Rapid Adaptation and Interspecific Introgression in the North American Crop Pest Helicoverpa zea.

Insect crop pests threaten global food security. This threat is amplified through the spread of nonnative species and through adaptation of native pests to control measures. Adaptations such as pesticide resistance can result from selection on variation within a population, or through gene flow from another population. We investigate these processes in an economically important noctuid crop pest, Helicoverpa zea, which has evolved resistance to a wide range of pesticides. Its sister species Helicoverpa armigera, first detected as an invasive species in Brazil in 2013, introduced the pyrethroid-resistance gene CYP337B3 to South American H. zea via adaptive introgression. To understand whether this could contribute to pesticide resistance in North America, we sequenced 237 H. zea genomes across 10 sample sites. We report H. armigera introgression into the North American H. zea population. Two individuals sampled in Texas in 2019 carry H. armigera haplotypes in a 4 Mbp region containing CYP337B3. Next, we identify signatures of selection in the panmictic population of nonadmixed H. zea, identifying a selective sweep at a second cytochrome P450 gene: CYP333B3. We estimate that its derived allele conferred a ∼5% fitness advantage and show that this estimate explains independently observed rare nonsynonymous CYP333B3 mutations approaching fixation over a ∼20-year period. We also detect putative signatures of selection at a kinesin gene associated with Bt resistance. Overall, we document two mechanisms of rapid adaptation: the introduction of fitness-enhancing alleles through interspecific introgression, and selection on intraspecific variation.

Non-Poissonian Bursts in the Arrival of Phenotypic Variation Can Strongly Affect the Dynamics of Adaptation.

Modeling the rate at which adaptive phenotypes appear in a population is a key to predicting evolutionary processes. Given random mutations, should this rate be modeled by a simple Poisson process, or is a more complex dynamics needed? Here we use analytic calculations and simulations of evolving populations on explicit genotype-phenotype maps to show that the introduction of novel phenotypes can be "bursty" or overdispersed. In other words, a novel phenotype either appears multiple times in quick succession or not at all for many generations. These bursts are fundamentally caused by statistical fluctuations and other structure in the map from genotypes to phenotypes. Their strength depends on population parameters, being highest for "monomorphic" populations with low mutation rates. They can also be enhanced by additional inhomogeneities in the mapping from genotypes to phenotypes. We mainly investigate the effect of bursts using the well-studied genotype-phenotype map for RNA secondary structure, but find similar behavior in a lattice protein model and in Richard Dawkins's biomorphs model of morphological development. Bursts can profoundly affect adaptive dynamics. Most notably, they imply that fitness differences play a smaller role in determining which phenotype fixes than would be the case for a Poisson process without bursts.

Skin colour: A window into human phenotypic evolution and environmental adaptation.

As modern humans ventured out of Africa and dispersed around the world, they faced novel environmental challenges that led to geographic adaptations including skin colour. Over the long history of human evolution, skin colour has changed dramatically, showing tremendous diversity across different geographical regions, for example, the majority of individuals from the expansive lands of Africa have darker skin, whereas the majority of people from Eurasia exhibit lighter skin. What adaptations did lighter skin confer upon modern humans as they migrated from Africa to Eurasia? What genetic mechanisms underlie the diversity of skin colour observed in different populations? In recent years, scientists have gradually gained a deeper understanding of the interactions between pigmentation gene and skin colour through population-based genomic studies of different groups around the world, particularly in East Asia and Africa. In this review, we summarize our current understanding of 26 skin colour-related pigmentation genes and 48 SNPs that influence skin colour. Important pigmentation genes across three major populations are described in detail: MFSD12, SLC24A5, PDPK1 and DDB1/CYB561A3/TMEM138 influence skin colour in African populations; OCA2, KITLG, SLC24A2, GNPAT and PAH are key to the evolution of skin pigmentation in East Asian populations; and SLC24A5, SLC45A2, TYR, TYRP1, ASIP, MC1R and IRF4 significantly contribute to the lightening of skin colour in European populations. We summarized recent findings in genomic studies of skin colour in populations that implicate diverse geographic environments, local adaptation among populations, gene flow and multi-gene interactions as factors influencing skin colour diversity.

Epistasis, core-genome disharmony, and adaptation in recombining bacteria.

