Within-species Variation Research Articles

Variable rate of ageing within species: insights from Darwin’s frogs

AbstractActuarial senescence, the increase in adult mortality risk with increasing age, is a widespread phenomenon across the animal kingdom. Although between-species variation in the rate of increase in mortality as organisms age (i.e. ageing rate) is now well documented, the occurrence of variation in ageing rate within a given species remains much more debatable. We evaluated the level of within-species variation in ageing rate in four populations of the southern Darwin’s frog (Rhinoderma darwinii) from Chile. Our results revealed strong among-population variation in ageing rates, and these were correlated with the population-specific generation time. A higher ageing rate occurred in populations where individuals exhibited a faster pace of life. Our results, along with recent studies in evolutionarily distant amphibian species, indicate that there can be substantial within-species variation in the rate of ageing, highlighting amphibians as emerging models to study the patterns and mechanisms of intraspecific variation in ageing rate.

Generalist–specialist continuum in soil oribatid mites (Acari): evidence from stable isotopes

Not all individuals are the same. How this applies to soil-living creatures received little attention. Within-species variability determines the niche differentiation of coexisting species.

Investigating causes and implications of morphological variation in a native pondweed (Stuckenia pectinata) of San Francisco Estuary

Morphological variation in widely distributed plants may be driven by phenotypic plasticity or underlying genetic differences. In the brackish to fresh open waters of San Francisco Estuary, there are at least two distinct growth forms of a native pondweed in the genus Stuckenia. We determined that all plants collected from throughout the region are S. pectinata by sequencing the nuclear ribosomal internal transcribed spacer (ITS) region. This led us to question if different morphologies result from intraspecific genetic differentiation or differences in water flow, which we explored using microsatellites and a common garden experiment, respectively. As only four of nine microsatellite loci developed in Europe were polymorphic for our samples, there was low resolution to detect differences; however, some multilocus genotypes found only in narrow-leaf samples hinted of within-species variation. Further, while morphological traits were plastic in response to flow manipulation, distinct morphotypes did not converge under the same conditions, implicating genetic differences. Regardless of mechanisms for contrasting growth forms, leaf size and quantity may affect available habitat for ecologically-important invertebrates. We found narrow/dense leaves supported greater invertebrate densities at both a low-salinity, and especially, a brackish site. The latter was dominated by an amphipod that we determined strongly prefers to consume narrower leaves. We conclude that both environmental conditions and genetic differentiation play a role in S. pectinata morphology. That these differences propagate to higher trophic levels calls for further investigation into the genetic basis for, as well as spatial extent of, the two morphotypes.

Pan-genome and multi-parental framework for high-resolution trait dissection in melon (Cucumis melo).

Linking genotype with phenotype is a fundamental goal in biology and requires robust data for both. Recent advances in plant-genome sequencing have expedited comparisons among multiple-related individuals. The abundance of structural genomic within-species variation that has been discovered indicates that a single reference genome cannot represent the complete sequence diversity of a species, leading to the expansion of the pan-genome concept. For high-resolution forward genetics, this unprecedented access to genomic variation should be paralleled and integrated with phenotypic characterization of genetic diversity. We developed a multi-parental framework for trait dissection in melon (Cucumis melo), leveraging a novel pan-genome constructed for this highly variable cucurbit crop. A core subset of 25 diverse founders (MelonCore25), consisting of 24 accessions from the two widely cultivated subspecies of C. melo, encompassing 12 horticultural groups, and 1 feral accession was sequenced using a combination of short- and long-read technologies, and their genomes were assembled de novo. The construction of this melon pan-genome exposed substantial variation in genome size and structure, including detection of ~300 000 structural variants and ~9 million SNPs. A half-diallel derived set of 300 F2 populations, representing all possible MelonCore25 parental combinations, was constructed as a framework for trait dissection through integration with the pan-genome. We demonstrate the potential of this unified framework for genetic analysis of various melon traits, including rind color intensity and pattern, fruit sugar content, and resistance to fungal diseases. We anticipate that utilization of this integrated resource will enhance genetic dissection of important traits and accelerate melon breeding.

Intraspecific Leaf Trait Variation across and within Five Common Wine Grape Varieties.

