Landscape genetics across the Andes Mountains: Environmental variation drives genetic divergence in the leaf-cutting ant Atta cephalotes

Disentangling the mechanisms underlying spatial distribution of genetic variation into those due to environment or physical barriers from mere geographic distance is challenging in complex landscapes. The Andean uplift represents one of the most heterogeneous habitats where these questions remain unexplored as multiple mechanisms might interact, confounding their relative roles. We explore this broad question in the leaf-cutting ant Atta cephalotes, a species distributed across the Andes Mountains using nuclear microsatellite markers and mtCOI gene sequences. We investigate spatial genetic divergence across the Western range of Northern Andes in Colombia by testing the relative role of alternative scenarios of population divergence, including geographic distance (IBD), climatic conditions (IBE), and physical barriers due to the Andes Mountains (IBB). Our results reveal substantial genetic differentiation among A. cephalotes populations for both types of markers, but only nuclear divergence followed a hierarchical pattern with multiple models of genetic divergence imposed by the Western range. Model selection showed that IBD, IBE (temperature and precipitation), and IBB (Andes mountains) models, often proposed as individual drivers of genetic divergence, interact, and explain up to 33% of genetic divergence in A. cephalotes. IBE models remained significant after accounting for IBD, suggesting that environmental factors play a more prominent role when compared to IBB. These factors in combination with idiosyncratic dispersal patterns of ants appear to determine hierarchical patterns of gene flow. This study enriches our understanding of the forces shaping population divergence in complex habitat landscapes.

Genetic history and stock identity of beluga whales in Kotzebue Sound

We investigate the recent history and stock identity of beluga whales (Delphinapterus leucas) in Kotzebue Sound in the Chukchi Sea, a region long frequented by large numbers of belugas in summer until their near disappearance in the 1980s. Wide variation in numbers since then suggests a complex recent history that hinders recovery efforts. Analysis of teeth sampled during the historical (pre-decline) era using ancient DNA (aDNA) methods found that the original Kotzebue Sound whales were differentiated for mitochondrial DNA (mtDNA) from other summering concentrations across the Pacific Arctic revealing a demographically distinct subpopulation where long-established migratory culture likely facilitated population divergence. Analysis of microsatellite (nDNA) and mtDNA markers in belugas from the contemporary (post-decline) era revealed that whales from other stocks likely visited Kotzebue Sound, including during two low ice years when relatively large numbers of whales were present. Some mtDNA lineages were found only in Kotzebue Sound, with one recorded in both the historical and contemporary eras. Exclusion tests found a number of whales in Kotzebue Sound during the contemporary era that had nDNA genotypes unlikely to arise in other contemporary stocks in the Pacific Arctic. Our findings indicate that the Kotzebue Sound belugas comprised a unique stock of which a few remnants likely still co-occur with belugas from other larger stocks. We recommend that the US government work through the co-management process to greatly reduce or eliminate the taking of belugas, especially adult females, likely to belong to the Kotzebue Sound stock, until they recover.

Specialization on Ficus Supported by Genetic Divergence and Morphometrics in Sympatric Host-Populations of the Camellia Aphid, Aphis aurantii

Adaptation to different host plants is considered to be an important driver of the divergence and speciation of herbivorous insects. The application of molecular data and integrated taxonomic practices in recent years may contribute to our understanding of population divergence and speciation, especially for herbivorous insects considered to be polyphagous. Aphis aurantii is an important agricultural and forestry pest with a broad range of host plants. In this study, samples of A. aurantii feeding on different host plants in the same geographical area were collected, and their population genetic divergence and morphological difference were analyzed. Phylogenetic analysis and haplotype network analysis based on five genes revealed that the population on Ficus exhibited significantly genetic divergence from populations on other host plants, which was also supported by the statistical analysis based on measurements of 38 morphological characters. Our results suggest that A. aurantii has undergone specialized evolution on Ficus, and the Ficus population may represent a lineage that is experiencing ongoing sympatric speciation.

