric molecule. Here, we take a systematic approach to the study of MH variation, analyzing patterns of genetic variation at MH class II? and II? loci of the seahorse, which together form the immunologically active peptide binding cleft of the MH class II molecule. Results: The seahorse carries a minimal class II system, consisting of single copies of both MH class II? and II?, which are physically linked and inherited in a Mendelian fashion. Both genes are ubiquitously expressed and detectible in the brood pouch of male seahorses throughout pregnancy. Genetic variability of the two genes is high, dominated by non-synonymous variation concentrated in their peptide-binding regions. Coding variation outside these regions is negligible, a pattern thought to be driven by intra- and interlocus recombination. Despite the tight physical linkage of MH II? and II? loci, recombination has produced novel composite alleles, increasing functional diversity at sites responsible for antigen recognition. Conclusions: Antigen recognition by the adaptive immune system of the seahorse is enhanced by high variability at both MH class II? and II? loci. Strong positive selection on sites involved in pathogen recognition, coupled with high levels of intra- and interlocus recombination, produce a patchwork pattern of genetic variation driven by genetic hitchhiking. Studies focusing on variation at individual MH loci may unintentionally overlook an important component of ecologically relevant variation.

December 19, 2014

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Background: Estimating divergence times in phylogenies using a molecular clock depends on accurate modeling of nucleotide substitution rates in DNA sequences. Rate heterogeneity among lineages is likely to affect estimates, especially in lineages with long stems and short crowns (“broom” clades) and no internal calibration. We evaluate the performance of the random local clocks model (RLC) and the more routinely employed uncorrelated lognormal relaxed clock model (UCLN) in situations in which a significant rate shift occurs on the stem branch of a broom clade. We compare the results of simulations to empirical results from analyses of a real rate-heterogeneous taxon – Australian grass trees (Xanthorrhoea) – whose substitution rate is slower than in its sister groups, as determined by relative rate tests. Results: In the simulated datasets, the RLC model performed much better than UCLN: RLC correctly estimated the age of the crown node of slow-rate broom clades, whereas UCLN estimates were consistently too young. Similarly, in the Xanthorrhoea dataset, UCLN returned significantly younger crown ages than RLC (mean estimates respectively 3–6 Ma versus 25–35 Ma). In both real and simulated datasets, Bayes Factor tests strongly favored the RLC model over the UCLN model. Conclusions: The choice of an unsuitable molecular clock model can strongly bias divergence time estimates. In particular, for data predicted to have more rate variation among than within clades, dating with RLC is much more likely to be accurate than with UCLN. The choice of clocks should be informed by the biology of the study group (e.g., life-form) or assessed with relative rate tests and post-hoc model comparisons.
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Background: The majority of DNA contained within vertebrate genomes is non-coding, with a certain proportion of this thought to play regulatory roles during development. Conserved Non-coding Elements (CNEs) are an abundant group of putative regulatory sequences that are highly conserved across divergent groups and thus assumed to be under strong selective constraint. Many CNEs may contain regulatory factor binding sites, and their frequent spatial association with key developmental genes ? such as those regulating sensory system development ? suggests crucial roles in regulating gene expression and cellular patterning. Yet surprisingly little is known about the molecular evolution of CNEs across diverse mammalian taxa or their role in specific phenotypic adaptations. We examined 3,110 vertebrate-specific and ~82,000 mammalian-specific CNEs across 19 and 9 mammalian orders respectively, and tested for changes in the rate of evolution of CNEs located in the proximity of genes underlying the development or functioning of auditory systems. As we focused on CNEs putatively associated with genes underlying the development/functioning of auditory systems, we incorporated echolocating taxa in our dataset because of their highly specialised and derived auditory systems. Results: Phylogenetic reconstructions of concatenated CNEs broadly recovered accepted mammal relationships despite high levels of sequence conservation. We found that CNE substitution rates were highest in rodents and lowest in primates, consistent with previous findings. Comparisons of CNE substitution rates from several genomic regions containing genes linked to auditory system development and hearing revealed differences between echolocating and non-echolocating taxa. Wider taxonomic sampling of four CNEs associated with the homeobox genes Hmx2 and Hmx3 ? which are required for inner ear development ? revealed family-wise variation across diverse bat species. Specifically within one family of echolocating bats that utilise frequency-modulated echolocation calls varying widely in frequency and intensity high levels of sequence divergence were found. Conclusions: Levels of selective constraint acting on CNEs differed both across genomic locations and taxa, with observed variation in substitution rates of CNEs among bat species. More work is needed to determine whether this variation can be linked to echolocation, and wider taxonomic sampling is necessary to fully document levels of conservation in CNEs across diverse taxa.

December 17, 2014

05:00
Background: Synonymous codon usage bias (SCUB) is an inevitable phenomenon in organismic taxa, generally referring to differences in the occurrence frequency of codons across different species or within the genome of the same species. SCUB happens in various degrees under pressure from nature selection, mutation bias and other factors in different ways. It also attaches great significance to gene expression and species evolution, however, a systematic investigation towards the codon usage in Bombyx mori (B. mori) has not been reported yet. Moreover, it is still indistinct about the reasons contributing to the bias or the relationship between the bias and the evolution of B. mori. Results: The comparison of the codon usage pattern between the genomic DNA (gDNA) and the mitochondrial DNA (mtDNA) from B. mori suggests that mtDNA has a higher level of codon bias. Furthermore, the correspondence analysis suggests that natural selection, such as gene length, gene function and translational selection, dominates the codon preference of mtDNA, while the composition constraints for mutation bias only plays a minor role. Additionally, the clustering results of the silkworm superfamily suggest a lack of explicitness in the relationship between the codon usage of mitogenome and species evolution. Conclusions: Among the complicated influence factors leading to codon bias, natural selection is found to play a major role in shaping the high bias in the mtDNA of B. mori from our current data. Although the cluster analysis reveals that codon bias correlates little with the species evolution, furthermore, a detailed analysis of codon usage of mitogenome provides better insight into the evolutionary relationships in Lepidoptera. However, more new methods and data are needed to investigate the relationship between the mtDNA bias and evolution.