Variability in traits forming the Leaf Economics Spectrum (LES) among and within crop species plays a key role in governing agroecosystem processes. However, studies evaluating the extent, causes, and consequences of within-species variation in LES traits for some of the world’s most common crops remain limited. This study quantified variations in nine leaf traits measured across 90 vines of five common wine grape (Vitis vinifera L.) varieties at two growth stages (post-flowering and veraison). Grape traits in these varieties covary along an intraspecific LES, in patterns similar to those documented in wild plants. Across the five varieties evaluated here, high rates of photosynthesis (A) and leaf nitrogen (N) concentrations were coupled with low leaf mass per area (LMA), whereas the opposite suite of traits defined the “resource-conserving end” of this intraspecific LES in grape. Variety identity was the strongest predictor of leaf physiological (A) and morphological traits (i.e., leaf area and leaf mass), whereas leaf chemical traits and LMA were best explained by growth stage. All five varieties expressed greater resource-conserving trait syndromes (i.e., higher LMA, lower N, and lower Amass) later in the growing season. Traits related to leaf hydraulics, including instantaneous water-use efficiency (WUE), were unrelated to LES and other resource capture traits, and were better explained by spatial location. These results highlight the relative contributions of genetic, developmental, and phenotypic factors in structuring trait variation in the five wine grape varieties evaluated here, and point to a key role of domestication in governing trait relationships in the world’s crops.

Patterns in Foliar Isotopic Nitrogen, Percent Nitrogen, and Site Index for Managed Forest Systems in the United States

Patterns in foliar nitrogen (N) stable isotope ratios (δ15N) have been shown to reveal trends in terrestrial N cycles, including the identification of ecosystems where N deficiencies limit forest ecosystem productivity. However, there is a gap in our understanding of within-species variation and species-level response to environmental gradients or forest management. Our objective is to examine the relationship between site index, foliar %N, foliar δ15N and spectral reflectance for managed Douglas-fir (Pseudotsuga menziesii) and loblolly pine (Pinus taeda) plantations across their geographic ranges in the Pacific Northwest and the southeastern United States, respectively. Foliage was measured at 28 sites for reflectance using a handheld spectroradiometer, and further analyzed for δ15N and N concentration. Unlike the prior work for grasslands and shrubland species, our results show that foliar δ15N and foliar %N are not well correlated for these tree species. However, multiple linear regression models suggest a strong predictive ability of spectroscopy data to quantify foliar δ15N, with some models explaining more than 65% of the variance in the δ15N. Additionally, moderate to strong explanations of variance were found between site index and foliar δ15N (R2 = 0.49) and reflectance and site index (R2 = 0.84) in the Douglas-fir data set. The development of relationships between foliar spectral reflectance, δ15N and measures of site productivity provides the first step toward mapping canopy δ15N for these managed forests with remote sensing.

The effect of sex, age and boldness on inhibitory control

Inhibitory control requires an individual to suppress impulsive actions in favour of more appropriate behaviours to gain a delayed reward. It plays an important role in activities such as foraging and initiating mating, but high within-species variation suggests that some individuals have greater inhibitory control than others. A standard index of inhibitory control used in many taxa is measuring how long an animal persists in trying to move itself or an appendage (e.g. its hand) through a transparent barrier to reach a reward. Although recent nonhuman studies have investigated how different factors are associated with variation in inhibitory control, these studies have rarely considered how these factors interact. Here we investigated how sex, age, personality (boldness) and the type of reward stimulus interact to predict the degree of motor inhibitory control in eastern mosquitofish, Gambusia holbrooki . We measured inhibitory control using a standard detour assay, ‘boldness’ (time to emergence in a novel environment), and the rate of learning. There were three different reward stimuli: a shoal of females, a shoal of males or a mixed-sex shoal. Individuals were tested in four consecutive trials, always with the same reward type, to quantify short-term learning. These measures were repeated at 7, 14 and 21 weeks after maturation to examine the effect of age. Females had significantly greater inhibitory control than males. Regardless of sex, older fish had significantly greater inhibitory control than younger fish, and boldness predicted learning ability. The type of reward stimuli had no sex-specific effect on inhibitory control. We discuss the biological significance of these sources of variation in inhibitory control, and the importance of accounting for them in studies examining individual differences in cognitive abilities. • Inhibitory control (IC) suppresses impulsive actions in favour of delayed rewards. • Both sex and age, but not their interaction, affected IC in 251 mosquitofish. • Individual's boldness did not affect IC, but bolder fish were faster learners. • Composition of a social reward (males/females/mixed) did not affect IC.

Stochastic Modeling of Gene Expression Evolution Uncovers Tissue- and Sex-Specific Properties of Expression Evolution in the Drosophila Genus.

