Wiley

Evolutionary Applications

Published by Wiley

Online ISSN: 1752-4571

Disciplines: Evolution

Journal websiteAuthor guidelines

Top read articles

206 reads in the past 30 days

The phylosweeper framework. This python script performs three filtering steps, which are controlled by three parameters that are indicated by the user (dashed‐line boxes). In the first step, the user defines a length variation cutoff. For example, a 5% cutoff means that sequences with a length greater than 105% or lower than 95% of the average length will be removed. In the second step, the user defines the maximum average of uncorrected pairwise distance. Possible values range from 0 to 100. In the third step, the user provides the maximum fraction of allowed missing data or gaps. For example, 0.05 means that sequences with more than 5% of missing data or gaps will be excluded. In steps 2 and 3, the alignments are performed using the trimmed sequences produced by step 1 but include only those that passed the filter.
Gene occupancy matrix for Anastrepha and A. fraterculus group datasets. (a) 73% gene occupancy of Anastrepha dataset matrix and heatmaps of samples per gene (bottom) and ortholog genes per sample (right). (b) 67% gene occupancy of A. fraterculus and heatmaps of samples per gene (bottom) and number of genes per sample (right). Colors in the matrix indicate presence (black) or absence (yellow) of an ortholog gene per sample.
Multispecies coalescent species tree of Anastrepha and five other Tephritidae species as outgroups based on 2591 genes inferred in ASTRAL‐III. Phylogenetic support measured by bootstrap, gene concordant factor, and quartet support are showed close to the nodes.
Phylogenetic analysis of the fraterculus group using A. psidivora and the striata group species as outgroups. Multispecies coalescent species trees were recovered based on 3031 genes (a) and 123 genes (b) in ASTRAL‐III. Phylogenetic support measured by bootstrap, gene concordant factor and quartet support are showed in that order close to the nodes.
Phylogenetic networks of fraterculus group lineages based on 3031 gene trees inferred under maximum pseudo‐likelihood approach in Phylonet. Though we inferred networks with 0–5 reticulations allowed, only the networks with 0–3 reticulations are shown here (a–d). Inheritance probabilities (γ) are displayed in sky‐blue.

+2

Phylogenomic analysis provides diagnostic tools for the identification of Anastrepha fraterculus (Diptera: Tephritidae) species complex

August 2023

·

206 Reads

·

·

·

[...]

·

Download

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.

Recent articles


The putatively high‐altitude adaptation of macaque monkeys: Evidence from the fecal metabolome and gut microbiome
  • New
  • Article
  • Full-text available

September 2023

·

5 Reads

Dayong Li

·

Wancai Xia

·

Xinyuan Cui

·

[...]

·

Lifeng Zhu

Animals living in high‐altitude environments, such as the Tibetan Plateau, must face harsh environmental conditions (e.g., hypoxia, cold, and strong UV radiation). These animals' physiological adaptations (e.g., increased red cell production and turnover rate) might also be associated with the gut microbial response. Bilirubin is a component of red blood cell turnover or destruction and is excreted into the intestine and reduced to urobilinoids and/or urobilinogen by gut bacteria. Here, we found that the feces of macaques living in high‐altitude regions look significantly browner (with a high concentration of stercobilin, a component from urobilinoids) than those living in low‐altitude regions. We also found that gut microbes involved in urobilinogen reduction (e.g., beta‐glucuronidase) were enriched in the high‐altitude mammal population compared to the low‐altitude population. Moreover, the spatial–temporal change in gut microbial function was more profound in the low‐altitude macaques than in the high‐altitude population, which might be attributed to profound changes in food resources in the low‐altitude regions. Therefore, we conclude that a high‐altitude environment's stress influences living animals and their symbiotic microbiota.
Share

Multifaceted framework for defining conservation units: An example from Atlantic salmon ( Salmo salar ) in Canada

September 2023

·

52 Reads

Conservation units represent important components of intraspecific diversity that can aid in prioritizing and protecting at‐risk populations, while also safeguarding unique diversity that can contribute to species resilience. In Canada, identification and assessments of conservation units is done by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC). COSEWIC can recognize conservation units below the species level (termed “designatable units”; DUs) if the unit has attributes that make it both discrete and evolutionarily significant. There are various ways in which a DU can meet criteria of discreteness and significance, and increasing access to “big data” is providing unprecedented information that can directly inform both criteria. Specifically, the incorporation of genomic data for an increasing number of non‐model species is informing more COSEWIC assessments; thus, a repeatable, robust framework is needed for integrating these data into DU characterization. Here, we develop a framework that uses a multifaceted, weight of evidence approach to incorporate multiple data types, including genetic and genomic data, to inform COSEWIC DUs. We apply this framework to delineate DUs of Atlantic salmon ( Salmo salar , L.), an economically, culturally, and ecologically significant species, that is also characterized by complex hierarchical population structure. Specifically, we focus on an in‐depth example of how our approach was applied to a previously data limited region of northern Canada that was defined by a single large DU. Application of our framework with newly available genetic and genomic data led to subdividing this DU into three new DUs. Although our approach was developed to meet criteria of COSEWIC, it is widely applicable given similarities in the definitions of a conservation unit.

of the experimental design with a map of our sampled populations in southern Sweden (high latitude) and southern Poland (central latitude). Geographic distribution of Ischnura elegans in central and northern Europe is shown in grey and occurrence of the spiny‐cheek crayfish Orconectes limosus is depicted by red crosses. On the left side, we show the design of the Analysis 1 focusing on different urbanization types (rural and urban populations) from central and high latitude reared at current (20°C) and warming (24°C) temperature. The plot shows the significant latitude × urbanization type interaction for the final larval instar (F‐0) mass with 1 SE. On the right side, we show the design of the Analysis 2 focusing on urban and rural populations from high latitude reared at current (20°C), warming (24°C), and heat wave (28°C) temperature and in a control or a predator cue treatment. The plot shows the significant interaction temperature × predator cue for the growth rate until F‐0 with 1 SE.
Larval (a) massF0 and (b) growth rateF0 (GRF0) across urbanization types (urban and rural populations) and current (20°C) and warming (24°C) temperature. Larval (c) massF0 and (d) GRF0 across urban and rural populations for females and males in Analysis 1 (N = 349). Given are estimated means with 1 SE.
Principal component analysis showing evolutionary changes before the treatment with predator cue in response to urbanization type at current (20°C) and warming (24°C) for (a) central‐ (N = 141) and (b) high latitude (N = 208) populations and plastic changes in response to temperature in rural and urban populations for (c) central‐ and (d) high latitude populations (sexes pooled). Rural and urban individuals are depicted by open circles and triangles respectively; temperature by colours (blue = 20°C and green = 24°C); filled circles and triangles correspond to the centroid of each group; solid lines connecting filled symbols represent the vector.
Phenotypic plasticity trajectory in response to (a) urbanization type at current (20°C), warming temperature (24°C) and heat wave (28°C) and to (b) temperature for rural and urban populations (N = 340). Rural and urban individuals are depicted by open circles and triangles respectively; temperature by colours (blue = 20°C, green = 24°C and red = 28°C); filled circles and triangles correspond to the centroid of each group; solid lines connecting filled symbols represent the vector.
Latitude‐specific urbanization effects on life history traits in the damselfly Ischnura elegans

August 2023

·

46 Reads

Many species are currently adapting to cities at different latitudes. Adaptation to urbanization may require eco‐evolutionary changes in response to temperature and invasive species that may differ between latitudes. Here, we studied single and combined effects of increased temperatures and an invasive alien predator on the phenotypic response of replicated urban and rural populations of the damselfly Ischnura elegans and contrasted these between central and high latitudes. Adult females were collected in rural and urban ponds at central and high latitudes. Their larvae were exposed to temperature treatments (current [20°C], mild warming [24°C], and heat wave [28°C; for high latitude only]) crossed with the presence or absence of chemical cues released by the spiny‐cheek crayfish (Faxonius limosus), only present at the central latitude. We measured treatment effects on larval development time, mass, and growth rate. Urbanization type affected all life history traits, yet these responses were often dependent on latitude, temperature, and sex. Mild warming decreased mass in rural and increased growth rate in urban populations. The effects of urbanization type on mass were latitude‐dependent, with central‐latitude populations having a greater phenotypic difference. Urbanization type effects were sex‐specific with urban males being lighter and having a lower growth rate than rural males. At the current temperature and mild warming, the predator cue reduced the growth rate, and this independently of urbanization type and latitude of origin. This pattern was reversed during a heat wave in high‐latitude damselflies. Our results highlight the context‐dependency of evolutionary and plastic responses to urbanization, and caution for generalizing how populations respond to cities based on populations at a single latitude.

Increase in the (a) absolute and (b) relative error with each iteration increase of error in the training data. The increase in absolute and relative error is compared to the baseline, where no error was introduced in the training data. Orange‐coloured dots represent the human data set, and blue represents the zebrafish data set.
Increase in the error of the training data with three methods of statistical tests. Increase in p‐value for t‐tests comparing (a) absolute and (b) relative error rate in data with simulated error to the baseline model. The p‐value has been transformed into ‐log10 (p‐value) to illustrate a positive increase. The horizontal red dotted line represents a p‐value = 0.05. (c) Cohen's d increase with training error. The coloured dotted lines show the considered small (0.2), medium (0.5) and large (0.8) effect sizes.
Calibrating epigenetic clocks with training data error

July 2023

·

51 Reads

Animal age data are valuable for management of wildlife populations. Yet, for most species, there is no practical method for determining the age of unknown individuals. However, epigenetic clocks, a molecular‐based method, are capable of age prediction by sampling specific tissue types and measuring DNA methylation levels at specific loci. Developing an epigenetic clock requires a large number of samples from animals of known ages. For most species, there are no individuals whose exact ages are known, making epigenetic clock calibration inaccurate or impossible. For many epigenetic clocks, calibration samples with inaccurate age estimates introduce a degree of error to epigenetic clock calibration. In this study, we investigated how much error in the training data set of an epigenetic clock can be tolerated before it resulted in an unacceptable increase in error for age prediction. Using four publicly available data sets, we artificially increased the training data age error by iterations of 1% and then tested the model against an independent set of known ages. A small effect size increase (Cohen's d >0.2) was detected when the error in age was higher than 22%. The effect size increased linearly with age error. This threshold was independent of sample size. Downstream applications for age data may have a more important role in deciding how much error can be tolerated for age prediction. If highly precise age estimates are required, then it may be futile to embark on the development of an epigenetic clock when there is no accurately aged calibration population to work with. However, for other problems, such as determining the relative age order of pairs of individuals, a lower‐quality calibration data set may be adequate.

Schematic of the conceptual design. Small circles with tails are sperm, while large circles are ovarian fluid and water. Arrows represent sperm velocity in water or ovarian fluid (the same semen sample was tested in both as separate aliquots of individual sperm). Ovarian fluids were predicted to show conspecific sperm preference, indicated by greater modification of conspecific sperm (bolded arrows) over heterospecific sperm (un‐bolded arrows). Modification was quantified as the ratio of sperm swimming performance (from the same semen sample) in ovarian fluid compared to that in water, which controls for individual variation in male quality (variable performance among males in water). Experimental replication was achieved with 12 groups of fish, and sperm activations were technically repeated three times for each comparison.
Reaction norms (top = proportion sperm motile, middle = swimming linearity, bottom = curvilinear swimming velocity) comparing sperm swimming performance from 6.0 to 6.5 s post‐activation in water to the average value in three ovarian fluid species. Each line represents an individual male (blue = char, pink = salmon, orange = trout) and is created by two points; means for water represent three technical replicate activations for each male, while those for ovarian fluid are from nine activations (three technical replications from each of three species of ovarian fluid). Positive slopes indicate up‐regulation of sperm swimming by ovarian fluid. Standardized (ovarian fluid/water) ratios >1.0 indicate positive up‐regulation and were on average 1.53 for MOT, 1.06 for LIN, and 1.30 for VCL.
Ratio of (top) sperm motility (% motile) and (middle) swimming linearity (LIN), and (bottom) curvilinear velocity (VCL μm/s) in specific ovarian fluid compared to water from 6.0 to 6.5 s post‐activation – any value above 1.0 indicates ovarian fluid up‐regulated sperm swimming performance. Black shapes represent the average (circles are conspecific sperm to the ovarian fluid, triangles are heterospecific sperm), and colored brackets 2 × standard error among 12 males and females within a species.
Can cryptic female choice prevent invasive hybridization in external fertilizing fish?

July 2023

·

59 Reads

Polyandrous mating systems result in females mating with multiple males, generating opportunities for strong pre‐mating and post‐mating sexual selection. Polyandry also creates the potential for unintended matings and subsequent sperm competition with hybridizing species. Cryptic female choice allows females to bias paternity towards preferred males under sperm competition and may include conspecific sperm preference when under hybridization risk. The potential for hybridization becomes particularly important in context of invasive species that can novelly hybridize with natives, and by definition, have evolved allopatrically. We provide the first examination of conspecific sperm preference in a system of three species with the potential to hybridize: North American native Atlantic salmon (Salmo salar) and brook char (Salvelinus fontinalis), and invasive brown trout (Salmo trutta) from Europe. Using naturalized populations on the island of Newfoundland, we measured changes in sperm swimming performance, a known predictor of paternity, to determine the degree of modification in sperm swimming to female cues related to conspecific sperm preference. Compared to water alone, female ovarian fluid in general had a pronounced effect and changed sperm motility (by a mean of 53%) and swimming velocity (mean 30%), but not linearity (mean 6%). However, patterns in the degree of modification suggest there is no conspecific sperm preference in the North American populations. Furthermore, female cues from both native species tended to boost the sperm of invasive males more than their own. We conclude that cryptic female choice via ovarian fluid mediated sperm swimming modification is too weak in this system to prevent invasive hybridization and is likely insufficient to promote or maintain reproductive isolation between the native North American species.

