The primary vector of the trypanosome parasite causing human and animal African trypanosomiasis in Uganda is the riverine tsetse fly Glossina fuscipes fuscipes (Gff). Our study improved the Gff ...genome assembly with whole genome 10× Chromium sequencing of a lab reared pupae, identified autosomal versus sex-chromosomal regions of the genome with ddRAD-seq data from 627 field caught Gff, and identified SNPs associated with trypanosome infection with genome-wide association (GWA) analysis in a subset of 351 flies. Results from 10× Chromium sequencing greatly improved Gff genome assembly metrics and assigned a full third of the genome to the sex chromosome. Results from ddRAD-seq suggested possible sex-chromosome aneuploidy in Gff and identified a single autosomal SNP to be highly associated with trypanosome infection. The top associated SNP was ∼1100 bp upstream of the gene lecithin cholesterol acyltransferase (LCAT), an important component of the molecular pathway that initiates trypanosome lysis and protection in mammals. Results suggest that there may be naturally occurring genetic variation in Gff in genomic regions in linkage disequilibrium with LCAT that can protect against trypanosome infection, thereby paving the way for targeted research into novel vector control strategies that can promote parasite resistance in natural populations.
•Improved genome assembly identified a third of the genome as sex chromosome associated, and suggested aneuploidy•GWAS accounted for chromosome-arm specific patterns of population structure and linkage disequilibrium•Identified a single SNP upstream of lecithin cholesterol acyltransferase associated with trypanosome infection•Suggests there are naturally occurring genetic mechanisms of protection against trypanosome infection in tsetse flies.
The effective population size (Ne) is a fundamental parameter in population genetics that determines the relative strength of selection and random genetic drift, the effect of migration, levels of ...inbreeding, and linkage disequilibrium. In many cases where it has been estimated in animals, Ne is on the order of 10%–20% of the census size. In this study, we use 12 microsatellite markers and 14,888 single nucleotide polymorphisms (SNPs) to empirically estimate Ne in Aedes aegypti, the major vector of yellow fever, dengue, chikungunya, and Zika viruses. We used the method of temporal sampling to estimate Ne on a global dataset made up of 46 samples of Ae. aegypti that included multiple time points from 17 widely distributed geographic localities. Our Ne estimates for Ae. aegypti fell within a broad range (~25–3,000) and averaged between 400 and 600 across all localities and time points sampled. Adult census size (Nc) estimates for this species range between one and five thousand, so the Ne/Nc ratio is about the same as for most animals. These Ne values are lower than estimates available for other insects and have important implications for the design of genetic control strategies to reduce the impact of this species of mosquito on human health.
Vector control is an effective strategy for reducing vector‐borne disease transmission, but requires knowledge of vector habitat use and dispersal patterns. Our goal was to improve this knowledge for ...the tsetse species Glossina pallidipes, a vector of human and animal African trypanosomiasis, which are diseases that pose serious health and socioeconomic burdens across sub‐Saharan Africa. We used random forest regression to (i) build and integrate models of G. pallidipes habitat suitability and genetic connectivity across Kenya and northern Tanzania and (ii) provide novel vector control recommendations. Inputs for the models included field survey records from 349 trap locations, genetic data from 11 microsatellite loci from 659 flies and 29 sampling sites, and remotely sensed environmental data. The suitability and connectivity models explained approximately 80% and 67% of the variance in the occurrence and genetic data and exhibited high accuracy based on cross‐validation. The bivariate map showed that suitability and connectivity vary independently across the landscape and was used to inform our vector control recommendations. Post hoc analyses show spatial variation in the correlations between the most important environmental predictors from our models and each response variable (e.g., suitability and connectivity) as well as heterogeneity in expected future climatic change of these predictors. The bivariate map suggests that vector control is most likely to be successful in the Lake Victoria Basin and supports the previous recommendation that G. pallidipes from most of eastern Kenya should be managed as a single unit. We further recommend that future monitoring efforts should focus on tracking potential changes in vector presence and dispersal around the Serengeti and the Lake Victoria Basin based on projected local climatic shifts. The strong performance of the spatial models suggests potential for our integrative methodology to be used to understand future impacts of climate change in this and other vector systems.