Gene expression evolution is typically modeled with the stochastic Ornstein-Uhlenbeck (OU) process. It has been suggested that the estimation of within-species variations using replicated data can increase the predictive power of such models, but this hypothesis has not been fully tested. We developed EvoGeneX, a computationally efficient implementation of the OU-based method that models within-species variation. Using extensive simulations, we show that modeling within-species variations and appropriate selection of species improve the performance of the model. Further, to facilitate a comparative analysis of expression evolution, we introduce a formal measure of evolutionary expression divergence for a group of genes using the rate and the asymptotic level of divergence. With these tools in hand, we performed the first-ever analysis of the evolution of gene expression across different body-parts, species, and sexes of the Drosophila genus. We observed that genes with adaptive expression evolution tend to be body-part specific, whereas the genes with constrained evolution tend to be shared across body-parts. Among the neutrally evolving gene expression patterns, gonads in both sexes have higher expression divergence relative to other tissues and the male gonads have even higher divergence than the female gonads. Among the evolutionarily constrained genes, the gonads show different divergence patterns, where the male gonads, and not the female gonads, show less constrained divergence than other body-parts. Finally, we show interesting examples of adaptive expression evolution, including adaptation of odor binding proteins.

Within-species variation of seed traits of dune engineering species across a European climatic gradient.

Within-species variation is a key component of biodiversity and linking it to climatic gradients may significantly improve our understanding of ecological processes. High variability can be expected in plant traits, but it is unclear to which extent it varies across populations under different climatic conditions. Here, we investigated seed trait variability and its environmental dependency across a latitudinal gradient of two widely distributed dune-engineering species (Thinopyrum junceum and Calamagrostis arenaria). Seed germination responses against temperature and seed mass were compared within and among six populations exposed to a gradient of temperature and precipitation regimes (Spiekeroog, DE; Bordeaux, FR; Valencia, ES; Cagliari, IT, Rome, IT; Venice, IT). Seed germination showed opposite trends in response to temperature experienced during emergence in both species: with some expectation, in populations exposed to severe winters, seed germination was warm-cued, whereas in populations from warm sites with dry summer, seed germination was cold-cued. In C. arenaria, variability in seed germination responses disappeared once the seed coat was incised. Seed mass from sites with low precipitation was smaller than that from sites with higher precipitation and was better explained by rainfall continentality than by aridity in summer. Within-population variability in seed germination accounted for 5 to 54%, while for seed mass it was lower than 40%. Seed trait variability can be considerable both within- and among-populations even at broad spatial scale. The variability may be hardly predictable since it only partially correlated with the analyzed climatic variables, and with expectation based on the climatic features of the seed site of origin. Considering seed traits variability in the analysis of ecological processes at both within- and among-population levels may help elucidate unclear patterns of species dynamics, thereby contributing to plan adequate measures to counteract biodiversity loss.

Population-specific call order in chimpanzee greeting vocal sequences

SummaryPrimates rarely learn new vocalizations, but they can learn to use their vocalizations in different contexts. Such “vocal usage learning,” particularly in vocal sequences, is a hallmark of human language, but remains understudied in non-human primates. We assess usage learning in four wild chimpanzee communities of Taï and Budongo Forests by investigating population differences in call ordering of a greeting vocal sequence. Whilst in all groups, these sequences consisted of pant-hoots (long-distance contact call) and pant-grunts (short-distance submissive call), the order of the two calls differed across populations. Taï chimpanzees consistently commenced greetings with pant-hoots, whereas Budongo chimpanzees started with pant-grunts. We discuss different hypotheses to explain this pattern and conclude that higher intra-group aggression in Budongo may have led to a local pattern of individuals signaling submission first. This highlights how within-species variation in social dynamics may lead to flexibility in call order production, possibly acquired via usage learning.

Keeping it cool to take the heat: tropical lizards have greater thermal tolerance in less disturbed habitats.

Global climate change has profound effects on species, especially those in habitats already altered by humans. Tropical ectotherms are predicted to be at highrisk from global temperature increases, particularly those adapted to cooler temperatures at higher altitudes. We investigated how one such species, the water anole (Anolis aquaticus), is affected by temperature stress similar to that of a warming climate across a gradient of human-altered habitats at high elevation sites. We conducted a field survey on thermal traits and measured lizard critical thermal maxima across the sites. From the field survey, we found that (1) lizards from the least disturbed site and (2) operative temperature models of lizards placed in the least disturbed site had lower temperatures than those fromsites with histories of human disturbance. Individuals from the least disturbed site also demonstrated greater tolerance to high temperatures than those from the more disturbed sites, in both their critical thermal maxima and the time spent at high temperatures prior to reaching critical thermal maxima. Our results demonstrate within-species variability in responses to high temperatures, depending on habitat type, and provide insight into how tropical reptiles may fare in a warming world.