Recombination of short DNA fragments via horizontal gene transfer (HGT) can introduce beneficial alleles, create genomic disharmony through negative epistasis, and create adaptive gene combinations through positive epistasis. For non-core (accessory) genes, the negative epistatic cost is likely to be minimal because the incoming genes have not co-evolved with the recipient genome and are frequently observed as tightly linked cassettes with major effects. By contrast, interspecific recombination in the core genome is expected to be rare because disruptive allelic replacement is likely to introduce negative epistasis. Why then is homologous recombination common in the core of bacterial genomes? To understand this enigma, we take advantage of an exceptional model system, the common enteric pathogens Campylobacter jejuni and C. coli that are known for very high magnitude interspecies gene flow in the core genome. As expected, HGT does indeed disrupt co-adapted allele pairings, indirect evidence of negative epistasis. However, multiple HGT events enable recovery of the genome's co-adaption between introgressing alleles, even in core metabolism genes (e.g., formate dehydrogenase). These findings demonstrate that, even for complex traits, genetic coalitions can be decoupled, transferred, and independently reinstated in a new genetic background-facilitating transition between fitness peaks. In this example, the two-step recombinational process is associated with C. coli that are adapted to the agricultural niche.IMPORTANCEGenetic exchange among bacteria shapes the microbial world. From the acquisition of antimicrobial resistance genes to fundamental questions about the nature of bacterial species, this powerful evolutionary force has preoccupied scientists for decades. However, the mixing of genes between species rests on a paradox: 0n one hand, promoting adaptation by conferring novel functionality; on the other, potentially introducing disharmonious gene combinations (negative epistasis) that will be selected against. Taking an interdisciplinary approach to analyze natural populations of the enteric bacteria Campylobacter, an ideal example of long-range admixture, we demonstrate that genes can independently transfer across species boundaries and rejoin in functional networks in a recipient genome. The positive impact of two-gene interactions appears to be adaptive by expanding metabolic capacity and facilitating niche shifts through interspecific hybridization. This challenges conventional ideas and highlights the possibility of multiple-step evolution of multi-gene traits by interspecific introgression.

Convergence in carnivorous pitcher plants reveals a mechanism for composite trait evolution.

Composite traits involve multiple components that, only when combined, gain a new synergistic function. Thus, how they evolve remains a puzzle. We combined field experiments, microscopy, chemical analyses, and laser Doppler vibrometry with comparative phylogenetic analyses to show that two carnivorous Nepenthes pitcher plant species independently evolved similar adaptations in three distinct traits to acquire a new, composite trapping mechanism. Comparative analyses suggest that this new trait arose convergently through "spontaneous coincidence" of the required trait combination, rather than directional selection in the component traits. Our results indicate a plausible mechanism for composite trait evolution and highlight the importance of stochastic phenotypic variation as a facilitator of evolutionary novelty.

The evolutionary dynamics of local adaptations under genetic rescue is determined by mutational load and polygenicity.

Inbred populations often suffer from increased mutational load and reduced fitness due to lower efficacy of purifying selection in groups with small effective population sizes. Genetic rescue (GR) is a conservation tool that is studied and deployed with the aim of increasing the fitness of such inbred populations by assisted migration of individuals from closely related outbred populations. The success of GR depends on several factors-such as their demographic history and distribution of dominance effects of mutations-that may vary across populations. While we understand the impact of these factors on the dynamics of GR, their impact on local adaptations remains unclear. To this end, we conduct a population genetics simulation study to evaluate the impact of trait complexity (Mendelian vs. polygenic), dominance effects, and demographic history on the efficacy of GR. We find that the impact on local adaptations depends highly on the mutational load at the time of GR, which is in turn shaped dynamically by interactions between demographic history and dominance effects of deleterious variation. Over time local adaptations are generally restored post-GR, though in the short term they are often compromised in the process of purging deleterious variation. We also show that while local adaptations are almost always fully restored, the degree to which ancestral genetic variation affecting the trait is replaced by donor variation can vary drastically and is especially high for complex traits. Our results provide insights on the impact of GR on trait evolution and considerations for the practical implementation of GR.

Ancient DNA genomics and the renaissance of herbaria.

Herbaria are undergoing a renaissance as valuable sources of genomic data for exploring plant evolution, ecology, and diversity. Ancient DNA retrieved from herbarium specimens can provide unprecedented glimpses into past plant communities, their interactions with biotic and abiotic factors, and the genetic changes that have occurred over time. Here, we highlight recent advances in the field of herbarium genomics and discuss the challenges and opportunities of combining data from modern and time-stamped historical specimens. We also describe how integrating herbarium genomics data with other data types can yield substantial insights into the evolutionary and ecological processes that shape plant communities. Herbarium genomic analysis is a tool for understanding plant life and informing conservation efforts in the face of dire environmental challenges.