Sex‐specific heritabilities across populations and years.
Evolution of length at maturity in a single generation in response to natural selection and artificial selection against jacks, as projected by the breeder's equation.
Changes in fecundity due to changes in female length at maturity as projected by the breeder's equation.
Sex‐specific heritabilities for length at maturity among Pacific salmonids and their consequences for evolution in response to artificial selection

July 2023

·

65 Reads

Artificial selection, whether intentional or coincidental, is a common result of conservation policies and natural resource management. To reduce unintended consequences of artificial selection, conservation practitioners must understand both artificial selection gradients on traits of interest and how those traits are correlated with others that may affect population growth and resilience. We investigate how artificial selection on male body size in Pacific salmon (Oncorhynchus spp.) may influence the evolution of female body size and female fitness. While salmon hatchery managers often assume that selection for large males will also produce large females, this may not be the case—in fact, because the fastest‐growing males mature earliest and at the smallest size, and because female age at maturity varies little, small males may produce larger females if the genetic architecture of growth rate is the same in both sexes. We explored this possibility by estimating sex‐specific heritability values of and natural and artificial selection gradients on length at maturity in four populations representing three species of Pacific salmon. We then used the multivariate breeder's equation to project how artificial selection against small males may affect the evolution of female length and fecundity. Our results indicate that the heritability of length at maturity is greater within than between the sexes and that sire–daughter heritability values are especially small. Salmon hatchery policies should consider these sex‐specific quantitative genetic parameters to avoid potential unintended consequences of artificial selection.

Representation of the genomic data and the differentiation between the five populations of Penicillium roqueforti: the three cheese populations (Roquefort, non‐Roquefort and Termignon) and the two non‐cheese populations (silage/food spoiler and lumber/spoiled food). (a) Reticulated network of P. roqueforti strains based on 190,387 single nucleotide polymorphisms, showing the five distinct populations with pictures of their respective environments of collection. The ID of the strains used for phenotyping are in bold. (b) Principal component analysis based on 190,387 single nucleotide polymorphisms. The names of the strains used in phenotype comparisons are indicated. The strain ESE00421 with intermediate assignments in various clusters with NGSadmix is shown in grey. (c) Population subdivision inferred with NGSadmix for K = 5 populations (see Figure S3 for K = 2 to 6). Colored bars represent the coefficients of membership in the K gene pools based on genomic data. Each bar represents a strain, its name being indicated at the bottom of the figure. The ID of the strains used for phenotyping are in bold. The same colour code as on the other figures is used in all three panels.
Principal component analysis (PCA) illustrating the phenotypic differences between Penicillium roqueforti populations based on growth response to temperature, water activity (salt), pH, various carbon sources (sucrose, glucose, lactose, galactose, maltose, cellobiose, xylose, starch, pectin and lactic acid) and to exposure to fungal inhibitors (lactic acid, potassium sorbate, tebuconazole and natamycin). (a) Strains on the first two axes of the PCA. A confidence ellipse is drawn for each of the five populations. The percentage of variance explained by the axes are indicated. The same colour code is used as in the other figures: green for the lumber/spoiled food population, orange for the silage population, dark blue for the non‐Roquefort cheese population, purple for the Roquefort cheese population and light blue for the Termignon cheese population. The strain IDs are provided in Table S1. (b) Association between the two PCA axes and the variables. Pectin.mu, lactose.mu, Maltose.mu, Xylose.mu, Sucrose.mu correspond to growth rate with pectin, lactose, maltose, xylose or sucrose as sole carbon sources, respectively. awopt.lambda.aw corresponds to optimal water activity (salt concentration minimising latency). Tmin.mu.T and Topt.mu.T corresponds to the minimal and optimal growth temperature; muopt.mu.T, muopt.mu.aw, muopt.mu.ph and muopt.mu.LA correspond the optimal parameter values for growth rate in terms of temperature, water activity (salt concentration), pH and lactic acid concentration, respectively. lambda.opt.lambda.aw, lambda.opt.lambda.pH and lambda.opt.lambda.LA, correspond to the optimal parameter values for inverse latency in terms of water activity (salt concentration), pH and lactic acid concentration, respectively. See Figure S1 for an illustration of parameter determination.
Growth parameters with differences between the Penicillium roqueforti five populations. The same colour code is used as in the other figures: green for the lumber/spoiled food population, orange for the silage population, dark blue for the non‐Roquefort cheese population, purple for the Roquefort cheese population and light blue for the Termignon cheese population. The results of the global test for a population effect is given at the top of each panel. Pairwise significant differences are indicated by asterisks. The boxplots represent the median (centre line), the first quartile and third quartile (box bounds), the maximum and minimum excluding outlier points (whiskers), points being the outliers, i.e., with values either below the first quartile minus 1.5 fold the interquartile range or above the third quartile plus 1.5 fold the interquartile range. (a) Optimal temperature, (b) Optimal water activity, (c) Minimal water activity (i.e., the fraction of available water for growth, which decreases for increasing salt concentrations), (d) Minimal pH and (e) Maximal pH.
Differences in growth rate with various carbon sources between the Penicillium roqueforti populations. Pairwise significant differences are indicated by asterisks. The same color code is used as in the other figures: green for the lumber/spoiled food population, orange for the silage population, dark blue for the non‐Roquefort cheese population, purple for the Roquefort cheese population and light blue for the Termignon cheese population. The boxplots represent the median (centre line), the first quartile and third quartile (box bounds), the maximum and minimum excluding outlier points (whiskers), points being the outliers, i.e., with values either below the first quartile minus 1.5 fold the interquartile range or above the third quartile plus 1.5 fold the interquartile range. (a) Optimal growth rate, i.e., estimated growth rate at the optimal temperature, in potato dextrose broth, obtained from temperature secondary modelling. The results of the global test for a population effect is given at the top. (b) Growth rate in minimal medium with glucose, galactose, lactic acid, lactose, cellobiose, maltose, pectin, sucrose and xylose as sole carbon sources.
Impact of lactic acid on growth parameters between the Penicillium roqueforti populations. Pairwise significant differences are indicated by asterisks. The same color code is used as in the other figures: green for the lumber/spoiled food population, orange for the silage population, dark blue for the non‐Roquefort cheese population, purple for the Roquefort cheese population and light blue for the Termignon cheese population. The boxplots represent the median (centre line), the first quartile and third quartile (box bounds), the maximum and minimum excluding outlier points (whiskers), points being the outliers, i.e., with values either below the first quartile minus 1.5 fold the interquartile range or above the third quartile plus 1.5 fold the interquartile range. (a) Maximal lactic acid concentrations allowing growth for each of the five Penicillium roqueforti populations. The results of the global test for an effect of population maximal lactic acid concentration is given at the top. (b) Relative growth rate with lactic acid concentration for each of the five Penicillium roqueforti populations. Relative growth rate corresponds to the observed growth rate normalized by the growth rate without lactic acid.
A new cheese population in Penicillium roqueforti and adaptation of the five populations to their ecological niche

July 2023

·

85 Reads

Domestication is an excellent case study for understanding adaptation and multiple fungal lineages have been domesticated for fermenting food products. Studying domestication in fungi has thus both fundamental and applied interest. Genomic studies have revealed the existence of four populations within the blue‐cheese‐making fungus Penicillium roqueforti. The two cheese populations show footprints of domestication, but the adaptation of the two non‐cheese populations to their ecological niches (i.e., silage/spoiled food and lumber/spoiled food) has not been investigated yet. Here, we reveal the existence of a new P. roqueforti population, specific to French Termignon cheeses, produced using small‐scale traditional practices, with spontaneous blue mould colonisation. This Termignon population is genetically differentiated from the four previously identified populations, providing a novel source of genetic diversity for cheese making. The Termignon population indeed displayed substantial genetic diversity, both mating types, horizontally transferred regions previously detected in the non‐Roquefort population, and intermediate phenotypes between cheese and non‐cheese populations. Phenotypically, the non‐Roquefort cheese population was the most differentiated, with specific traits beneficial for cheese making, in particular higher tolerance to salt, to acidic pH and to lactic acid. Our results support the view that this clonal population, used for many cheese types in multiple countries, is a domesticated lineage on which humans exerted strong selection. The lumber/spoiled food and silage/spoiled food populations were not more tolerant to crop fungicides but showed faster growth in various carbon sources (e.g., dextrose, pectin, sucrose, xylose and/or lactose), which can be beneficial in their ecological niches. Such contrasted phenotypes between P. roqueforti populations, with beneficial traits for cheese‐making in the cheese populations and enhanced ability to metabolise sugars in the lumber/spoiled food population, support the inference of domestication in cheese fungi and more generally of adaptation to anthropized environments.

Timeline of experimental design. Lime addition and shaking treatments were performed factorially, with lime added on day 1 and shaking at 210 rpm starting on day 14. Pseudomonas aeruginosa was added to all microcosms on day 14. Microcosms were destructively sampled on day 28. Six replicates were used for all treatments (24 microcosms in total).
The final pH of microcosms containing river water and sediment after 28 days of incubation. We used a factorial design with limed and shaken treatments, each with six replicates (each represented by a coloured circle). The starting pH was 5.8. The significant effect of liming on pH (p < 0.001) was increased through an interaction with shaking (p < 0.001).
The maximum optical density (OD600) of P. aeruginosa populations after 18 h incubation with toxic copper (1 g/L copper sulphate) relative to their maximum OD600 when grown without copper (log w). Populations above the horizontal dashed line at 0 (log of 1) have a higher relative max OD600 when grown with copper, whereas those below the line have reduced maximum growth. The white box shows the ancestral strain, whereas the grey boxes show populations incubated in microcosms containing river water and sediment for 14 days. Circles show individual replicates (n = 6), and colours show the different treatments.
Mean virulence of Pseudomonas aeruginosa evolved in metal‐contaminated aquatic communities as a function of (a) mean total siderophore production and (b) mean pyoverdine production. Virulence was quantified using the Galleria mellonella infection model (n = 20 per replicate) and given as the mean time to death. Pyoverdine and total siderophore production were measured in standardized fluorescence units per OD600. Individual circles show the mean production by 24 clones from each replicate. Colours and shapes represent different treatments: grey and □ = static, no lime, blue and + = static, limed, black and △ = shaken, no lime and red and ✕ = shaken, limed. Panel (c) shows the change in the survival probability of larvae over time within each treatment. These do not significantly differ from one another. Shaded areas represent 95% confidence intervals.
The proportion of 24 Pseudomonas aeruginosa clones per replicate (n = 6) resistant to (a) apramycin (15 μg/mL), (b) cefotaxime (50 μg/mL) and (c) trimethoprim (60 μg/mL) antibiotics. Clones were tested after 2 weeks of evolution in microcosms containing metal‐contaminated river water and sediment whilst embedded in the resident microbial community. The concentrations of each of the antibiotics used are greater than the MIC of the ancestral strain, which was determined prior to this assay. Circles show individual replicates; those with a red outline are from the same sample, which is the least resistant to all three antibiotics.
The effect of metal remediation on the virulence and antimicrobial resistance of the opportunistic pathogen Pseudomonas aeruginosa

July 2023

·

25 Reads

Anthropogenic metal pollution can result in co‐selection for antibiotic resistance and potentially select for increased virulence in bacterial pathogens. Metal‐polluted environments can select for the increased production of siderophore molecules to detoxify non‐ferrous metals. However, these same molecules also aid the uptake of ferric iron, a limiting factor for within‐host pathogen growth, and are consequently a virulence factor. Anthropogenic methods to remediate environmental metal contamination commonly involve amendment with lime‐containing materials. However, whether this reduces in situ co‐selection for antibiotic resistance and siderophore‐mediated virulence remains unknown. Here, using microcosms containing non‐sterile metal‐contaminated river water and sediment, we test whether liming reduces co‐selection for these pathogenicity traits in the opportunistic pathogen Pseudomonas aeruginosa. To account for the effect of environmental structure, which is known to impact siderophore production, microcosms were incubated under either static or shaking conditions. Evolved P. aeruginosa populations had greater fitness in the presence of toxic concentrations of copper than the ancestral strain and showed increased resistance to the clinically relevant antibiotics apramycin, cefotaxime and trimethoprim, regardless of lime addition or environmental structure. Although we found virulence to be significantly associated with siderophore production, neither virulence nor siderophore production significantly differed between the four treatments. Furthermore, liming did not mitigate metal‐imposed selection for antibiotic resistance or virulence in P. aeruginosa. Consequently, metal‐contaminated environments may select for antibiotic resistance and virulence traits even when treated with lime.

(a) Map showing the sampling sites in Levante Bay, Vulcano Island. The star indicates the location of the primary vent, and the circles indicate the low pH site and the control (ctrl) site. (b) Picture of the study species Gobius incognitus in the wild.
Overall transcript expression pattern across the 16 samples from the natural CO2 seep and control site at Vulcano Island. Principal component analysis (PCA) was performed using the regularized log‐transformed (rlog) counts of all expressed transcripts. The circles represent the individuals from the control site, and the triangles represent the individuals from the low pH site. The blue and grey region is the 95% confidence interval of the samples from the CO2 seep and control sites, respectively.
Functional groups associated with the differentially expressed transcripts. Each circle represents one transcript, and the colour represents the FDR corrected p‐value (padj) from the differential expression analysis.
Relative expression levels of transcripts with enriched functions of fish from control and CO2 seep sites. Each row represents a transcript, and the row z‐score is calculated from the log2 transformed transcripts per million (TPM) values for each transcript. The transcripts are clustered based on expression levels.
Brain transcriptome of gobies inhabiting natural CO2 seeps reveal acclimation strategies to long‐term acidification

June 2023

·

54 Reads

Ocean acidification (OA) is known to affect the physiology, survival, behaviour and fitness of various fish species with repercussions at the population, community and ecosystem levels. Some fish species, however, seem to acclimate rapidly to OA conditions and even thrive in acidified environments. The molecular mechanisms that enable species to successfully inhabit high CO2 environments have not been fully elucidated especially in wild fish populations. Here, we used the natural CO2 seep in Vulcano Island, Italy to study the effects of elevated CO2 exposure on the brain transcriptome of the anemone goby, a species with high population density in the CO2 seep and investigate their potential for acclimation. Compared to fish from environments with ambient CO2, gobies living in the CO2 seep showed differences in the expression of transcripts involved in ion transport and pH homeostasis, cellular stress, immune response, circadian rhythm and metabolism. We also found evidence of potential adaptive mechanisms to restore the functioning of GABAergic pathways, whose activity can be affected by exposure to elevated CO2 levels. Our findings indicate that gobies living in the CO2 seep may be capable of mitigating CO2‐induced oxidative stress and maintaining physiological pH while meeting the consequent increased energetic costs. The conspicuous difference in the expression of core circadian rhythm transcripts could provide an adaptive advantage by increasing the flexibility of physiological processes in elevated CO2 conditions thereby facilitating acclimation. Our results show potential molecular processes of acclimation to elevated CO2 in gobies enabling them to thrive in the acidified waters of Vulcano Island.

