Intense research efforts on phylogeography over the last two decades uncovered major biogeographical trends and renewed our understandings of plant domestication in the Mediterranean. We aim to investigate the evolutionary history and the origin of domestication of the carob tree that has been cultivated for millennia for food and fodder. We used >1000 microsatellite genotypes to identify carob evolutionary units (CEUs) based on genetic diversity structure and geography. We investigated genome-wide diversity and evolutionary patterns of the CEUs with 3557 SNPs generated by restriction-site associated DNA sequencing (RADseq). The 56 populations sampled across the Mediterranean basin, classified as natural, semi-natural or cultivated, were examined. Although, RADseq data are consistent with previous studies identifying a strong West-to-East genetic structure and considerable admixture in some geographic parts, we reconstructed a new phylogeographic scenario with two migration routes occurring from a single refugium likely located in South-Western Morocco. Our results do not favour the regionally bound or single origin of domestication. Indeed, our findings support a cultivation model of locally selected wild genotypes, albeit punctuated by long-distance westward dispersals of domesticated varieties by humans, concomitant with major cultural waves by Romans and Arabs in the regions of dispersal. Ex-situ efforts to preserve carob genetic resources should prioritize accessions from both western and eastern populations, with emphasis on the most differentiated CEUs situated in South-Western Morocco, South Spain and Eastern Mediterranean. Our study underscores the relevance of natural and seminatural habitats of Mediterranean forests and their refugia in the conservation efforts of tree crops.
Resistance evolution, from genetic mechanism to ecological contextRegina S. Baucom1, Veronica Iriart2, Julia Kreiner3, and Sarah Yakimowski41Ecology and Evolutionary Biology Department, University of Michigan, Ann Arbor, Michigan, USA2Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, USA3Biodiversity Research Centre & Department of Botany, The University of British Columbia, Vancouver, BC V6T 1Z44Department of Biology, Queen’s University, Kingston, ON K7L 3N6CorrespondenceRegina S. Baucom, Ecology and Evolutionary Biology Department, University of Michigan, Ann Arbor, Michigan, 48109.Email: firstname.lastname@example.org*Authors contributed equallyPesticide use by humans has induced strong selective pressures, reshaping evolutionary trajectories, ecological networks, and even influencing ecosystem dynamics. The evolution of pesticide resistance across weeds, insects, and fungi often leads to negative impacts on both human health and the economy while concomitantly providing excellent systems for studying the process of evolution. In fact, the study of pesticide resistance has been a feature of evolutionary biology since the Evolutionary Synthesis, with Dobzhansky noting in his book The Genetics and Origins of Species (1937) that cyanide resistance in the California red scale constituted the “best proof of the effectiveness of natural selection yet obtained”. Following the pioneering work of James Crow and others in the 1950’s—which greatly expanded our knowledge of the genetics underlying adaptation—the study of pesticide resistance has shed light on a variety of topics, such as the repeatability of phenotypic evolution across the landscape, ‘hotspots’ of evolution across the genome, and information on the number and type of genetic solutions that populations may employ to strong selection pressures.Landscape level approaches have come to the forefront over the last 20 years of resistance evolution research, often taking advantage of the fact that replicated populations of the same species are exposed to the same pesticide. Further, the resistance evolution field is turning more attention to the ecological context within which resistance evolution occurs, likely stemming, at least in part, from an historical focus on fitness costs (Cousens & Fournier-Level 2018; Baucom 2019). This special feature, ‘Resistance evolution, from genetic mechanism to ecological context’ in Molecular Ecology captures the current state of resistance evolution with contributions broadly addressing the question ‘What has the rapid evolution of pesticide resistance taught us about genome dynamics and adaptation as well as the ecological context within which resistance evolution occurs?’ Below, we contextualize the manuscripts in this special issue that provide insight into the state of the art investigations of resistance evolution across various species of insects, weeds and fungi.