Adaptive responses to thermal stress in poikilotherms plays an important role in determining competitive ability and species distributions. Amino acid substitutions that affect protein stability and ...modify the thermal optima of orthologous proteins may be particularly important in this context. Here, we examine a set of 2,770 protein-coding genes to determine if proteins in a highly invasive heat tolerant blue mussel (Mytilus galloprovincialis) contain signals of adaptive increases in protein stability relative to orthologs in a more cold tolerant M. trossulus. Such thermal adaptations might help to explain, mechanistically, the success with which the invasive marine mussel M. galloprovincialis has displaced native species in contact zones in the eastern (California) and western (Japan) Pacific. We tested for stabilizing amino acid substitutions in warm tolerant M. galloprovincialis relative to cold tolerant M. trossulus with a generalized linear model that compares in silico estimates of recent changes in protein stability among closely related congeners. Fixed substitutions in M. galloprovincialis were 3,180.0 calories per mol per substitution more stabilizing at genes with both elevated dN/dS ratios and transcriptional responses to heat stress, and 705.8 calories per mol per substitution more stabilizing across all 2,770 loci investigated. Amino acid substitutions concentrated in a small number of genes were more stabilizing in M. galloprovincialis compared with cold tolerant M. trossulus. We also tested for, but did not find, enrichment of a priori GO terms in genes with elevated dN/dS ratios in M. galloprovincialis. This might indicate that selection for thermodynamic stability is generic across all lineages, and suggests that the high change in estimated protein stability that we observed in M. galloprovincialis is driven by selection for extra stabilizing substitutions, rather than by higher incidence of selection in a greater number of genes in this lineage. Nonetheless, our finding of more stabilizing amino acid changes in the warm adapted lineage is important because it suggests that adaption for thermal stability has contributed to M. galloprovincialis' superior tolerance to heat stress, and that pairing tests for positive selection and tests for transcriptional response to heat stress can identify candidates of protein stability adaptation.
Aedes albopictus originates from Southeast Asia and is considered one of the most invasive species globally. This mosquito is a nuisance and a disease vector of significant public health relevance. ...In Europe, Ae. albopictus is firmly established and widespread south of the Alps, a mountain range that forms a formidable biogeographic barrier to many organisms. Recent reports of Ae. albopictus north of the Alps raise questions of (1) the origins of its recent invasion, and (2) if this mosquito has established overwintering populations north of the Alps. To answer these questions, we analyzed population genomic data from >4000 genome‐wide SNPs obtained through double‐digest restriction site‐associated DNA sequencing. We collected SNP data from specimens from six sites in Switzerland, north and south of the Alps, and analyzed them together with specimens from other 33 European sites, five from the Americas, and five from its Asian native range. At a global level, we detected four genetic clusters with specimens from Indonesia, Brazil, and Japan as the most differentiated, whereas specimens from Europe, Hong Kong, and USA largely overlapped. Across the Alps, we detected a weak genetic structure and high levels of genetic admixture, supporting a scenario of rapid and human‐aided dispersal along transportation routes. While the genetic pattern suggests frequent re‐introductions into Switzerland from Italian sources, the recovery of a pair of full siblings in two consecutive years in Strasbourg, France, suggests the presence of an overwintering population north of the Alps. The suggestion of overwintering populations of Ae. albopictus north of the Alps and the expansion patterns identified points to an increased risk of further northward expansion and the need for increased surveillance of mosquito populations in Northern Europe.
Population genomics study to investigate the recent invasion of Aedes albopictus in Europe across the Alps. While we detected a weak genetic structure and high levels of genetic admixture, the recovery of a pair of full sibling consecutive years in Strasbourg, France, suggests the presence of an overwintering population north of the Alps. The expansion patterns points to an increased risk of further spread and the need for increased surveillance of mosquito population in Europe.
