Evolutionary Applications最新文献

Fast-paced selective pressures imposed by climate change and anthropogenic activities call for adaptive evolutionary responses to emerge at ecological timescales. However, the evolution and heritability of genomic variation underlie mechanistic constraints, which dictate a slower pace of adaptation exclusively relying on standing genetic variation and novel mutations. Environmentally responsive epigenetic mechanisms can allow acclimatisation and adaptive phenotypes to arise faster than DNA sequence-based mechanisms alone. Nevertheless, the knowledge gap between identifying epigenetic marks and effectively deeming them functional is still wide in a natural context and often outside the scope of model organisms. With this Special Issue, we aimed to narrow this gap by presenting a compilation of original research articles, reviews and opinions on the topic of epigenetics in wild populations. We contextualised this collection within the overarching topic of conservation biology, as we firmly propose that epigenetic research can significantly enhance the effectiveness of conservation measures. Contributions highlighted the putative role of epigenetic variation in the acclimatisation and adaptive potential of species and populations directly and indirectly affected by climatic shifts and anthropogenic actions. They further exemplified how epigenetic variation can be used as biomarkers for monitoring variations in physiology, phenology and behaviour. Lastly, reviews and perspective articles illustrated the past and present of epigenetic research in wild populations while suggesting future research avenues.

Biological invasions have caused the loss of freshwater biodiversity worldwide. The interplay between adaptive responses and demographic characteristics of populations impacted by invasions is expected to be important for their resilience, but the interaction between these factors is poorly understood. The freshwater gastropod Amnicola limosus is native to the Upper St. Lawrence River and distributed along a water calcium concentration gradient within which high-calcium habitats are impacted by an invasive predator fish (Neogobius melanostomus, round goby), whereas low-calcium habitats provide refuges for the gastropods from the invasive predator. Our objectives were to (1) test for adaptation of A. limosus to the invasive predator and the low-calcium habitats, and (2) investigate if migrant gastropods could move from refuge populations to declining invaded populations (i.e., demographic rescue), which could also help maintain genetic diversity through gene flow (i.e., genetic rescue). We conducted a laboratory reciprocal transplant of wild F₀ A. limosus sourced from the two habitat types (high calcium/invaded and low calcium/refuge) to measure adult survival and fecundity in home and transplant treatments of water calcium concentration (low/high) and round goby cue (present/absent). We then applied pooled whole-genome sequencing of 12 gastropod populations from across the calcium/invasion gradient. We identified patterns of life-history traits and genetic differentiation across the habitats that are consistent with local adaptation to low-calcium concentrations in refuge populations and to round goby predation in invaded populations. We also detected restricted gene flow from the low-calcium refugia towards high-calcium invaded populations, implying that the potential for demographic and genetic rescue is limited by natural dispersal. Our study highlights the importance of considering the potentially conflicting effects of local adaptation and gene flow for the resilience of populations coping with invasive predators.

Many methods are now available to calculate N_e, but their performance varies depending on assumptions. Although simulated data are useful to discover certain types of bias, real empirical data supported by detailed known population histories allow us to discern how well methods perform with actual messy and complex data. Here, we focus on two genomic data sets of grey wolf populations for which population size changes of the past 40–120 years are well documented. We use this background to explore in what detail we can retrieve the known population history from these populations, in the light of pitfalls relating to population history, sampling design and the change in the spatial scale at which N_e is estimated as we go further back in time. The Scandinavian wolf population was founded in the early 1980s from a few individuals and has gradually expanded up to 510 wolves. Although the founder event of the Scandinavian population was detected by GONE, the founding effective population size was strongly overestimated when the most recent samples were used, but less so when older samples were considered. Nevertheless, the present-day N_e corresponds to theoretical expectations. The western Great Lakes wolf population of Minnesota is the only population in the contiguous United States that persisted throughout the 20th century, surviving intense persecution. We found a good concordance between the estimated N_e and trends in census size data, but the reconstruction of N_e clearly highlights the difficulty of interpreting results in spatially structured populations that underwent demographic fluctuations.

We are still largely reliant on pesticides for the suppression of arthropod pests which threaten human health and food production, but the recent rise of evolved resistance among important pest species has reduced pesticide efficacy. Despite this, our understanding of strategies that effectively limit the evolution of resistance remains weak. Male-killing sex ratio distorting microbes (SRDMs), such as Wolbachia and Spiroplasma, are common among arthropod species. Previous theoretical work has suggested that they could limit adaptive potential in two ways: first, because by distorting sex ratios they reduce the effective population size, and second, because infected females produce no male offspring which restricts gene flow. Here we present the results of a novel experiment in which we test the extent by which these two mechanisms limit the adaptive response of arthropods to pesticide. Using a fully factorial design, we manipulated the adult sex ratio of laboratory populations of Drosophila melanogaster, both in the presence and absence of SRDMs, and exposed these populations to six generations of pesticide poisoning. This design allows the effects of SRDMs on sex ratio and their effects on gene flow to be estimated separately. After six generations, individuals from populations with even sex ratios displayed a higher resistance to pesticide relative to individuals from female-biased populations. By contrast, we found no effect of the presence of SRDMs in host populations on pesticide resistance independent of sex ratio. In addition, males were more susceptible to pesticide than females—this was true of flies from both naïve and previously exposed populations. These findings provide the first empirical proof of concept that sex ratio distortion arising from SRDMs can limit adaptation to pesticides, but cast doubt on the theoretical effect of male-killers limiting adaptation by disrupting gene flow.

