Although the process of species formation is notoriously idiosyncratic, the observation of pervasive patterns of reproductive isolation across species pairs suggests that generalities, or “rules”, underlie species formation in all animals. Haldane’s rule states that whenever a sex is absent, rare or sterile in a cross between two taxa, that sex is usually the heterogametic sex. Yet, understanding how Haldane’s rule first evolves and whether it is associated to genome wide barriers to gene flow remains a challenging task because this rule is usually studied in highly divergent taxa that no longer hybridize in nature. Here, we address these questions using the meadow grasshopper Pseudochorthippus parallelus where populations that readily hybridize in two natural hybrid zones show hybrid male sterility in laboratorial crosses. Using mitochondrial data, we infer that such populations have diverged some 100,000 years ago, surviving multiple glacial periods in isolated Pleistocenic refugia. Nuclear data shows that secondary contact has led to extensive introgression throughout the species range, including between populations showing hybrid male sterility. We find repeatable patterns of genomic differentiation across the two hybrid zones, yet such patterns are consistent with shared genomic constraints across taxa rather than their role in reproductive isolation. Together, our results suggest that Haldane’s rule can evolve relatively quickly within species, particularly when associated to strong demographic changes. At such early stages of species formation, hybrid male sterility still permits extensive gene flow, allowing future studies to identify genomic regions associated with reproductive barriers.
Animal pollinators mediate gene flow among plant populations, but, in contrast to well-studied topographic and (Pleistocene) environmental isolating barriers, their impact on population genetic differentiation remains largely unexplored. Comparatively investigating how these multifarious factors drive microevolutionary histories is, however, crucial for better resolving macroevolutionary patterns of plant diversification. We here combined genomic analyses with landscape genetics and niche modelling across six related Neotropical plant species (424 individuals across 33 localities) differing in pollination strategy to test the hypothesis that highly mobile (vertebrate) pollinators more effectively link isolated localities than less mobile (bee) pollinators. We found consistently higher genetic differentiation (FST) among localities of bee- than vertebrate-pollinated species with increasing geographic distance, topographic barriers and historic climatic instability. High admixture among montane populations further suggested relative climatic stability of Neotropical montane forests during the Pleistocene. Overall, our results indicate that pollinators may differentially impact the potential for allopatric speciation, thereby critically influencing diversification histories at macroevolutionary scales.
Bacteria in the human gut contend with numerous fluctuating environmental variables, including bouts of extreme selective agents like antibiotics. Theory predicts that oscillations in the adaptive landscape can impose balancing selection on bacterial populations, leaving characteristic signatures in the sequence variation of functionally significant genomic loci. Despite their potential importance for gut bacterial adaptation, the metagenomic targets of balancing selection have not been identified. Here, I present population genetic evidence that balancing selection maintains allelic diversity in multidrug efflux pumps of multiple predominant bacterial species in the human gut metagenome. Metagenome wide scans of 566,958 core open reading frames (CORFs) from 287 bacterial species represented by 118,617 metagenome assembled genomes (MAGs) indicated that most CORFs have been conserved by purifying selection. However, dozens of CORFs displayed positive Tajima’s D values that deviated significantly from their species’ genomic backgrounds, indicating the action of balancing selection. The AcrB subunit of a multidrug efflux pump (MEP) in Bacteroides dorei displayed the highest Tajima’s D of any CORF, and AcrB and other MEPs from a diversity of bacterial species were significantly enriched among the CORFs with the highest Tajima’s D values. Crystal structures indicated that the regions under balancing selection bind tetracycline and macrolide antibiotics. Other proteins identified as targets of balancing selection included synthases, hydrolases, and ion transporters. Intriguingly, bacterial species experiencing balancing selection were the most abundant in the human gut based on metagenomic data, further suggesting fitness benefits of the allelic variation identified.
Rivers provide excellent models to understand how species diversity is generated and maintained across heterogeneous habitats. The lower Congo River (LCR) consists of a dynamic hydroscape exhibiting extraordinary aquatic biodiversity, endemicity, and ecological specialization. Previous studies have suggested that the numerous high-energy rapids throughout the LCR form physical barriers to gene flow, thus facilitating diversification and speciation, and generating ichthyofaunal diversity. However, this hypothesis has not been fully explored using genome-wide SNPs for fish species distributed across the LCR. In this study, we examined four species of lamprologine cichlids endemic to the LCR, of which three are sequentially distributed along the LCR without range overlap. Using genome-wide SNP data, we tested the hypotheses that high-energy rapids serve as physical barriers to gene flow that generate genetic divergence at inter- and intraspecific levels, and that gene flow occurs primarily in a downstream direction. Our results are consistent with the prediction that the rapids sometimes serve to reduce gene flow, but also suggest that at certain temporal and spatial scales, they may also act as promoters of gene flow. Furthermore, we detected both upstream and downstream gene flow between some populations of Lamprologus tigripictilis as well as hybridization between congeneric species. These results suggest that powerful high-energy rapids may therefore provide occasional multidirectional dispersal opportunities for riverine cichlid fishes, highlighting the complexity of factors driving evolutionary processes in the LCR.