Sample collection sites and regional patterns of genetic differentiation. (a) A total of 959 yellow perch (Perca flavescens) were collected and genotyped from 20 sites, representing 26 collections (Table 1), circumscribing Lake Michigan. (b) Principal component analysis (PCA) for all genotyped individuals illustrates substantial genetic differences between Green Bay and main basin yellow perch. Also notice the larger spread of Green Bay individuals along axis 2, which suggests more variation among sites within Green Bay than sites within the main basin despite the much larger size of the main basin. (c) Results from STRUCTURE further illustrate the large genetic differences between Green Bay and main basin yellow perch where the proportion of Green Bay (red) or main basin (blue) ancestry is depicted for every individual as a single vertical line. Mean pairwise FST between Green Bay and main basin sites is equal to 0.11. The key to site name abbreviations is provided in Table 1.
Patterns of genetic differentiation among yellow perch populations within each region of Lake Michigan. For Green Bay populations (red), principal coordinate analysis (PCoA) of pairwise FST values, where larger distances in two‐dimensional space reflect higher pairwise FST values (a), STRUCTURE output for K = 3 (b), and principal component analyses (PCA) for individual genotypes (c) all reveal genetic differentiations between Big Bay de Noc (BDN; representing two life stages: young‐of‐year (BDNYO) and adults (BDN19), Little Bay de Noc (LBD; representing two life stages: young‐of‐year (LBDYO) and adults (LBD19), and southern Green Bay (SGB; representing adults from two separate collection sites (MEN and SGB) where SGB adults were sampled in two consecutive years). For the main basin populations, there is subtle population structure between northern (MAN, NUB, CHE, CHX, SUT, and NPT) and southern Lake Michigan collection sites as again determined by principal coordinate analysis of pairwise FST values (d), STRUCTURE output for K = 2 (e), and principal component analyses for all individual genotypes (f). Collection site information and IDs can be found in Table 1.
Relationships between predictive FST values among main basin Lake Michigan yellow perch populations obtained from our eco‐genetic model parameterized with biophysical current data and empirical estimates of FST from 9302 SNPs. (a) Connectivity matrices (n = 216; Table 2) derived from our biophysical model that were characterized by higher population connectivity (x‐axis) performed better at predicting (here measured as goodness of fit) our empirical estimates of FST, after passing through the eco‐genetic model to generate predictive FST values, than connectivity matrices characterized by low population connectivity. (b) To track simulated particles in the biophysical models, Lake Michigan was divided into 40 roughly equally sized polygons. (c) The relationship between predictive FST and empirical FST for 10 replicated simulations for the connectivity matrix with the highest predictive ability. Each point represents a single pairwise FST comparison between two main basin sites estimated from a single simulation (x‐axis) and from RAD‐Seq data (y‐axis). A perfect fit (i.e., perfect prediction) would result in all points laying directly on the 1:1 line (dashed line). (d) The corresponding connectivity matrix with the best predictive ability (used to create predictive FST values illustrated in panel c) occurred during a time period with high connectivity among neighboring sites. (e) The relationship between predictive FST and empirical FST for 10 replicated simulations for the connectivity matrix with the lowest predictive ability. Notice that many predictive pairwise comparisons had FST values 2–3 times higher than those observed empirically. (f) The corresponding connectivity matrix, with low predictive ability, showed much lower connectivity among sites (inset illustrates color scale used in d and f where dark blue represents no connectivity between grid regions). For all scenarios, including those illustrated in panels c and e, predictive ability was assessed with 100 replicate simulations, but is illustrated here with 10 replicate simulations for visual clarity. Note that while Green Bay was included in the biophysical model (grid regions 1–3 in panel b and grids 1–3 in panels d and f), it was not included in the eco‐genetic models because the orders of magnitude higher FST made it challenging to resolve patterns among main basin populations.
Drivers of population connectivity and genetic differentiation in main basin Lake Michigan yellow perch. Points represent the average correlation (x axis) and slope (y axis) values between predictive (generated from the integrated biophysical eco‐genetic model) and empirical FST for 100 simulations per unique set of parameter values (Table 3). A perfect fit between predictive and empirical values would lie on the 1:1 line y=x and would have a correlation and slope equal to one. Colors represent the effect of particular parameters (across all sets of parameter values) for the top 20% of correlation and slope estimates (see Figure S15 for full color). Insets illustrate the relative contributions of particular parameter values contributing to the top 20% of model predictions. Across all parameters, the specific year and week that particles were released in the biophysical model had high predictive ability (a, b), as did vertical swimming ability (c). Pelagic larval duration, the number of years that the eco‐genetic model was run (“duration”), and the local population size had lower predictive ability (d–f).
Relative contribution of dispersive currents and other drivers of genetic population connectivity in main basin yellow perch. (a) The effect of release year and week (across all sets of parameter values) for the top 20% of correlation and slope estimates illustrates that predictive values generated from connectivity matrices for specific weeks (especially those in 2016 and weeks 5 and 6) constituted a higher proportion of all integrated biophysical eco‐genetic simulations and thus have high predictive ability. The connectivity matrices with high predictive ability reflect time periods with highly dispersive currents (see Figure 3; Figure S18). Conversely, certain weeks had low predictive ability that never appeared in the top 20% of estimates (e.g., 2014). Release weeks correspond to: 1 = last week of May, 2 = 1st week of June, 3 = 2nd week of June, 4 = 3rd week of June, 5 = 4th week of June, 6 = 1st week of July. (b) The percent of variance explained by model parameters. The specific release year and week explained most of the variation, followed by vertical swimming behavior (Swim), year alone (Year), and pelagic larval duration (PLD). The week of release alone (Week), local population size (N), and number of generations that the eco‐genetic model was run (Gens) explained the least amount of variation.
Dispersive currents explain patterns of population connectivity in an ecologically and economically important fish

June 2023

·

74 Reads

How to identify the drivers of population connectivity remains a fundamental question in ecology and evolution. Answering this question can be challenging in aquatic environments where dynamic lake and ocean currents coupled with high levels of dispersal and gene flow can decrease the utility of modern population genetic tools. To address this challenge, we used RAD‐Seq to genotype 959 yellow perch (Perca flavescens), a species with an ~40‐day pelagic larval duration (PLD), collected from 20 sites circumscribing Lake Michigan. We also developed a novel, integrative approach that couples detailed biophysical models with eco‐genetic agent‐based models to generate “predictive” values of genetic differentiation. By comparing predictive and empirical values of genetic differentiation, we estimated the relative contributions for known drivers of population connectivity (e.g., currents, behavior, PLD). For the main basin populations (i.e., the largest contiguous portion of the lake), we found that high gene flow led to low overall levels of genetic differentiation among populations (FST = 0.003). By far the best predictors of genetic differentiation were connectivity matrices that were derived from periods of time when there were strong and highly dispersive currents. Thus, these highly dispersive currents are driving the patterns of population connectivity in the main basin. We also found that populations from the northern and southern main basin are slightly divergent from one another, while those from Green Bay and the main basin are highly divergent (FST = 0.11). By integrating biophysical and eco‐genetic models with genome‐wide data, we illustrate that the drivers of population connectivity can be identified in high gene flow systems.

Time‐scaled phylogeny of DFTD mitochondrial sequences in the West Pencil Pine devil population. Branches are coloured based on clade designations (A2, B & C) from a Tasmania‐wide analysis (Kwon et al., 2020). Well‐supported putative sub‐clades (B2–4) are also shown. Node size reflects posterior support (see legend). *Denotes diploid tumour clade. All other clades are tetraploid. Nodes are scaled by posterior support (see legend) and grey lines indicating MRCA estimates for well‐supported nodes (posterior support >0.9). ‘I’ indicates the basal node that distinguishes Clade C from the other clades and ‘II’ indicates the node that distinguishes Clade B from A2.
(a) Devil population size at West Pencil Pine (dotted line with purple confidence intervals) and DFTD genetic diversity (solid line with green confidence intervals). The top panel in grey illustrates the distribution of sampling and coalescent events and shows that diversity was not dependent on sampling intensity. (b) DFTD prevalence (solid line with red confidence intervals) and DFTD force of infection (FOI, vertical bars).
(a) Heat map showing contemporaneous Pearson correlation coefficients for the relationships between estimated DFTD genetic diversity, prevalence, force of infection (FOI) and devil population size. (b–d) Cross‐correlation functions (CCFs) for each pair of variables in relation to the mean estimated devil population. (e) CCF for the relationship between FOI and DFTD genetic diversity. The blue dotted line indicates the significance threshold (p = 0.05).
The tumour is in the detail: Local phylogenetic, population and epidemiological dynamics of a transmissible cancer in Tasmanian devils

June 2023

·

60 Reads

Infectious diseases are a major threat for biodiversity conservation and can exert strong influence on wildlife population dynamics. Understanding the mechanisms driving infection rates and epidemic outcomes requires empirical data on the evolutionary trajectory of pathogens and host selective processes. Phylodynamics is a robust framework to understand the interaction of pathogen evolutionary processes with epidemiological dynamics, providing a powerful tool to evaluate disease control strategies. Tasmanian devils have been threatened by a fatal transmissible cancer, devil facial tumour disease (DFTD), for more than two decades. Here we employ a phylodynamic approach using tumour mitochondrial genomes to assess the role of tumour genetic diversity in epidemiological and population dynamics in a devil population subject to 12 years of intensive monitoring, since the beginning of the epidemic outbreak. DFTD molecular clock estimates of disease introduction mirrored observed estimates in the field, and DFTD genetic diversity was positively correlated with estimates of devil population size. However, prevalence and force of infection were the lowest when devil population size and tumour genetic diversity was the highest. This could be due to either differential virulence or transmissibility in tumour lineages or the development of host defence strategies against infection. Our results support the view that evolutionary processes and epidemiological trade‐offs can drive host‐pathogen coexistence, even when disease‐induced mortality is extremely high. We highlight the importance of integrating pathogen and population evolutionary interactions to better understand long‐term epidemic dynamics and evaluating disease control strategies.

Sampling locations and genetic background of the Nile tilapia (Oreochromis niloticus) populations used in the current study.
Population structure of Nile tilapia (Oreochromis niloticus) populations in study. Principal components analysis (a) based on 2 M SNPs from Poolseq and (b) based on 16 K SNPs from SNP array data. (c) STRUCTURE analyses (K = 2,3,4,5, in descending order) generated using SNP array data.
Manhattan plots indicating the FST patterns among Nile tilapia (Oreochromis niloticus) populations. FST values were estimated when comparing GIFTw to other Nile tilapia populations. Vertical dashed line indicates the outlier region on Oni06 identified across comparisons. Red dots represent the outliers found for each comparison.
Genome‐wide ZHp values for different Nile tilapia (Oreochromis niloticus) populations, including (a) Abbassa, (b) Kenya, (c) FAST, (d) GIFTd, (e) GIFTp, and (f) GIFTw. Red dots represent the outliers found within each population.
Genetic differentiation following recent domestication events: A study of farmed Nile tilapia (Oreochromis niloticus) populations

June 2023

·

226 Reads

Nile tilapia (Oreochromis niloticus) is among the most farmed finfish worldwide, distributed across different environmental conditions. Its wide distribution has mainly been facilitated by several breeding programs and widespread dissemination of genetically improved strains. In the first Nile tilapia study exploiting a whole‐genome pooled sequencing (Poolseq) approach, we identified the genetic structure and signatures of selection in diverse, farmed Nile tilapia populations, with a particular focus on the GIFT strain, developed in the 1980s, and currently managed by WorldFish (GIFTw). We also investigated important farmed strains from The Philippines and Africa. Using both SNP array data and Poolseq SNPs, we characterized the population structure of these samples. We observed the greatest separation between the Asian and African populations and greater admixture in the Asian populations than in the African ones. We also established that the SNP array data were able to successfully resolve relationships between these diverse Nile tilapia populations. The Poolseq data identified genomic regions with high levels of differentiation (FST) between GIFTw and the other populations. Gene ontology terms associated with mesoderm development were significantly enriched in the genes located in these regions. A region on chromosome Oni06 was genetically differentiated in pairwise comparisons between GIFTw and all other populations. This region contains genes associated with muscle‐related traits and overlaps with a previously published QTL for fillet yield, suggesting that these traits may have been direct targets for selection on GIFT. A nearby region was also identified using XP‐EHH to detect genomic differentiation using the SNP array data. Genomic regions with high or extended homozygosity within each population were also identified. This study provides putative genomic landmarks associated with the recent domestication process in several Nile tilapia populations, which could help to inform their genetic management and improvement.