Frequent, infinitesimal bottlenecks maximize the rate of microbial adaptation.

Serial passaging is a fundamental technique in experimental evolution. The choice of bottleneck severity and frequency poses a dilemma: longer growth periods allow beneficial mutants to arise and grow over more generations, but simultaneously necessitate more severe bottlenecks with a higher risk of those same mutations being lost. Short growth periods require less severe bottlenecks, but come at the cost of less time between transfers for beneficial mutations to establish. The standard laboratory protocol of 24-h growth cycles with severe bottlenecking has logistical advantages for the experimenter but limited theoretical justification. Here we demonstrate that contrary to standard practice, the rate of adaptive evolution is maximized when bottlenecks are frequent and small, indeed infinitesimally so in the limit of continuous culture. This result derives from revising key assumptions underpinning previous theoretical work, notably changing the metric of optimization from adaptation per serial transfer to per experiment runtime. We also show that adding resource constraints and clonal interference to the model leaves the qualitative results unchanged. Implementing these findings will require liquid-handling robots to perform frequent bottlenecks, or chemostats for continuous culture. Further innovation in and adoption of these technologies has the potential to accelerate the rate of discovery in experimental evolution.

Transposable Elements: Epigenetic Silencing Mechanisms or Modulating Tools for Vertebrate Adaptations? Two Sides of the Same Coin.

Transposable elements constitute one of the main components of eukaryotic genomes. In vertebrates, they differ in content, typology, and family diversity and played a crucial role in the evolution of this taxon. However, due to their transposition ability, TEs can be responsible for genome instability, and thus silencing mechanisms were evolved to allow the coexistence between TEs and eukaryotic host-coding genes. Several papers are highlighting in TEs the presence of regulatory elements involved in regulating nearby genes in a tissue-specific fashion. This suggests that TEs are not sequences merely to silence; rather, they can be domesticated for the regulation of host-coding gene expression, permitting species adaptation and resilience as well as ensuring human health. This review presents the main silencing mechanisms acting in vertebrates and the importance of exploiting these mechanisms for TE control to rewire gene expression networks, challenging the general view of TEs as threatening elements.

North African fox genomes show signatures of repeated introgression and adaptation to life in deserts.

Elucidating the evolutionary process of animal adaptation to deserts is key to understanding adaptive responses to climate change. Here we generated 82 individual whole genomes of four fox species (genus Vulpes) inhabiting the Sahara Desert at different evolutionary times. We show that adaptation of new colonizing species to a hot arid environment has probably been facilitated by introgression and trans-species polymorphisms shared with older desert resident species, including a putatively adaptive 25 Mb genomic region. Scans for signatures of selection implicated genes affecting temperature perception, non-renal water loss and heat production in the recent adaptation of North African red foxes (Vulpes vulpes), after divergence from Eurasian populations approximately 78 thousand years ago. In the extreme desert specialists, Rueppell's fox (V. rueppellii) and fennec (V. zerda), we identified repeated signatures of selection in genes affecting renal water homeostasis supported by gene expression and physiological differences. Our study provides insights into the mechanisms and genetic underpinnings of a natural experiment of repeated adaptation to extreme conditions.

Marked inter-strain heterogeneity in the differential expression of some key stress response and virulence-related genes between planktonic and biofilm cells in Listeria monocytogenes.