Genetic Factors Associated with Variation in Abundance of the Invasive Yellow Crazy Ant (Anoplolepis gracilipes)

<p>A key component of successful invasion is the ability of an introduced population to reach sufficient abundance to persist, spread, and alter or dominate the recipient biological community. Genetic diversity is one of many factors that may contribute to population dynamics, but has important ramifications for biological fitness, and thus invasion success in the long term. I explored genetic factors associated with variation in abundance (i.e., differential invasion success) of the yellow crazy ant Anoplolepis gracilipes in the Indo-Pacific region, primarily focussing on Arnhem Land in Australia's Northern Territory. I explored five aspects that I hypothesised could contribute to variation in the abundance of this ant: 1) I investigated the unusual reproductive mode of A. gracilipes, and tested whether it involved dependent-lineage genetic caste determination (DL GCD) in Arnhem Land. In DL GCD systems populations require hybridisation between genetically distinct groups to produce both reproductive and worker castes. Asymmetry in the ratio of different lineages may result in low abundance and population collapse. I found no evidence for a DL GCD system in A. gracilipes, and thus its abundance in Arnhem Land does not appear to be constrained by any lineage ratio asymmetry. Worker reproduction (either of males or asexual production of other workers) also appeared unlikely. The reproductive mode of the species remains fascinating but enigmatic; 2) I explored whether multiple source populations were responsible for the observed variation in abundance in Arnhem Land (i.e., is abundance associated with propagule pressure, or populations from different sources), and if the population has diverged since introduction. The A. gracilipes population in Arnhem Land stemmed from a single source, and thus propagule pressure was apparently not responsible for variation in abundance. In contrast to many invasive ants, population divergence has occurred since introduction; 3) I tested the hypotheses that genetic variation was associated with variation in abundance in Arnhem Land, and that ecological success was density-dependent. While the population divergence found in Chapter 3 was not related to variation in abundance, genotypic diversity was higher in more abundant nest clusters. These more abundant nest clusters were in turn associated with lower native ant species diversity, and a difference in composition of the invaded ant community (i.e., greater ecological success); 4) I revisited the invasion of the yellow crazy ant in Tokelau to determine whether a haplotype that was linked to greater abundance and dominance of the ant community has increased in distribution. Although ants of the inferred dominant haplotype were implicated in most new invasions, their abundance was substantially lower than previously observed in Tokelau; 5) I conducted a preliminary analysis of the metagenomic diversity of A. gracilipes endogenous parasites and symbionts among populations from Christmas Island, Okinawa, Samoa and Arnhem Land. Bacterial community composition and diversity differed between the study populations. Variation in abundance among A. gracilipes populations in Arnhem Land was not due to parasite load on populations with low abundance. However, low abundance of A. gracilipes was correlated with lower microbial diversity overall, and higher prevalence of some groups, notably two that confer antibiotic properties. Together, my findings suggest that propagule pressure, reproductive mode and haplotype-specific effects do not appear to be associated with variation in A. gracilipes abundance. Other genetic factors I investigated do appear to be associated with the variation in A. gracilipes abundance and effects on the invaded ant communities. Genotypic diversity was positively related to the abundance of A. gracilipes in Arnhem Land, and this relationship may be affected by population divergence through population bottlenecks. In addition, differences in bacterial diversity among populations highlighted several candidate bacteria that could be associated with variation in abundance, which would be a topic of future work. Although genetic factors are often implicated in the successful establishment of invasive species, my thesis demonstrates that genetic factors may also be associated with post-establishment population dynamics.</p>

Genetic Factors Associated with Variation in Abundance of the Invasive Yellow Crazy Ant (Anoplolepis gracilipes)