Genomic variation in the Black-throated Green Warbler (Setophaga virens) suggests divergence in a disjunct Atlantic Coastal Plain population (S. v. waynei)

AbstractWe used whole-genome resequencing to estimate genetic distinctiveness in the Black-throated Green Warbler (Setophaga virens)—including S. v. waynei—a putative subspecies that occupies a narrow disjunct breeding range along the Atlantic Coastal Plain. Despite detecting low-global differentiation (FST = 0.027) across the entire species, the principal components analysis of genome-wide differences shows the main axis of variation separates S. v. waynei from all other S. v. virens samples. We also estimated a low-migration rate for S. v. waynei, but found them to be most similar to another disjunct population from the Piedmont of North Carolina, and detected evidence of a historical north-to-south geographic dispersal among the entire species. New World wood warblers (family: Parulidae) can exhibit strong phenotypic differences among species, particularly, in song and plumage; however, within-species variation in these warblers—often designated as subspecies—is much more subtle. The existence of several isolated Black-throated Green Warbler populations across its eastern North American breeding range offers an excellent opportunity to further understand the origin, maintenance, and conservation status of subspecific populations. Our results, combined with previously documented ecological and morphological distinctiveness, support that S. v. waynei be considered a distinct and recognized subspecies worthy of targeted conservation efforts.

Shading Gradients Drive Differential Responses of Leaf Traits in an Early Community Germinated by Forest Topsoil

Seedling performance in the early stage is crucial to natural forest restoration, and functional traits have been widely employed in exploring plant adaptation under field conditions. However, the responses and variabilities of leaf traits have not been clearly defined at the light gradients that are used in restoration practices. We evaluated the variation in leaf treats in species and community levels in a controlled field plot with shading treatments. We found that the variation characteristics differed across different species and trait types along shading gradients. Individuals of most species had a larger leaf area (LA) and specific leaf area (SLA) in the shaded habitats, while only a few tree species showed significant responses in their leaf shape and chlorophyll concentration. Although LA and SLA showed similar directions and trends of changes in the trait mean, four response models were observed based on the light points corresponding to initial responses and following trends. The extent of within-species trait variation for each treatment was similar at the community level due to diverse changes in the direction and degrees of variation in co-occurring species. Intraspecific variation was limited within each shading treatment, while it noticeably contributed to the local adaptation in the entire heterogeneous restoration community. Our findings indicate that species with different trait combinations will have different responses to light gradients, and that the mean and degree of variation in leaf traits will also lead to distinctive strategies being created to match the different shading conditions. Vegetation restoration should consider the adaptive traits and their response diversity when selecting species and for habitat management with specific trait–environment interactions.

Same, same but different! Exploring children’s understandings of within-species variation

ABSTRACT The importance of genetic diversity, especially within small populations of endangered species, is becoming increasingly apparent. Genetic engineering techniques that could potentially enhance diversity are now being developed. However, the use of such techniques would require social licence and yet within the general population there is limited understanding of the importance of variation within a species. This qualitative study explored the potential of introducing the concept of within-species variation to New Zealand primary school children (5 to 11 year olds) with the aim of preparing these students to make critical decisions about the use of these techniques in their futures. Eighty-four children participated in the study and their explanations for the impact that differences between individuals may have were analysed revealing their scientifically acceptable understanding of the concept. But findings also highlighted potential misconceptions that they may retain. These misconceptions include a belief that animals think and behave in a manner similar to humans or that variations within a species are for identification purposes only. Findings showed that the concept of within-species variation could be introduced to primary school children. However, to do this successfully curriculum documents may need to be reviewed and teachers may require specific professional development.

Electrocommunication signals and aggressive behavior vary among male morphs in an apteronotid fish, Compsaraia samueli.

