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Metatranscriptomics is a powerful method for studying the composition and function of complex microbial communities. The application of metatranscriptomics to multi-species parasite infections is of particular interest, as research on parasite evolution and diversification has been hampered by technical challenges to genome-scale DNA sequencing. In particular, blood parasites of vertebrates are abundant and diverse though they often occur at low infection intensities and exist as multi-species infections, rendering the isolation of genomic sequence data challenging. Here, we use birds and their diverse haemosporidian parasites to illustrate the potential for metatranscriptome sequencing to generate large quantities of genome-wide sequence data from multiple blood parasite species simultaneously. We used RNA-Seq on 24 blood samples from songbirds in North America to show that metatranscriptomes can yield large proportions of haemosporidian protein-coding gene repertoires even when infections are low-intensity (<0.1% red blood cells infected) and consist of multiple parasite taxa. By bioinformatically separating host and parasite transcripts and assigning them to the haemosporidian genus of origin, we found that transcriptomes detected ~23% more total parasite infections across all samples than were identified using microscopy and DNA barcoding. For single-species infections, we obtained data for upwards of 1,300 loci from samples with as low as 0.03% parasitemia, with the number of loci increasing with infection intensity. In total, we provide data for 1,502 single-copy orthologous loci from a phylogenetically-diverse set of 33 haemosporidian mitochondrial lineages. The metatranscriptomic approach described here has the potential to accelerate ecological and evolutionary research on haemosporidians and other diverse parasites.
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A comparative study of the closely related species of the genus Gastridium (Poaceae, Tribe: Poeae, Subtribe: Agrostidinae), G. ventricosum, G. phleoides, and G. scabrum was assessed based on a critical examination of both fresh and dried specimens, including relevant material, and a morphometric analysis of herbarium specimens collected in Italy. The study aimed to provide new diagnostic tools to improve the taxonomy of the genus and confirm species delimitation. Thus, variation in floral morphology in the three species was further explored using seven quantitative and ten qualitative characters measured on 318 spikelets, both awned and unawned. Statistical methods, including principal components analysis (PCA) and non‐metric multidimensional scaling (NMDS), were used. Numerical analyses showed a general distinctness of spikelets and florets, consistent with the three studied species, and revealed among and within species variation patterns in between‐ both spikelet types. Accordingly, the most informative quantitative characters appeared to be the width and length of glumes and the length of awns, useful to distinguish G. phleoides with the substantially narrowest glumes and the significantly higher length of awns from the others, especially from G. scabrum, in which the width of glumes reaches the highest value. The most informative qualitative characters appeared to be the presence/absence of thick hairs or minute tubercles on the upper side of the lemma. The autonomy of the three studied species was confirmed. The taxonomic significance of the results was briefly discussed, and notes on the species dispersal were added. Some nomenclatural and taxonomic notes on G. scabrum, of which literature still showed evidence of a general unawareness, were given.
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Rainforests on Borneo support exceptional concentrations of endemic insect biodiversity, but many of these forest-dependent species are threatened by land-use change. Totally protected areas (TPAs) of forest are key for conserving biodiversity, and we examined the effectiveness of the current TPA network for conserving range-restricted butterflies in Sabah (Malaysian Borneo). We found that mean diurnal temperature range and precipitation of the wettest quarter of the year were the most important predictors of butterfly distributions (N = 77 range-restricted species), and that species richness increased with elevation and aboveground forest carbon. On average across all species, TPAs were effective at conserving ~43% of species’ ranges, but encompassed only ~40% of areas with high species richness (i.e. containing at least 50% of our study species). The TPA network also included only 33-40% of areas identified as high priority for conserving range-restricted species, as determined by a systematic conservation prioritization analysis. Hence, the current TPA network is reasonably effective at conserving range-restricted butterflies, although considerable areas of high species richness (6565 km2) and high conservation priority (11,152-12,531 km2) are not currently protected. Sabah’s remaining forests, and the range-restricted species they support, are under continued threat from agricultural expansion and urban development, and our study highlights important areas of rainforest that require enhanced protection.
