# Evolutionary Applications

Online ISSN: 1752-4571
Print ISSN: 1752-4563
Discipline: Evolution
Aims and scope

Evolutionary Applications is a fully peer reviewed open access journal. It publishes papers that utilize concepts from evolutionary biology to address biological questions of health, social and economic relevance. Papers are expected to employ evolutionary concepts or methods to make contributions to areas such as (but not limited to): medicine, agriculture, forestry, exploitation and management (fisheries and wildlife), aquaculture, conservation biology, environmental sciences (including climate change and invasion biology), microbiology, and toxicology. All taxonomic groups are covered from microbes, fungi, plants and animals. In order to better serve the community, we also now strongly encourage submissions of papers making use of modern molecular and genetic methods (population and functional genomics, transcriptomics, proteomics, epigenetics, quantitative genetics, association and linkage mapping) to address important questions in any of these disciplines and in an applied evolutionary framework. Theoretical, empirical, synthesis or perspective papers are welcome.

## Editors

Recent publications
Diverse geographic, environmental, and ecological factors affect gene flow and adaptive genomic variation within species. With recent advances in landscape ecological modelling and high‐throughput DNA sequencing it is now possible to effectively quantify and partition their relative contributions. Here we use landscape genomics to identify determinants of genomic differentiation in the forest tent caterpillar, Malacosoma disstria, a widespread and irruptive pest of numerous deciduous tree species in North America. We collected larvae from multiple populations across eastern Canada, where the species experiences a diversity of environmental gradients and feeds on a number of different host tree species, including trembling aspen (Populus tremuloides), sugar maple (Acer saccharum), red oak (Quercus rubra), and white birch (Betula papyrifera). Using a combination of reciprocal causal modelling (RCM) and distance‐based redundancy analyses (dbRDA), we show that differentiation of thousands of genome‐wide single nucleotide polymorphisms (SNPs) among individuals is best explained by a combination of isolation by distance, isolation by environment (differences in summer temperatures and length of the growing season), and differences in host association. Configuration of suitable habitat inferred from ecological niche models was not significantly related to genomic differentiation, suggesting that M. disstria dispersal is agnostic with respect to habitat quality. Although population structure was not discretely related to host association, our modelling framework provides the first molecular evidence of host‐associated differentiation in M. disstria, congruent with previous documentation of reduced growth and survival of larvae moved between natal host species. We conclude that ecologically‐mediated selection is contributing to variation within M. disstria, and that divergent adaptation related to both environmental conditions and host association should be considered in ongoing research and management of this important forest pest.

Global climate change has threatened world crop production and food security. Decoding the adaptive genetic basis of wild relatives provides an invaluable genomic resource for climate-smart crop breedinG. Here, we performed whole-genome sequencing of 185 diverse wild soybean (Glycine soja) accessions collected from three major agro-ecological zones in China to parse the genomic basis of local adaptation in wild soybean. The population genomic diversity pattern exhibited clear agro-ecological zone-based population structure, and multiple environmental factors were observed to contribute to the genetic divergence. Demographic analysis shows that wild soybeans from the three ecological zones diverged about 1 × 105 years ago, and then the effective population sizes have undergone different degrees of expansions. Genome-environment association identified multiple genes involved in the local adaptation, such as flowering time and temperature-related genes. A locus containing two adjacent MADS-box transcription factors on chromosome 19 was identified for multiple environmental factors, and it experienced positive selection that enables the adaptation to high-latitude environment. This study provides insights into the genetic mechanism of ecological adaptation in wild soybean that may facilitate climate-resilient soybean breeding.

Understanding patterns of genetic structure and adaptive variation in natural populations is crucial for informing conservation and management. Past genetic research using 11 microsatellite loci identified six genetic stocks of lake whitefish (Coregonus clupeaformis) within Lake Michigan, USA. However, ambiguity in genetic stock assignments suggested those neutral microsatellite markers did not provide adequate power for delineating lake whitefish stocks in this system, prompting calls for a genomics approach to investigate stock structure. Here, we generated a dense genomic dataset to characterize population structure and investigate patterns of neutral and adaptive genetic diversity among lake whitefish populations in Lake Michigan. Using Rapture sequencing, we genotyped 829 individuals collected from 17 baseline populations at 197,588 SNP markers after quality filtering. Although the overall pattern of genetic structure was similar to the previous microsatellite study, our genomic data provided several novel insights. Our results indicated a large genetic break between the northwestern and eastern sides of Lake Michigan, and we found a much greater level of population structure on the eastern side compared to the northwestern side. Collectively, we observed five genomic islands of adaptive divergence on five different chromosomes. Each island displayed a different pattern of population structure, suggesting that combinations of genotypes at these adaptive regions are facilitating local adaptation to spatially heterogenous selection pressures. Additionally, we identified a large linkage disequilibrium block of ~8.5 Mb on chromosome 20 that is suggestive of a putative inversion but with a low frequency of the minor haplotype. Our study provides a comprehensive assessment of population structure and adaptive variation that can help inform management of Lake Michigan’s lake whitefish fishery and highlights the utility of incorporating adaptive loci into fisheries management.

Two opposing models currently dominate Near Eastern plant domestication research. The core area‐one event model depicts a knowledge‐based, conscious, geographically centered, rapid single‐event domestication, while the protracted‐autonomous model emphasizes a non‐centered, millennia‐long process based on unconscious dynamics. The latter model relies, in part, on quantitative depictions of diachronic changes (in archaeological remains) in proportions of spikelet shattering to non‐shattering, towards full dominance of the non‐shattering (domesticated) phenotypes in cultivated cereal populations. Recent wild wheat genome assembly suggests that shattering and non‐shattering spikelets may originate from the same (individual) genotype. Therefore, their proportions among archaeobotanical assemblages cannot reliably describe the presumed protracted‐selection dynamics underlying wheat domestication. This calls for a reappraisal of the ‘domestication syndrome’ concept associated with cereal domestication.

Sustainable management of exploited populations benefits from integrating demographic and genetic considerations into assessments, as both play a role in determining harvest yields and population persistence. This is especially important in populations subject to size‐selective harvest, because size selective harvesting has the potential to result in significant demographic, life‐history, and genetic changes. We investigated harvest‐induced changes in the effective number of breeders (N̂b$${\hat{N}}_b$$) for introduced brook trout populations (Salvelinus fontinalis) in alpine lakes from western Canada. Three populations were subject to 3 years of size‐selective harvesting, while three control populations experienced no harvest. The N̂c$${\hat{N}}_c$$ decreased consistently across all harvested populations (on average 60.8%) but fluctuated in control populations. There were no consistent changes in N̂b$${\hat{N}}_b$$ between control or harvest populations, but one harvest population experienced a decrease in N̂b$${\hat{N}}_b$$ of 63.2%. The N̂b$${\hat{N}}_b$$/N̂c$${\hat{N}}_c$$ ratio increased consistently across harvest lakes; however we found no evidence of genetic compensation (where variance in reproductive success decreases at lower abundance) based on changes in family evenness (FÊ$$\hat{FE}$$) and the number of full‐sibling families (N̂fam$${\hat{N}}_{fam}$$). We found no relationship between FÊ$$\hat{FE}$$ and N̂c$${\hat{N}}_c$$ or between N̂fam$${\hat{N}}_{fam}$$/N̂c$${\hat{N}}_c$$ and FÊ$$\hat{FE}$$. We posit that change in N̂b$${\hat{N}}_b$$ was buffered by constraints on breeding habitat prior to harvest, such that the same number of breeding sites were occupied before and after harvest. These results suggest that effective size in harvested populations may be resilient to considerable changes in Nc in the short‐term, but it is still important to monitor exploited populations to assess the risk of inbreeding and ensure their long‐term survival.

For hundreds of years, the color diversity of Mollusca shells has been a topic of interest for humanity. However, the genetic control underlying color expression is still poorly understood in mollusks. The pearl oyster Pinctada margaritifera is increasingly becoming a biological model to study this process due to its ability to produce a large range of colors. Previous breeding experiments demonstrated that color phenotypes were partly under genetic control, and while a few genes were found in comparative transcriptomics and epigenetic experiments, genetic variants associated to the phenotypes have not yet been investigated. Here, we used a pooled‐sequencing approach on 172 individuals to investigate color‐associated variants on three color phenotypes of economic interest for pearl farming, in three wild and one hatchery populations. While our results uncovered SNPs targeting pigment‐related genes already identified in previous studies, such as PBGD, tyrosinases, GST, or FECH, we also identified new color‐related genes occurring in the same pathways, like CYP4F8, CYP3A4 and CYP2R1. Moreover, we identified new genes involved in novel pathways unknown to be involved in shell coloration for P. margaritifera, like the carotenoid pathway, BCO1. These findings are essential to possibly implement future breeding programs focused on individual selection for specific color production in pearl oysters and improve the footprint of perliculture on Polynesian lagoon by producing less, but with a better quality.