Effects of hunting rate (φ, with flow scale ε = 0.50 and timing of harvest overlap with migrations ω = 0.35) on the annual (a) mean breeding value for male horn length (cm), (b) mean horn length of 6‐year‐old males (cm), (c) standard deviation of horn length of 6‐year‐old males (cm), and (d) mean proportion of legal males in the harvested population. Lines and shades represent the averages, and the associated 95% confidence intervals over all replicate runs. The vertical dashed line marks the start of annual harvest at TH = 15 years.
Combined effects of hunting rate (φ, with timing of harvest overlap with migrations ω = 0.35) and flow scale (ε) on changes over 60 years of harvest in mean breeding value for horn length of bighorn sheep males (∆bvm, differences in cm between the average value at TF = 75 years and before TH = 15 years) in the (a) harvested and (b) protected populations. The black line in the box indicates the median, the lower and upper edges mark the 1st and 3rd quartiles, and the lower and upper whiskers extend to the smallest and largest values no further than 1.5 times the inter‐quartile range over all replicate runs. Violin shapes represent density estimates of the y‐axis variables in each combination of values for φ and ε.
Effects of flow scale (ε) under different hunting rates (φ = 0.37 or 0.70, with timing of harvest overlap with migrations ω = 0.35) on the annual proportion of legal males in harvested (a, c) and protected (b, d) populations. Lines and shades represent averages and associated 95% confidence intervals over all replicate runs. The vertical dashed line marks the start of annual harvest at TH = 15 years.
Effects (from harvest start at TH = 15 years) of flow scale (ε) under different hunting rates (φ = 0.35 or 0.70, with timing of harvest overlap with migrations ω = 0.35) on the annual mean of male horn length (cm) of hunted bighorn sheep males according to their origin (a, c: residents from the harvested population; or b, d: migrants from the protected population). Lines and shades represent the averages and the associated 95% confidence interval between all replicate runs.
Effects of timing of harvest overlap with migrations (ω = 0.00, 0.35 or 0.70) under different hunting rates (φ = 0.35 or 0.70, with flow scale ε = 0.50) on the annual mean breeding value for male horn length (cm) within harvested (a, c) and protected (b, d) populations. Lines and shades represent averages and associated 95% confidence intervals of all replicate runs. The vertical dashed line marks the start of annual harvest at TH = 15 years.
Genetic rescue from protected areas is modulated by migration, hunting rate, and timing of harvest

May 2023

·

103 Reads

In terrestrial and marine ecosystems, migrants from protected areas may buffer the risk of harvest‐induced evolutionary changes in exploited populations that face strong selective harvest pressures. Understanding the mechanisms favoring genetic rescue through migration could help ensure evolutionarily sustainable harvest outside protected areas and conserve genetic diversity inside those areas. We developed a stochastic individual‐based metapopulation model to evaluate the potential for migration from protected areas to mitigate the evolutionary consequences of selective harvest. We parameterized the model with detailed data from individual monitoring of two populations of bighorn sheep subjected to trophy hunting. We tracked horn length through time in a large protected and a trophy‐hunted populations connected through male breeding migrations. We quantified and compared declines in horn length and rescue potential under various combinations of migration rate, hunting rate in hunted areas and temporal overlap in timing of harvest and migrations, which affects the migrants' survival and chances to breed within exploited areas. Our simulations suggest that the effects of size‐selective harvest on male horn length in hunted populations can be dampened or avoided if harvest pressure is low, migration rate is substantial, and migrants leaving protected areas have a low risk of being shot. Intense size‐selective harvest impacts the phenotypic and genetic diversity in horn length, and population structure through changes in proportions of large‐horned males, sex ratio and age structure. When hunting pressure is high and overlaps with male migrations, effects of selective removal also emerge in the protected population, so that instead of a genetic rescue of hunted populations, our model predicts undesirable effects inside protected areas. Our results stress the importance of a landscape approach to management, to promote genetic rescue from protected areas and limit ecological and evolutionary impacts of harvest on both harvested and protected populations.

Genomics reveal the origins and current structure of a genetically depauperate freshwater species in its introduced Alaskan range

May 2023

·

88 Reads

Invasive species are a major threat to global biodiversity, yet also represent large‐scale unplanned ecological and evolutionary experiments to address fundamental questions in nature. Here we analyzed both native and invasive populations of predatory northern pike (Esox lucius) to characterize landscape genetic variation, determine the most likely origins of introduced populations, and investigate a presumably postglacial population from Southeast Alaska of unclear provenance. Using a set of 4329 SNPs from 351 individual Alaskan northern pike representing the most widespread geographic sampling to date, our results confirm low levels of genetic diversity in native populations (average 𝝅 of 3.18 × 10⁻⁴) and even less in invasive populations (average 𝝅 of 2.68 × 10⁻⁴) consistent with bottleneck effects. Our analyses indicate that invasive northern pike likely came from multiple introductions from different native Alaskan populations and subsequently dispersed from original introduction sites. At the broadest scale, invasive populations appear to have been founded from two distinct regions of Alaska, indicative of two independent introduction events. Genetic admixture resulting from introductions from multiple source populations may have mitigated the negative effects associated with genetic bottlenecks in this species with naturally low levels of genetic diversity. Genomic signatures strongly suggest an excess of rare, population‐specific alleles, pointing to a small number of founding individuals in both native and introduced populations consistent with a species' life history of limited dispersal and gene flow. Lastly, the results strongly suggest that a small isolated population of pike, located in Southeast Alaska, is native in origin rather than stemming from a contemporary introduction event. Although theory predicts that lack of genetic variation may limit colonization success of novel environments, we detected no evidence that a lack of standing variation limited the success of this genetically depauperate apex predator.

Map of China, showing the 21 sampling localities (brownish red dots) and the important geographic barriers including the Yellow River, the Yangtze River, the boundary between the third and second terrain steps, and the boundary between the second and first terrain steps (a). Results of the ADMIXTURE analysis of B. gargarizans samples (K = 2–5, with an optimal K of 3) based on high‐quality loci (b). Results of PCA (c), each dot represents an individual, and the ovals represent 85% confidence intervals for different evolutionary clusters. AK: Ankang, Shanxi; AQ: Anqing, Anhui; BD: Baoding, Hebei; BT: Litang, Sichuan; CD: Changde, Hunan; CDE: Chengde, Hebei; CY: Chaoyang, Liaoning; DZ: Dazhou, Sichuan; GL: Guilin, Guangxi; MHK: Meihekou, Jilin; LN: Longnan, Gansu; LYG: Lianyungang, Jiangsu; QZ: Quzhou, Zhejiang; PL: Pingliang, Gansu; SCA: Shimian2, Sichuan; SCB: Shimian2, Sichuan; SCC: Kangding, Sichuan; SY: Shenyang, Liaoning; XX: Xiaoxian, Anhui; ZMD: Zhumadian, Henan; ZY: Zunyi, Guizhou.
Pairwise visual heatmap showing reciprocal causal modeling results. Red and blue in individual cells respectively represent positive and negative values of the reciprocal model. The variables with more positive values have a stronger support.
Fitted I‐splines of the generalized dissimilarity modelling for the relationship between observed compositional dissimilarity and predicted ecological distance (a), and the environmental correlates of partial ecological distance based on three important variables, maximum temperature of the warmest month (b), Euclidean distance (c) and precipitation of wettest month (d). Black dots indicate FST values between populations. The black line represents the model fit, and the shaded area is the error bands (±one standard deviation). Each curve indicates the relative importance of an environmental variable in explaining changes in allele frequency, holding all other variables constant. The shape of each curve shows the rate at which allele frequencies change along the gradient.
Climate change‐related genetic offset predicted from generalized dissimilarity modeling based on an average scenario of SSP245 in the 2100's climate. The color scale indicates the magnitude of the mismatch between current and future climate‐driven turnover of alleles, the more genomic offset to future climate conditions and higher risks of population decline.
Genomic insights into local adaptation in the Asiatic toad Bufo gargarizans, and its genomic offset to climate warming

May 2023

·

192 Reads

Genomic signatures of local adaptation have been identified in many species but remain sparsely studied in amphibians. Here, we explored genome‐wide divergence within the Asiatic toad, Bufo gargarizans, to study local adaptation and genomic offset (i.e., the mismatch between current and future genotype‐environment relationships) under climate warming scenarios. We obtained high‐quality SNP data for 94 Asiatic toads from 21 populations in China to study spatial patterns of genomic variation, local adaptation, and genomic offset to warming in this wide‐ranging species. Population structure and genetic diversity analysis based on high‐quality SNPs revealed three clusters of B. gargarizans in the western, central‐eastern, and northeastern portions of the species' range in China. Populations generally dispersed along two migration routes, one from the west to the central‐east and one from the central‐east to the northeast. Both genetic diversity and pairwise FST were climatically correlated, and pairwise FST was also correlated with geographic distance. Spatial genomic patterns in B. gargarizans were determined by the local environment and geographic distance. Global warming will increase the extirpation risk of B. gargarizans.

Centaurea solstitialis sampling sites in (a) Turkey and Spain (native), and non‐native regions of (b) California coast, (c) central Argentina and Chile, and (d) SE Australia. Each dot corresponds to a population.
Principal component analysis (PCA) on six phenotypic traits – comparison between native and non‐native ranges. PCA1 and PCA2 together explained 54.2% of the inertia variance in the two axes. The first PC axis was negatively associated with the length of the largest spine and positively associated with the days to first flower while the second PC axis was negatively associated with the number of capitula. The larger symbol of the two groups represents the centroid (i.e., the average coordinates of samples in that group).
Capitula number and seed size variation along climatic gradients in Turkey (native range) and Argentina, Chile, and California (introduced range).
(a) Individual assignments from STRUCTURE analysis based on 1975 neutral SNP loci of 144 individuals of C. solstitialis. Each vertical bar shows the proportional representation of the estimated group membership for a single individual. K is the number of genetic groups. The best estimate of K is K = 2. (b) Discriminant analysis of principal components (DAPC) based on neutral SNPs and using geographic regions as prior clusters. Ovals are 95% inertia ellipses. Lines connect each individual to the regional mean value.
Trait evolution during a rapid global weed invasion despite little genetic differentiation

April 2023

·

183 Reads

Invasive species often possess a great capacity to adapt to novel environments in the form of spatial trait variation, as a result of varying selection regimes, genetic drift, or plasticity. We explored the geographic differentiation in several phenotypic traits related to plant growth, reproduction, and defense in the highly invasive Centaurea solstitialis by measuring neutral genetic differentiation (FST), and comparing it with phenotypic differentiation (PST), in a common garden experiment in individuals originating from regions representing the species distribution across five continents. Native plants were more fecund than non‐native plants, but the latter displayed considerably larger seed mass. We found indication of divergent selection for these two reproductive traits but little overall genetic differentiation between native and non‐native ranges. The native versus invasive PST–FST comparisons demonstrated that, in several invasive regions, seed mass had increased proportionally more than the genetic differentiation. Traits displayed different associations with climate variables in different regions. Both capitula numbers and seed mass were associated with winter temperature and precipitation and summer aridity in some regions. Overall, our study suggests that rapid evolution has accompanied invasive success of C. solstitialis and provides new insights into traits and their genetic bases that can contribute to fitness advantages in non‐native populations.

Fine-scale spatial genetic structure in a locally abundant native bunchgrass (Achnatherum thurberianum) including distinct lineages revealed within seed transfer zones

April 2023

·

72 Reads

Analyses of the factors shaping genetic variation in widespread plant species are important for understanding the evolutionary history and local adaptation and have applied significance for guiding conservation and restoration decisions. Thurber's needlegrass (Achnatherum thurberianum) is a widespread, locally abundant grass that inhabits heterogeneous arid environments of western North America and is of restoration significance. It is a common component of shrubland steppe communities in the Great Basin Desert, where drought, fire, and invasive grasses have degraded natural communities. Using a reduced representation sequencing approach, we generated SNP data at 5677 loci across 246 individuals from 17 A. thurberianum populations spanning five previously delineated seed zones from the western Great Basin. Analyses revealed a pronounced population genetic structure, with individuals forming consistent geographical clusters across a variety of population genetic analyses and spatial scales. Low levels of genetic diversity within populations, as well as high population estimates of linkage disequilibrium and relatedness, were consistent with self-fertilization as a contributor to population differentiation. Variance partitioning and partial redundancy analysis (pRDA) indicated local adaptation to environment as additionally influencing the spatial distribution of genetic variation. The environmental variables driving these results were similar to those implicated in recent geneco-logical work which inferred local adaptation for seed zone delineation. Our analyses also revealed a complex evolutionary history of A. thurberianum in the Great Basin, where previously delineated seed zones contain distantly related populations. Our results indicate evolutionary history, mating system, and differentiation across distinct geographic and environmental scales have shaped genetic variation in A. thur-berianum and illustrate how numerous aspects of population genetic variation might require consideration for restoration planning.

Experimental design. There were five treatments assigned randomly across 20 channels: river water only (without wastewater or ultrafiltration; 0% WW) and two concentrations of wastewater (30%WW and 80%WW) with ultrafiltration (30% WW‐UF and 80% WW‐UF) or without ultrafiltration (30% WW and 80% WW). Within each channel, there were three experimental containers, each containing 10 individuals (juveniles, males, or females) and five leaf discs. Host performance was measured as survival, growth, and food consumed. For analyses of the gut microbiome, a subset of two males and two females (per experimental container) were dissected to collect midguts and hindguts, which were used for 16S rRNA amplicon sequencing.
Treatment effects on host performance. (a–c) Influence of wastewater and filtration on host growth and feeding. Juveniles, males, and females are shown with green, blue, and pink points, respectively. (a) Boxplots represent variation for growth, measured as change in mean size (in mm²) among wastewater treatments (0%, 30%, and 80% wastewater). (b) Scatter plot representing the relationship between growth and initial size (as mean area, in mm²) of A. aquaticus. (c) Boxplots represent variation in food consumption (change in mean leaf area, in mm²) between nonfiltered wastewater and ultrafiltration (UF: ultrafiltered) treatments (0% WW, 30% WW, 80% WW, 30% WW UF, and 80% WW UF). Statistically significant effects are shown above the plots (for detailed results see Table S6).
Microbiome composition and abundance. (a) Stacked bar plots show relative abundances of different bacterial taxa (averaged per gut tissue and pooled across treatments) at the level of phylum (left) and class (right). Relative abundances per individual samples can be found in Figure S2I. (b) Differential abundance of operational taxonomic units (zOTUs) between tissues. Dot plot shows those zOTUs that were significantly differentially abundant between gut tissues at the taxonomic level of class (DESeq2; p adj <0.001). Dots are colored by the taxonomic order to which each zOTUs belongs to.
Effects of wastewater on microbiome composition. (a) Indicator taxa in different wastewater concentrations in the hindgut. Dot plot shows significant zOTUs (p adj <0.05) at the taxonomic level of class. Dot size represents the p value, and dot color represents the taxonomic order to which each zOTUs belongs to. (b) Stacked barplots show relative abundance averaged per wastewater concentration (0%, 30%, or 80%WW) of different bacterial taxa at the level of class in the hindgut. Relative abundances per individual samples can be found in Figure S3A. (c) Indicator taxa in different wastewater concentrations in the midgut. Dot plot shows every significant zOTU (p adj < 0.05), at the taxonomic level of class. Dot size represents the p value, and dot color represents the taxonomic order to which each zOTU belongs to. (d) Ordination plot of the principal coordinate analysis (PCoA) for hindgut samples based on Bray–Curtis (BC) distances colored and grouped by treatment, with 0%, 30%, and 80% wastewater in green, orange, and purple, respectively. Ellipses denote the 95% confidence interval.
Effects of wastewater‐associated bacteria on microbiome composition. (a). Stacked bar plots show relative abundances of different bacterial taxa (averaged per ultrafiltration (UF) treatment) of different bacterial taxa at the taxonomic level of class in males (left plot) and females (right plot). Wastewater treatments without ultrafiltration (i.e. non‐UF: 30%WW and 80%WW) and with ultrafiltration (i.e. UF: 30%WW‐UF and 80%WW‐UF) are pooled in these plots. The relative abundances per individual samples can be found in Figure S1B. (b) Indicator taxa associated with the ultrafiltration (UF) treatments (pooled across different WW dilution treatments) in the hindguts of females and males. Dot plot shows every significant zOTUs (p adj < 0.05), at the taxonomic level of class. Dot size represents the p value, and dot color represents the taxonomic order to which each zOTUs belongs to.
Effects of anthropogenic stress on hosts and their microbiomes: Treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus)

