In 1859, Charles Darwin proposed that species are not fundamentally different from subspecies or the varieties from which they evolve. A century later, Dobzhansky (1958) suggested that many such lineages are ephemeral and are likely to revert differentiation through introgression (Fig. 1A); only a few evolve complete reproductive isolation and persist in sympatry. In this issue of Molecular Ecology, Bouzid et al. (2021) show how new analytical methods, when applied to genome data, allow us to more precisely determine whether or not species formation follows the paths outlined by Darwin and Dobzhansky (Fig. 1B). The authors study the diversification of the lizard Sceloporus occidentalis, finding a continuum of genetic interactions between the preservation of genetic identity to genetic merger, analogous to what is exemplified by ring species. In doing so, they teach us two tales on species formation: that lineages are fractal byproducts of evolutionary processes such as genetic drift and selection, and that lineages are often ephemeral and do not always progress into species. Studying ephemeral lineages like those in S. occidentalis allows us to capture divergence at its earliest stages, and potentially to determine the factors that allow lineages to remain distinct despite pervasive gene flow. These lineages thus serve as a natural laboratory to address long standing hypotheses on species formation.
Understanding how eco-evolutionary processes and environmental factors drive population differentiation and adaptation are key challenges in evolutionary biology of relevance for biodiversity protection. Differentiation requires at least partial reproductive separation, which may result from different modes of isolation such as geographic isolation (allopatry) or isolation by distance (IBD), resistance (IBR), and environment (IBE). Despite that multiple modes might jointly influence differentiation, studies that compare the relative contributions are scarce. Using RADseq, we analyse neutral and adaptive genetic diversity and structure in 11 pike (Esox lucius) populations along a latitudinal gradient (54.9 - 63.6°N), to investigate the relative effects of IBD, IBE and IBR, and to assess whether the effects differ between neutral and adaptive variation, or across structural levels. Patterns of neutral and adaptive variation differed, likely reflecting that they have been differently affected by stochastic and deterministic processes. The importance of the different modes of isolation differed between neutral and adaptive diversity, yet were consistent across structural levels. Neutral variation was influenced by interactions among all three modes of isolation, with IBR (seascape features) playing a central role, wheares adaptive variation was mainly influenced by IBE (environmental conditions). Taken together, this and previous studies suggest that it is common that multiple modes of isolation interactively shape patterns of genetic variation, and that their relative contributions differ among systems. To enable identification of general patterns and understand how various factors influence the relative contributions, it is important that several modes are simultaneously investigated in additional populations, species and environmental settings.
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.
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.
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.
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.
We investigated responses of tomato to two functional guilds of nematodes - plant parasite (Meloidogyne javanica) and entomopathogens (Heterorhabditis bacteriophora, Steinernema feltiae belowground, 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. 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 root zone, by rapidly activating polyphenol oxidase (PPO) and guaiacol peroxidase (GP) activity in roots, but simultaneously suppressed this activity in aboveground tissues. We quantified changes in gene expression in tomato that may play essential roles in defense response to RKN, which were also coincidentally triggered by EPN. Overall, EPN inoculation directly mediated enhanced plant defense and reduced subsequent RKN infection. Likewise, we show that EPNs modulate plant defense against RKN invasion. 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 which could explain an observed decrease in egg laying and developmental performance exhibited by herbivores on EPN-inoculated plants. Our results support the hypothesis that subterranean EPNs activate a battery of plant defenses associated with systemic acquired resistance (SAR) and/or induced systemic resistance (ISR) with antagonistic effects on temporally co-occurring subterranean plant pathogenic nematodes a
The long-term persistence of a population which has suffered a bottleneck partly depends on how historical demographic dynamics impacted its genetic diversity and the accumulation of deleterious mutations. Here we provide genomic evidence for the detrimental genetic effect of a recent population bottleneck in the endangered black-faced spoonbill (Platalea minor) even after its rapid population recovery. Our population genomic data suggest that the bird’s effective population size, Ne, had been relatively stable (7,500-9,000) since the end of the last glacial maximum; however, a recent brief yet severe bottleneck (Ne= 20) around the 1940s wiped out more than 99% of its historical Ne in roughly three generations. By comparing it with its sister species, the royal spoonbill (P. regia) whose conservation status is of lesser concern, we found that despite a more than 15-fold population recovery since 1988, genetic drift has led to higher levels of inbreeding (7.4 times more runs of homozygosity longer than 100 Kb) in the black-faced spoonbill than in the royal spoonbill genome. Although the two spoonbills have similar levels of genome-wide nucleotide diversity and heterozygosity, because of relaxed purifying selection, individual black-faced spoonbills carry 3% more nonsynonymous substitutions than royal spoonbills each of which is 7% more deleterious. Our results imply that the persistence of a threatened species cannot be inferred from a recovery in its population. They also highlight the necessity of continually using genomic indices to monitor its genetic health and employing all possible measures to assure its long-term persistence in the ever-changing environment.
Present-day ecology and population structure are the legacies of past climate and habitat perturbations, and this is particularly true for species that are widely distributed at high latitudes. The red knot, Calidris canutus, is an arctic-breeding, long-distance migratory shorebird with six recognized subspecies defined by differences in morphology, migration behavior, and annual-cycle phenology, in a global distribution thought to have arisen just since the Last Glacial Maximum (LGM). We used nextRAD sequencing of 10,881 single-nucleotide polymorphisms (SNPs) to assess the neutral genetic structure and phylogeographic history of 172 red knots representing all known global breeding populations. Using population genetics approaches, including model-based scenario-testing in an approximate Bayesian computation (ABC) framework, we infer that red knots derive from two main lineages that diverged ca. 34,000 years ago, and thus persisted at the LGM in both Palearctic and Nearctic refugia, followed by at least two instances of secondary contact and admixture. In two flyways, we detected clear genetic structure between population pairs with similar migrations and substantial geographic overlap in the non-breeding season. Conversely, other populations were only weakly differentiated despite clearly divergent migratory phenotypes and little or no apparent contact throughout the annual cycle. In general, the magnitude of genetic differentiation did not match that of phenotypic differences among populations, suggesting that flyway-specific phenotypes developed quite rapidly and do not necessarily impose barriers to gene flow. Our results suggest that population structure and migratory phenotypes in red knots arose from a complex interplay among phylogeography, plasticity, and selective processes.