The current extinction crisis requires effective assessment and monitoring tools. Genetic approaches are appealing given the relative ease of field sampling required to estimate genetic diversity characteristics assumed related to population size, evolutionary potential, and extinction risk, and to evaluate hybridization with non‐native species simultaneously. However, linkages between population genetic metrics of diversity from survey‐style field collections and demographic estimates of population size and extinction risk are still in need of empirical examples, especially for remotely distributed species of conservation concern where the approach might be most beneficial. We capitalized on an exceptional opportunity to evaluate congruence between genetic diversity metrics and demographic‐based estimates of abundance and extinction risk from a comprehensive Multiple Population Viability Analysis (MPVA) in a threatened fish, the Lahontan cutthroat trout (LCT). We sequenced non‐native trout reference samples and recently collected and archived tissue samples of most remaining populations of LCT (N=60) and estimated common genetic assessment metrics, predicting minimal hybridization with non‐native trout, low diversity, and declining diversity over time. We further hypothesized genetic metrics would correlate positively with MPVA‐estimated abundance and negatively with extinction probability. We uncovered several instances of hybridization that pointed to immediate management needs. After removing hybridized individuals, cautious interpretation of low effective population sizes (2‐63) suggested reduced evolutionary potential for many LCT populations. Other genetic metrics did not decline over time nor correlate with MPVA‐based estimates of harmonic mean abundance or 30‐year extinction probability. Our results demonstrate benefits of genetic monitoring for efficiently detecting hybridization and, though genetic results were disconnected from demographic assessment of conservation status, they suggest reduced evolutionary potential and likely a higher conservation risk than currently recognized for this threatened fish. We emphasize that genetic information provides essential complementary insight, in addition to demographic information, for evaluating species status.

Estimating the demographic parameters of contemporary populations is essential to the success of elasmobranch conservation programmes, and to understanding their recent evolutionary history. For benthic elasmobranchs such as skates, traditional fisheries-independent approaches are often unsuitable as the data may be subject to various sources of bias, whilst low recapture rates can render mark-recapture programmes ineffectual. Close-kin mark-recapture (CKMR), a novel demographic modelling approach based on the genetic identification of close relatives within a sample, represents a promising alternative approach as it does not require physical recaptures. We evaluated the suitability of CKMR as a demographic modelling tool for the critically endangered blue skate (Dipturus batis) in the Celtic Sea using samples collected during fisheries-dependent trammel-net surveys that ran from 2011 to 2017. We identified three full-sibling and 16 half-sibling pairs among 662 skates, which were genotyped across 6,291 genome-wide single nucleotide polymorphisms (SNPs), 15 of which were cross-cohort half-sibling pairs that were included in a CKMR model. Despite limitations owing to a lack of validated life-history trait parameters for the species, we produced the first estimates of adult breeding abundance, population growth rate, and annual adult survival rate for D. batis in the Celtic Sea. The results were compared to estimates of genetic diversity, effective population size (Ne), and to catch per unit effort (CPUE) estimates from the trammel-net survey. Although each method was characterised by wide uncertainty bounds, together they suggested a stable population size across the time-series. Recommendations for the implementation of CKMR as a conservation tool for data-limited elasmobranchs are discussed. In addition, the spatio-temporal distribution of the 19 sibling pairs revealed a pattern of site-fidelity in D. batis, and supported field observations suggesting an area of critical habitat that could qualify for protection might occur near the Isles of Scilly.

Outcrossing can be advantageous in a changing environment because it promotes the purge of deleterious mutations and increases the genetic diversity within a population, which may improve population persistence and evolutionary potential. Some species may therefore switch their reproductive mode from inbreeding to outcrossing when under environmental stress. This switch may have consequences on the demographic dynamics and evolutionary trajectory of populations. For example, it may directly influence the sex ratio of a population. However, much remains to be discovered about the mechanisms and evolutionary implications of sex ratio changes in a population in response to environmental stress. Populations of the androdioecious nematode Caenorhabditis elegans, are composed of selfing hermaphrodites and rare males. Here we investigate the changes in sex ratio of C. elegans populations exposed to radioactive pollution for 60 days or around 20 generations. We experimentally exposed populations to three levels of ionizing radiation (i.e. 0 mGy.h‐1, 1.4 mGy.h‐1, and 50 mGy.h‐1). We then performed reciprocal transplant experiments to evaluate genetic divergence between populations submitted to different treatments. Finally, we used a mathematical model to examine the evolutionary mechanisms that could be responsible for the change in sex ratio. Our results showed an increase in male frequency in irradiated populations, and this effect increased with the dose rate. The model showed that an increase in male fertilization success or a decrease in hermaphrodite self‐fertilization could explain this increase in the frequency of males. Moreover, males persisted in populations after transplant back into the control conditions. These results suggested selection favoring outcrossing under irradiation conditions. This study shows that ionizing radiation can sustainably alter the reproductive strategy of a population, likely impacting its long‐term evolutionary history. This study highlights the need to evaluate the impact of pollutants on the reproductive strategies of populations when assessing the ecological risks.

Assigning individuals to their source populations is crucial for conservation research, especially for endangered species threatened by illegal trade and translocations. Genetic assignment can be achieved with different types of molecular markers, but technical advantages and cost saving are recently promoting the shift from short tandem repeats (STRs) to single nucleotide polymorphisms (SNPs). Here, we designed, developed, and tested a small panel of SNPs for cost‐effective geographic assignment of individuals with unknown origin of the endangered Mediterranean tortoise Testudo hermanni. We started by performing a ddRAD‐seq experiment on 70 wild individuals of T. hermanni from 38 locations. Results obtained using 3,182 SNPs are comparable to those previously obtained using STR markers in terms of genetic structure and power to identify the macro‐area of origin. However, our SNPs revealed further insights into the substructure in Western populations, especially in Southern Italy. A small panel of highly informative SNPs was then selected and tested by genotyping 190 individuals using the KASP genotyping chemistry. All the samples from wild populations of known geographic origin were genetically re‐assigned with high accuracy to the original population. This reduced SNPs panel represents an efficient molecular tool that enables individuals to be genotyped at low cost (less than €15 per sample) for geographical assignment and identification of hybrids. This information is crucial for the management in‐situ of confiscated animals and their possible re‐allocation in the wild. Our methodological pipeline can easily be extended to other species.

Molecular epidemiology studies are essential to refine our understanding of migrations of phytopathogenic bacteria, the major determining factor in their emergence, and to understand the factors that shape their population structure. Microsatellite and minisatellite typing are useful techniques for deciphering the population structure of Xanthomonas citri pv. citri, the causal agent of Asiatic citrus canker. This paper presents a molecular epidemiology study, which has improved our understanding of the history of the pathogen’s introductions into the Arabian Peninsula, since it was first reported in the 1980s. An unexpectedly high genetic diversity of the pathogen was revealed. The four distinct genetic lineages within X. citri pv. citri, which have been reported throughout the world, were identified in the Arabian Peninsula, most likely as the result of multiple introductions. No copper‐resistant X. citri pv. citri strains were identified. The pathogen’s population structure on Mexican lime (their shared host species) was closely examined in two countries, Saudi Arabia and Yemen. We highlighted the marked prevalence of specialist pathotype A* strains in both countries, which suggests that specialist strains of X. citri pv. citri may perform better than generalist strains when they occur concomitantly in this environment. Subclade 4.2 was the prevailing lineage identified. Several analyses (genetic structure deciphered by discriminant analysis of principal components, RST‐based genetic differentiation, geographic structure) congruently suggested the role of human activities in the pathogen’s spread. We discuss the implications of these results on the management of Asiatic citrus canker in the region.