March 2023

·

95 Reads

Human activity is a major driver of ecological and evolutionary change in wild populations and can have diverse effects on eukaryotic organisms as well as on environmental and host‐associated microbial communities. Although host–microbiome interactions can be a major determinant of host fitness, few studies consider the joint responses of hosts and their microbiomes to anthropogenic changes. In freshwater ecosystems, wastewater is a widespread anthropogenic stressor that represents a multifarious environmental perturbation. Here, we experimentally tested the impact of treated wastewater on a keystone host (the freshwater isopod Asellus aquaticus) and its gut microbiome. We used a semi‐natural flume experiment, in combination with 16S rRNA amplicon sequencing, to assess how different concentrations (0%, 30%, and 80%) of nonfiltered wastewater (i.e. with chemical toxicants, nutrients, organic particles, and microbes) versus ultrafiltered wastewater (i.e. only dissolved pollutants and nutrients) affected host survival, growth, and food consumption as well as mid‐ and hindgut bacterial community composition and diversity. Our results show that while host survival was not affected by the treatments, host growth increased and host feeding rate decreased with nonfiltered wastewater – potentially indicating that A. aquaticus fed on organic matter and microbes available in nonfiltered wastewater. Furthermore, even though the midgut microbiome (diversity and composition) was not affected by any of our treatments, nonfiltered wastewater influenced bacterial composition (but not diversity) in the hindgut. Ultrafiltered wastewater, on the other hand, affected both community composition and bacterial diversity in the hindgut, an effect that in our system differed between sexes. While the functional consequences of microbiome changes and their sex specificity are yet to be tested, our results indicate that different components of multifactorial stressors (i.e. different constituents of wastewater) can affect hosts and their microbiome in distinct (even opposing) manners and have a substantial impact on eco‐evolutionary responses to anthropogenic stressors.

Phases of acceleration, deceleration, and decline as a function of age in simulations yielding a gain in LRS >1%. Figure shows that, for those simulations, deceleration and decline exist in a substantial part of the parameter space. To be contrasted with Supp. Figure 2 shows that, when CS does not allow for a gain in LRS, deceleration and decline are more rarely observed.
(a) Dynamics of accumulation of damaged (in red) and senescent (in green) cells. Shows the strategy of diverting a proportion of cells toward senescence up to a certain point (dashed red line). (b) Cellular dynamics translate into mortality components: Cancer (in red) and ageing‐related (green). Organismal incidence curves mirror cellular accumulation curves. Blue line depicts survival and shows that, when the decline of cancer incidence starts, survival is less than 10%.
Lifetime prevalence of cancer is affected by life‐history traits (here, extrinsic mortality) and by the existence of a deceleration/decline of incidence at late ages. It shows the importance of life‐history traits when addressing whether cellular senescence evolved as an adaptation against cancer and that deceleration and decline are drivers of cancer prevalence.
Trajectories of (a) incidence of cancer and (b) incidence of ageing‐related causes of mortality before senolysis (dashed lines) and after senolysis (solid lines). It shows that senolysis leads to an increase in cancer incidence (red) and a decrease in ageing‐related causes (green).
Percentage change in the cumulative incidence of (a) cancer and (b) ageing‐related causes after senolysis.
Modeling of senescent cell dynamics predicts a late‐life decrease in cancer incidence

March 2023

·

47 Reads

Current oncogenic theories state that tumors arise from cell lineages that sequentially accumulate (epi)mutations, progressively turning healthy cells into carcinogenic ones. While those models found some empirical support, they are little predictive of intraspecies age‐specific cancer incidence and of interspecies cancer prevalence. Notably, in humans and lab rodents, a deceleration (and sometimes decline) of cancer incidence rate has been found at old ages. Additionally, dominant theoretical models of oncogenesis predict that cancer risk should increase in large and/or long‐lived species, which is not supported by empirical data. Here, we explore the hypothesis that cellular senescence could explain those incongruent empirical patterns. More precisely, we hypothesize that there is a trade‐off between dying of cancer and of (other) ageing‐related causes. This trade‐off between organismal mortality components would be mediated, at the cellular scale, by the accumulation of senescent cells. In this framework, damaged cells can either undergo apoptosis or enter senescence. Apoptotic cells lead to compensatory proliferation, associated with an excess risk of cancer, whereas senescent cell accumulation leads to ageing‐related mortality. To test our framework, we build a deterministic model that first describes how cells get damaged, undergo apoptosis, or enter senescence. We then translate those cellular dynamics into a compound organismal survival metric also integrating life‐history traits. We address four different questions linked to our framework: can cellular senescence be adaptive, do the predictions of our model reflect epidemiological patterns observed among mammal species, what is the effect of species sizes on those answers, and what happens when senescent cells are removed? Importantly, we find that cellular senescence can optimize lifetime reproductive success. Moreover, we find that life‐history traits play an important role in shaping the cellular trade‐offs. Overall, we demonstrate that integrating cellular biology knowledge with eco‐evolutionary principles is crucial to solve parts of the cancer puzzle.

Principles of natural and human‐directed selection with levers and tools for improvement, origin of the effects on genome, if any, and advantages and drawbacks. Several objectives were considered. GEN.*ENV., Genotype–Environment interaction.
Proposed strategies for the selection of honey bee populations surviving infestations with Varroa destructor in absence of varroacidal treatments. The process varies according to the objective of the natural selection programme: productive beekeeping, conservation or rewilding (see the Glossary).
Prospects, challenges and perspectives in harnessing natural selection to solve the 'varroa problem' of honey bees

February 2023

·

364 Reads

Honey bees, Apis mellifera, of European origin are major pollinators of crops and wild flora. Their endemic and exported populations are threatened by a variety of abiotic and biotic factors. Among the latter, the ectoparasitic mite Varroa destructor is the most important single cause behind colony mortality. The selection of mite resistance in honey bee populations has been deemed a more sustainable solution to its control than varroacidal treatments. Because natural selection has led to the survival of some European and African honey bee populations to V. destructor infestations, harnessing its principles has recently been highlighted as a more efficient way to provide honey bee lineages that survive infestations when compared with conventional selection on resistance traits against the parasite. However, the challenges and drawbacks of harnessing natural selection to solve the varroa problem have only been minimally addressed. We argue that failing to consider these issues could lead to counterpro-ductive results, such as increased mite virulence, loss of genetic diversity reducing host resilience, population collapses or poor acceptance by beekeepers. Therefore, it appears timely to evaluate the prospects for the success of such programmes and the qualities of the populations obtained. After reviewing the approaches proposed in the literature and their outcomes, we consider their advantages and drawbacks and propose perspectives to overcome their limitations. In these considerations, we not only reflect on the theoretical aspects of host-parasite relationships but also on the currently largely neglected practical constraints, that is, the requirements for productive beekeeping, conservation or rewilding objectives. To optimize natural selection-based programmes towards these objectives, we suggest designs based on a combination of nature-driven phenotypic differentiation and human-directed selection of traits. Such a dual strategy aims at allowing field-realistic evolutionary approaches towards the survival of V. destructor infestations and the improvement of honey bee health.

Schematic of model workflow (top) and visualization of univariate parameter space in four simulation experiments (bottom). Experiment 1 (blue) shows how increasing phenotypic variance in return day (σ²Return Day) increases the likelihood that an offspring's trait value will deviate from their mid‐parent value (dashed gray line). Experiment 2 (orange) shows the phenotypic relationship between return day and reproductive lifespan under different phenotypic correlations (⍴). Experiment 3 (green) shows how the optimal return day (θReturn Day) for a given cohort is more likely to deviate from the mean (θ¯Return Day) when variance (σ²θ Return Day) is high. Experiment 4 (purple) gives expected fitness values associated with return day, for three different strengths of selection regime (ω, quantified using Equation 1).
Demographic output parameters (y‐axes) over 10 generations (x‐axes) for three simulations with variable input parameter values for phenotypic variance in return day (σ²Return Day; color shades). The mating system within simulations was either assortative (left) or random (right). Output parameters of interest (points), from top to bottom, were census population size (Nc), ratio of effective to census population size (Nc/Ne), mean return day, and mean reproductive lifespan. Output parameters were estimated as the mean of 100 model iterations and are bounded by 95% confidence intervals.
Demographic output parameters (y‐axes) over 10 generations (x‐axes) for three simulation experiments (colors). Each experiment consisted of three variations of a single input parameter (shades), while all other parameters were constant under an assortative mating system. The input parameters of interest were phenotypic correlation between return day and reproductive lifespan (⍴; oranges), variance in optimum return day (σ²θ Return Day; greens), and strength of selection regime (ω; purples). Output parameters of interest (points), from top to bottom, were census population size (Nc), ratio of effective to census population size (Nc/Ne), mean return day, and mean reproductive lifespan. Output parameters were estimated as the mean of 100 model iterations and are bounded by 95% confidence intervals. Comparisons within the 10th generation are provided in the supplemental materials (Figure S4).
Assortative mating for reproductive timing affects population recruitment and resilience in a quantitative genetic model

January 2023

·

80 Reads

Quantitative models that simulate the inheritance and evolution of fitness‐linked traits offer a method for predicting how environmental or anthropogenic perturbations can affect the dynamics of wild populations. Random mating between individuals within populations is a key assumption of many such models used in conservation and management to predict the impacts of proposed management or conservation actions. However, recent evidence suggests that non‐random mating may be underestimated in wild populations and play an important role in diversity‐stability relationships. Here we introduce a novel individual‐based quantitative genetic model that incorporates assortative mating for reproductive timing, a defining attribute of many aggregate breeding species. We demonstrate the utility of this framework by simulating a generalized salmonid lifecycle, varying input parameters, and comparing model outputs to theoretical expectations for several eco‐evolutionary, population dynamic scenarios. Simulations with assortative mating systems resulted in more resilient and productive populations than those that were randomly mating. In accordance with established ecological and evolutionary theory, we also found that decreasing the magnitude of trait correlations, environmental variability, and strength of selection each had a positive effect on population growth. Our model is constructed in a modular framework so that future components can be easily added to address pressing issues such as the effects of supportive breeding, variable age structure, differential selection by sex or age, and fishery interactions on population growth and resilience. With code published in a public Github repository, model outputs may easily be tailored to specific study systems by parameterizing with empirically generated values from long‐term ecological monitoring programs.

Bridging the genotype–phenotype gap. Highlighted techniques (grey) contribute to a detailed understanding of gene regulation on the different levels of the central dogma and enable causal connection of genotypes to phenotypes (pink). Abbreviations: CRISPR‐Cas9, clustered regularly interspaced short palindromic repeats; dFISH, double fluorescent in‐situ hybridization; FIB‐SEM, focussed ion beam scanning electron microscopy; HCR, hybridization chain reaction; ISH, in‐situ hybridization; NGS, next generation sequencing; scATAC‐seq, single‐cell assay for transposase‐accessible chromatin sequencing; scProteomics, single‐cell proteomics; scRNA‐seq, single‐cell RNA sequencing; SEM, Scanning electron microscopy; TEM, transmission electron microscopy; TRGs, taxonomically restricted genes.
Pyramid of animal research organisms. Schematic representation of selected animal model systems (a) and their phylogeny (b) after (Dunn et al., 2014). Animals are separated into different categories from genetic systems (blue), over closed life cycle transgenics (yellow), transient transgenics (red), and gene knockdown (green) to all others (grey). All images were freely accessible from PhyloPic, except Macrostomum lignano (Platyhelminth). The Kinorhyncha (credit Noah Schlottman, photo by Martin V. Sørensen), Priapulida (credit Bruno C. Vellutini), Nematomorpha (credit Eduard Solà Vázquez, vectored by Yan Wong), Gastropoda (credit Armelle Ansart (photograph), Maxime Dahirel (digitization)), and Arthropoda (credit Maija Karala) silhouettes were used under the following license (https://creativecommons.org/licenses/by‐sa/3.0/) with no changes.
Marine animal evolutionary developmental biology—Advances through technology development

January 2023

·

293 Reads

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.