Within-species variation in male morphology is common among vertebrates and is often characterized by dramatic differences in behavior and hormonal profiles. Males with divergent morphs also often use communication signals in a status-dependent way. Weakly electric knifefish are an excellent system for studying variation in male morphology and communication and its hormonal control. Knifefish transiently modulate the frequency of their electric organ discharge (EOD) during social encounters to produce chirps and rises. In the knifefish Compsaraia samueli, males vary extensively in jaw length. EODs and their modulations (chirps and rises) have never been investigated in this species, so it is unclear whether jaw length is related to the function of these signals. We used three behavioral assays to analyze EOD modulations in male C. samueli: (1) artificial playbacks, (2) relatively brief, live agonistic dyadic encounters, and (3) long-term overnight recordings. We also measured circulating levels of two androgens, 11-ketotestosterone and testosterone. Chirp structure varied within and across individuals in response to artificial playback, but was unrelated to jaw length. Males with longer jaws were more often dominant in dyadic interactions. Chirps and rises were correlated with and preceded attacks regardless of status, suggesting these signals function in aggression. In longer-term interactions, chirp rate declined after 1week of pairing, but was unrelated to male morphology. Levels of circulating androgens were low and not predictive of jaw length or EOD signal parameters. These results suggest that communication signals and variation in male morphology are linked to outcomes of non-breeding agonistic contests.

Potential for identification of wild night-flying moths by remote infrared microscopy.

There are hundreds of thousands of moth species with crucial ecological roles that are often obscured by their nocturnal lifestyles. The pigmentation and appearance of moths are dominated by cryptic diffuse shades of brown. In this study, 82 specimens representing 26 moth species were analysed using infrared polarimetric hyperspectral imaging in the range of 0.95–2.5 µm. Contrary to previous studies, we demonstrate that since infrared light does not resolve the surface roughness, wings appear glossy and specular at longer wavelengths. Such properties provide unique reflectance spectra between species. The reflectance of the majority of our species could be explained by comprehensive models, and a complete parametrization of the spectral, polarimetric and angular optical properties was reduced to just 11 parameters with physical units. These parameters are complementary and, compared with the within-species variation, were significantly distinct between species. Counterintuitively to the aperture-limited resolution criterion, we could deduce microscopic features along the surface from their infrared properties. These features were confirmed by electron microscopy. Finally, we show how our findings could greatly enhance opportunities for remote identification of free-flying moth species, and we hypothesize that such flat specular wing targets could be expected to be sensed over considerable distances.

Lack of Statistical Rigor in DNA Barcoding Likely Invalidates the Presence of a True Species' Barcode Gap

DNA barcoding has been largely successful in satisfactorily exposing levels of standing genetic diversity for a wide range of taxonomic groups through the employment of only one or a few universal gene markers. However, sufficient coverage of geographically-broad intra-specific haplotype variation within genomic databases like the Barcode of Life Data Systems (BOLD) and GenBank remains relatively sparse. As reference sequence libraries continue to grow exponentially in size, there is now the need to identify novel ways of meaningfully analyzing vast amounts of available DNA barcode data. This is an important issue to address promptly for the routine tasks of specimen identification and species discovery, which have seen broad adoption in areas as diverse as regulatory forensics and resource conservation. Here, it is demonstrated that the interpretation of DNA barcoding data is lacking in statistical rigor. To highlight this, focus is set specifically on one key concept that has become a household name in the field: the DNA barcode gap. Arguments outlined herein specifically center on DNA barcoding in animal taxa and stem from three angles: (1) the improper allocation of specimen sampling effort necessary to capture adequate levels of within-species genetic variation, (2) failing to properly visualize intra-specific and interspecific genetic distances, and (3) the inconsistent, inappropriate use, or absence of statistical inferential procedures in DNA barcoding gap analyses. Furthermore, simple statistical solutions are outlined which can greatly propel the use of DNA barcoding as a tool to irrefutably match unknowns to knowns on the basis of the barcoding gap with a high degree of confidence. Proposed methods examined herein are illustrated through application to DNA barcode sequence data from Canadian Pacific fish species as a case study.

Inter-Individual Budburst Variation in Fagus sylvatica Is Driven by Warming Rate.

The onset of the growing season in temperate forests is relevant for forest ecology and biogeochemistry and is known to occur earlier with climate change. Variation in tree phenology among individual trees of the same stand and species, however, is not well understood. Yet, natural selection acts on this inter-individual variation, which consequently affects the adaptive potential to ongoing environmental changes. Budburst dates of 146 mature individuals of Fagus sylvatica, the dominant natural forest tree of central Europe, were recorded over 12 years in one forest stand of 1 ha in the Müritz National Park, Germany. The tree-specific location, topographical differences, as well as social status, were measured to explain the inter-individual variation in budburst. Furthermore, inter-individual differences in bud dormancy were quantified. Additional phenology and weather data across Germany from 405 sites over a 25-year period was used to put the insights from the single stand into perspective. Consistent phenological ranking over the years with respect to early and late flushing trees was observed within the single forest stand, with 23 trees consistently flushing 3–6 days earlier and 22 trees consistently flushing 3–10 days later than the median. Trees flushing consistently early varied most in their spring budburst dates and were less dormant than late-flushing trees already in mid-winter. The higher variation in earlier flushing trees was best explained by a slower warming rate during their budburst period in the observed stand as well as across Germany. Likewise, years with a lower warming rate during the budburst period were more variable in budburst dates. The rate of warming during spring time is crucial to accurately project future within-species variation and the resulting adaptive potential in spring phenology of dominant forest tree species.