Obtaining dispersal estimates for a species is key to understanding local adaptation and population dynamics, and to implementing conservation actions. Genetic isolation‐by‐distance patterns can be used for estimating dispersal, and these patterns are especially useful for marine species in which few other methods are available. In this study, we genotyped coral reef fish (Amphiprion biaculeatus) at 16 microsatellite loci across 8 sites across 210 km in the central Philippines to generate fine‐scale estimates of dispersal. All sites except for one followed isolation‐by‐distance patterns. Using isolation‐by‐distance theory, we estimated a larval dispersal kernel spread of 8.9 km (95% confidence interval of 2.3‐18.4 km). Genetic distance to the remaining site correlated strongly with the inverse probability of larval dispersal from an oceanographic model. Ocean currents were a better explanation for genetic distance at large spatial extents (sites greater than 150 km apart), while geographic distance remained the best explanation for spatial extents less than 150 km. Our study demonstrates the utility of combining isolation‐by‐distance patterns with oceanographic simulations to understand connectivity in marine environments and to guide marine conservation strategies.

Gene flow between wild and domestic populations has been repeatedly demonstrated across a diverse range of taxa. Ultimately, the genetic impacts of gene flow from domestic into wild populations depends both on the degree of domestication and the original source of the domesticated population. Atlantic Salmon, Salmo salar, used in North American aquaculture are ostensibly of North American origin. However, evidence of European introgression into North American aquaculture salmon has accumulated in recent decades, even though the use of diploid European salmon has never been approved in Canada. The full extent of such introgression as well as the potential impacts on wild salmon in the Northwest Atlantic remains uncertain. Here, we extend previous work comparing North American and European wild salmon (n=5799) using a 220K SNP array to quantify levels of recent European introgression into samples of domestic salmon, aquaculture escapees, and wild salmon collected throughout Atlantic Canada. Analysis of North American farmed salmon (n=403) and escapees (n=289) displayed significantly elevated levels of European ancestry by comparison with wild individuals (p<0.001). Of North American farmed salmon sampled between 2011 and 2018, ~17% had more than 10% European ancestry and several individuals exceeded 40% European ancestry. Samples of escaped farmed salmon similarly displayed elevated levels of European ancestry, with two individuals classified as 100% European. Analysis of juvenile salmon collected in rivers proximate to aquaculture locations also revealed evidence of elevated European ancestry and larger admixture tract in comparison to individuals collected at distance from aquaculture. Overall, our results demonstrate that even though diploid European salmon have never been approved for use in Canada, individuals of full and partial European ancestry have been in use over the last decade, and that some of these individuals have escaped and hybridized in the wild.

Identifying areas of high evolutionary potential is a judicious strategy for developing conservation priorities in the face of environmental change. For wide‐ranging species occupying heterogeneous environments, the evolutionary forces that shape distinct populations can vary spatially. Here, we investigate patterns of genomic variation and genotype‐environment associations in the hermit thrush (Catharus guttatus), a North American songbird, at broad (across the breeding range) and narrow spatial scales (at a hybrid zone). We begin by building a genoscape or map of genetic variation across the breeding range and find five distinct genetic clusters within the species, with the greatest variation occurring in the western portion of the range. Genotype‐environment association analyses indicate higher allelic turnover in the west compared to the east, with measures of temperature surfacing as key predictors of putative adaptive genomic variation rangewide. Since broad patterns detected across a species’ range represent the aggregate of many locally adapted populations, we investigate whether our broadscale analysis is consistent with a finer scale analysis. We find that top rangewide temperature‐associated loci vary in their clinal patterns (e.g., steep clines vs. fixed allele frequencies) across a hybrid zone in British Columbia, suggesting that the environmental predictors and the associated candidate loci identified in the rangewide analysis are of variable importance in this particular region. However, two candidate loci exhibit strong concordance with the temperature gradient in British Columbia, suggesting a potential role for temperature‐related barriers to gene flow and/or temperature‐driven ecological selection in maintaining putative local adaptation. This study demonstrates how the patterns identified at the broad (macrogeographic) scale can be validated by investigating genotype‐environment correlations at the local (microgeographic) scale. Further, our results highlight the importance of considering the spatial distribution of putative adaptive variation when assessing population‐level sensitivity to climate change and other stressors.

Western redcedar (WRC) is an ecologically and economically important forest tree species characterized by low genetic diversity with high self‐compatibility and high heartwood durability. Using sequence capture genotyping of target genic and non‐genic regions, we genotyped 44 parent trees and 1520 offspring trees representing 26 polycross (PX) families collected from three progeny test sites using 45,378 SNPs. Trees were phenotyped for eight traits related to growth, heartwood and foliar chemistry associated with wood durability and deer browse resistance. We used the genomic realized relationship matrix for paternity assignment, maternal pedigree correction, and to estimate genetic parameters. We compared genomics‐based (GBLUP) and two pedigree‐based (ABLUP: polycross and reconstructed full‐sib (FS) pedigrees) models. Models were extended to estimate dominance genetic effects. Pedigree reconstruction revealed significant unequal male contribution and separated the 26 PX families into 438 FS families. Traditional maternal PX pedigree analysis resulted in up to 51% overestimation in genetic gain and 44% in diversity. Genomic analysis resulted in up to 22% improvement in offspring breeding value (BV) theoretical accuracy, 35% increase in expected genetic gain for forward selection, and doubled selection intensity for backward selection. Overall, all traits showed low to moderate heritability (0.09–0.28), moderate genotype by environment interaction (type‐B genetic correlation: 0.51–0.80), low to high expected genetic gain (6.01–55%), and no significant negative genetic correlation reflecting no large trade‐offs for multi‐trait selection. Only three traits showed significant dominance effect. GBLUP resulted in smaller but more accurate heritability estimates for five traits, but larger estimates for the wood traits. Comparison between all, genic‐coding, genic‐non‐coding and intergenic SNPs showed little difference in genetic estimates. In summary, we show that GBLUP overcomes the PX limitations, successfully captures expected historical and hidden relatedness as well as linkage disequilibrium (LD), and results in increased breeding efficiency in WRC.

The European flat oyster (Ostrea edulis L.) is a bivalve naturally distributed across Europe that was an integral part of human diets for centuries, until anthropogenic activities and disease outbreaks severely reduced wild populations. Despite a growing interest in genetic applications to support population management and aquaculture, a reference genome for this species is lacking to date. Here we report a chromosome‐level assembly and annotation for the European Flat oyster genome, generated using Oxford Nanopore, Illumina, Dovetail OmniCTM proximity ligation and RNA sequencing. A contig assembly (N50: 2.38Mb) was scaffolded into the expected karyotype of 10 pseudo‐chromosomes. The final assembly is 935.13 Mb, with a scaffold‐N50 of 95.56 Mb, with a predicted repeat landscape dominated by unclassified elements specific to O. edulis. The assembly was verified for accuracy and completeness using multiple approaches, including a novel linkage map built with ddRAD‐Seq technology, comprising 4,016 SNPs from four full‐sib families (8 parents and 163 F1 offspring). Annotation of the genome integrating multi‐tissue transcriptome data, comparative protein evidence and ab‐initio gene prediction identified 35,699 protein‐coding genes. Chromosome level synteny was demonstrated against multiple high‐quality bivalve genome assemblies, including an O. edulis genome generated independently for a French O. edulis individual. Comparative genomics was used to characterize gene family expansions during Ostrea evolution that potentially facilitated adaptation. This new reference genome for European flat oyster will enable high‐resolution genomics in support of conservation and aquaculture initiatives, and improves our understanding of bivalve genome evolution.

The characterization and preservation of genetic variation in crops is critical to meeting the challenges of breeding in the face of changing climates and markets. In recent years the use of Single Nucleotide Polymorphisms (SNPs) has become routine, allowing to understand the population structure, find divergent lines for crosses, and illuminate the origin of crops. However, the focus on SNPs overlooks other forms of variation, such as Copy Number Variation (CNVs). Lentil is the third most important cold‐season legume and was domesticated in the Fertile Crescent. We genotyped 324 accessions that represent its global diversity and using both SNPs and CNVs we dissected the population structure, genetic variation, and identified candidate genes.k.bett@usask.ca Eight clusters were detected, most of them located in or near the Fertile Crescent, even though different clusters were present in distinct regions. The cluster from South Asia was particularly differentiated and presented low diversity, contrasting with the clusters from the Mediterranean and the northern temperate. Accessions from North America were mainly assigned to one cluster and were highly diverse, reflecting the efforts of breeding programs to integrate variation. Thirty‐three genes were identified as candidates under selection and among their functions were sporopollenin synthesis in pollen, a component of chlorophyll B reductase that partially determines the antenna size, and two genes related to the import system of chloroplasts. Eleven percent of all lentil genes, and 21% of lentil disease resistance genes, were affected by CNVs. The gene categories overrepresented in these genes were ‘Enzymes’, ‘Cell Wall Organization’ and ‘External Stimuli Response’. All the genes found in the latter were associated with pathogen response. CNVs provided information about population structure and might have played a role in adaptation. The incorporation of CNVs in diversity studies is needed for a broader understanding of how they evolve and contribute to domestication.