The tsetse fly
, the major vector of the parasite that causes animal African trypanosomiasis in Kenya, has been subject to intense control measures with only limited success. The
population dynamics ...and dispersal patterns that underlie limited success in vector control campaigns remain unresolved, and knowledge on genetic connectivity can provide insights, and thereby improve control and monitoring efforts. We therefore investigated the population structure and estimated migration and demographic parameters in
using genotypic data from 11 microsatellite loci scored in 250 tsetse flies collected from eight localities in Kenya. Clustering analysis identified two genetically distinct eastern and western clusters (mean between-cluster
= 0.202) separated by the Great Rift Valley. We also found evidence of admixture and migration between the eastern and western clusters, isolation by distance, and a widespread signal of inbreeding. We detected differences in population dynamics and dispersal patterns between the western and eastern clusters. These included lower genetic diversity (allelic richness; 7.48 versus 10.99), higher relatedness (percent related individuals; 21.4% versus 9.1%), and greater genetic differentiation (mean within-cluster
; 0.183 versus 0.018) in the western than the eastern cluster. Findings are consistent with the presence of smaller, less well-connected populations in Western relative to eastern Kenya. These data suggest that recent anthropogenic influences such as land use changes and vector control programs have influenced population dynamics in
in Kenya, and that vector control efforts should include some region-specific strategies to effectively control this disease vector.
Tsetse flies (Glossina spp.) are vectors of parasitic trypanosomes, which cause human (HAT) and animal African trypanosomiasis (AAT) in sub-Saharan Africa. In Uganda, Glossina fuscipes fuscipes (Gff) ...is the main vector of HAT, where it transmits Gambiense disease in the northwest and Rhodesiense disease in central, southeast and western regions. Endosymbionts can influence transmission efficiency of parasites through their insect vectors via conferring a protective effect against the parasite. It is known that the bacterium Spiroplasma is capable of protecting its Drosophila host from infection with a parasitic nematode. This endosymbiont can also impact its host's population structure via altering host reproductive traits. Here, we used field collections across 26 different Gff sampling sites in northern and western Uganda to investigate the association of Spiroplasma with geographic origin, seasonal conditions, Gff genetic background and sex, and trypanosome infection status. We also investigated the influence of Spiroplasma on Gff vector competence to trypanosome infections under laboratory conditions. Generalized linear models (GLM) showed that Spiroplasma probability was correlated with the geographic origin of Gff host and with the season of collection, with higher prevalence found in flies within the Albert Nile (0.42 vs 0.16) and Achwa River (0.36 vs 0.08) watersheds and with higher prevalence detected in flies collected in the intermediate than wet season. In contrast, there was no significant correlation of Spiroplasma prevalence with Gff host genetic background or sex once geographic origin was accounted for in generalized linear models. Additionally, we found a potential negative correlation of Spiroplasma with trypanosome infection, with only 2% of Spiroplasma infected flies harboring trypanosome co-infections. We also found that in a laboratory line of Gff, parasitic trypanosomes are less likely to colonize the midgut in individuals that harbor Spiroplasma infection. These results indicate that Spiroplasma infections in tsetse may be maintained by not only maternal but also via horizontal transmission routes, and Spiroplasma infections may also have important effects on trypanosome transmission efficiency of the host tsetse. Potential functional effects of Spiroplasma infection in Gff could have impacts on vector control approaches to reduce trypanosome infections.
Seagrass populations are in decline worldwide. Eelgrass (Zostera marina L.), one of California's native seagrasses, is no exception to this trend. In the last 8 years, the estuary in Morro Bay, ...California, has lost 95% of its eelgrass. Population bottlenecks like this one often result in severe reductions in genetic diversity; however, this is not always the case. The decline of eelgrass in Morro Bay provides an opportunity to better understand the effects of population decline on population genetics. Furthermore, the failure of recent restoration efforts necessitates a better understanding of the genetic underpinnings of the population. Previous research on eelgrass in California has demonstrated a link between population genetic diversity and eelgrass bed health, ecosystem functioning, and resilience to disturbance and extreme climatic events. The genetic diversity and population structure of Mono Bay eelgrass have not been assessed until this study. We also compare Morro Bay eelgrass to Bodega Bay eelgrass in Northern California We conducted fragment length analysis of nine microsatellite loci on 133 Morro Bay samples, and 20 Bodega Bay samples. We found no population differentiation between the remaining beds in Morro Bay and no difference among samples growing at different tidal depths. Comparisons with Bodega Bay revealed that Morro Bay eelgrass contains three first-generation migrants from the north, but Morro Bay remains considerably genetically differentiated from Bodega Bay. Despite the precipitous loss of eelgrass in Morro Bay between 2008 and 2017, genetic diversity remains relatively high and comparable to other populations on the west coast.