Listeria monocytogenes is a facultatively intracellular pathogenic bacterium that can provoke invasive listeriosis, a severe foodborne infection in humans. Outside the host, this is capable to survive for long periods in soil, and water, as well as on plants, while, like many other microorganisms, this can also attach to abiotic surfaces, such as food contact ones, forming biofilms on them. It has been suggested that inside those sessile communities, L. monocytogenes cells not only display an increased stress tolerance but may also boost their pathogenicity. In this work, the expression of ten key stress response and/or virulence-related genes (i.e., groEL, hly, iap, inlA, inlB, lisK, mdrD, mdrL, prfA, and sigB) was studied in three different L. monocytogenes strains (AAL20066, AAL20107, and PL24), all isolated from foods and each belonging to a different listeriosis-associated serovar (1/2a, 1/2b, and 1/2c, respectively). For this, each strain was initially left to develop a mature biofilm on a model polystyrene surface (Petri dish) by incubating for 144 h (6 days) at 20 °C in tryptone soya broth (with medium renewal every 48 h). Following incubation, both biofilm and the surrounding free-swimming (planktonic) cells were recovered, and their gene expressions were comparatively evaluated through targeted reverse transcription-quantitative polymerase chain reactions (RT-qPCR). Results revealed a strain-dependent differential gene expression between the two cell types. Thus, for instance, in strain AAL20107 (ser. 1/2b) biofilm growth worryingly resulted in a significant overexpression of all the studied genes (P < 0.05), whereas in strain PL24 (ser. 1/2c), the expression of most genes (8/10) did not change upon biofilm growth, with only two of them (groEL and hly) being again significantly upregulated. Such transcriptomic strain variability in stress adaptation and/or virulence induction should be generally considered in the physiological studies of pathogenic biofilms and preferably upon designing and implementing novel and more efficient eradication methods.

Selection signatures for local and regional adaptation in Chinese Mongolian horse breeds reveal candidate genes for hoof health.

BACKGROUND: Thousands of years of natural and artificial selection since the domestication of the horse has shaped the distinctive genomes of Chinese Mongolian horse populations. Consequently, genomic signatures of selection can provide insights into the human-mediated selection history of specific traits and evolutionary adaptation to diverse environments. Here, we used genome-wide SNPs from five distinct Chinese Mongolian horse populations to identify genomic regions under selection for the population-specific traits, gait, black coat colour, and hoof quality. Other global breeds were used to identify regional-specific signatures of selection. RESULTS: We first identified the most significant selection peak for the Wushen horse in the region on ECA23 harbouring DMRT3, the major gene for gait. We detected selection signatures encompassing several genes in the Baicha Iron Hoof horse that represent good biological candidates for hoof health, including the CSPG4, PEAK1, EXPH5, WWP2 and HAS3 genes. In addition, an analysis of regional subgroups (Asian compared to European) identified a single locus on ECA3 containing the ZFPM1 gene that is a marker of selection for the major domestication event leading to the DOM2 horse clade. CONCLUSIONS: Genomic variation at these loci in the Baicha Iron Hoof may be leveraged in other horse populations to identify animals with superior hoof health or those at risk of hoof-related pathologies. The overlap between the selection signature in Asian horses with the DOM2 selection peak raises questions about the nature of horse domestication events, which may have involved a prehistoric clade other than DOM2 that has not yet been identified.

Introgression from extinct species facilitates adaptation to its vacated niche.

Anthropogenic disturbances of ecosystems are causing a loss of biodiversity at an unprecedented rate. Species extinctions often leave ecological niches underutilized, and their colonization by other species may require new adaptation. In Lake Constance, on the borders of Germany, Austria and Switzerland, an endemic profundal whitefish species went extinct during a period of anthropogenic eutrophication. In the process of extinction, the deep-water species hybridized with three surviving whitefish species of Lake Constance, resulting in introgression of genetic variation that is potentially adaptive in deep-water habitats. Here, we sampled a water depth gradient across a known spawning ground of one of these surviving species, Coregonus macrophthalmus, and caught spawning individuals at greater depths (down to 90 m) than historically recorded. We sequenced a total of 96 whole genomes, 11-17 for each of six different spawning depth populations (4, 12, 20, 40, 60 and 90 m), to document genomic intraspecific differentiation along a water depth gradient. We identified 52 genomic regions that are potentially under divergent selection between the deepest (90 m) and all shallower (4-60 m) spawning habitats. At 12 (23.1%) of these 52 loci, the allele frequency pattern across historical and contemporary populations suggests that introgression from the extinct species potentially facilitates ongoing adaptation to deep water. Our results are consistent with the syngameon hypothesis, proposing that hybridization between members of an adaptive radiation can promote further niche expansion and diversification. Furthermore, our findings demonstrate that introgression from extinct into extant species can be a source of evolvability, enabling rapid adaptation to environmental change, and may contribute to the ecological recovery of ecosystem functions after extinctions.

Out of Asia? Expansion of Eurasian Lyme borreliosis causing genospecies display unique evolutionary trajectories.