Biocides are used to control microorganisms across different applications, but emerging resistance may pose risks for those applications. Resistance to biocides has commonly been studied using adaptive laboratory evolution (ALE) experiments with growth at subinhibitory concentrations linked to serial subculturing. It has been shown recently that Escherichia coli adapts to repeated lethal stress imposed by the biocide benzalkonium chloride (BAC) by increased survival (i.e., tolerance) and not by evolving the ability to grow at increased concentrations (i.e., resistance). Here, we investigate the contributions of evolution for tolerance as opposed to resistance for the outcome of ALE experiments with E. coli exposed to BAC. We find that BAC concentrations close to the half maximal effective concentration (EC₅₀, 4.36 μg mL⁻¹) show initial killing (~40%) before the population resumes growth. This indicates that cells face a two-fold selection pressure: for increased survival and for increased growth. To disentangle the effects of both selection pressures, we conducted two ALE experiments: (i) one with initial killing and continued stress close to the EC₅₀ during growth and (ii) another with initial killing and no stress during growth. Phenotypic characterization of adapted populations showed that growth at higher BAC concentrations was only selected for when BAC was present during growth. Whole genome sequencing revealed distinct differences in mutated genes across treatments. Treatments selecting for survival-only led to mutations in genes for metabolic regulation (cyaA) and cellular structure (flagella fliJ), while treatments selecting for growth and survival led to mutations in genes related to stress response (hslO and tufA). Our results demonstrate that serial subculture ALE experiments with an antimicrobial at subinhibitory concentrations can select for increased growth and survival. This finding has implications for the design of ALE experiments to assess resistance risks of antimicrobials in different scenarios such as disinfection, preservation, and environmental pollution.

Genetic diversity is rapidly lost from small, isolated populations by genetic drift. Measuring the level of genetic drift using effective population size (N_e) is highly useful for management. Single-cohort genetic N_e estimators approximate the number of breeders in one season (N_b): a value < 100 signals likely inbreeding depression. Per-generation N_e < 1000 estimated from multiple cohort signals reduced adaptive potential. Natural populations rarely meet assumptions of N_e-estimation, so interpreting estimates is challenging. Macquarie perch is an endangered Australian freshwater fish threatened by severely reduced range, habitat loss, and fragmentation. To counteract low N_e, augmented gene flow is being implemented in several populations. In the Murrumbidgee River, unknown effects of water management on among-site connectivity impede the design of effective interventions. Using DArT SNPs for 328 Murrumbidgee individuals sampled across several sites and years with different flow conditions, we assessed population structure, site isolation, heterozygosity, inbreeding, and N_e. We tested for inbreeding depression, assessed genetic diversity and dispersal, and evaluated whether individuals translocated from Cataract Reservoir to the Murrumbidgee River bred, and interbred with local fish. We found strong genetic structure, indicating complete or partial isolation of river fragments. This structure violates assumptions of N_e estimation, resulting in strongly downwardly biased N_b estimates unless assessed per-site, highlighting the necessity to account for population structure while estimating N_e. Inbreeding depression was not detected, but with low N_b at each site, inbreeding and inbreeding depression are likely. These results flagged the necessity to address within-river population connectivity through flow management and genetic mixing through translocations among sites and from other populations. Three detected genetically diverse offspring of a translocated Cataract fish and a local parent indicated that genetic mixing is in progress. Including admixed individuals in estimates yielded lower N_e but higher heterozygosity, suggesting heterozygosity is a preferable indicator of genetic augmentation.

