Aleksandra Biedrzycka

Invasive species pose a major threat to ecosystems through habitat destruction, disease transmission and competition for resources. Invasion success depends on the adaptive potential (i.e. the ability to respond to selection pressures that is dependent on the levels of genetic variation) of the invading species. Here, we used reduced representation sequencing of native and European invasive raccoon populations to identify putatively adaptive changes across geographic regions. Our findings indicate that invasive raccoon populations experienced a genome-wide reduction in genetic diversity; however, we detected putative signatures of selection that could be related to local adaptation within the invasive range. Analysis of candidate loci, associated with either native or invasive populations, revealed putative parallel selection pressures between the invasive range and one of the native populations, all inhabiting similar climatic and habitat niches. In contrast, the native population from a different climatic region experienced distinct selective pressures. These results highlight the importance of habitat similarity in invasion processes. They demonstrate that, when predicting the potential range of an invasive species, it is not only the geographic distribution of the native range that should be considered, but also the specific characteristics of the habitat. Candidate genomic regions were linked to traits that promote rapid expansion, including reproduction, cognitive function, stress response, immunity and energy production. Overall, this study illuminates how contemporary selection in raccoons may accelerate the invasion process.

While microbiome associations are known to impact species survival, the extent to which microbiome variation aids in invasion dynamics is largely unknown. Here, we studied the microbiome diversity and composition of native and invasive raccoon populations to assess the microbiome’s role in invasion success. We found that native and invasive populations possess highly distinct microbiomes, with the invasive populations displaying greater gut and oral microbiota diversity without signs of instability or functional decline. Significant differences were found between the microbiota of each pair of invasive populations. The core microbiome of introduced populations consisted of a higher number of taxa than that found in native populations, suggesting a lack of microbiome deterioration in invasive populations. However, this may also reflect insufficient time for the establishment of a stable microbiome. Nevertheless, we found no evidence of reduced diversity of the microbiota linked to the population bottleneck or of increased microbiome dispersion indicating lower community stability. Native populations exhibited no microbiome differentiation between distant locations and showed lower, but still reasonably high, alpha diversity, suggesting the stability of the microbiome. Our findings imply that the invasion process changed the microbiota composition while preserving functional capability across different populations. This study highlights the microbiome as a potential factor aiding the adaptation of invasive populations.

Invasion biology aims to identify traits and mechanisms that contribute to successful invasions, while also providing general insights into the mechanisms underlying population expansion and adaptation to rapid climate and habitat changes. Certain phenotypic attributes have been linked to successful invasions, and the role of genetics has been critical in understanding adaptation of invasive species. Nevertheless, a comprehensive summary evaluating the most common evolutionary mechanisms associated with successful invasions across species and environments is still lacking. Here we present a systematic review of studies since 2015 that have applied genomic tools to investigate mechanisms of successful invasions across different organisms. We examine demographic patterns such as changes in genomic diversity at the population level, the presence of genetic bottlenecks and gene flow in the invasive range. We review mechanisms of adaptation such as selection from standing genetic variation and de novo mutations, hybridisation and introgression, all of which can have an impact on invasion success. This comprehensive review of recent articles on the genomic diversity of invasive species led to the creation of a searchable database to provide researchers with an accessible resource. Analysis of this database allowed quantitative assessment of demographic and adaptive mechanisms acting in invasive species. A predominant role of admixture in increasing levels of genetic diversity enabling molecular adaptation in novel habitats is the most important finding of our study. The “genetic paradox” of invasive species was not validated in genomic data across species and ecosystems. Even though the presence of genetic drift and bottlenecks is commonly reported upon invasion, a large reduction in genomic diversity is rarely observed. Any decrease in genetic diversity is often relatively mild and almost always restored via gene flow between different invasive populations. The fact that loci under selection are frequently detected suggests that adaptation to novel habitats on a molecular level is not hindered. The above findings are confirmed herein for the first time in a semi‐quantitative manner by molecular data. We also point to gaps and potential improvements in the design of studies of mechanisms driving rapid molecular adaptation in invasive populations. These include the scarcity of comprehensive studies that include sampling from multiple native and invasive populations, identification of invasion sources, longitudinal population sampling, and the integration of fitness measures into genomic analyses. We also note that the potential of whole genome studies is often not exploited fully in predicting invasive potential. Comparative genomic studies identifying genome features promoting invasions are underrepresented despite their potential for use as a tool in invasive species control.