Horizontal gene transfer via plasmids is important for the dissemination of antibiotic resistance genes among medically relevant pathogens. Specifically, the transfer of IncHI1A plasmids is believed to facilitate the spread of antibiotic resistance genes, such as carbapenemases, within the clinically important family Enterobacteriaceae. The microbial community of urban wastewater treatment plants has been shown to be highly permissive towards conjugal transfer of IncP1 plasmids. Here, we tracked the transfer of the P1 plasmid pB10 and the clinically relevant HI1A plasmid R27 in the microbial communities present in urban residential sewage entering full-scale wastewater treatment plants. We found that both plasmids readily transferred to these communities and that strains in the sewage were able to further disseminate them. Furthermore, that R27 has a broad potential host range, but a low host divergence. Interestingly, although the majority of R27 transfer events were to members of Enterobacteriaceae, we found a subset of transfer to other families, even other phyla. Indicating, that HI1A plasmids facilitate horizontal gene transfer both within Enterobacteriaceae, but also across families of especially Gammaproteobacteria, such as Moraxellaceae, Pseudomonadaceae and Shewanellaceae. pB10 displayed a similar potential host range as R27. In contrast to R27, pB10 had a high host divergence. By culture enrichment of the transconjugant communities, we show that sewage strains of Enterobacteriaceae and Aeromonadaceae can stably maintain R27 and pB10, respectively. Our results suggest that dissemination in the urban residual water system of HI1A plasmids may result in an accelerated acquisition of antibiotic resistance genes among pathogens.
Hybridization plays an important and underappreciated role in shaping the evolutionary trajectories of species. Following the introduction of a non-native organism to a novel habitat, hybridization with a native congener may affect the probability of establishment of the introduced species. In most documented cases of hybridization between a native and a non-native species, a mosaic hybrid zone is formed, with hybridization occurring heterogeneously across the landscape. In contrast, most naturally occurring hybrid zones are clinal in structure. Here we report on a long-term microsatellite dataset that monitored hybridization between the invasive winter moth, Operophtera brumata (Lepidoptera: Geometridae), and the native Bruce spanworm, O. bruceata, over a 12-year period. Our results document one of the first examples of the real-time formation and geographic settling of a clinal hybrid zone. In addition, by comparing one transect in Massachusetts where extreme winter cold temperatures have been hypothesized to restrict the distribution of winter moth, and one in coastal Connecticut, where winter temperatures are moderated by Long Island Sound, we find that the location of the hybrid zone appears to be independent of environmental variables and maintained under a tension model wherein the stability of the hybrid zone is constrained by population density, reduced hybrid fitness, and low dispersal rates. Documenting the formation of a contemporary clinal hybrid zone may provide important insights into the factors that shaped other well-established hybrid zones.
Plant pathogens often adapt to plant genetic resistance so characterization of the architecture under-lying such an adaptation is required to understand the adaptive potential of pathogen populations. Erosion of banana quantitative resistance to a major leaf disease caused by polygenic adaptation of the causal agent, the fungus Pseudocercospora fijiensis, was recently identified in the northern Caribbean region. Genome scan and quantitative genetics approaches were combined to investigate the adaptive architecture underlying this adaptation. Thirty-two genomic regions showing host se-lection footprints were identified by pool sequencing of isolates collected from seven plantation pairs of two cultivars with different levels of quantitative resistance. Individual sequencing and phenotyping of isolates from one pair revealed significant and variable levels of correlation be-tween haplotypes in 17 of these regions with a quantitative trait of pathogenicity (the diseased leaf area). The multilocus pattern of haplotypes detected in the 17 regions was found to be highly varia-ble across all the population pairs studied. These results suggest complex adaptive architecture un-derlying plant pathogen adaptation to quantitative resistance with a polygenic basis, redundancy, and a low level of parallel evolution between pathogen populations. Candidate genes involved in quantitative pathogenicity and host adaptation of P. fijiensis were highlighted in genomic regions combining annotation analysis with available biological data.