Variance explained by each of three mixture distributions (σg2 × 10⁻² = large effect; σg2 × 10⁻³ = small effect and σg2 × 10⁻⁴ = polygenic effect) for each trait as determined by the approach of BayesR (Moser et al., 2015).
Overlap of trait‐associated SNPs for growth and terpene chemistry traits in WRC. Single dots indicate SNPs unique to each trait. Dots with connecting lines indicate SNPs shared between traits. (a) Overlap of SNPs with large effect between all assessed traits. Blue: foliar terpene traits; Yellow: wood terpene traits; Red: growth traits; Purple: traits of different categories. (b) Overlap of all trait‐associated SNPs for foliar terpene traits. (c) Overlap of all trait‐associated SNPs for wood terpene traits. (d) Overlap of all trait‐associated SNPs for growth traits.
Despite a noticeable increase in the inbreeding coefficient F in all selfing line trees with each successive selfing generation, the only significant predictor of height growth was whether a line was under deliberate artificial selection for height. (a) Change in F during selfing. F increases with each selfing generation similarly within both random and select lines. (b) Change in height BV during selfing. Height BVs increased with each selfing generation in select lines, while height BVs in random lines declined somewhat. Black line represents the regression of height BV on generation, indicating that change in height is not significant when line type is ignored. (c) Interaction plot of predicted height BV and F. In the absence of selection, increasing values of F are negatively correlated with growth. However, under selection, height BV increases despite an increase in F, indicating the effects of inbreeding are readily mitigated by moderate‐selective pressures in WRC.
Genetic architecture of terpene chemistry and growth traits and the impact of inbreeding on these traits in western redcedar (Thuja plicata)

January 2023

·

93 Reads

Western redcedar (WRC; Thuja plicata) is a conifer of the Pacific Northwest of North America prized for its durable and rot‐resistant wood. WRC has naturally low outcrossing rates and readily self‐fertilizes in nature. Challenges faced in WRC breeding and propagation involve selecting trees for accelerated growth while also ensuring enhanced heartwood rot resistance and resistance to ungulate browsing, as well as mitigating potential effects of inbreeding depression. Terpenes, a large and diverse class of specialized metabolites, confer both rot and browse resistance in the wood and foliage of WRC, respectively. Using a Bayesian modelling approach, we isolated single nucleotide polymorphism (SNP) markers estimated to be associated with three different foliar terpene traits and four different heartwood terpene traits, as well as two growth traits. We found that all traits were complex, being associated with between 1700 and 3600 SNPs linked with putatively causal loci, with significant polygenic components. Growth traits tended to have a larger polygenic component while terpene traits had larger major gene components; SNPs with small or polygenic effect were spread across the genome, while larger‐effect SNPs tended to be localized to specific linkage groups. To determine whether there was inbreeding depression for terpene chemistry or growth traits, we used mixed linear models for a genomic selection training population to estimate the effect of the inbreeding coefficient F on foliar terpenes, heartwood terpenes and several growth and dendrochronological traits. We did not find significant inbreeding depression for any assessed trait. We further assessed inbreeding depression across four generations of complete selfing and found that not only was inbreeding depression not significant but that selection for height growth was the only significant predictor for growth during selfing, suggesting that inbreeding depression due to selfing during operational breeding can be mitigated by increased selection intensity.

Distribution of R. ferrumequinum sampling sites and the supertype number in China. The supertype number is shown in the pie charts. Pie slice size is proportional to the number of supertypes. (a) Supertype number of populations. (b) Supertype number of genetic lineages and genetic diversity values for the MHC II‐DRB exon 2 loci in populations and genetic lineages of R. ferrumequinum. Genetic diversity values for MHC II‐DRB exon 2: P = private allele; S = number of segregating sites; π = average nucleotide diversity; h = number of haplotypes; NaI = mean number of alleles per individual; AR = allelic richness. MHC functional supertypes values: ST = number of supertypes; ST_SUM = total number of supertypes. (c) Genetic diversity of populations. (d) Genetic diversity of genetic lineages.
(a) Haplotype networks of MHC II ‐DRB exon 2 alleles at the nucleotide level from R. ferrumequinum. Nodes are proportional to the number of bats carrying each haplotype and are colored by the environments where the bats were trapped (see legend). Hatch marks represent mutations. Interruptions in lines indicate the presence of more than ten mutations. (b) Phylogenetic relationships of MHC II‐DRB exon 2 alleles from R. ferrumequinum and other chiropterans based on a Bayesian approach.
Pairwise population differentiation between 12 populations based on the Dest values (a) MHC II‐DRB exon 2; (b) microsatellite; (c) non‐metric two‐dimensional scaling of the R. ferrumequinum pairwise Dest values matrix.
(a) Correlations between MHC pairwise Dest/(1− Dest) values and geographic distances (km). (b) Correlations between microsatellite pairwise Dest/(1− Dest) values and geographic distances (km). (c) The distribution of 5000 bootstrapped replicates of mean pairwise Dest values derived from microsatellites (left) and the MHC locus (right). (d) Comparisons of Dest values of microsatellites to MHC class IIB for each pairwise population in this study. Error bars indicate 95% confidence intervals and were estimated using bootstrapping.
Diversifying selection and climatic effects on major histocompatibility complex class II gene diversity in the greater horseshoe bat

January 2023

·

86 Reads

Heterogeneous pathogenic stress can shape major histocompatibility complex (MHC) diversity by influencing the functional plasticity of the immune response. Therefore, MHC diversity could reflect environmental stress, demonstrating its importance in uncovering the mechanisms of adaptive genetic variation. In this study, we combined neutral microsatellite loci, an immune‐related MHC II‐DRB locus, and climatic factors to unravel the mechanisms affecting the diversity and genetic differentiation of MHC genes in the greater horseshoe bat (Rhinolophus ferrumequinum), a species with a wide geographical distribution that has three distinct genetic lineages in China. First, increased genetic differentiation at the MHC locus among populations compared using microsatellites indicated diversifying selection. Second, the genetic differentiation of MHC and microsatellites were significantly correlated, suggesting that demographic processes exist. However, MHC genetic differentiation was significantly correlated with geographical distance among populations, even after controlling for the neutral markers, suggesting a major effect of selection. Third, although the MHC genetic differentiation was larger than that for microsatellites, there was no significant difference in the genetic differentiation between the two markers among genetic lineages, indicating the effect of balancing selection. Fourth, combined with climatic factors, MHC diversity and supertypes showed significant correlations with temperature and precipitation, but not with the phylogeographic structure of R. ferrumequinum, suggesting an effect of local adaptation driven by climate on MHC diversity. Moreover, the number of MHC supertypes varied between populations and lineages, suggesting regional characteristics and support for local adaptation. Taken together, the results of our study provide insights into the adaptive evolutionary driving forces at different geographic scales in R. ferrumequinum. In addition, climate factors may have played a vital role in driving adaptive evolution in this species.

The organization of CeMEB illustrated as a sailing ship, where the different sails illustrate the most important driving forces of the centre's scientific progress
The seven CeMEB target species for which draft reference genomes have been developed. From upper left: the brittlestar Amphiura filiformis, the diatom Skeletonema marinoi, the isopod Idotea balthica, the barnacle Balanus improvisus, the bladderwrack Fucus vesiculosus, the sandgoby Pomatoschistus minutus and the snail Littorina saxatilis
Ten years of marine evolutionary biology—Challenges and achievements of a multidisciplinary research initiative

January 2023

·

204 Reads

The Centre for Marine Evolutionary Biology (CeMEB) at the University of Gothenburg, Sweden, was established in 2008 through a 10‐year research grant of 8.7 m€ to a team of senior researchers. Today, CeMEB members have contributed >500 scientific publications, 30 PhD theses and have organised 75 meetings and courses, including 18 three‐day meetings and four conferences. What are the footprints of CeMEB, and how will the centre continue to play a national and international role as an important node of marine evolutionary research? In this perspective arcticle we first look back over the 10 years of CeMEB activities and briefly survey some of the many achievements of CeMEB. We furthermore compare the initial goals, as formulated in the grant application, with what has been achieved, and discuss challenges and milestones along the way. Finally, we bring forward some general lessons that can be learnt from a research funding of this type, and we take also look ahead, discussing how CeMEB’s achievements and lessons can be used as a springboard to the future of marine evolutionary biology.

A decade of progress in marine evolutionary biology

December 2022

·

223 Reads

This article summarizes the Evolutionary Applications Special Issue, “A decade of progress in Marine Evolutionary Biology.” The globally connected ocean, from its pelagic depths to its highly varied coastlines, inspired Charles Darwin to develop the theory of evolution during the voyage of the Beagle. As technology has developed, there has been a dramatic increase in our knowledge about life on our blue planet. This Special Issue, composed of 19 original papers and seven reviews, represents a small contribution to the larger picture of recent research in evolutionary biology, and how such advancements come about through the connection of researchers, their fields, and their knowledge. The first European network for marine evolutionary biology, the Linnaeus Centre for Marine Evolutionary Biology (CeMEB), was developed to study evolutionary processes in the marine environment under global change. Though hosted by the University of Gothenburg in Sweden, the network quickly grew to encompass researchers throughout Europe and beyond. Today, more than a decade after its foundation, CeMEB's focus on the evolutionary consequences of global change is more relevant than ever, and knowledge gained from marine evolution research is urgently needed in management and conservation. This Special Issue, organized and developed through the CeMEB network, contains contributions from all over the world and provides a snapshot of the current state of the field, thus forming an important basis for future research directions.

Overall description of phenotypes and genotypes of the sample of Norway spruce. (a) Principal component analysis of the genotypes of the half‐sib families. Families are colored according to their genetic clusters (ordered by decreasing latitude in the legend): Central and South Sweden (CSE, dark red), Russia‐Baltics (RBA, light green), Northern Poland (NPL, green), Central Europe (CEU, light blue), Alps (ALP, blue), and hybrids between CSE and ALP (CSE‐ALP, pink). PC1 and PC2 explained 3.42% and 0.45% of the variance, respectively. (b) Admixture plot of the half‐sib families, with K = 3. Individuals are grouped by population and sorted according to their coancestry coefficient. (c) Principal component analysis of the phenotypes: Diameter at breast height (DBH), ring width (RW), wood density (WD), tracheid radial width (TRW), tracheid tangential width (TTW), and tracheid Wall thickness (TWT). Left panel only shows variable axes and 60% confidence ellipses. On the right panel, each datum (dot) is colored according to its cambial age (3rd year in light blue up until 13th year in dark blue). PC1 and PC2 explained 41.2% and 38.3% of the variance, respectively.
Genetic control of wood properties in Norway spruce. (a) ANOVA of genetic clusters in model (2) as a function of cambial age (from 3 to 13), and of traits: DBH (plain circle), RW (plain triangle), WD (plain square), TRW (circle), TTW (triangle), and TWT (square). (b) Principal component analysis of the residuals of the phenotypes according to model (2): Diameter at breast height (DBH), ring width (RW), wood density (WD), tracheid radial width (TRW), tracheid tangential width (TTW), and tracheid Wall thickness (TWT). Left panel only shows variable axes and 10% confidence ellipses (zoomed ×2.5), where clusters were ordered in decreasing latitude from right to left. On the right panel, each data (dot) are colored according to its genetic cluster (ordered by decreasing latitude in the legend): Central and South Sweden (CSE, dark red), Russia‐Baltics (RBA, light green), Northern Poland (NPL, green), Central Europe (CEU, light blue), Alps (ALP, blue), and hybrids between CSE and ALP (CSE‐ALP, pink). PC1 and PC2 explained 57.5% and 18.2% of the variance, respectively. (c) Distribution of pairwise FST across the genome, averaged among pairs of populations. The vertical solid black line is the average FST over the genome (0.0488), and vertical dotted lines are the QST estimated for different traits (averaged across rings): Diameter at breast height (DBH, red, QST = 0.281), ring width (RW, green, QST = 0.302), wood density (WD, brown, QST = 0.121), tracheid radial width (TRW, turquoise, QST = 0.0579), tracheid tangential width (TTW, blue, QST = 0.177), Tracheid Wall thickness (TWT, purple, QST = 0.112), and age at breast height (ABH, pink, QST = 0.066).
Divergent selection predating the Last Glacial Maximum mainly acted on macro‐phenotypes in Norway spruce

December 2022

·

85 Reads

The current distribution and population structure of many species were, to a large extent, shaped by cycles of isolation in glacial refugia and subsequent population expansions. Isolation in and postglacial expansion through heterogeneous environments led to either neutral or adaptive divergence. Norway spruce is no exception, and its current distribution is the consequence of a constant interplay between evolutionary and demographic processes. We investigated population differentiation and adaptation of Norway spruce for juvenile growth, diameter of the stem, wood density, and tracheid traits at breast height. Data from 4461 phenotyped and genotyped Norway spruce from 396 half‐sib families in two progeny tests were used to test for divergent selection in the framework of QST vs. FST. We show that the macroscopic resultant trait (stem diameter), unlike its microscopic components (tracheid dimensions) and juvenile growth, was under divergent selection that predated the Last Glacial Maximum. Altogether, the current variation in these phenotypic traits in Norway spruce is better explained by local adaptation to ancestral environments than to current ones, where populations were partly preadapted, mainly through growth‐related traits.

Genetic diversity and structure of a recent fish invasion: Tench (Tinca tinca) in eastern North America

December 2022

·

160 Reads

Introduced and geographically expanding populations experience similar eco‐evolutionary challenges, including founder events, genetic bottlenecks, and novel environments. Theory predicts that reduced genetic diversity resulting from such phenomena limits the success of introduced populations. Using 1900 SNPs obtained from restriction‐site‐associated DNA sequencing, we evaluated hypotheses related to the invasion history and connectivity of an invasive population of Tench (Tinca tinca), a Eurasian freshwater fish that has been expanding geographically in eastern North America for three decades. Consistent with the reported history of a single introduction event, our findings suggest that multiple introductions from distinct genetic sources are unlikely as Tench had a small effective population size (~114 [95% CI = 106–123] individuals), no strong population subdivision across time and space, and evidence of a recent genetic bottleneck. The large genetic neighbourhood size (220 km) and weak within‐population genetic substructure suggested high connectivity across the invaded range, despite the relatively large area occupied. There was some evidence for a small decay in genetic diversity as the species expanded northward, but not southward, into new habitats. As eradicating the species within a ~112 km radius would be necessary to prevent recolonization, eradicating Tench is likely not feasible at watershed—and possibly local—scales. Management should instead focus on reducing abundance in priority conservation areas to mitigate adverse impacts. Our study indicates that introduced populations can thrive and exhibit relatively high levels of genetic diversity despite severe bottlenecks (<1.5% of the ancestral effective population size) and suggests that landscape heterogeneity and population demographics can generate variability in spatial patterns of genetic diversity within a single range expansion.

Complex patterns shape immune genes diversity during invasion of common raccoon in Europe – Selection in action despite genetic drift

December 2022

·

35 Reads

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.