DNA metabarcoding has been widely used to access and monitor species. However, several challenges remain open for its mainstream application in ecological studies, particularly when dealing with a quantitative approach. In a from the Cover article in this issue of Molecular Ecology, Cédric et al. (2021) report species-level ichthyoplankton dynamics for 97 fish species from two Amazon river basins using a clever quantitative metabarcoding approach employing a probe capture method. They clearly show that most species spawned during the rainy season when the floods started, but interestingly, species from the same genus reproduced in distinct periods (i.e., inverse phenology). Opportunistically, Cédric et al. (2021) reported that during an intense hydrological anomaly, several species had a sharp reduction in spawning activity, demonstrating a quick response to environmental cues. This is an interesting result since the speed at which fish species can react to environmental changes, during the spawning period, is largely unknown. Thus, this study brings remarkable insights into basic life history information that is imperative for proposing strategies that could lead to a realistic framework for sustainable fisheries management practices and conservation, fundamental for an under-studied and threatened realm, such as the Amazon River basin.
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.
The paradox of how invasive species cope with novel selective pressures with limited genetic variation is a fundamental question in molecular ecology. Several mechanisms have been proposed, but they can lack generality and predictive power. Here, we introduce an alternative mechanism, genetic redundancy, wherein changes in multiple combinations of loci can achieve a fitness optimum for polygenic traits, and thus the variations left after the founder effect may be sufficient for adaptation. We tested the potential importance of genetic redundancy in environmental adaptation of Colorado potato beetle (CPB) in introduced Eurasia. Population genomic analyses showed substantial genetic depletion following a single introduction event, which supports invasive CPB as a classic system for the paradox study. Genome-environment association analyses revealed a suite of loci and gene functions plausibly related to cold stress. Notably, a substantial portion of loci showed different contributions to similar or identical environments. Such non-parallel evolution indicates their potential redundancy to overall fitness. Furthermore, one important adaptive gene function, “phospholipid production”, was represented by more than one independent linkage cluster, suggesting some gene functional redundancy in cold resistance. Taken together, these results support the hypothesis that genetic redundancy can promote the adaptability of polygenic traits despite strong genetic depletion, thus providing a general mechanism for resolving the genetic paradox of invasion. More broadly, genetic redundancy, as an inherent feature of the genome, may have contributed to the evolutionary success of invasive species in many aspects.
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.
Extreme environments are inhospitable to the majority of species, but some organisms are able to survive in such hostile conditions due to evolutionary adaptations. For example, modern bony fishes have colonized various aquatic environments, including perpetually dark, hypoxic, hypersaline and toxic habitats. Eurasian perch (Perca fluviatilis) is among the few fish species of northern latitudes that is able to live in extremely acidic humic lakes. Such lakes represent almost “nocturnal” environments; they contain high levels of dissolved organic matter, which in addition to creating a challenging visual environment, also affects a large number of other habitat parameters and biotic interactions. To reveal the genomic targets of humic-associated selection, we performed whole-genome sequencing of perch originating from 16 humic and 16 clear-water lakes in northern Europe. We identified over 800,000 SNPs, of which >10,000 were identified as potential candidates under selection (associated with >3,000 genes) using multiple outlier approaches. Our findings suggest that adaptation to the humic environment involves hundreds of regions scattered across the genome. Putative signals of adaptation were detected in genes and gene families with diverse functions, including organism development and ion transportation. The observed excess of variants under selection in regulatory regions highlights the importance of adaptive evolution via regulatory elements, rather than via protein sequence modification. Our study demonstrates the power of whole-genome analysis to illuminate multifaceted nature of humic adaptation and highlights the next challenge moving from high-throughput outlier identification towards functional validation of causal mutations underlying phenotypic traits of ecological and evolutionary importance.