<p>A key component of successful invasion is the ability of an introduced population to reach sufficient abundance to persist, spread, and alter or dominate the recipient biological community. Genetic diversity is one of many factors that may contribute to population dynamics, but has important ramifications for biological fitness, and thus invasion success in the long term. I explored genetic factors associated with variation in abundance (i.e., differential invasion success) of the yellow crazy ant Anoplolepis gracilipes in the Indo-Pacific region, primarily focussing on Arnhem Land in Australia's Northern Territory. I explored five aspects that I hypothesised could contribute to variation in the abundance of this ant: 1) I investigated the unusual reproductive mode of A. gracilipes, and tested whether it involved dependent-lineage genetic caste determination (DL GCD) in Arnhem Land. In DL GCD systems populations require hybridisation between genetically distinct groups to produce both reproductive and worker castes. Asymmetry in the ratio of different lineages may result in low abundance and population collapse. I found no evidence for a DL GCD system in A. gracilipes, and thus its abundance in Arnhem Land does not appear to be constrained by any lineage ratio asymmetry. Worker reproduction (either of males or asexual production of other workers) also appeared unlikely. The reproductive mode of the species remains fascinating but enigmatic; 2) I explored whether multiple source populations were responsible for the observed variation in abundance in Arnhem Land (i.e., is abundance associated with propagule pressure, or populations from different sources), and if the population has diverged since introduction. The A. gracilipes population in Arnhem Land stemmed from a single source, and thus propagule pressure was apparently not responsible for variation in abundance. In contrast to many invasive ants, population divergence has occurred since introduction; 3) I tested the hypotheses that genetic variation was associated with variation in abundance in Arnhem Land, and that ecological success was density-dependent. While the population divergence found in Chapter 3 was not related to variation in abundance, genotypic diversity was higher in more abundant nest clusters. These more abundant nest clusters were in turn associated with lower native ant species diversity, and a difference in composition of the invaded ant community (i.e., greater ecological success); 4) I revisited the invasion of the yellow crazy ant in Tokelau to determine whether a haplotype that was linked to greater abundance and dominance of the ant community has increased in distribution. Although ants of the inferred dominant haplotype were implicated in most new invasions, their abundance was substantially lower than previously observed in Tokelau; 5) I conducted a preliminary analysis of the metagenomic diversity of A. gracilipes endogenous parasites and symbionts among populations from Christmas Island, Okinawa, Samoa and Arnhem Land. Bacterial community composition and diversity differed between the study populations. Variation in abundance among A. gracilipes populations in Arnhem Land was not due to parasite load on populations with low abundance. However, low abundance of A. gracilipes was correlated with lower microbial diversity overall, and higher prevalence of some groups, notably two that confer antibiotic properties. Together, my findings suggest that propagule pressure, reproductive mode and haplotype-specific effects do not appear to be associated with variation in A. gracilipes abundance. Other genetic factors I investigated do appear to be associated with the variation in A. gracilipes abundance and effects on the invaded ant communities. Genotypic diversity was positively related to the abundance of A. gracilipes in Arnhem Land, and this relationship may be affected by population divergence through population bottlenecks. In addition, differences in bacterial diversity among populations highlighted several candidate bacteria that could be associated with variation in abundance, which would be a topic of future work. Although genetic factors are often implicated in the successful establishment of invasive species, my thesis demonstrates that genetic factors may also be associated with post-establishment population dynamics.</p>

The Recombination Landscape of the Khoe-San - the Upper Limits of Recombination Divergence in Humans

Recombination maps are important resources for epidemiological and evolutionary analyses, however, there are currently no recombination maps representing any African population outside of those with West African ancestry. We inferred the demographic history for the Nama, an indigenous Khoe-San population of southern Africa, and derived a novel, population-specific recombination map from the whole genome sequencing of 54 Nama individuals. We hypothesized that there are no publicly available recombination maps representative of the Nama, considering the deep population divergence and subsequent isolation of the Khoe-San from other African groups. We showed that the recombination landscape of the Nama does not cluster with any continental groups with publicly available representative recombination maps. Finally, we used selection scans as an example of how fine-scale differences between the Nama recombination map and the combined Phase II HapMap recombination map can impact the outcome of selection scans.

Large-scale comparative genomics of Salmonella enterica to refine the organization of the global Salmonella population structure