Glossina pallidipes is a major vector of both Human and Animal African Trypanosomiasis (HAT and AAT) in Kenya. The disease imposes economic burden on endemic regions in Kenya, including south-western ...Kenya, which has undergone intense but unsuccessful tsetse fly control measures. We genotyped 387 G. pallidipes flies at 13 microsatellite markers to evaluate levels of temporal genetic variation in two regions that have been subjected to intensive eradication campaigns from the 1960s to the 1980s. One of the regions, Nguruman Escarpment, has been subject to habitat alteration due to human activities, while the other, Ruma National Park, has not. In addition, Nguruman Escarpment is impacted by the movement of grazing animals into the area from neighboring regions during the drought season. We collected our samples from three geographically close sampling sites for each of the two regions. Samples were collected between the years 2003 and 2015, spanning ~96 tsetse fly generations.
We established that allelic richness averaged 3.49 and 3.63, and temporal N
estimates averaged 594 in Nguruman Escarpment and 1120 in Ruma National Park. This suggests that genetic diversity is similar to what was found in previous studies of G. pallidipes in Uganda and Kenya, implying that we could not detect a reduction in genetic diversity following the extensive control efforts during the 1960s to the 1980s. However, we did find differences in temporal patterns of genetic variation between the two regions, indicated by clustering analysis, pairwise F
, and Fisher's exact tests for changes in allele and genotype frequencies. In Nguruman Escarpment, findings indicated differentiation among samples collected in different years, and evidence of local genetic bottlenecks in two locations previous to 2003, and between 2009 and 2015. In contrast, there was no consistent evidence of differentiation among samples collected in different years, and no evidence of local genetic bottlenecks in Ruma National Park.
Our findings suggest that, despite extensive control measures especially between the 1960s and the 1980s, tsetse flies in these regions persist with levels of genetic diversity similar to that found in populations that did not experience extensive control measures. Our findings also indicate temporal genetic differentiation in Nguruman Escarpment detected at a scale of > 80 generations, and no similar temporal differentiation in Ruma National Park. The different level of temporal differentiation between the two regions indicates that genetic drift is stronger in Nugruman Escarpment, for as-yet unknown reasons, which may include differences in land management. This suggests land management may have an impact on G. pallidipes population genetics, and reinforces the importance of long term monitoring of vector populations in estimates of parameters needed to model and plan effective species-specific control measures.
Glossina fuscipes fuscipes is a tsetse species of high economic importance in Uganda where it is responsible for transmitting animal African trypanosomiasis (AAT) and both the chronic and acute forms ...of human African trypanosomiasis (HAT). We used genotype data from 17 microsatellites and a mitochondrial DNA marker to assess temporal changes in gene frequency for samples collected between the periods ranging from 2008 to 2014 in nine localities spanning regions known to harbor the two forms of HAT in northern Uganda.
Our findings suggest that the majority of the studied populations in both HAT foci are genetically stable across the time span sampled. Pairwise estimates of differentiation using standardized FST and Jost's DEST between time points sampled for each site were generally low and ranged between 0.0019 and 0.1312 for both sets of indices. We observed the highest values of FST and DEST between time points sampled from Kitgum (KT), Karuma (KR), Moyo (MY) and Pader (PD), and the possible reasons for this are discussed. Effective population size (Ne) estimates using Waple's temporal method ranged from 103 (95% CI: 73-138) in Kitgum to 962 (95% CI: 669-1309) in Oculoi (OC). Additionally, evidence of a bottleneck event was detected in only one population at one time point sampled; Aminakwach (AM-27) from December 2014 (P < 0.03889).
Findings suggest general temporal stability of tsetse vectors in foci of both forms of HAT in northern Uganda. Genetic stability and the moderate effective population sizes imply that a re-emergence of vectors from local residual populations missed by control efforts is an important risk. This underscores the need for more sensitive sampling and monitoring to detect residual populations following control activities.
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