This volume of Evolutionary Applications sees the publication of two genomes for the European native flat oyster Ostrea edulis, a species of significant evolutionary, ecological and commercial value. Each is a highly contiguous chromosome‐level assembly from individuals of different genetic backgrounds, which have been benchmarked against one another. This situation has resulted from the serendipitous discovery that two independent research groups were both deep into the process of building, annotating and investigating separately produced assemblies. Due to constraints with funder requirements and the need to recognize early career researchers for their work, alongside the technical challenge of integrating assemblies from two very different genomes, there was limited capacity to merge the sequences into one publication at the stage of discovery. This issue is likely to become very common over the next few years until the technologies for working with multiple genomes at once, for example, graph genomes, become commonplace in nonmodel species. Consequently, both of our teams have decided to collaborate rather than compete, recognizing the benefit to copublishing two separate genome resources for the research community, each with distinct scientific investigations, and working collaboratively to benchmark the assemblies.

Dramatic phenotypic differences between domestic pigs and wild boars (Sus scrofa) provide opportunities to investigate molecular mechanisms underlying the formation of complex traits, including morphology, physiology, and behaviour. Most studies comparing domestic pigs and wild boars have focused on variations in DNA sequences and mRNA expression, but not on epigenetic changes. Here, we present a genome‐wide comparative study on H3K27ac enhancer activities and the corresponding mRNA profiling in the brain and liver tissues of adult Bama Xiang pigs (BMXs) and Chinese wild boars (CWBs). We identified a total of 1,29,487 potential regulatory elements, among which 11,241 H3K27ac peaks showed differential activity between CWBs and BMXs in at least one tissue. These peaks were overrepresented by binding motifs of FOXA1, JunB, ATF3, and BATF, and overlapped with differentially expressed genes that are involved in female mating behaviour, response to growth factors and hormones, and lipid metabolism. We also identified 4,118 non‐redundant super‐enhancers from ChIP‐seq data on H3K27ac. Notably, we identified differentially active peaks located close to or within candidate genes, including TBX19, MSTN, AHR, and P2RY1, which were identified in DNA sequence‐based population differentiation studies. This study generates a valuable dataset on H3K27ac profiles of the brain and liver from domestic pigs and wild boars, which helps gain insights into the changes in enhancer activities from wild boars to domestic pigs.

Although all marine ecosystems have experienced global‐scale losses, oyster reefs have shown the greatest. Therefore, substantial efforts have been dedicated to restoration of such ecosystems during the last two decades. In Europe, several pilot projects for the restoration of the native European flat oyster, Ostrea edulis, recently begun and recommendations to preserve genetic diversity and to conduct monitoring protocols have been made. In particular, an initial step is to test for genetic differentiation against homogeneity among the oyster populations potentially involved in such programs. Therefore we conducted a new sampling of wild populations at the European scale and a new genetic analysis with 203 markers to (1) confirm and study in more detail the pattern of genetic differentiation between Atlantic and Mediterranean populations, (2) identify potential translocations that could be due to aquaculture practices, (3) investigate the populations at the fringe of the geographical range, since they seemed related despite their geographic distance. Such information should be useful to enlighten the choice of the animals to be translocated or reproduced in hatcheries for further restocking. After the confirmation of the general geographical pattern of genetic structure and the identification of one potential case of aquaculture transfer at a large scale, we were able to detect genomic islands of differentiation mainly in the form of two groups of linked markers, which could indicate the presence of polymorphic chromosomal rearrangements. Furthermore, we observed a tendency for these two islands and the most differentiated loci to show a parallel pattern of differentiation, grouping the North Sea populations with the Eastern Mediterranean and Black Sea populations, against geography. We discussed the hypothesis that this genetic parallelism could be the sign of a shared evolutionary history of the two groups of populations despite them being at the border of the distribution nowadays.

Many coral reef fishes display remarkable genetic and phenotypic variation across their geographic ranges. Understanding how historical and contemporary processes have shaped these patterns remains a focal question in evolutionary biology, since they reveal how diversity is generated and how it may respond to future environmental change. Here we compare the population genomics and demographic histories of a commercially and ecologically important coral reef fish, the common coral grouper (Plectropomus leopardus [Lacépède 1802]), across two adjoining regions (the Great Barrier Reef; GBR, and the Coral Sea, Australia) spanning approximately 14 degrees of latitude and 9 degrees of longitude. We analysed 4,548 single nucleotide polymorphism (SNP) markers across 11 sites and show that genetic connectivity between regions is low, despite their relative proximity (~ 100 km) and an absence of any obvious geographic barrier. Inferred demographic histories using 10,479 markers suggest that the Coral Sea population was founded by a small number of GBR individuals and that divergence occurred ~ 190 kya under a model of isolation with asymmetric migration. We detected population expansions in both regions, but estimates of contemporary effective population sizes were approximately 50 % smaller in Coral Sea sites, which also had lower genetic diversity. Our results suggest that P. leopardus in the Coral Sea have experienced a long period of isolation that precedes the recent glacial period (~ 10 – 120 kya) and may be vulnerable to localised disturbances due to their relative reliance on local larval replenishment. While it is difficult to determine the underlying events that led to the divergence of Coral Sea and GBR lineages, we show that even geographically proximate populations of a widely dispersed coral reef fish can have vastly different evolutionary histories.

Biological invasions offer a unique opportunity to investigate evolution over contemporary time‐scales. Rapid adaptation to local climates during range expansion can be a major determinant of invasion success, yet fundamental questions remain about its genetic basis. This study sought to investigate the genetic basis of climate adaptation in invasive common ragweed (Ambrosia artemisiifolia). Flowering time adaptation is key to this annual species’ invasion success, so much so that it has evolved repeated latitudinal clines in size and phenology across its native and introduced ranges despite high gene flow among populations. Here, we produced a high‐density linkage map (4,493 SNPs) and paired this with phenotypic data from an F2 mapping population (n=336) to identify one major and two minor quantitative trait loci (QTL) underlying flowering time and height differentiation in this species. Within each QTL interval, several candidate flowering time genes were also identified. Notably, the major flowering time QTL detected in this study was found to overlap with a previously identified haploblock (putative inversion). Multiple genetic maps of this region identified evidence of suppressed recombination in specific genotypes, consistent with inversions. These discoveries support the expectation that a concentrated genetic architecture with fewer, larger and more tightly‐linked alleles should underlie rapid local adaptation during invasion, particularly when divergently‐adapting populations experience high‐levels of gene flow.

Reconstructing the dispersal routes of pathogens can help identify the key drivers of their evolution and provides a basis for disease control. The cereal cyst nematode Heterodera avenae is one of the major nematode pests on cereals that can cause 10–90% crop yield losses worldwide. Through extensive sampling on wheat and grasses, the Chinese population of H. avenae is widely identified in virtually all wheat growing regions in China, with H1 being the predominant haplotype. The monoculture of wheat in north China might have been the key driver for the prevalence of H1 population, which should date no earlier than the Han Dynasty (202 BCE–220 CE). Molecular phylogenetic and biogeographic analyses of Chinese H. avenae suggest a Pleistocene northwest China origin and an ancestral host of grasses. We assume the prosperity of Heterodera in this region is a result of their favor cooler climate and various grass hosts, which only appeared after the uplift of Qinghai‐Tibetan Plateau and aridification of Inner Asia. Nematode samples from the current and historical floodplains show a significant role of the Yellow River in the distribution of Chinese H. avenae. Whereas mechanical harvesters that operate on an inter‐provincial basis suggest the importance in the transmission of this species in eastern China in recent times. This study highlights the role of environmental change, river dynamics, and anthropogenic factors in the origin and long‐distance dissemination of pathogens.