Mitigating loss of genetic diversity is a major global biodiversity challenge^1–4. To meet recent international commitments to maintain genetic diversity within species^5,6, we need to understand relationships between threats, conservation management and genetic diversity change. Here we conduct a global analysis of genetic diversity change via meta-analysis of all available temporal measures of genetic diversity from more than three decades of research. We show that within-population genetic diversity is being lost over timescales likely to have been impacted by human activities, and that some conservation actions may mitigate this loss. Our dataset includes 628 species (animals, plants, fungi and chromists) across all terrestrial and most marine realms on Earth. Threats impacted two-thirds of the populations that we analysed, and less than half of the populations analysed received conservation management. Genetic diversity loss occurs globally and is a realistic prediction for many species, especially birds and mammals, in the face of threats such as land use change, disease, abiotic natural phenomena and harvesting or harassment. Conservation strategies designed to improve environmental conditions, increase population growth rates and introduce new individuals (for example, restoring connectivity or performing translocations) may maintain or even increase genetic diversity. Our findings underscore the urgent need for active, genetically informed conservation interventions to halt genetic diversity loss.

Understanding the evolutionary mechanisms behind invasion success enables predicting which alien species and populations are the most predisposed to become invasive. Parasites may mediate the success of biological invasions through their effect on host fitness. The evolution of increased competitive ability (EICA) hypothesis assumes that escape from parasites during the invasion process allows introduced species to decrease investment in immunity and allocate resources to dispersal and reproduction. Consequently, the selective pressure of parasites on host species in the invasive range should be relaxed. We used the case of the raccoon Procyon lotor invasion in Europe to investigate the effect of gastrointestinal pathogen pressure on non-MHC immune genetic diversity of newly established invasive populations. Despite distinct differences in parasite prevalence between analysed populations, we detected only marginal associations between two analysed SNPs and infection intensity. We argue that the differences in parasite prevalence are better explained by detected earlier associations with specific MHC-DRB alleles. While the escape from native parasites seems to allow decreased investment in overall immunity, which relaxes selective pressure imposed on immune genes, a wide range of MHC variants maintained in the invasive range may protect from newly encountered parasites.

Effective, evidence‐based management is required to ensure long‐term coexistence between people and wildlife in an increasingly humanized world. Although behavioural individuality is recognized as a key factor affecting evolutionary and ecological processes, it has rarely been explicitly assessed in relation to human–wildlife conflicts. The ‘problem individual’ paradigm states that some conspecifics within a given population have a disproportionately large contribution to conflicts. To the best of our knowledge, no studies have so far systematically tested this assumption in large carnivores. Here, we investigated the variation in conflict behaviour among brown bears Ursus arctos within the population inhabiting the Polish Eastern Carpathians. We inspected all sites notified as damaged by bears in 2014–2017 to determine the number and sex of the individuals involved. We conducted systematic noninvasive genetic sampling to estimate the size of the local population by spatially explicit capture–recapture models. We assessed the fraction and sex ratio of damage‐making bears in relation to the population, as well as the behavioural patterns by classifying and differentiating between occasional and repetitive damage‐makers. Approximately one‐third of the estimated 72 (95% CI 45.2–115.5) brown bears inhabiting the Polish Eastern Carpathians were responsible for damage occurrence in the region. The majority of damage‐makers were female (65% vs. 35% of male), which reflected the sex ratio of the local population (0.57). Thirty‐three per cent of the damage‐making bears (i.e. nine individuals) were classified as ‘problem individuals’, exhibiting repetitive conflict behaviour. Synthesis and applications. This study provides evidence of intraspecific differences in conflict behaviour in a large carnivore species, the brown bear, and indicates that damage‐making behaviour is not exhibited with the same frequency by all individuals within a population. Managers and policy‐makers should be aware that targeting individuals involved in conflicts without reference to the whole population may lead to misleading conclusions or an incomplete picture of the mechanisms underlying the conflicts, and thus, to mismanagement. Unravelling the behavioural patterns of individual engagement in damage through large‐scale and population‐wide studies is needed to accurately assess the magnitude of damage and enhance human–wildlife coexistence in areas experiencing conflicts.