Why do we need predictions? (1) To test hypotheses of evolution for a better fundamental understanding of evolving systems. Based on their phylogenetic history we can predict how species evolve when exposed to a given treatment. These predictions can be tested with experimental evolution approaches. (2) To be prepared for future outbreaks, we aim to match vaccines with the most common influenza strains each year. (3) To have control over evolutionary outcomes and design treatment strategies that prevent the evolution of resistance from happening in pathogens. In this review, we focus on predicting evolution for goals (2) and (3), while (1) plays a role in obtaining the information on the basis of these predictions.
Selection of methods that are used to predict evolution
Towards evolutionary predictions: Current promises and challenges

December 2022

·

386 Reads

Evolution has traditionally been a historical and descriptive science, and predicting future evolutionary processes has long been considered impossible. However, evolutionary predictions are increasingly being developed and used in medicine, agriculture, biotechnology and conservation biology. Evolutionary predictions may be used for different purposes, such as to prepare for the future, to try and change the course of evolution or to determine how well we understand evolutionary processes. Similarly, the exact aspect of the evolved population that we want to predict may also differ. For example, we could try to predict which genotype will dominate, the fitness of the population or the extinction probability of a population. In addition, there are many uses of evolutionary predictions that may not always be recognized as such. The main goal of this review is to increase awareness of methods and data in different research fields by showing the breadth of situations in which evolutionary predictions are made. We describe how diverse evolutionary predictions share a common structure described by the predictive scope, time scale and precision. Then, by using examples ranging from SARS‐CoV2 and influenza to CRISPR‐based gene drives and sustainable product formation in biotechnology, we discuss the methods for predicting evolution, the factors that affect predictability and how predictions can be used to prevent evolution in undesirable directions or to promote beneficial evolution (i.e. evolutionary control). We hope that this review will stimulate collaboration between fields by establishing a common language for evolutionary predictions.

Comparison of bacterial suppression by phage cocktails, dual‐receptor generalists, and coevolutionarily trained phages

December 2022

·

155 Reads

The evolution and spread of antibiotic‐resistant bacteria have renewed interest in phage therapy, the use of bacterial viruses (phages) to combat bacterial infections. The delivery of phages in cocktails where constituent phages target different modalities (e.g., receptors) may improve treatment outcomes by making it more difficult for bacteria to evolve resistance. However, the multipartite nature of cocktails may lead to unintended evolutionary and ecological outcomes. Here, we compare a 2‐phage cocktail with a largely unconsidered group of phages: generalists that can infect through multiple, independent receptors. We find that λ phage generalists and cocktails that target the same receptors (LamB and OmpF) suppress Escherichia coli similarly for ~2 days. Yet, a “trained” generalist phage, which previously adapted to its host via 28 days of coevolution, demonstrated superior suppression. To understand why the trained generalist was more effective, we measured the resistance of bacteria against each of our phages. We find that, when bacteria were assailed by two phages in the cocktail, they evolved mutations in manXYZ, a host inner‐membrane transporter that λ uses to move its DNA across the periplasmic space and into the cell for infection. This provided cross‐resistance against the cocktail and untrained generalist. However, these mutations were ineffective at blocking the trained generalist because, through coevolutionary training, it evolved to bypass manXYZ resistance. The trained generalist's past experiences in training make it exceedingly difficult for bacteria to evolve resistance, further demonstrating the utility of coevolutionary phage training for improving the therapeutic properties of phages.

Low genetic diversity, local‐scale structure, and distinct genetic integrity of Korean chum salmon (Oncorhynchus keta) at the species range margin suggest a priority for conservation efforts

November 2022

·

81 Reads

Chum salmon (Oncorhynchus keta) is an ecologically and economically important species widely distributed across the North Pacific Ocean. However, the population size of this fishery resource has declined globally. Identifying genetic integrity, diversity and structure, and phylogenetic relationships of wild populations of O. keta over an entire species' range is central for developing its effective conservation and management plans. Nevertheless, chum salmon from the Korean Peninsula, which are comprised of its southwestern range margins, have been overlooked. By using mtDNA control region and 10 microsatellite loci, we here assessed the genetic diversity and structure for 16 populations, including 10 wild and six hatchery populations, encompassing the species entire geographic range in South Korea. The analyses showed that genetic diversity is significantly higher for wild than for hatchery populations. Both marker sets revealed significant genetic differentiation between some local populations. Comparisons of six wild and their respective hatchery populations indicated that allele/haplotype frequencies considerably differ, perhaps due to a strong founder effect and/or homogenizing of hatchery populations for stocking practice. Despite its single admixed gene pool for the Korean chum salmon, some local populations housing their own unique lineages should be accorded with a high priority to safeguard their genetic integrities. The results of our comparative analyses of the Korean population with other North Pacific chum salmons (inhabiting regions of Japan, Russia, and North America) revealed a lower diversity but higher contribution to the overall species‐level genetic diversity, and also its unique genetic integrity. These findings advocate for the evolutionary significance of the Korean population for species‐level conservation.

Attachment rate and load varies with host genotype. (a) Attachment rate is the percentage of hosts with endospores attached to their cuticle. The bars represent means across replicates, and error bars indicate standard error. Different letters indicate significant differences among host lines (p < 0.05) based on post hoc Tukey's tests. (b) Attachment load is the number of endospores attached to the cuticle of hosts that had one or more endospores attached. The boxes represent the interquartile range, the horizontal black lines indicate the medians, whiskers extend to 25% and 75% quartiles. Black points represent load for individual hosts, and the blue diamond indicates the mean. For both (a) and (b), each host line was tested against four parasite sources with six replicates per source (i.e., 24 replicate flasks per host line).
Attachment rate and load varies with parasite source. (a) Attachment rate and (b) load are estimated and represented as in Figure 1, with means taken across replicate flasks (six replicate flasks x 13 isofemale lines = 78 flasks per parasite source).
Attachment rate and load varies with the combination of host and parasite. (a) Attachment rate and (b) load for each combination of host line and parasite source. The cells are shaded such that darker colors indicate relatively high attachment rate or load. The number in each cell gives the combination's (a) mean percentage of hosts with endospores attached to the cuticle and (b) the mean number of endospores attached per host with one or more endospores attached. Crossed cells indicate combinations for which we had no data. For a more detailed presentation of the data, see Figure S1 for (a) and Figure S2 for (b).
Increasing parasite diversity increases attachment rate. Each of four host lines was exposed to eight low‐diversity parasite populations (single parasite sources) and one high‐diversity parasite population (eight parasite sources combined). Each combination was tested in four replicates with up to 30 hosts examined per replicate. Panel (a) shows the mean attachment rate according to parasite diversity level, and panel (b) breaks this down according to individual host lines. Error bars show standard error of the mean. See Figure S3 for further detail.
A diverse parasite pool can improve effectiveness of biological control constrained by genotype‐by‐genotype interactions

November 2022

·

41 Reads

The outcomes of biological control programs can be highly variable, with natural enemies often failing to establish or spread in pest populations. This variability has posed a major obstacle in use of the bacterial parasite Pasteuria penetrans for biological control of Meloidogyne species, economically devastating plant‐parasitic nematodes for which there are limited management options. A leading hypothesis for this variability in control is that infection is successful only for specific combinations of bacterial and nematode genotypes. Under this hypothesis, failure of biological control results from the use of P. penetrans genotypes that cannot infect local Meloidogyne genotypes. We tested this hypothesis using isofemale lines of M. arenaria derived from a single field population and multiple sources of P. penetrans from the same and nearby fields. In strong support of the hypothesis, susceptibility to infection depended on the specific combination of host line and parasite source, with lines of M. arenaria varying substantially in which P. penetrans source could infect them. In light of this result, we tested whether using a diverse pool of P. penetrans could increase infection and thereby control. We found that increasing the diversity of the P. penetrans inoculum from one to eight sources more than doubled the fraction of M. arenaria individuals susceptible to infection and reduced variation in susceptibility across host lines. Together, our results highlight genotype‐by‐genotype specificity as an important cause of variation in biological control and call for the maintenance of genetic diversity in natural enemy populations.

The proportion of either Drosophila suzukii (selection treatment) or Drosophila melanogaster (control treatment) pupae that had successful parasitoid emergence of either Pachycrepoideus vindemmiae (a) or Trichopria drosophilae (b) during laboratory selection over 10 generations. Means ± 95% confidence intervals are shown for three replicated populations for each treatment in each generation. Transparent dots display the raw data and are jittered to reduce the overlap. Both for P. vindemmiae and T. drosophilae, emergence rates on D. suzukii increased between generation 0 and 3, and generation 0 and 10, but not between generation 3 and 10. The emergence rate of the control populations of P. vindemmiae on D. melanogaster decreased between generation 3 and 10, and generation 0 and 10. The emergence rate of the control populations of T. drosophilae increased between generations 0 and 3, but then decreased between generations 3 and 10 resulting in no change overall from generation 1 to 10 (see Section 3 for details).
The proportion of either Drosophila suzukii (selection treatment) or Drosophila melanogaster (control treatment) pupae that had successful parasitoid emergence of either Pachycrepoideus vindemmiae (a and b) or Trichopria drosophilae (c and d) during experimental evolution over 10 generations. Replicates are shown in different shades of grey. Dots indicate outlier observations, the horizontal line indicates the median with the box representing the interquartile range, and vertical lines are 1.5 times the interquartile range.
The proportion of Pachycrepoideus vindemmiae and Trichopria drosophilae females emerging from Drosophila suzukii (selection treatment) or Drosophila melanogaster (control treatment) during laboratory selection over 10 generations. The mean ± 95% confidence intervals of three replicated populations are shown for each generation and treatment. Transparent dots display the raw data and are jittered to reduce the overlap. For P. vindemmiae, the proportion of females emerging on D. suzukii decreased between generations 0 and 3 but then rebounded in generation 10 (left panel). For T. drosophilae, the proportion of females emerging on D. suzukii decreased from generations 0 to 10 (right panel). For both P. vindemmiae and T. drosophilae, the proportion of females emerging on D. melanogaster did not change throughout the experiment (see Section 3 for details).
The preference of Pachycrepoideus vindemmiae and Trichopria drosophilae parasitoids reared on Drosophila suzukii (selection) or reared on Drosophila melanogaster (control) in generations 0, 3, and 10. Preference was defined as the number of parasitoids emerging from D. melanogaster minus the number of parasitoids emerging from D. suzukii. The mean ± 95% confidence intervals of three replicate populations are shown for each generation and treatment. Transparent dots display the raw data and are jittered to reduce the overlap. For P. vindemmiae, preference did not change throughout the experiment in either the control or the selection treatments. For T. drosophilae, preference did not change in the control treatment. For the selection treatment, T. drosophilae increased preference towards D. suzukii between generations 0 and 3 but moved back towards increased preference for D. melanogaster in generation 10 (see Section 3 for details).
Limited gains in native parasitoid performance on an invasive host beyond three generations of selection

November 2022

·

96 Reads

Co‐evolved natural enemies provide sustainable and long‐term control of numerous invasive insect pests, but the introduction of such enemies has declined sharply due to increasing regulations. In the absence of co‐evolved natural enemies, native species may attack exotic invasive pests; however, they usually lack adaptations to control novel hosts effectively. We investigated the potential of two native pupal parasitoids, Pachycrepoideus vindemmiae and Trichopria drosophilae, to increase their developmental success on the invasive Drosophila suzukii. Replicated populations of the two parasitoids were subjected to 10 generations of laboratory selection on D. suzukii with Drosophila melanogaster serving as the co‐evolved host. We assessed developmental success of selected and control lines in generations 0, 3, and 10. Changes in host preference, sex ratio, development time, and body size were measured to evaluate correlated responses with adaptation. Both parasitoid species responded rapidly to selection by significantly increasing their developmental success on the novel host within three generations, which remained constant for seven additional generations without further improvement. The generalist parasitoid species P. vindemmiae was able to reach similar developmental success as the control populations, while the performance of the more specialized parasitoid T. drosophilae remained lower on the novel than on the co‐evolved host. There was no increase in preference towards the novel host over 10 generations of selection nor were there changes in development time or body size associated with adaptation in either parasitoid species. The sex ratio became less female‐biased for both parasitoids after three generations of selection but rebounded in P. vindemmiae by generation 10. These results suggest that a few generations of selection may be sufficient to improve the performance of native parasitoids on invasive hosts, but with limits to the degree of improvement for managing invasive pests when exotic co‐evolved natural enemies are not available.

Three evolutionary aspects to be considered when releasing a BCA to a new environment. (i) Establishment of natural enemies is better if their genetic diversity is high because small founder populations are subjected to the Allee effect, genetic drift and inbreeding that frequently result in the fixation of deleterious alleles and a reduced capacity for local adaptation. (ii) Enemy release in new habitats benefits natural enemies both directly through lower mortality and indirectly through the selection of genotypes with low resource allocation to defense and high allocation to competitive abilities. (iii) Host range of natural enemies is liable to evolve depending on the environment, and phylogenetic approaches are useful to predict the likelihood of impacts of biological control on nontarget species (e.g., parasitoids and their hosts, Heimpel et al., 2021).
Selective and nonselective (italic text) forces influencing frequencies of protective heritable symbionts in host natural populations. These forces can explain temporal and spatial variations of protective symbionts in nature and are modulated by the genomes of the interacting species and/or local environmental conditions.
Key components for trait evolution, evolutionary processes, and consequences for biocontrol. A source of heritable information (genes, epigenetics, or heritable symbionts) and inter‐individual trait variation are required for trait evolution. Three main types of evolutionary processes (human manipulations of evolution, natural processes of evolution, and stochastic processes) can lead to trait evolution. Selection, inbreeding, drift, and flow of heritable information (e.g., gene flow) among populations together shape the structure or adaptive and neutral heritable variation within and among populations. In the case of human manipulations of evolution, strong and directional selective forces can lead to rapid genetic improvements of BCA traits of interest for biocontrol such as mass rearing, attack rate, and thermal tolerance. Depending on environmental stochasticity, population size, and diversity, stochastic processes can induce genetic drift and inbreeding, which can lead to issues with mass rearing and field performance.
Biological control needs evolutionary perspectives of ecological interactions

November 2022

·

271 Reads

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.