Invertebrates are important for restoration processes as they are key drivers of many landscape-scale ecosystem functions, including pollination, nutrient cycling and soil formation. However, invertebrates are often overlooked in restoration monitoring because they are highly diverse, poorly described, and time-consuming to survey, and require increasingly scarce taxonomic expertise to enable identification. DNA metabarcoding is a relatively new tool for rapid survey that is able to address some of these concerns, and provide information about the taxa with which invertebrates are interacting via food webs and habitat. Here we evaluate how invertebrate communities may be used to determine ecosystem trajectories during restoration. We collected ground-dwelling and airborne invertebrates across chronosequences of mine-site restoration in three ecologically disparate locations in Western Australia and identified invertebrate and plant communities using DNA metabarcoding. Ground-dwelling invertebrates showed the clearest restoration signals, with communities becoming more similar to reference communities over time. These patterns were weaker in airborne invertebrates, which have higher dispersal abilities and therefore less local fidelity to environmental conditions. Although we detected directional changes in community composition indicative of invertebrate recovery, patterns observed were inconsistent between study locations. The inclusion of plant assays allowed identification of plant species, as well as potential food sources and habitat. We demonstrate that DNA metabarcoding of invertebrate communities can be used to evaluate restoration trajectories. Testing and incorporating new monitoring techniques such as DNA metabarcoding is critical to improving restoration outcomes.
The disjunct temperate rainforests of the Pacific Northwest of North America (PNW) are characterized by late-successional dominant tree species western redcedar (Thuja plicata) and western hemlock (Tsuga heterophylla). The demographics of these species, along with the PNW rainforest ecosystem in its entirety, have been heavily impacted by the geological and climatic changes the PNW has experienced over the last 5 million years, including mountain orogeny and repeated Pleistocene glaciations. These environmental events have ultimately shaped the history of these species, with inland segments potentially being extirpated during the Pleistocene glaciation. Here, we collect genomic data for both species across their ranges in order to develop multiple demographic models, each reflecting a different hypothesis on how the ecosystem dominant species may have responded to dramatic climatic change. Results indicate that inland and coastal populations in both species diverged an estimated ~2.5 million years ago and experienced a decrease in population size during glaciation, with a subsequent population expansion. Importantly, we found evidence for gene-flow between coastal and inland populations during the mid-Holocene. It is likely that intermittent migration in these species has prevented allopatric speciation. In conclusion, the combination of genomic data and population demographic inference procedures involving machine learning establish that populations of the ecosystem dominants Thuja plicata and Tsuga heterophylla persisted in refugia located in both the coastal and inland regions, with populations expanding and contracting in response to glacial cycles with occasional gene-flow.
Temperature and precipitation regimes are rapidly changing, resulting in forest dieback and local extinction events, particularly in Mediterranean-type climates. Strategic forest management approaches that enhance forests’ resilience to future climates are urgently required, however adaptation to climates in heterogeneous landscapes with multiple selection pressures may be complex. For widespread trees in Mediterranean-type climates we hypothesized that patterns of local adaptation are associated with climate; precipitation is a stronger factor of adaptation than temperature; functionally related genes show similar signatures of adaptation; and adaptive variants are independently sorting across the landscape. To test our hypotheses, we sampled 28 populations across the geographic and climatic distribution of Eucalyptus marginata (jarrah), in south-west Western Australia, and obtained 13,534 independent single nucleotide polymorphic (SNP) markers across the genome. While overall levels of population differentiation were low (FST=0.04), environmental association analyses found a total of 2,336 unique SNPs potentially associated with five climate variables of temperature and precipitation. Allelic turnover was identified for SNPs associated with temperate seasonality and mean precipitation of the warmest quarter (39.2% and 36.9% deviance explained, respectively), suggesting that both temperature and precipitation are important factors in adaptation. SNPs within similarly function genes, according to gene ontology enrichment analysis, had analogous allelic turnover along climate gradients, while SNPs among temperature and precipitation variables had orthogonal patterns of adaptation. These contrasting patterns of adaptation provide evidence that there may be standing genomic variation adapted to changing climates, providing the substrate needed to promote adaptive management strategies to bolster forest resilience in the future.