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Aim: Bees play an important role in natural ecosystems and the world’s food supply. In the past decades, bee abundance and diversity have declined globally. This has resulted in decreased pollination services for natural ecosystems and the agricultural sector at the field scale. One of the causes of the decline in bee abundance and diversity is the use of pesticides. Linking pesticide use, land use and bee presence could provide crucial insights into areas and pesticides that pose a significant threat to the abundance and diversity of bees. Obtaining actual figures of farmer pesticide use is rarely possible. Therefore, we designed a method to study the effects of potential pesticide use on the survival and distribution of honey- and bumblebees. Location: The Netherlands. Methods: A pesticide risk model was implemented incorporating a hazard quotient as the risk assessment. The number of allowed pesticide active ingredients per crop that could pose a risk to honeybees and bumblebees were linked to the Dutch crop parcel locations for 2015 and 2016. The potential pesticide risk maps were analyzed using honeybee colony survival and bumblebee presence data. Results: Non-significant negative effects of potential pesticide risk on honeybee colony survival and bumblebee presence were found. A significant negative effect of greenhouses was identified for both honeybees and bumblebees. The most important factors in the models predicting honeybee colony survival and bumblebee presence were urban land areas and natural grasslands respectively, both showing a positive effect. Main conclusions: Here, the first attempt to estimate and map pesticide risk to bees in the Netherlands in a country-wide manner is presented. The results could provide crucial high-resolution insights for bee conservation action and facilitate the increase of pollination services in natural ecosystems and the agricultural sector on a local and country-wide scale.
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Although genotyping-by-sequencing (GBS) is a well-established marker technology in diploids, the development of best practices for tetraploid species is a topic of current research. We determined the theoretical relationship between read depth and the phred-scaled probability of genotype misclassification, conditioned on the true genotype, which we call Expected Genotype Quality (EGQ). If the GBS method has 0.5% allelic error, then 17 reads are needed to classify simplex tetraploids as heterozygous with 95% accuracy (EGQ = 13) compared with 61 reads to determine allele dosage. We developed an R script to convert tetraploid GBS data in Variant Call Format (VCF) into diploidized genotype calls and applied it to 267 interspecific hybrids of the tetraploid forage grass Urochloa (syn. Brachiaria). When reads were aligned to a mock reference genome created from GBS data of the U. brizantha cultivar ‘Marandu’, 25,678 bi-allelic SNPs were discovered, compared to approximately 3000 SNPs when aligning to the closest true reference genomes, Setaria viridis and S. italica. Cross-validation revealed that missing genotypes were imputed by the Random Forest method with a median accuracy of 0.85, regardless of heterozygote frequency. Using the Urochloa spp. hybrids, we illustrated how filtering samples based only on GQ creates genotype bias; a depth threshold based on EGQ is also needed, regardless of whether genotypes are called using a diploidized or allele dosage model.
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C. elegans is an animal with few cells, but a striking diversity of cell types. Here, we characterize the molecular basis for their specification by profiling the transcriptomes of 86,024 single embryonic cells. We identify 502 terminal and pre-terminal cell types, mapping most single cell transcriptomes to their exact position in C. elegans’ invariant lineage. Using these annotations, we find that: 1) the correlation between a cell’s lineage and its transcriptome increases from mid to late gastrulation, then falls dramatically as cells in the nervous system and pharynx adopt their terminal fates; 2) multilineage priming contributes to the differentiation of sister cells at dozens of lineage branches; and 3) most distinct lineages that produce the same anatomical cell type converge to a homogenous transcriptomic state.
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Our understanding of the ecology and phylogenetic relationships of Pachycormiformes, a group of Mesozoic stem teleosts including the iconic Leedsichthys, has often been hindered by a lack of comprehensive morphological information. Micro‐CT scanning of an articulated, although flattened, cranium of the edentulous Martillichthys renwickae from the Middle Jurassic (Callovian) Oxford Clay of the UK reveals previously unknown internal details of the most complete suspension‐feeding pachycormiform skull known, including the palate, braincase and branchial skeleton. The latter preserves gill rakers with elongate, pointed projections similar to those of Asthenocormus, in contrast to the finer fimbriations associated with Leedsichthys. We also reinterpret some previously described features, including dermal bone patterns of the snout, skull roof and lower jaw, and the morphology of the ventral hyoid arch. These new anatomical data reinforce the phylogenetic placement of Martillichthys as part of the Jurassic clade of edentulous pachycormiforms. The elongate skull geometry of these Jurassic taxa is strikingly similar to that of Ohmdenia, the sister taxon to edentulous pachycormiforms, but contrasts sharply with the morphology of the Late Cretaceous edentulous pachycormiform Bonnerichthys, raising questions over the phylogenetic relationships among these taxa. Most significantly, Martillichthys shows specialized characters with a restricted phylogenetic distribution among suspension‐feeding pachycormiforms, including the distinctive gill rakers and a greatly extended occipital stalk. Our analysis of Martillichthys supports past interpretations of a close relationship with Asthenocormus, and provides a model for interpreting the less complete remains of other members of this enigmatic group of fishes.