Genetic monitoring of populations currently attracts interest in the context of the Convention on Biological Diversity but needs long-term planning and investments. Genetic diversity has been largely neglected in biodiversity monitoring, and when addressed is treated separately, detached from other conservation issues, such as habitat alteration due to climate change. Genetic monitoring supports the conservation and management of fisheries, game, and threatened populations. It also can contribute to the assessment of predicted and realized impacts of climate change, and their management. We report the first accounting of genetic monitoring efforts among countries in Europe (their ‘genetic monitoring capacity’, GMC) to determine where GMC suggests the combination of national infrastructure, political support and resources for continued and expanded monitoring. Overlaying GMC with areas where species ranges approach current and future climate niche limits (i.e., niche marginality) helps identify whether GMC coincides with anticipated climate change effects on biodiversity. Our analysis suggests that country area extent, financial resources, and conservation policy influence GMC, high values of which inconsistently match joint species patterns of climate niche marginality. Populations at niche margins likely hold genetic diversity that is important to adaptation to changing climate, and our results illuminate the need in Europe for expanded genetic monitoring across the climate gradients occupied by species, a need arguably greatest in southeastern European countries.

Rapid adaptation is common in invasive populations and is crucial to their long‐term success. The primary target of selection in the invasive species' new range is standing genetic variation. Therefore, genetic drift and natural selection acting on existing variation are key evolutionary processes through which invaders will evolve over a short timescale. In this study, we used the case of the raccoon Procyon lotor invasion in Europe to identify the forces shaping the diversity of immune genes during invasion. The genes involved in the defence against infection should be under intense selection pressure in the invasive range where novel pathogens are expected to occur. To disentangle the selective and demographic processes shaping the adaptive immune diversity of its invasive and expanding populations, we have developed species‐specific single‐nucleotide polymorphism markers located in the coding regions of targeted immune‐related genes. We characterised the genetic diversity of 110 functionally important immune genes in two invasive and one native raccoon genetic clusters, each presenting a different demographic history. Despite the strong effect of demographic processes in the invasive clusters, we detected a subset of genes exhibiting the diversity pattern suggestive of selection. The most likely process shaping the variation in those genes was balancing selection. The selected genes belong to toll‐like receptors and cytokine‐related genes. Our results suggest that the prevalence of selection depends on the level of diversity, that is – less genetically diverse invasive population from the Czech Republic displayed fewer signs of selection. Our results highlight the role of standing genetic variation in adapting to new environment. Understanding the evolutionary mechanisms behind invasion success would enable predicting how populations may respond to environmental change.

Editorial: Genomic basis of adaptations to new environments in expansive and invasive species

Aim: The aim of the study was to assess the effect of changes in population size and migration on variation in functional immunity genes in the previously bottlenecked population of the grey wolf, Canis lupus.Location: Eastern/Central Europe: Poland, Czechia, Slovakia.Methods: We genotyped 7 immunity genes: three MHC‐DLA genes (dog leukocyte antigen) and four Toll‐like receptor (TLR) genes among 130 wolves originating from three populations: two lowland (Baltic and Central European), and highland Carpathian. We contrasted the population structure in immunity genes with a neutral structure based on 13 microsatellites, and we analysed signatures of selection in the immunity loci.Results: We found high overall genetic variance in immunity genes and no evidence for decreased diversity in the recently established populations. The population structure in immunity loci was weak, with pairwise F_ST lower than for neutral markers. Although the results of neutrality tests were not significant, we identified codons under selection, both positive and negative.Main Conclusions: We demonstrated that despite recent population expansion which is expected to result in decreased genetic diversity, the diversity of immunity genes in the newly established wolf population is similar to those in the source population. This suggests that migrations do not cause allele loss in grey wolf. Signatures of selection on codon level, but not in tests using allele frequencies, suggest the contrasting effects of demography and selection.