Stock structure is of paramount importance for sustainable management of exploited resources. In that context, genetic markers have been used for more than two decades to resolve spatial structure of marine exploited resources and to fully fathom stock dynamics and interactions. While genetic markers such as allozymes and RFLP dominated the debate in the early era of genetics, technology advances have provided scientists with new tools every decade to better assess stock discrimination and interactions (i.e. gene flow). Here, we provide a review of genetic studies performed to understand stock structure of Atlantic cod in Icelandic waters, from the early allozyme approaches to the genomic work currently carried out. We further highlight the importance of the generation of a chromosome anchored genome assembly together with whole‐genome population data, which drastically changed our perception of the possible management units to consider. After nearly 60 years of genetic investigation of Atlantic cod structure in Icelandic waters, genetic (and later genomic) data combined with behavioural monitoring using Data Storage Tags (DSTs) shifted the attention from geographical population structures to behavioural ecotypes. This review also demonstrates the need for future research to further disentangle the impact of these ecotypes (and gene flow among them) on the population structure of Atlantic cod in Icelandic waters. It also highlights the importance of whole‐genome data to unravel unexpected within‐species diversity related to chromosomal inversions and associated supergenes, which are important to consider for future development of sustainable management programmes of the species within the North Atlantic.

Our experimental work illustrates how microbial ecosystems can be shaped by selective pressures over long‐term ecological time scales. Natural microbial ecosystems generally consist of various co‐existing species, where community composition describes the frequency at which species or types are present. Overall functionality of the system is achieved by interacting species. Upon short‐term selection, for instance by transfer to a novel environment, community composition and functionality may change in a process referred to as species sorting. Various factors, such as initial community composition and selective pressures from the environment, may influence this change. Mabisi is a traditional fermented food from Zambia that naturally contains a bacterial community of around twenty unique bacterial types. We used six comparable but different natural bacterial Mabisi communities, each split into five identical replicates, for 16 propagation cycles in a novel, common laboratory environment. Composition of the bacterial communities changed upon propagation. The influence of four main factors on community composition, i.e. initial composition (history), impact of the environment (adaptation), changes due to interaction between species, and random processes (chance) in species dynamics, was tested using maximum likelihood ratios. Initial community composition seemed to determine the change in community composition, followed by random processes. Interestingly, we observed convergence at the level of ecosystem functionality, which was measured as profiles of metabolic output. This suggests different combinations of species or types can achieve similar eco‐system functionality.

By applying morphological and molecular data on two genera of the nudibranch molluscs it is shown that the tension between taxonomic practice and evolutionary processes persists. A review of the related genera Catriona and Tenellia is used to demonstrate that the fine‐scale taxonomic differentiation is an important tool in the integration of morphological and molecular data. This is highlighted by the hidden species problem and provides strong argument that the genus must be kept as a maximally narrowly‐defined entity. Otherwise, we are forced to compare a highly disparate species under the putatively lumped name “Tenellia”. We demonstrate this in the present study by applying a suite of delimitation methods and describing a new species of Tenellia from the Baltic Sea. The new species possesses fine‐scale morphological distinguishing features, which were not investigated before. The true, narrowly defined genus Tenellia represents a peculiar taxon with a clearly expressed paedomorphic characters and predominantly brackish‐water habitats. The phylogenetically related genus Catriona, of which three new species are described here, clearly demonstrates different features. A lumping decision to call many morphologically and evolutionary different taxa as “Tenellia” will downgrade the taxonomic and phylogenetic resolution of the entire family Trinchesiidae to just a single genus. The dissolution of the dilemma of “lumpers & splitters”, which still significantly affects taxonomy, will further help to make systematics a true evolutionary discipline.

Habitat fragmentation impacts the distribution of genetic diversity and population genetic structure. Therefore protecting the evolutionary potential of species, especially in the context of the current rate of human‐induced environmental change, is an important goal. In riverine ecosystems, migration barriers affect the genetic structure of native species, while also influencing the spread of invasive species. In this study, we compare genetic patterns of two native and one highly invasive riverine fish species in a Belgian river basin, namely the native three‐spined stickleback (Gasterosteus aculeatus) and stone loach (Barbatula barbatula), and the non‐native and invasive topmouth gudgeon (Pseudorasbora parva). We aimed to characterize both natural and anthropogenic determinants of genetic diversity and population genetic connectivity. Genetic diversity was highest in topmouth gudgeon followed by stone loach and three‐spined stickleback. The correlation between downstream distance and genetic diversity, a pattern often observed in riverine systems, was only marginally significant in stone loach and three‐spined stickleback, while genetic diversity strongly declined with increasing number of barriers in topmouth gudgeon. An Isolation‐By‐Distance pattern characterizes the population genetic structure of each species. Population differentiation was only associated with migration barriers in the invasive topmouth gudgeon, while genetic composition of all species seemed at least partially determined by the presence of migration barriers. Among the six barrier types considered (watermills, sluices, tunnels, weirs, riverbed obstructions, and others), the presence of watermills was the strongest driver of genetic structure and composition. Our results indicate that conservation and restoration actions, focusing on conserving genetic patterns, cannot be generalized across species. Moreover, measures might target either on restoring connectivity, while risking a rapid spread of the invasive topmouth gudgeon, or not restoring connectivity, while risking native species extinction in upstream populations.

The European flat oyster (Ostrea edulis L.) is a native bivalve of the European coasts. Harvest of this species has declined during the last decades, because of the appearance of two parasites that have led to the collapse of the stocks and the loss of the natural oyster beds. O. edulis has been the subject of numerous studies and programs in population genetics and on the presence of the parasites Bonamia ostreae and Marteilia refringens. These studies investigated immune responses to these parasites at the molecular and cellular levels. Several genetic improvement programs have been initiated especially for parasite resistance. Within the framework of a European project (PERLE 2) which aims to produce genetic lines of O. edulis with hardiness traits (growth, survival, resistance) for the purpose of repopulating natural oyster beds in Brittany and reviving the culture of this species on the foreshore, obtaining a reference genome becomes essential as done recently in many bivalve species of aquaculture interest. Here, we present a chromosome‐level genome assembly and annotation for the European flat oyster, generated by combining PacBio, Illumina, 10X linked and Hi‐C sequencing. The finished assembly is 887.2 Mb with a scaffold‐N50 of 97.1 Mb scaffolded on the expected 10 pseudo‐chromosomes. Annotation of the genome revealed the presence of 35962 protein‐coding genes. We analyzed in details the transposable element (TE) diversity in the flat oyster genome, highlighted some specificities in tRNA and miRNA composition and provided first insights into the molecular response of O. edulis to M. refringens. This genome provides a reference for genomic studies on O. edulis to better understand its basic physiology and as a useful resource for genetic breeding in support of aquaculture and natural reef restoration.

Microbes can play a prominent role in the evolution of their hosts, facilitating adaptation to various environments and promoting ecological divergence. The Wave and Crab ecotypes of the intertidal snail Littorina saxatilis is an evolutionary model of rapid and repeated adaptation to environmental gradients. While patterns of genomic divergence of the Littorina ecotypes along the shore gradients have been extensively studied, their microbiomes have been so far overlooked. The aim of the present study is to start filling this gap by comparing gut microbiome composition of the Wave and Crab ecotypes using metabarcoding approach. Since Littorina snails are micro‐grazers feeding on the intertidal biofilm, we also compare biofilm composition (i.e. typical snail diet) in the crab and wave habitats. In the results, we found that bacterial and eukaryotic biofilm composition varies between the typical habitats of the ecotypes. Further, the snail gut bacteriome was different from outer environments, being dominated by Gammaproteobacteria, Fusobacteria, Bacteroidia and Alphaproteobacteria. There were clear differences in the gut bacterial communities between the Crab and the Wave ecotypes as well as between the Wave ecotype snails from the low and high shores. These differences were both observed in the abundances and in the presence of different bacteria, as well as at different taxonomic level, from bacterial OTU’s to families. Altogether, our first insights show that Littorina snails and their associated bacteria are a promising marine system to study co‐evolution of the microbes and their hosts, which can help us to predict the future for wild species in the face of rapidly changing marine environments.