1.AbstractSince the introduction of the White-Kauffmann-Le Minor (WKL) scheme for Salmonella serotyping, the nomenclature remains the most widely used for reporting the disease prevalence of Salmonella enterica across the globe. With the advent of whole genome sequencing (WGS), traditional serotyping has been increasingly replaced by in-silico methods that couple the detection of genetic variations in antigenic determinants with sequence-based typing. However, despite the integration of genomic-based typing by in-silico serotyping tools such as SeqSero2 and SISTR, in-silico serotyping in certain contexts remains ambiguous and insufficiently informative due to polyphyletic serovars. Furthermore, in spite of the widespread acknowledgement of polyphyly from genomic studies, the serotyping nomenclature remains unaltered. To prompt refinements to the Salmonella typing nomenclature for disease reporting, we herein performed a systematic characterization of putative polyphyletic serovars and the global Salmonella population structure by comparing 180,098 Salmonella genomes (representing 723 predicted serovars) from GenomeTrakr and PubMLST databases. We identified a range of core genome MLST typing thresholds that result in stable population structure, potentially suitable as the foundation of a genomic-based typing nomenclature for longitudinal surveillance. From the genomic comparisons of hundreds of predicted serovars, we demonstrated that in-silico serotyping classifications do not consistently reflect the population divergence observed at the genomic level. The organization of Salmonella subpopulations based on antigenic determinants can be confounded by homologous recombination and niche adaptation, resulting in shared classification of highly divergent genomes and misleading distinction between highly similar genomes. In consideration of the pivotal role of Salmonella serotyping, a compendium of putative polyphyletic serovars was compiled and made publicly available to provide additional context for future interpretations of in-silico serotyping results in disease surveillance settings. To refine the typing nomenclatures used in Salmonella surveillance reports, we foresee an improved typing scheme to be a hybrid that integrates both genomic and antigenic information such that the resolution from WGS is leveraged to improve the precision of subpopulation classifications while preserving the common names defined by the WKL scheme. Lastly, we stress the importance of controlled vocabulary integration for typing information in open data settings in order for the global Salmonella population dynamics to be fully trackable.2.Impact StatementSalmonella enterica (S. enterica) is a major foodborne pathogen responsible for an annual incidence rate of more than 90 million cases of foodborne illnesses worldwide. To surveil the high order Salmonella lineages, compare disease prevalence across jurisdictions worldwide, and inform risk assessments, in-silico serotyping has been established as the gold standard for typing the bacteria. However, despite previous Salmonella genomic studies reporting discordance between phylogenomic clades and serovars, refinements have yet been made to the serotyping scheme. Here, we analyzed over 180,000 Salmonella genomes representing 723 predicted serovars to subdivide the population into evolutionarily stable clusters in order to propose a stable organization of the Salmonella population structure that can form the basis of a genomic-based typing scheme for the pathogen. We described numerous instances in which genomes between serotypes are more similar than genomes within a serotype to reflect the inconsistencies of subpopulation classifications based on antigenic determinants. Moreover, we found inconsistencies between predicted serovars and reported serovars which highlighted potential errors in existing in-silico serotyping tools and the need to implement controlled vocabularies for reporting Salmonella subtypes in public databases. The findings of our study aim to motivate the future development of a standardized genomic-based typing nomenclature that more accurately captures the natural populations of S. enterica.3.Data SummaryThe assembly accession numbers of the genomes analyzed in this study (n = 204,952) and the associated metadata (e.g. sampling location, collection date, FTP address for retrieval) are documented in Table S1. The GenomeTrakr genomes were retrieved from the National Center for Biological Information GenBank database. The PubMLST genomes were retrieved using the BIGSdb API.

Mitonuclear mismatch alters nuclear gene expression in naturally introgressed Rhinolophus bats

Background Mitochondrial function involves the interplay between mitochondrial and nuclear genomes. Such mitonuclear interactions can be disrupted by the introgression of mitochondrial DNA between taxa or divergent populations. Previous studies of several model systems (e.g. Drosophila) indicate that the disruption of mitonuclear interactions, termed mitonuclear mismatch, can alter nuclear gene expression, yet few studies have focused on natural populations. Results Here we study a naturally introgressed population in the secondary contact zone of two subspecies of the intermediate horseshoe bat (Rhinolophus affinis), in which individuals possess either mitonuclear matched or mismatched genotypes. We generated transcriptome data for six tissue types from five mitonuclear matched and five mismatched individuals. Our results revealed strong tissue-specific effects of mitonuclear mismatch on nuclear gene expression with the largest effect seen in pectoral muscle. Moreover, consistent with the hypothesis that genes associated with the response to oxidative stress may be upregulated in mitonuclear mismatched individuals, we identified several such gene candidates, including DNASE1L3, GPx3 and HSPB6 in muscle, and ISG15 and IFI6 in heart. Conclusion Our study reveals how mitonuclear mismatch arising from introgression in natural populations is likely to have fitness consequences. Underlying the processes that maintain mitonuclear discordance is a step forward to understand the role of mitonuclear interactions in population divergence and speciation.