Evaluating the factors that promote invasive ant abundance is critical to assess their ecological impact and inform their management. Many invasive ant species show reduced nestmate recognition and an absence of boundaries between unrelated nests, which allow populations to achieve greater densities due to reduced intraspecific competition. We examined nestmate discrimination and colony boundaries in introduced populations of the red imported fire ant (Solenopsis invicta; hereafter, fire ant). Fire ants occur in two social forms: monogyne (colonies with a single egg-laying queen) and polygyne (colonies with multiple egg-laying queens). In contrast with monogyne nests, polygyne nests are thought to be interconnected due to the reduced antagonism between non-nestmate polygyne workers, perhaps because polygyne workers habituate the colony to an odor unique to Gp-9b-carrying adults. However, colony boundaries and nestmate discrimination are poorly documented, particularly for worker-brood interactions. To delimit boundaries between field colonies, we correlated the exchange of a 15N-glycine tracer dissolved in a sucrose solution with social form. We also evaluated nestmate discrimination between polygyne workers and larvae in the laboratory. Counter to our expectations, polygyne colonies behaved identically to monogyne colonies, suggesting both social forms maintain strict colony boundaries. Polygyne workers also preferentially fed larval nestmates and may have selectively cannibalized non-nestmates. The levels of relatedness among workers in polygyne colonies was higher than those previously reported in North America (mean ±SE: 0.269 ± 0.037). Our study highlights the importance of combining genetic analyses with direct quantification of resource exchange to better understand the factors influencing ant invasions.
Structural variations (SVs) have been associated with genetic diversity and adaptation in diverse taxa. Despite these observations, it is not yet clear what their relative importance is for microevolution, especially with respect to known drivers of diversity, e.g., nucleotide substitutions, in rapidly adapting species. Here we examine the significance of SVs in pesticide resistance evolution of the agricultural super-pest, the Colorado potato beetle, Leptinotarsa decemlineata. By employing a trio-binning procedure, we develop near chromosomal reference genomes to characterize structural variation within this species. These updated assemblies represent >100-fold improvement of contiguity and include derived pest and ancestral non-pest individuals. We identify >200,000 SVs, which appear to be non-randomly distributed across the genome as they co-occur with transposable elements. SVs intersect exons for genes associated with insecticide resistance, development, and transcription, most notably cytochrome P450 (CYP) genes. To understand the role that SVs might play in adaptation, we incorporate an additional 66 genomes among pest and non-pest populations of North America into the SV graph. Single nucleotide polymorphisms (SNPs) and SVs have a similar proportion in coding and non-coding regions of the genome, but there is a deficit of SNPs in SVs, suggesting SVs may be under selection. Using multiple lines of evidence, we identify 28 positively selected genes that include 337 SVs and 442 outlier SNPs. Among these, there are four associated with insecticide resistance. Two of these genes (CYP4g15 and glycosyltransferase-13) are physically linked by a structural variant and have previously been shown to be co-induced during insecticide exposure.
Host switching allows parasites to expand their niches. However, successful switching may require suites of adaptations and also may decrease performance on the old host. As a result, reductions in gene flow accompany many host switches, driving speciation. Because host switches tend to be rapid, it is difficult to study their demographic parameters in real-time. Fundamental factors that control subsequent parasite evolution, such as the size of the switching population or the extent of immigration from the original host, remain largely unknown. To shed light on the host switching process, we explored the history of independent switches by two ectoparasitic honey bee mites (Varroa destructor and V. jacobsoni). Both switched to the western honey bee (Apis mellifera) after it was brought into contact with their ancestral host (Apis cerana), ~70 and ~12 years ago, respectively. Varroa destructor subsequently caused worldwide collapses of honey bee populations. Using whole-genome sequencing on 63 mites collected in their native ranges from both the ancestral and novel hosts, we were able to reconstruct the known temporal dynamics of the switch. We further found multiple previously undiscovered mitochondrial lineages on the novel host, along with the genetic equivalent of tens of individuals that were involved in the initial host switch. Despite being greatly reduced, some gene flow remains between mites adapted to different hosts. Our findings suggest that while reproductive isolation may facilitate the fixation of traits beneficial for exploitation of the new host, ongoing genetic exchange may allow genetic amelioration of inbreeding effects.