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Analysing genomic variation within and between sister species is a first step towards understanding species boundaries. We focused on two sister species of cold-resistant leaf beetles, Gonioctena quinquepunctata and G. intermedia, whose ranges overlap in the Alps. A previous study of DNA sequence variation had revealed multiple instances of mitochondrial genome introgression in this region, suggesting recent hybridizations between the two species. To evaluate the extent of gene exchange resulting from these hybridization events, we sampled individuals of both species inside and outside the hybrid zone and analysed genomic variation among them using RAD-seq markers. Individual levels of introgression in the nuclear genome were estimated first by defining species-specific SNPs (displaying a fixed difference between species) a priori, and second by using model-based methods. Both types of analyses indicated little gene exchange, if any, between species at the level of the nuclear genome. While the first method suggested slightly more gene flow, we argue that it has likely overestimated introgression in the phylogeographic context of this study. We conclude that strong intrinsic barriers prevent genetic exchange at the level of the nuclear genome between the two species. The apparent discrepancy observed between introgression occurring in the nuclear and mitochondrial genomes could be explained by selection acting in favour of the latter. Also, these results have consequences for the phylogeographic study of each species, since we can assume that genetic diversity in the overlapping portion of their ranges is not the product of introgression.
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Information on how migratory populations are genetically structured during the overwintering season of the annual cycle can improve our understanding of the strength of migratory connectivity and help identify populations as units for management. Here, we use a genotype-by-sequencing approach to investigate whether population genetic structure exists among overwintering aggregations of the Pacific Dunlin subspecies (Calidris alpina pacifica) sampled at two spatial scales (i.e. within and among overwintering sites) in the eastern Pacific Flyway. Genome-wide analyses of 874 single nucleotide polymorphisms across 80 sampled individuals revealed no evidence for genetic differentiation among aggregations overwintering at three locations within the Fraser River Estuary (FRE) of British Columbia. Similarly, comparisons of aggregations in the FRE and those overwintering in southern sites in California and Mexico indicated no genetic segregation between northern and southern overwintering areas. These results suggest that Pacific Dunlin residing within the FRE, Sacramento Valley (California) and Guerrero Negro (Mexico) are genetically homogeneous, with no evident genetic structure between sampled sites or regions across the overwintering range. Despite no evidence for differentiation among aggregations, we identified a significant effect of geographical distance between sites on the distribution of individual genotypes in a redundancy analysis; however, a small proportion of the total genotypic variance (R2 = 0.036, P = 0.011) was explained by the combined effect of latitude and longitude, suggesting weak genomic patterns of isolation-by-distance that are consistent with chain-like migratory connectivity between breeding and overwintering areas. Our study represents the first genome-scale investigation of population structure for a Dunlin subspecies and provides essential baseline estimates of genomic diversity and differentiation within the Pacific Dunlin.
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Mathematical models of childhood diseases date back to the early twentieth century. In several cases, models that make the simplifying assumption of homogeneous time-dependent transmission rates give good agreement with data in the absence of secular trends in population demography or transmission. The prime example is afforded by the dynamics of measles in industrialized countries in the pre-vaccine era. Accurate description of the transient dynamics following the introduction of routine vaccination has proved more challenging, however. This is true even in the case of measles which has a well-understood natural history and an effective vaccine that confers long-lasting protection against infection. Here, to shed light on the causes of this problem, we demonstrate that, while the dynamics of homogeneous and age-structured models can be qualitatively similar in the absence of vaccination, they diverge subsequent to vaccine roll-out. In particular, we show that immunization induces changes in transmission rates, which in turn reshapes the age distribution of infection prevalence, which effectively modulates the amplitude of seasonality in such systems. To examine this phenomenon empirically, we fit transmission models to measles notification data from London that span the introduction of the vaccine. We find that a simple age-structured model provides a much better fit to the data than does a homogeneous model, especially in the transition period from the pre-vaccine to the vaccine era. Thus, we propose that age structure and heterogeneities in contact rates are critical features needed to accurately capture transient dynamics in the presence of secular trends.
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