European flat oyster (Ostrea edulis) is an ecologically and economically important marine bivalve, that has been severely affected by the intracellular parasite Bonamia ostreae. In this study, a flat oyster SNP array (~14,000 SNPs) was used to validate previously reported outlier loci for divergent selection associated with B. ostreae exposure in the Northeast Atlantic Area. A total of 134 wild and hatchery individuals from the North Sea, collected in naïve (NV) and long‐term affected (LTA) areas, were analysed. Genetic diversity and differentiation were related to the sampling origin (wild vs hatchery) when using neutral markers, and to bonamiosis status (NV vs LTA) when using outlier loci for divergent selection. Two genetic clusters appeared intermingled in all sampling locations when using outlier loci and their frequency was associated with their bonamiosis status. When both clusters were compared, outlier datasets showed high genetic divergence (FST > 0.25) unlike neutral loci (FST not ≠ 0). Moreover, the cluster associated with LTA samples showed much higher genetic diversity and significant heterozygote excess with outlier loci, but not with neutral data. Most outliers mapped on chromosome 8 (OE‐C8) of the flat oyster genome, supporting a main genomic region underlying resilience to bonamiosis. Furthermore, differentially expressed genes previously reported between NV and LTA strains showed higher mapping density on OE‐C8. A range of relevant immune functions were specifically enriched among genes annotated on OE‐C8, providing hypotheses for resilience mechanisms to an intracellular parasite. The results suggest that marker‐assisted selection could be applied to breed resilient strains of O. edulis to bonamiosis, if lower parasite load and / or higher viability of the LTA genetic cluster following B. ostreae infection is demonstrated.

As fundamental components of RNA silencing, small RNA (sRNA) molecules ranging from 20‐32 nucleotides in length have been found as potent regulators of gene expression and genome stability in many biological processes of eukaryotes. Three major small RNAs are active in animals, including the microRNA (miRNA), short interfering RNA (siRNA), and PIWI‐interacting RNA (piRNA). Cnidarians, the sister group to bilaterians, are at a critical phylogenetic node to better model eukaryotic small RNA pathway evolution. To date, most of our understanding of sRNA regulation and its potential contribution to evolution has been limited to a few triploblastic bilaterian and plant models. The diploblastic non‐bilaterians, including the cnidarians, are understudied in this regard. Therefore, this review will present the current‐known small RNA information in cnidarians to enhance our understanding of the development of the small RNA pathways in early branch animals.

Humans have built ports on all the coasts of the world, allowing people to travel, exploit the sea, and develop trade. The proliferation of these artificial habitats and the associated maritime traffic are not predicted to fade in the coming decades. Ports share common characteristics: species find themselves in novel singular environments, with particular abiotic properties ‐e.g., pollutants, shading, protection from wave action‐ within novel communities in a melting‐pot of invasive and native taxa. Here we discuss how this drives evolution, including setting‐up of new connectivity hubs and gateways, adaptive responses to exposure to new chemicals or new biotic communities, and hybridization between lineages that would have never come into contact naturally. There are still important knowledge gaps however, such as the lack of experimental tests to distinguish adaptation from acclimation processes, the lack of studies to understand the putative threats of port lineages to natural populations, or to better understand the outcomes and fitness effects of anthropogenic hybridization. We thus call for further research examining “biological portuarization”, defined as the repeated evolution of marine species in port‐ecosystems under human‐altered selective pressures. Furthermore, we argue that ports act as giant mesocosms often isolated from the open sea by seawalls and locks, and so provide replicated life‐size evolutionary experiments essential to support predictive evolutionary sciences.

Species invasions are a global problem of increasing concern, especially in highly connected aquatic environments. Despite this, salinity conditions can pose physiological barriers to their spread and understanding them is important for management. In Scandinavia’s largest cargo port, the invasive round goby (Neogobius melanostomus), is established across a steep salinity gradient. We used 12 937 SNPs to identify the genetic origin and diversity of three sites along the salinity gradient and round goby from western, central and northern Baltic Sea, as well as north European rivers. Fish from two sites from the extreme ends of the gradient were also acclimated to freshwater and seawater, and tested for respiratory and osmoregulatory physiology. Fish from the high salinity environment in the outer port showed higher genetic diversity, and closer relatedness to the other regions, compared to fish from lower salinity upstream the river. Fish from the high salinity site also had higher maximum metabolic rate, fewer blood cells and lower blood Ca2+. Despite these genotypic and phenotypic differences, salinity acclimation affected fish from both sites in the same way: seawater increased the blood osmolality and Na+ levels, and freshwater increased the levels of the stress hormone cortisol. Our results show genotypic and phenotypic differences over short spatial scales across this steep salinity gradient. These patterns of the physiologically robust round goby are likely driven by multiple introductions into the high salinity site, and a process of sorting, likely based on behaviour or selection, along the gradient. Since this euryhaline fish risks spreading from this area, seascape genomics and phenotypic characterisation can inform management strategies even within an area as small as a coastal harbour inlet.

Pathogen populations differ in the amount of genetic diversity they contain. Populations carrying higher genetic diversity are thought to have a greater evolutionary potential than populations carrying less diversity. We used published studies to estimate the range of values associated with two critical components of genetic diversity, the number of unique pathogen genotypes and the number of spores produced during an epidemic, for the septoria tritici blotch pathogen Zymoseptoria tritici. We found that wheat fields experiencing typical levels of infection are likely to carry between 3.1 and 14.0 million pathogen genotypes per hectare and produce at least 2.1 to 9.9 trillion pycnidiospores per hectare. Given the experimentally derived mutation rate of 3 x 10‐10 substitutions per site per cell division, we estimate that between 27 and 126 million pathogen spores carrying adaptive mutations to counteract fungicides and resistant cultivars will be produced per hectare during a growing season. This suggests that most of the adaptive mutations that have been observed in Z. tritici populations can emerge through local selection from standing genetic variation that already exists within each field. The consequences of these findings for disease management strategies are discussed.

Trade‐offs between host resistance to parasites and host growth or reproduction can occur due to the allocation of limited available resources between competing demands. To predict potential trade‐offs arising from genetic selection for host resistance, a better understanding of the associated nutritional costs is required. Here we studied resistance costs by using sheep from lines divergently selected on their resistance to a common blood‐feeding gastro‐intestinal parasite (Haemonchus contortus). First, we assessed the effects of selection for high or low host resistance on condition traits (body weight, back fat and muscle thickness) and infection traits (parasite fecal egg excretion, loss in blood haematocrit) at various life stages, in particular during the periparturient period when resource allocation to immunity may limit host resistance. Second, we analysed the condition‐infection relationship to detect a possible trade‐off, in particular during the periparturient period. We experimentally infected young females in four stages over their first two years of life, including twice around parturition (at one year and at two years of age). Linear mixed model analyses revealed a large and consistent between‐line difference in infection traits during growth and outside of the periparturient period, whereas this difference was strongly attenuated during the periparturient period. Despite their different responses to infection, lines had similar body condition traits. Using covariance decomposition, we then found that the phenotypic relationship between infection and condition was dominated by direct infection costs arising from parasite development within the host. Accounting for these within‐individual effects, a cost of resistance on body weight was detected among ewes during their first reproduction. Although this cost and the reproductive constraint on resistance are unlikely to represent a major concern for animal breeding in nutrient‐rich environments, this study provides important new insights regarding the nutritional costs of parasite resistance at different lifestages and how these may affect response to selection.

Marine microorganisms have the potential to disperse widely with few obvious barriers to gene flow. However, among microalgae, several studies have demonstrated that species can be highly genetically structured with limited gene flow among populations, despite hydrographic connectivity. Ecological differentiation and local adaptation have been suggested as drivers of such population structure. Here we tested whether multiple strains from two genetically distinct Baltic Sea populations of the diatom Skeletonema marinoi showed evidence of local adaptation to their local environments; the estuarine Bothnian Sea and the marine Kattegat Sea. We performed reciprocal transplants of multiple strains between culture media based on water from the respective environments, and we also allowed competition between strains of estuarine and marine origin in both salinities. When grown alone, both marine and estuarine strains performed best in the high salinity environment, and estuarine strains always grew faster than marine strains. This result suggests local adaptation through countergradient selection, i.e. genetic effects counteract environmental effects. However, higher growth rate of the estuarine strains appears to have a cost in the marine environment and when strains were allowed to compete, marine strains performed better than estuarine strains in the marine environment. Thus, other traits are likely to also affect fitness. We provide evidence that tolerance to pH could be involved, and that estuarine strains which are adapted to a more fluctuating pH continue growing at higher pH than marine strains.