Chromosomal inversions play a role in the adaptation and diversification of different systems, mainly due to supergenes resulting from recombination suppression. Supergenes are “clusters” of genes in linkage disequilibrium (LD) whose frequencies may be associated with environmental variables. The grasshopper “species complex” Trimerotropis pallidipennis is considered to have several genetic lineages distributed from North to South America in arid and semi-arid high-altitude environments. The southernmost lineage, Trimerotropis sp., bears 4 to 7 putative inversion polymorphisms with clinal variation, possibly allowing adaptation to temperate environments. We analyzed chromosomal, mitochondrial and genome-wide SNP markers in 19 Trimerotropis sp. populations mainly distributed along two altitudinal gradients (MS and Ju). We show that populations across Argentina are formed by two main chromosomally and genetically differentiated lineages: one distributed in the southernmost border of the “Andes Centrales”, adding evidence for a differentiation hotspot in this area; and the other widely distributed in Argentina. Within the latter, genomic architecture analysis revealed four clusters of loci in high LD that correspond to inversions, of which at least one is associated to a chromosomal rearrangement, confirming its status as “true inversion”. We demonstrated the stability of chromosome polymorphisms for more than 20 generations and the occurrence of non-neutral markers associated with inversions and environmental variables. Inversion clines could be the consequence of coupling between extrinsic postzygotic barriers, leading to a hybrid zone, and spatially varying selection along environmental gradients. These results provide a framework for future investigations about candidate genes implicated in the rapid adaptation to new environments.
Heterogeneous seascapes and strong environmental gradients in coastal waters are expected to influence adaptive divergence, particularly in species with large population sizes where selection is expected to be highly efficient. However, these influences might also extend to species characterized by strong social structure, natal philopatry and small home ranges. We implemented a seascape genomic study to test this hypothesis in Indo-Pacific bottlenose dolphins (Tursiops aduncus) distributed along the environmentally heterogeneous coast of southern Australia. The datasets included oceanographic and environmental variables thought to be good predictors of local adaptation in dolphins and 8,081 filtered single nucleotide polymorphisms (SNPs) genotyped for individuals sampled from six different bioregions. From a neutral perspective, population structure and connectivity of the dolphins were generally influenced by habitat type and social structuring. Genotype-environment association analysis identified 241 candidate adaptive loci and revealed that sea surface temperature and salinity gradients influenced adaptive divergence in these animals at both large- (1,000s km) and fine-scales (<100 km). Enrichment analysis and annotation of candidate genes revealed functions related to sodium-activated ion transport, kidney development, adipogenesis and thermogenesis. The findings of spatial adaptive divergence and inferences of putative physiological adaptations challenge previous suggestions that marine megafauna is most likely to be affected by environmental and climatic changes via indirect, trophic effects. Our work contributes to conservation management of coastal bottlenose dolphins subjected to anthropogenic disturbance and to efforts of clarifying how seascape heterogeneity influences adaptive diversity and evolution in small cetaceans.
Adaptation to derived habitats often occurs from standing genetic variation (SGV). The maintenance within ancestral populations of genetic variants favorable in derived habitats is commonly ascribed to long-term antagonism between purifying selection and gene flow resulting from hybridization across habitats. A largely unexplored alternative idea based on quantitative genetic models of polygenic adaptation is that variants favored in derived habitats are neutral in ancestral populations when their frequency is relatively low. To explore the latter, we first identify genetic variants important to the adaptation of threespine stickleback fish to a rare derived habitat – nutrient-depleted acidic lakes – based on whole-genome sequence data. Sequencing marine stickleback from six locations across the Atlantic ocean then allows us to infer that the frequency of these derived variants in the ancestral habitat is unrelated to the likely opportunity for gene flow of these variants from acidic-adapted populations. This result is consistent with the selective neutrality of derived variants within the ancestor. Our study thus supports an underappreciated explanation for the maintenance of SGV, and calls for a better understanding of the fitness consequences of adaptive genetic variation across habitats and genomic backgrounds.
Changes in land use and agricultural intensification threaten biodiversity and ecosystem functioning of small water bodies. We studied 67 kettle holes (KH) in an agricultural landscape in northeastern Germany using landscape-scale metatranscriptomics, to understand the responses of active communities across the three domains of life, Bacteria, Archaea, and eukaryotes, to land use. These KH are proxies of the millions of small standing water bodies of glacial origin spread across the northern hemisphere. Like other landscapes in Europe, the study area has been used for intensive agriculture since the 1950s. In contrast to a parallel eDNA study which revealed the homogenization of biodiversity across KH conceivably resulting from long-lasting intensive agriculture, land-use type affected the structure of the active KH communities during spring crop fertilization, but not a month later. This effect was more pronounced in eukaryotes than in bacteria. In contrast, gene expression patterns did not differ between months or across land-use type, suggesting a high degree of functional redundancy across the KH communities. Variability in gene expression was best explained by active community structure, suggesting that these changes in functioning are primarily driven by interactions between organisms. Our results show that influences of the surrounding landscape result in temporary changes in the activity of different community members. Thus, even in KH where biodiversity has been homogenized, communities continue to respond to land management. This needs to be considered when developing sustainable management options for restoration purposes and for successful mitigation of further biodiversity loss in agricultural landscapes.