Human-associated microorganisms are ideal models to study the impact of environmental changes on species evolution and adaptation. The yeast Brettanomyces bruxellensis is a good example of organism facing anthropogenic-driven selective pressures. It is associated with fermentation processes in which it can be considered either as a spoiler (e.g. winemaking, bioethanol production) or as a beneficial microorganism (e.g. production of specific beers, kombucha). Besides its industrial interests, noteworthy parallels and dichotomies with Saccharomyces cerevisiae propelled B. bruxellensis as a valuable complementary yeast model. In this review, we emphasize that the broad genetic and phenotypic diversity of this species is only beginning to be revealed. Population genomic studies have revealed the co-existence of auto- and allotriploidization events with different evolutionary outcomes. The various diploid, autotriploid and allotriploid subpopulations are associated with specific fermented processes, suggesting independent adaptation phenomena to anthropized environments. Phenotypically, B. bruxellensis is renowned for its ability to metabolize a wide variety of carbon and nitrogen sources, which may explain its ability to colonize already fermented environments showing low-nutrient contents. Several traits of interest could be related to adaptation to human activities (e.g. nitrate metabolization in bioethanol production, resistance to sulphite treatments in winemaking). However, phenotypic traits are insufficiently studied in view of the great genomic diversity of the species. Future work will have to take into account strains of varied substrates, geographical origins as well as displaying different ploidy levels. Finally, we discuss the characteristics of B. bruxellensis which may prove to be of wider interest in future research.
The development of high-throughput sequencing (HTS) technologies has greatly improved our capacity to identify fungi and unveil their ecological roles across a variety of ecosystems. Here we provide an overview about current best practices in metabarcoding analysis of fungal communities, from experimental design through molecular and computational analyses. By re-analysing published datasets, we find that operational taxonomic units (OTUs) outperform amplified sequence variants (ASVs) in recovering fungal diversity, which is particularly evident for long markers. Additionally, analysis of the full-length ITS region allows more accurate taxonomic placement of fungi and other eukaryotes compared with the ITS2 subregion. We conclude that metabarcoding analyses of fungi are especially promising for co-analyses with the functional metagenomic or transcriptomic data, integrating fungi in the entire microbiome, recovery of novel fungal lineages and ancient organisms as well as barcoding of old specimens including type material.
Colonization of a novel environment by a few individuals can lead to rapid evolutionary change, yet evidence of the relative contributions of neutral and selective factors in promoting divergence during the early stages of colonization remain scarce. We explore the role of neutral and selective forces in the divergence of a unique urban population of the dark-eyed junco (Junco hyemalis), which became established on the campus of the University of California at San Diego (UCSD) in the early 1980s. Previous studies based on microsatellite loci documented significant genetic differentiation of the urban population as well as divergence in phenotypic traits relative to nearby montane populations, yet the geographic origin of the colonization and the factors involved remained uncertain. Our genome-wide SNP dataset confirmed the marked genetic differentiation of the UCSD population, and we identified the coastal subspecies pinosus from central California as its sister group instead of the neighboring mountain population. Demographic inference recovered a separation from pinosus as recent as 20 to 32 generations ago after a strong bottleneck, suggesting a role for drift in genetic differentiation. However, we also found significant associations between habitat variables and genome-wide variants linked to functional genes, some of which have been reported as potentially adaptive in birds inhabiting modified environments. These results suggest that the interplay between founder events and selection may result in rapid shifts in neutral and adaptive loci across the genome, and reveal the UCSD junco population as a case of contemporary evolutionary divergence in an anthropogenic environment.
While adaptation is commonly thought to result from selection on DNA sequence-based variation, recent studies have highlighted an analogous epigenetic component as well. However, the extent to which these adaptive mechanisms to adaptation to environmental heterogeneity are redundant or complementary remains unclear. To address the underlying genetic and epigenetic mechanisms and their relationship underlying environmental adaptation, we screened the genomes and epigenomes of nine global populations of a predominately sessile marine invasive tunicate, Botryllus schlosseri. We detected clear population genetic and epigenetic differentiation, which were both significantly influenced by local environments, and the minimum annual sea surface temperature (T_min) was simultaneously identified as the top explanatory variable for both types of variation. However, there remain some degree of difference in population structure patterns between two levels, suggesting a certain level of autonomy in epigenetic variation. From the functional perspective, a set of functional genes and biological pathways were shared between two levels, indicating a conjoint contribution of genetic and epigenetic variation to environmental adaptation. Moreover, we also detected genetic- or epigenetic-specific genes/pathways in relation to a wide variety of core processes potentially underlying adaptation to local environmental factors, suggesting the partly independent relationship between two mechanisms. We infer that complementary genetic and epigenetic routes to adaptation are available in this system. Collectively, these mechanisms may facilitate population persistence under environmental changes and sustain successful invasions in novel but contrasting environments.
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: email@example.com*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.