Understanding the spatiotemporal dynamics of pesticide resistance at the landscape scale is essential to anticipate the evolution and spread of new resistance phenotypes. In crop mosaics, host plant specialization in pest populations is likely to dampen the spread of pesticide resistance between different crops even in mobile pests such as aphids. Here, we assessed the contribution of host‐based genetic differentiation to the dynamics of resistance alleles in Myzus persicae, a major aphid pest which displays several insecticide resistance mechanisms. We obtained a representative sample of aphids from a crop mosaic through a suction trap for 7 years and from various crops as a reference collection. We genotyped these aphids at 14 microsatellite markers and four insecticide‐resistant loci, analyzed the genetic structure, and assigned host‐based genetic groups from field‐collected aphids. Four well‐defined genetic clusters were found in aerial samples, three of which with strong association with host‐plants. The fourth group was exclusive to aerial samples and highly divergent from the others, suggesting mixture with a closely related taxon of M. persicae associated with unsampled plants. We found a sharp differentiation between individuals from peach and herbaceous plants. Individuals from herbaceous hosts were separated into two genetic clusters, one more strongly associated with tobacco. The 4‐loci resistance genotypes showed a strong association with the four genetic clusters, indicative of barriers to the spread of resistance. However, we found a small number of clones with resistant alleles on multiple host‐plant species, which may spread insecticide resistance between crops. The 7‐year survey revealed a rapid turn‐over of aphid genotypes as well as the emergence, frequency increase and persistence of clones with resistance to several families of insecticides. This study highlights the importance of considering landscape‐scale population structure to identify the risk of emergence and spread of insecticide resistance for a particular crop.

Genomic studies are uncovering extensive cryptic diversity within reef‐building corals, suggesting that evolutionarily and ecologically relevant diversity is highly underestimated in the very organisms that structure coral reefs. Furthermore, endosymbiotic algae within coral host species can confer adaptive responses to environmental stress and may represent additional axes of coral genetic variation that are not constrained by taxonomic divergence of the cnidarian host. Here, we examine genetic variation in a common and widespread, reef‐building coral, Acropora tenuis, and its associated endosymbiotic algae along the entire expanse of the Great Barrier Reef (GBR). We use SNPs derived from genome‐wide sequencing to characterise the cnidarian coral host and organelles from zooxanthellate endosymbionts (genus Cladocopium). We discover three distinct and sympatric genetic clusters of coral hosts, whose distributions appear associated with latitude and inshore‐offshore reef position. Demographic modelling suggests that the divergence history of the three distinct host taxa ranges from 0.5 – 1.5 million years ago, preceding the GBR’s formation, and has been characterised by low to moderate ongoing inter‐taxon gene flow, consistent with occasional hybridisation and introgression typifying coral evolution. Despite this differentiation in the cnidarian host, A. tenuis taxa share a common symbiont pool, dominated by the genus Cladocopium (Clade C). Cladocopium plastid diversity is not strongly associated with host identity but varies with reef location relative to shore: inshore colonies contain lower symbiont diversity on average but have greater differences between colonies as compared to symbiont communities from offshore colonies. Spatial genetic patterns of symbiont communities could reflect local selective pressures maintaining coral holobiont differentiation across an inshore‐offshore environmental gradient. The strong influence of environment (but not host identity) on symbiont community composition supports the notion that symbiont community composition responds to habitat, and may assist in the adaptation of corals to future environmental change.

OXA‐23 is the predominant carbapenemase in carbapenem‐resistant Acinetobacter baumannnii. The co‐evolutionary dynamics of A. baumannii and OXA‐23‐encoding plasmids are poorly understood. Here, we transformed A. baumannnii ATCC 17978 with pAZJ221, a blaOXA‐23‐containing plasmid from clinical A. baumannnii isolate A221, and subjected the transformant to experimental evolution in the presence of a sub‐inhibitory concentration of imipenem for nearly 400 generations. We used population sequencing to track genetic changes at six time‐points and evaluated phenotypic changes. Increased fitness of evolving populations, temporary duplication of blaOXA‐23 in pAZJ221, interfering allele dynamics, and chromosomal locus‐level parallelism were observed. To characterize genotype‐to‐phenotype associations, we focused on six mutations in parallel targets predicted to affect small RNAs and a cyclic dimeric (3’→5’) GMP‐metabolizing protein. Six isogenic mutants with or without pAZJ221 were engineered to test for the effects of these mutations on fitness costs and plasmid kinetics, and the evolved plasmid containing two copies of blaOXA‐23 was transferred to ancestral ATCC 17978. Five of the six mutations contributed to improved fitness in the presence of pAZJ221 under imipenem pressure, and all but one of them impaired plasmid conjugation ability. The duplication of blaOXA‐23 increased host fitness under carbapenem pressure but imposed a burden on the host in antibiotic‐free media relative to the ancestral pAZJ221. Overall, our study provides a framework for the co‐evolution of A. baumannii and a clinical blaOXA‐23‐containing plasmid in the presence of imipenem, involving early blaOXA‐23 duplication followed by chromosomal adaptations that improved the fitness of plasmid‐carrying cells.

In species with alternative reproductive tactics, there is much empirical support that parasitically spawning males have larger testes and greater sperm numbers as an evolved response to a higher degree of sperm competition, but support for higher sperm performance (motility, longevity, speed) by such males is inconsistent. We used the sand goby (Pomatoschistus minutus) to test whether sperm performance differed between breeding‐coloured males (small testes, large mucus‐filled sperm‐duct glands; build nests lined with sperm‐containing mucus, provide care) and parasitic sneaker‐morph males (no breeding colouration, large testes, rudimentary sperm‐duct glands; no nest, no care). We compared motility (proportion motile sperm), velocity, longevity of sperm, gene expression of testes, and sperm morphometrics between the two morphs. We also tested if sperm‐duct gland contents affected sperm performance. We found a clear difference in gene expression of testes between the male morphs with 109 transcripts differentially expressed between the morphs. Notably, several mucin genes were upregulated in breeding‐coloured males and two ATP‐related genes were upregulated in sneaker‐morph males. There was a partial evidence of higher sperm velocity in sneaker‐morph males, but no difference in sperm motility. Presence of sperm‐duct gland contents significantly increased sperm velocity, and non‐significantly tended to increase sperm motility, but equally so for the two morphs. The sand goby has remarkably long‐lived sperm, with only small or no decline in motility and velocity over time (5 min vs 22 h), but again, this was equally true for both morphs. Sperm length (head, flagella, total, flagella‐to‐head ratio) did not differ between morphs, and did not correlate with sperm velocity for either morph. Thus, other than a clear difference in testes gene expression, we found only modest differences between the two male morphs, confirming previous findings that increased sperm performance as an adaptation to sperm competition is not a primary target of evolution.

While ecological interactions have been identified as determinant for biological control efficiency, the role of evolution remains largely underestimated in biological control programs. With the restrictions on the use of both pesticides and exotic biological control agents (BCAs), the evolutionary optimization of local BCAs becomes central for improving the efficiency and the resilience of biological control. In particular, we need to better account for the natural processes of evolution to fully understand the interactions of pests and BCAs, including in biocontrol strategies integrating human manipulations of evolution (i.e. artificial selection and genetic engineering). In agro‐ecosystems, the evolution of BCAs traits and performance depends on heritable phenotypic variation, trait genetic architecture, selection strength, stochastic processes, and other selective forces. Humans can manipulate these natural processes to increase the likelihood of evolutionary trait improvement, by artificially increasing heritable phenotypic variation, strengthening selection, controlling stochastic processes, or overpassing evolution through genetic engineering. We highlight these facets by reviewing recent studies addressing the importance of natural processes of evolution and human manipulations of these processes in biological control. We then discuss the interactions between the natural processes of evolution occurring in agroecosystems and affecting the artificially improved BCAs after their release. We emphasize that biological control cannot be summarized by interactions between species pairs because pests and biological control agents are entangled in diverse communities and are exposed to a multitude of deterministic and stochastic selective forces that can change rapidly in direction and intensity. We conclude that the combination of different evolutionary approaches can help optimize BCAs to remain efficient under changing environmental conditions and, ultimately, favor agroecosystem sustainability.

Evolutionary developmental biology, the interdisciplinary effort of illuminating the conserved similarities and difference during animal development across all phylogenetic clades, has gained renewed interest in the past decades. As technology (immunohistochemistry, next generation sequencing, advanced imaging, computational resources) has advanced, so has our ability of resolving fundamental hypotheses and overcoming the genotype‐phenotype gap. This rapid progress, however, has also exposed gaps in the collective knowledge around the choice and representation of model organisms. It has become clear that evo‐devo requires a comparative, large‐scale approach including marine invertebrates to resolve some of the most urgent questions about the phylogenetic positioning and character traits of the last common ancestors. Many invertebrates at the base of the tree of life inhabit marine environments and have been used for some years due to their accessibility, husbandry, and morphology. Here, we briefly review the major concepts of evolutionary developmental biology and discuss the suitability of established model organisms to address current research questions, before focussing on the importance, application and state‐of‐the‐art of marine evo‐devo. We highlight novel technical advances that progress evo‐devo as a whole.