Historic climate changes had always driven geographical populations of coastal plants to contract and recover dynamically, even die out completely. Species suffering from such bottlenecks usually lose intraspecific genetic diversity, but how do these events influence population subdivision patterns of coastal plants? We investigated this question in the typical coastal plant: mangrove species Aegiceras corniculatum. Inhabiting the intertidal zone of the tropical and subtropical coast of the Indo-West Pacific oceans, its populations are deemed to be greatly shaped by historic sea-level fluctuations. Using dual methods of Sanger and Illumina Solexa sequencing, we found that the 18 sampled populations were structured into two groups, namely, the “Indo-Malayan” group, comprising three subgroups (the northern South China Sea, Gulf of Bengal, and Bali), and the “Pan-Australasia” group, comprising the subgroups of the southern South China Sea and Australasia. Based on simulations using the approximate Bayesian computation method, we inferred that the southern South China Sea subgroup, which penetrates the interior of the “Indo-Malayan” group, originated from the Australasia subgroup, accompanied by a severe bottleneck event, with a spot of gene flow from both the Australasia and “Indo-Malayan” groups. Geographical barriers such as the Sundaland underlie the genetic break between Indian and Pacific Oceans, but the discontinuity between southern and northern South China Sea was originated from genetic drift in the bottleneck event. Hence, we revealed a case evidencing that the bottleneck event promoted population subdivision. This conclusion may be applicable in other taxa beyond coastal plants.
1. We investigated responses of tomato (Solanum lycopersicum) to belowground presence of two functional guilds of nematodes - plant parasite (Meloidogyne javanica) and entomopathogens (Heterorhabditis bacteriophora, Steinernema feltiae, and S. carpocapsae) - as well as a leaf mining insect (Tuta absoluta) aboveground. Our results indicate that entomopathogenic nematodes (EPNs): 1) induced plant defense responses, 2) reduced root knot nematode (RKN) infestation belowground and 3) reduced herbivore (T. absoluta) host preference and performance aboveground. 2. Concurrently, we investigated the plant signaling mechanisms underlying these interactions using biochemical and transcriptome analyses. We found that both entomopathogen and parasite triggered immune responses in plant roots with shared gene expression. Tomato plants responded similarly to presence of RKN or EPN in the rootzone, by rapidly activating polyphenol oxidase (PPO) and guaiacol peroxidase (GP) activity in roots, but simultaneously suppressed this activity in aboveground tissues. 3. We quantified changes in expression of candidate resistance genes in tomato that may play essential roles in defense response to RKN, which were also coincidentally triggered with EPN. For example, PR-14 expression was greater in plants inoculated with EPN than in plants co-inoculated with both nematode functional guilds. Overall, EPN inoculation directly mediated enhanced plant defense and reduced subsequent RKN infection. Likewise, EPNs may modulate plant defense against RKN invasion, in part, by suppressing active expression of antioxidant enzymes. 4. Inoculation of tomato roots with EPNs belowground reduced both host preference and performance of the aboveground herbivore, T. absoluta. Inoculations of roots with EPN also triggered an immune response in tomato via up-regulated phenylpropanoid metabolism and synthesis of protease inhibitors (PIs) in plant tissues, which could explain an observed decrease in egg laying and developmental performance exhibited by herbivores on EPN-inoculated plants. 5. Synthesis. Our results add to a growing body of evidence indicating that subterranean EPNs activate systemic acquired resistance (SAR) and/or induced systemic resistance (ISR) in plants with concomitant antagonistic effects on temporally co-occurring subterranean plant pathogenic nematodes and terrestrial herbivores.