Global genetic diversity status and trends: towards a suite of Essential Biodiversity Variables (EBVs) for genetic composition.

ABSTRACTBiodiversity underlies ecosystem resilience, ecosystem function, sustainable economies, and human well‐being. Understanding how biodiversity sustains ecosystems under anthropogenic stressors and global environmental change will require new ways of deriving and applying biodiversity data. A major challenge is that biodiversity data and knowledge are scattered, biased, collected with numerous methods, and stored in inconsistent ways. The Group on Earth Observations Biodiversity Observation Network (GEO BON) has developed the Essential Biodiversity Variables (EBVs) as fundamental metrics to help aggregate, harmonize, and interpret biodiversity observation data from diverse sources. Mapping and analyzing EBVs can help to evaluate how aspects of biodiversity are distributed geographically and how they change over time. EBVs are also intended to serve as inputs and validation to forecast the status and trends of biodiversity, and to support policy and decision making. Here, we assess the feasibility of implementing Genetic Composition EBVs (Genetic EBVs), which are metrics of within‐species genetic variation. We review and bring together numerous areas of the field of genetics and evaluate how each contributes to global and regional genetic biodiversity monitoring with respect to theory, sampling logistics, metadata, archiving, data aggregation, modeling, and technological advances. We propose four Genetic EBVs: (i) Genetic Diversity; (ii) Genetic Differentiation; (iii) Inbreeding; and (iv) Effective Population Size (N e). We rank Genetic EBVs according to their relevance, sensitivity to change, generalizability, scalability, feasibility and data availability. We outline the workflow for generating genetic data underlying the Genetic EBVs, and review advances and needs in archiving genetic composition data and metadata. We discuss how Genetic EBVs can be operationalized by visualizing EBVs in space and time across species and by forecasting Genetic EBVs beyond current observations using various modeling approaches. Our review then explores challenges of aggregation, standardization, and costs of operationalizing the Genetic EBVs, as well as future directions and opportunities to maximize their uptake globally in research and policy. The collection, annotation, and availability of genetic data has made major advances in the past decade, each of which contributes to the practical and standardized framework for large‐scale genetic observation reporting. Rapid advances in DNA sequencing technology present new opportunities, but also challenges for operationalizing Genetic EBVs for biodiversity monitoring regionally and globally. With these advances, genetic composition monitoring is starting to be integrated into global conservation policy, which can help support the foundation of all biodiversity and species' long‐term persistence in the face of environmental change. We conclude with a summary of concrete steps for researchers and policy makers for advancing operationalization of Genetic EBVs. The technical and analytical foundations of Genetic EBVs are well developed, and conservation practitioners should anticipate their increasing application as efforts emerge to scale up genetic biodiversity monitoring regionally and globally.

Rates of Mutations and Transcript Errors in the Foodborne Pathogen Salmonella enterica subsp. enterica.

Because errors at the DNA level power pathogen evolution, a systematic understanding of the rate and molecular spectra of mutations could guide the avoidance and treatment of infectious diseases. We thus accumulated tens of thousands of spontaneous mutations in 768 repeatedly bottlenecked lineages of 18 strains from various geographical sites, temporal spread, and genetic backgrounds. Entailing over ∼1.36 million generations, the resultant data yield an average mutation rate of ∼0.0005 per genome per generation, with a significant within-species variation. This is one of the lowest bacterial mutation rates reported, giving direct support for a high genome stability in this pathogen resulting from high DNA-mismatch-repair efficiency and replication-machinery fidelity. Pathogenicity genes do not exhibit an accelerated mutation rate, and thus, elevated mutation rates may not be the major determinant for the diversification of toxin and secretion systems. Intriguingly, a low error rate at the transcript level is not observed, suggesting distinct fidelity of the replication and transcription machinery. This study urges more attention on the most basic evolutionary processes of even the best-known human pathogens and deepens the understanding of their genome evolution.