Structural variations (SVs) are important DNA polymorphisms that contribute to genetic diversity and evolution in humans, animals and plants. In this study, we present a novel swine SV dataset of 79,919 deletions, 23,638 duplications and 9,333 inversions with average sequence depths of 24.1× from 24 varieties of worldwide pig populations, encompassing 305 individuals. Genotypes of SVs, particularly deletions, can accurately group individuals based on their population identity. We showed that exon‐covering deletions were subject to negative selection. Fixation index and differential allele frequency analysis identified highly differentiated SVs between European and Asian indigenous pigs, including deletions in NR6A1 and PLAG1, which are significantly associated with vertebrate numbers and growth performances, respectively. The growth‐enhancing allele at the deletion in PLAG1 was shared by European commercial pigs and Northern Chinese indigenous pigs including Laiwu and Min pigs, suggesting potential introgression from European commercial breeds into Chinese indigenous breeds. Moreover, we uncovered highly differentiated SVs in 139 genes between domesticated pigs and wild boars in Asia, temperature and altitude‐adaptation associated SVs in 41 genes and population specific SVs in 718 genes. This study provides novel insights into the role of porcine SVs in domestication, environmental adaptation and breed formation.

Understanding genetic structure and diversity within species can uncover associations with environmental and geographic attributes that highlight adaptive potential and inform conservation and management. The California gnatcatcher, Polioptila californica, is a small songbird found in desert and coastal scrub habitats from the southern end of Baja California Sur to Ventura County, California. Lack of congruence among morphological subspecies hypotheses and lack of measurable genetic structure found in a few genetic markers led to questions about the validity of subspecies within P. californica and the listing status of the coastal California gnatcatcher, P. c. californica. As a U.S. federally threatened subspecies, P. c. californica is recognized as a flagship for coastal sage scrub conservation throughout southern California. We used restriction site‐associated DNA sequencing to develop a genomic dataset for the California gnatcatcher. We sampled throughout the species' range, examined genetic structure, gene–environment associations, and demographic history, and tested for concordance between genetic structure and morphological subspecies groups. Our data support two distinct genetic groups with evidence of restricted movement and gene flow near the U.S.‐ Mexico international border. We found that climate‐associated outlier loci were more strongly differentiated than climate neutral loci, suggesting that local climate adaptation may have helped to drive differentiation after Holocene range expansions. Patterns of habitat loss and fragmentation are also concordant with genetic substructure throughout the southern California portion of the range. Finally, our genetic data supported the morphologically defined P. c. californica as a distinct group, but there was little evidence of genetic differentiation among other previously hypothesized subspecies in Baja California. Our data suggest that retaining and restoring connectivity, and protecting populations, particularly at the northern range edge, could help preserve existing adaptive potential to allow for future range expansion and long‐term persistence of the California gnatcatcher.

The efficacy of fisheries management strategies depends on stock assessment and management actions being carried out at appropriate spatial scales. This requires understanding of spatial and temporal population structure and connectivity, which is challenging in weakly structured and highly connected marine populations. We carried out a population genomics study of the heavily exploited snapper (Chrysophrys auratus) along ~2,600 km of the Australian coastline, with a focus on Western Australia (WA). We used 10,903 filtered SNPs in 341 individuals from eight sampling locations to characterise population structure and connectivity in snapper across WA and to assess if current spatial scales of stock assessment and management agree with evidence from population genomics. Our dataset also enabled us to investigate temporal stability in population structure as well as connectivity between WA and its nearest, eastern jurisdictional neighbor. As expected for a species influenced by the extensive ocean boundary current in the region, low genetic differentiation and high connectivity was uncovered across WA. However, we did detect strong isolation by distance and genetic discontinuities in the mid‐west and south‐east. The discontinuities correlate with boundaries between biogeographic regions, influenced by on‐shelf oceanography, and the sites of important spawning aggregations. We also detected temporal instability in genetic structure at one of our sites, possibly due to interannual variability in recruitment in adjacent regions. Our results partly contrast with the current spatial management of snapper in WA, indicating the likely benefits of a review. This study supports the value of population genomic surveys in informing the management of weakly‐structured and wide‐ranging marine fishery resources.

Introgressive hybridisation is a process that enables gene flow across species barriers through the backcrossing of hybrids into a parent population. This may make genetic material, potentially including relevant environmental adaptations, rapidly available in a gene pool. Consequently, it has been postulated to be an important mechanism for enabling evolutionary rescue, i.e. the recovery of threatened populations through rapid evolutionary adaptation to novel environments. However, predicting the likelihood of such evolutionary rescue for individual species remains challenging. Here, we use the example of Zosterops silvanus, an endangered East African highland bird species suffering from severe habitat loss and fragmentation, to investigate whether hybridisation with its congener Zosterops flavilateralis might enable evolutionary rescue of its Taita Hills population. To do so, we employ an empirically parameterised individual‐based model to simulate the species’ behaviour, physiology and genetics. We test the population’s response to different assumptions of mating behaviour as well as multiple scenarios of habitat change. We show that as long as hybridisation does take place, evolutionary rescue of Z. silvanus is likely. Intermediate hybridisation rates enable the greatest long‐term population growth, due to trade‐offs between adaptive and maladaptive introgressed alleles. Habitat change did not have a strong effect on population growth rates, as Z. silvanus is a strong disperser and landscape configuration is therefore not the limiting factor for hybridisation. Our results show that targeted gene flow may be a promising avenue to help accelerate the adaptation of endangered species to novel environments, and demonstrate how to combine empirical research and mechanistic modelling to deliver species‐specific predictions for conservation planning.

The admixture of domestic pig into French wild boar populations has been monitored since the 1980s thanks to the existence of a cytogenetic difference between the two sub‐species. The number of chromosomes is 2n=36 in wild boar and 2n=38 in pig, respectively. This difference makes it possible to assign the “hybrid” status to wild boar individuals controlled with 37 or 38 chromosomes. However, it does not make it possible to determine the timing of the hybridization(s), nor to guarantee the absence of domestic admixture in an animal with 2n=36 chromosomes. In order to analyze hybridization in greater detail and to avoid the inherent limitations of the cytogenetic approach, 362 wild boars recently collected in different French geographical areas and in different environments (farms, free ranging in protected or unprotected areas, animals with 2n=36, 37 or 38 chromosomes) were genotyped on a 70K SNP chip. Principal component analyses allowed the identification of 13 “outliers” (3.6%), for which the proportion of the genome of “domestic” origin was greater than 40% (Admixture analyses). These animals were probably recent hybrids, having Asian domestic pig ancestry for most of them. For the remaining 349 animals studied, the proportion of the genome of “wild” origin varied between 83 and 100% (median: 94%). This proportion varied significantly depending on how the wild boar populations were managed. Local ancestry analyses revealed adaptive introgression from domestic pig, suggesting a critical role of genetic admixture in improving the fitness and population growth of wild boars. Overall, our results show that the methods used to monitor the domestic genetic contributions to wild boar populations should evolve in order to limit the level of admixture between the two gene pools.

Vietnam harnesses a rich diversity of rice landraces adapted to a range of conditions, which constitute a largely untapped source of diversity for the continuous improvement of cultivars. We previously identified a strong population structure in Vietnamese rice, which is captured in five Indica and four Japonica subpopulations, including an outlying Indica-5 group. Here, we leveraged that strong differentiation and 672 native rice genomes to identify genomic regions and genes putatively selected during the breeding of rice in Vietnam. We identified significant distorted patterns in allele frequency (XP-CLR) and population differentiation scores (FST) resulting from differential selective pressures between native subpopulations, and later annotated them with QTLs previously identified by GWAS in the same panel. We particularly focused on the outlying Indica-5 subpopulation because of its likely novelty and differential evolution, where we annotated 52 selected regions, which represented 8.1% of the rice genome. We annotated the 4,576 genes in these regions and selected 65 candidate genes as promising breeding targets, several of which harboured alleles with non-synonymous substitutions. Our results highlight genomic differences between traditional Vietnamese landraces, which are likely the product of adaption to multiple environmental conditions and regional culinary preferences in a very diverse country. We also verified the applicability of this genome scanning approach to identify potential regions harbouring novel loci and alleles to breed a new generation of sustainable and resilient rice.

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48 days
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4.929 (2021)
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8.2 (2021)
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Top-cited authors
• McGill University
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• University of Melbourne
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