Vector-borne pathogens exist in obligate transmission cycles between vector and reservoir host species. Host and vector shifts can lead to geographic expansion of infectious agents and the emergence of new diseases in susceptible individuals. Three bacterial genospecies (Borrelia afzelii, Borrelia bavariensis, and Borrelia garinii) predominantly utilize two distinct tick species as vectors in Asia (Ixodes persulcatus) and Europe (Ixodes ricinus). Through these vectors, the bacteria can infect various vertebrate groups (e.g., rodents, birds) including humans where they cause Lyme borreliosis, the most common vector-borne disease in the Northern hemisphere. Yet, how and in which order the three Borrelia genospecies colonized each continent remains unclear including the evolutionary consequences of this geographic expansion. Here, by reconstructing the evolutionary history of 142 Eurasian isolates, we found evidence that the ancestors of each of the three genospecies probably have an Asian origin. Even so, each genospecies studied displayed a unique substructuring and evolutionary response to the colonization of Europe. The pattern of allele sharing between continents is consistent with the dispersal rate of the respective vertebrate hosts, supporting the concept that adaptation of Borrelia genospecies to the host is important for pathogen dispersal. Our results highlight that Eurasian Lyme borreliosis agents are all capable of geographic expansion with host association influencing their dispersal; further displaying the importance of host and vector association to the geographic expansion of vector-borne pathogens and potentially conditioning their capacity as emergent pathogens.

Functional genomics analysis reveals the evolutionary adaptation and demographic history of pygmy lorises.

Lorises are a group of globally threatened strepsirrhine primates that exhibit many unusual physiological and behavioral features, including a low metabolic rate, slow movement, and hibernation. Here, we assembled a chromosome-level genome sequence of the pygmy loris (Xanthonycticebus pygmaeus) and resequenced whole genomes from 50 pygmy lorises and 6 Bengal slow lorises (Nycticebus bengalensis). We found that many gene families involved in detoxification have been specifically expanded in the pygmy loris, including the GSTA gene family, with many newly derived copies functioning specifically in the liver. We detected many genes displaying evolutionary convergence between pygmy loris and koala, including PITRM1. Significant decreases in PITRM1 enzymatic activity in these two species may have contributed to their characteristic low rate of metabolism. We also detected many evolutionarily convergent genes and positively selected genes in the pygmy loris that are involved in muscle development. Functional assays demonstrated the decreased ability of one positively selected gene, MYOF, to up-regulate the fast-type muscle fiber, consistent with the lower proportion of fast-twitch muscle fibers in the pygmy loris. The protein product of another positively selected gene in the pygmy loris, PER2, exhibited weaker binding to the key circadian core protein CRY, a finding that may be related to this species' unusual circadian rhythm. Finally, population genomics analysis revealed that these two extant loris species, which coexist in the same habitat, have exhibited an inverse relationship in terms of their demography over the past 1 million years, implying strong interspecies competition after speciation.

Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals.

The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.

RNA-seq analysis reveals the genes/pathways responsible for genetic plasticity of rice to varying environmental conditions on direct-sowing and transplanting.

Rice cultivation by transplanting requires plenty of water. It might become a challenging task in future to grow rice by transplanting due to the climatic change, water and labor scarcities. Direct-sown rice (DSR) is emerging as a resource-conserving and climate-smart alternative to transplanted rice (TPR). However, no specific variety has been bred for dry/direct-sown conditions. The present study was undertaken to decipher the molecular basis of genetic plasticity of rice under different planting methods. Comparative RNA-seq analysis revealed a number (6133) of genes exclusively up-regulated in Nagina-22 (N-22) leaf under DSR conditions, compared to that (3538) in IR64 leaf. Several genes up-regulated in N-22 were down-regulated in IR64. Genes for growth-regulation and nutrient-reservoir activities, transcription factors, translational machinery, carbohydrate metabolism, cell cycle/division, and chromatin organization/epigenetic modifications were considerably up-regulated in the leaf of N-22 under DSR conditions. Complementary effects of these factors in rendering genetic plasticity were confirmed by the agronomic/physiological performance of rice cultivar. Thus, growth-regulation/nutrient-reservoir activities, transcription factors, and translational machinery are important molecular factors responsible for the observed genetic plasticity/adaptability of Nagina-22 to different planting methods. This might help to develop molecular markers for DSR breeding, replacing TPR with DSR for better water-productivity, and minimizing greenhouse-gas emission necessary for negative emission agriculture.