Estimating and understanding the ratio between effective population size (N_e) and census population size (N_c) are pivotal in the conservation of large marine pelagic fish species, including bony fish such as tunas and cartilaginous fish such as sharks, given the challenges associated with obtaining accurate estimates of their abundance. The difficulties inherent in capturing and monitoring these species in vast and dynamic marine environments often make direct estimation of their population size challenging. By focusing on N_e, it is conceivable in certain cases to approximate census size once the N_e/N_c ratio is known, although this ratio can vary and does not always increase linearly, as it is influenced by various ecological and evolutionary factors. Thus, this ratio presents challenges and complexities in the context of pelagic species conservation. To delve deeper into these challenges, firstly, we recall the diverse types of effective population sizes, including contemporary and historical sizes, and their implications in conservation biology. Secondly, we outline current knowledge about the influence of life history traits on the N_e/N_c ratio in the light of examples drawn from large and abundant pelagic fish species. Despite efforts to document an increasing number of marine species using recent technologies and statistical methods, establishing general rules to predict N_e/N_c remains elusive, necessitating further research and investment. Finally, we recall statistical challenges in relating N_e and N_c emphasizing the necessity of aligning temporal and spatial scales. This last part discusses the roles of generation and reproductive cycle effective population sizes to predict genetic erosion and guiding management strategies. Collectively, these sections underscore the multifaceted nature of effective population size estimation, crucial for preserving genetic diversity and ensuring the long-term viability of populations. By navigating statistical and theoretical complexities, and addressing methodological challenges, scientists should be able to advance our understanding of the N_e/N_c ratio.

Microorganisms associated with animals harbour a unique set of functional traits pivotal for the normal functioning of their hosts. This realisation has led researchers to hypothesise that animal-associated microbial communities may boost the capacity of their hosts to acclimatise and adapt to environmental changes, two eco-evolutionary processes with significant applied relevance. Aiming to assess the importance of microorganisms for wild vertebrate conservation, we conducted a quantitative systematic review to evaluate the scientific evidence for the contribution of gut microorganisms to the acclimation and adaptation capacity of wild vertebrate hosts. After screening 1974 publications, we scrutinised the 109 studies that met the inclusion criteria based on 10 metrics encompassing study design, methodology and reproducibility. We found that the studies published so far were not able to resolve the contribution of gut microorganisms due to insufficient study design and research methods for addressing the hypothesis. Our findings underscore the limited application to date of microbiome knowledge in vertebrate conservation and management, highlighting the need for a paradigm shift in research approaches. Considering these results, we advocate for a shift from observational studies to experimental manipulations, where fitness or related indicators are measured, coupled with an update in molecular techniques used to analyse microbial functions. In addition, closer collaboration with conservation managers and practitioners from the inception of the project is needed to encourage meaningful application of microbiome knowledge in adaptive wildlife conservation management.

Species invading non-native habitats can cause irreversible environmental damage and economic harm. Yet, how introduced species become widespread invaders remains poorly understood. Adaptation within native-range habitats and rapid adaptation to new environments may both influence invasion success. Here, we examine these hypotheses using 7058 SNPs from 36 native, 40 introduced and 19 farmed populations of tench, a fish native to Eurasia. We examined genetic structure among these populations and accounted for long-term evolutionary history within the native range to assess whether introduced populations exhibited lower genetic diversity than native populations. Subsequent to infer genotype–environment correlations within native-range habitats, we assessed whether adaptation to native environments may have shaped the success of some introduced populations. At the broad scale, two glacial refugia contributed to the ancestry and genomic diversity of tench. However, native, introduced and farmed populations of admixed origin exhibited up to 10-fold more genetic diversity (i.e., observed heterozygosity, expected heterozygosity and allelic richness) compared to populations with predominantly single-source ancestry. The effects of introduction to a new location were also apparent as introduced populations exhibited fewer private alleles (mean = 9.9 and 18.9 private alleles in introduced and native populations, respectively) and higher population-specific Fst compared to native populations, highlighting their distinctiveness relative to the pool of allelic frequencies across tench populations. Finally, introduced populations with varying levels of genetic variation and similar genetic compositions have become established and persisted under strikingly different climatic and ecological conditions. Our results suggest that lack of prior adaptation and low genetic variation may not consistently hinder the success of introduced populations for species with a demonstrated ability to expand their native range.

Brook Trout (Salvelinus fontinalis) populations have experienced marked declines throughout their native range and are presently threatened due to isolation in small habitat fragments, land use changes, and climate change. The existence of numerous, spatially distinct populations poses substantial challenges for monitoring population status (e.g., abundance, recruitment, or occupancy). Genetic monitoring with estimates of effective number of breeders (N_b) provides a potentially powerful metric to complement existing population monitoring, assessment, and prioritization. We estimated N_b for 71 Brook Trout habitat units in mid-Atlantic region of the United States and obtained a mean N_b of 73.2 (range 6.90–493). Our modeling approach tested whether N_b estimates were sensitive to differences in habitat size, presence of non-native salmonids, base flow index, temperature, acidic precipitation, and indices of anthropogenic disturbance. We found significant support for three of our hypotheses including the positive influences of available habitat and base flow index and negative effect of temperature. Our results are consistent with presently observed and predicted future impacts of climate change on populations of this cold-water fish. Importantly, these findings support the use of N_b in population assessments as an index of relative population status.