Re‐evaluating Coho salmon (Oncorhynchus kisutch) conservation units in Canada using genomic data

October 2022

·

322 Reads

Conservation units (CUs) are important tools for supporting the implementation of standardized management practices for exploited species. Following the adoption of the Wild Salmon Policy in Canada, CUs were defined for Pacific salmon based on characteristics related to ecotype, life history and genetic variation using microsatellite markers as indirect measures of local adaptation. Genomic data sets have the potential to improve the definition of CUs by reducing variance around estimates of population genetic parameters, thereby increasing the power to detect more subtle patterns of population genetic structure and by providing an opportunity to incorporate adaptive information more directly with the identification of variants putatively under selection. We used one of the largest genomic data sets recently published for a nonmodel species, comprising 5662 individual Coho salmon (Oncorhynchus kisutch) from 149 sampling locations and a total of 24,542 high‐quality SNPs obtained using genotyping‐by‐sequencing and mapped to the Coho salmon reference genome to (1) evaluate the current delineation of CUs for Coho in Canada and (2) compare patterns of population structure observed using neutral and outlier loci from genotype–environment association analyses to determine whether separate CUs that capture adaptive diversity are needed. Our results reflected CU boundaries on the whole, with the majority of sampling locations managed in the same CU clustering together within genetic groups. However, additional groups that are not currently represented by CUs were also uncovered. We observed considerable overlap in the genetic clusters identified using neutral or candidate loci, indicating a general congruence in patterns of genetic variation driven by local adaptation and gene flow in this species. Consequently, we suggest that the current CU boundaries for Coho salmon are largely well‐suited for meeting the Canadian Wild Salmon Policy's objective of defining biologically distinct groups, but we highlight specific areas where CU boundaries may be refined.

Genomic differentiation in Pacific cod using Pool‐Seq

October 2022

·

114 Reads

Patterns of genetic differentiation across the genome can provide insight into selective forces driving adaptation. We used pooled whole genome sequencing, gene annotation, and environmental covariates to evaluate patterns of genomic differentiation and to investigate mechanisms responsible for divergence among proximate Pacific cod (Gadus macrocephalus) populations from the Bering Sea and Aleutian Islands and more distant Washington Coast cod. Samples were taken from eight spawning locations, three of which were replicated to estimate consistency in allele frequency estimation. A kernel smoothing moving weighted average of relative divergence (FST) identified 11 genomic islands of differentiation between the Aleutian Islands and Bering Sea samples. In some islands of differentiation, there was also elevated absolute divergence (dXY) and evidence for selection, despite proximity and potential for gene flow. Similar levels of absolute divergence (dXY) but roughly double the relative divergence (FST) were observed between the distant Bering Sea and Washington Coast samples. Islands of differentiation were much smaller than the four large inversions among Atlantic cod ecotypes. Islands of differentiation between the Bering Sea and Aleutian Island were associated with SNPs from five vision system genes, which can be associated with feeding, predator avoidance, orientation, and socialization. We hypothesize that islands of differentiation between Pacific cod from the Bering Sea and Aleutian Islands provide evidence for adaptive differentiation despite gene flow in this commercially important marine species.

Chromosomal assembly of the flat oyster (Ostrea edulis L.) genome as a new genetic resource for aquaculture

October 2022

·

147 Reads

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.

Identifying genes associated with genetic control of color polymorphism in the pearl oyster Pinctada margaritifera var. cumingii (Linnaeus 1758) using a comparative whole genome pool‐sequencing approach

September 2022

·

114 Reads

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.

Map of sample sites from LCT populations in Nevada, California, and Oregon, United States, with single (filled circles) and temporal (open circles) samples denoted; samples from several out of basin transplanted populations are also indicated. Bold lines denote three Major Geographic Management Units for LCT (Western, Eastern, Northwestern), and major river basins are noted. Location of a reference sample of naturalized rainbow trout and a previously assessed hybrid sample are also shown.
(a) Principal Components Analysis of full dataset of individual LCT collected in the field as well as naturalized rainbow trout from the Truckee River, California and Nevada (Local_RBT, orange dots); 1406 rainbow trout collected from across the Columbia River basin (Micheletti et al., 2018, Columbia_RBT, purple dots), individuals previously assessed as LCT‐RBT hybrids (MCD, lime green dots); and 58 YCT individuals (YCT, green dots), see text for further description. Lahontan watersheds containing individuals with notable hybridization detailed in the text are colored by major basin (South Fork Humboldt = SFH, gold, and Little Truckee River = LTR, pink); all others are shown in black (Other). (b) Results of admixture analysis using the clustering approach in ngsAdmix; each vertical bar represents an individual fish, with colors within indicating membership proportion in each of three clusters (k = 3). Along the x‐axis, YCT contains the YCT samples, represented in green; LCT contains the LCT samples largely represented in orange, with individuals at right demonstrating some hybridization with mostly RBT (purple); Local_RBT and Columbia_RBT contain the Truckee River naturalized rainbow trout and the 1406 rainbow trout collected from across the Columbia River basin (purple, Micheletti et al., 2018).
Comparison of estimates of various genetic diversity metrics with estimates of abundance and extinction probability generated from MPVA across nonhybridized LCT field populations meeting inclusion criteria (see text). Top 2 rows display results of linear models evaluating correlations between MPVA estimates of log10 30‐year Extinction (a, left three columns) and log10 Harmonic Mean Abundance (b, right three columns) versus nucleotide diversity (π), homozygosity (Ho), Tajima's theta (ΘT), Watterson's theta (ΘW), and theta skew (see text, Θdiff). Bottom row (c) displays regression results from Random Forest Models of 30‐year Extinction (left) and Harmonic Mean Abundance (right) MPVA estimates (left and right panels, respectively) considering the above genetic metrics; observed value from data (x‐axis) versus weighted predicted tree values (y‐axis, see text for details).
Difference in various genetic metrics over time for field nonhybridized populations of LCT that were temporally sampled (twenty populations, with the year span between sample periods ranging from 2 to 20 and averaging 12 years). Genetic metrics are nucleotide diversity (π), homozygosity (ho), Tajima's theta (ΘT), Watterson's theta (ΘW), and theta skew (Θdiff, see text).
Evaluation of the relationship between change in estimates generated from a Multiple Population Viability Model of LCT versus the change in genetic estimates over time (Delta statistic/Year). For populations with temporal genetic sampling, change in harmonic mean abundance (Delta Estimated Harmonic Mean N, top panel) and 30‐year extinction probability (static probability, Estimated PVA Extinction Risk, lower panel) versus per‐year average change for each genetic diversity statistic: nucleotide diversity (π), homozygosity (Ho), Watterson's theta (ΘW), Tajima's theta (ΘT), and theta skew (see text, Θdiff). See Table S1b for associated uncorrected and corrected p values.
Population genomic monitoring provides insight into conservation status but no correlation with demographic estimates of extinction risk in a threatened trout

September 2022

·

141 Reads

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.

Genomic evidence of recent European introgression into North American farmed and wild Atlantic Salmon

August 2022

·

183 Reads

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.

The western redcedar range and the location of the three polycross progeny tests in the province of British Columbia, Canada. The test sites are located at Jordan River, Port McNeill and Powell River. The climate variables (annual temperature, mean annual precipitation, heat moisture index, and degree days over 0 degrees) for the three sites are: Jordan River (7.7, 2480 mm, 7.1, and 168); Port McNeill (8.2, 2302 mm, 7.9, and 135); and Powell River (9.2, 1400 mm, 13.7, and 132).
Heat‐map of pairwise PX‐pedigree (APX matrix in the lower diagonal) and genomic relationship matrix (G matrix in the diagonal and upper diagonal) for parents and offspring. Parent relationships are on the top and offspring are ordered by corrected maternal families. We observe no relationship between parents (in the first 44 rows and columns) in both matrices. Parent‐offspring relationship can be seen in the first 44 columns (in the APX matrix) and the first 44 rows (in the G matrix). The upper diagonal (G matrix) shows ideal HS relationship within corrected maternal families, which is represented by the squared matrices on the diagonal, and scattered HS and FS relationships in the remaining upper off‐diagonals. The lower diagonal (APX matrix) shows pedigree errors in the form of a lot of unrelated individuals within the squared matrices on the diagonal (corrected maternal families), and incorrect HS‐relationship (in scattered lines) in the remaining lower off‐diagonals.
Histogram of pairwise genomic relationships for one out of the eight maternal families showing two possible genotypes. (a) Parent‐offspring relationship; showing two clusters, the peak at 0 relationship coefficient represents the offspring group not related to the genotyped parent, while the peak, around 0.4 relationship coefficient, represents the offspring group related to the genotyped parent. (b) Offspring‐offspring relationship within the same family; showing two clusters, the peak at 0 relationship coefficient represents the half‐sib offspring group not related to each other, while the peak around 0.2 relationship coefficient represent the HS offspring group related to each other. (c and d) Offspring‐offspring relationship of the two groups separately showing the disappearance of the peak at 0 relationship coefficient, and half‐sib relationship within each new corrected maternal family around 0.2 relationship coefficient.
Unequal male contribution leads to unbalanced FS family sizes. (a) Histogram of unequal male contribution. Number of offspring per pollen donor ranges from 7 to 181. The dashed line represents the expected equal male contribution of 68 offspring per pollen donor. The blue bars represent the 1433 (out of 1510) trees assigned one of the 21 males used in the pollen mix. The red and yellow bars represent pollen contamination; yellow bar represents 8 trees who were not assigned to any male parent; red bars represent trees identified as selfs or assigned foreign males other than the 21 males in the pollen mix, which were identified from sib‐sib analysis or parent‐offspring relationship with other genotyped parents. (b) Histogram of full‐sib (FS) family size distribution showing small and unbalanced sizes ranged from 1 to 15 offspring per family, total of 438 FS families.
Genomic selection reveals hidden relatedness and increased breeding efficiency in western redcedar polycross breeding

August 2022

·

100 Reads

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.

OE_Roslin_V1 assembly quality evaluation. (a) Omni‐C contact map highlighting the top 10 super‐scaffolds generated by HiRise. The contact map was visualized using Juicebox (Durand, Robinson, et al., 2016). (b) Merqury k‐mer copy number spectrum plot for the curated genome assembly. Nearly half of the single‐copy k‐mers (black region) were missing from the heterozygous peak, indicating efficient purging of haplotigs from the final assembly. K‐mers missing from the assembly (black region in the homozygous peak) indicates bases present in the Illumina data missing from the assembly. (c) BUSCO scores for the final scaffolded OE_Roslin_V1 assembly (mollusca_odb10 database). (d) Circos map highlighting the concordance between the 10 super‐scaffolds (RL1 to RL10) and linkage groups (LG1 to LG10). Blue dotted squares within super‐scaffolds 1 and 2 highlight the manual scaffolding performed on the basis of 3D contact information in the Omni‐C data (Figure S1).
Annotation of the O. edulis OE_Roslin_V1 assembly. (a) Summary of genome repeat classes. (b) Density plot showing gene, exon and intron lengths. (c) Circos plot highlighting annotated features across the ten super‐scaffolds (window size 0.5 Mb except track‐v, which is 0.1 Mb). Tracks as follows: i: 10 super‐scaffolds OE‐1 to OE‐10; ii: GC percentage (33–38%), with red and green bars indicating GC >36.5% and <34.5%, respectively; iii: genic content (sum of annotated gene models) expressed as percentage of total window size, regions with <20% genic content are coloured blue, while 20 to 40% are coloured grey and >40% are coloured red; iv: gene density (0–80); v: mean Illumina sequencing depth, with values <45 and >150 shown as red points; vi: classified repeats expressed as percentage of total window size (0–35%); vii: novel unclassified repeat elements expressed as percentage of total window size (0–35%).
Chromosome‐level synteny between the OE_Roslin_V1 O. edulis assembly and three independent bivalve assemblies. Circos plots are shown comparing the ten super‐scaffolds (OE‐1 to OE‐10) with putative chromosomes of (a) C. gigas, (b) C. virginica, (c) P. maximus chromosomes and (d) an independent O. edulis assembly reported in Boutet et al. (2022) (‘RC’ denotes super‐scaffolds from Boutet et al. (2022); ‘RS’ denotes super‐scaffolds from OE_Roslin_V1).
Classification of gene family expansion during O. edulis evolution. (a) Species tree of bivalve genomes used in the analysis, (b–g) different categories of gene family expansion (classified as described in Methods). Branch annotations: blue circles indicate putative expansion; green circles indicates no expansion; red circle indicates an absence of species along that branch for the affected orthogroups. Full data are provided in Table S7.
Most represented protein domains in expanded O. edulis gene families. (a) Top 20 represented IPR domains. (b and c) Example maximum‐likelihood phylogenetic trees highlighting gene family expansions in O. edulis. Blue squares at nodes indicate bootstrap support value >50%.
Chromosome level reference genome for European flat oyster ( Ostrea edulis L.)

August 2022

·

222 Reads

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.

(a) Global distribution of the lentil diversity panel (LDP). The size of the circles represents the number of accessions from different countries, and the colors indicate the clusters to which they belong. (b) Principal component analysis (PCA) for the first three principal components using the single nucleotide polymorphism (SNP) data set. (c) Ancestry plot of the LDP. The distributions of the lentil genetic clusters are: 1 = the Middle East (Iran, Turkey); 2 = the Middle East (Syria, Turkey); 3 = Iran; 4 = South Asia (India, Pakistan) and Syria; 5 = East African highlands and South Levant (Ethiopia, Jordan, and Egypt); 6 = Central Asia (Afghanistan, Iran); 7 = Mediterranean costs (Spain) and South America (Chile); 8 = Temperate Mediterranean (France) and North America (Canada).
(a) Tajima's D distribution estimated for each of the eight population clusters estimated for the lentil diversity panel (LDP). (b) Principal component analysis (PCA) inferred from the normalized depth of copy number variation (CNV) loci with each population cluster represented by dots in different colors. (c) Site frequency spectrum (SFS) of the individual LDP clusters. The observed SFS constructed from single nucleotide polymorphisms (SNPs) and from CNVs is indicated with different bar colors. Black dots and lines show the expected SFS.
Distribution of copy number variation (CNV) loci along the lentil chromosomes. Green indicates the CNV density, and gray indicates the disease resistance gene frequency, in 1 mb windows.
MapMan classification of the genes in copy number variation (CNV) regions. The first column shows the classification of all lentil genes, while the rest of the columns indicate the classification of genes affected by CNV loci that were presented within each cluster in a frequency higher than 0.20. The “Not assigned” category was not included in the figure. Asterisks show the categories that were overrepresented in the genes affected by CNVs. See Figure S9 for more details about subcategories of enzymes, nucleotide metabolism, external stimuli response, and Cell Wall Organization.
An evolutionary look into the history of lentil reveals unexpected diversity

August 2022

·

207 Reads

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.

Two parallel chromosome‐level reference genomes to support restoration and aquaculture of European flat oyster Ostrea edulis

August 2022

·

123 Reads

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.

Evolutionary insights into porcine genomic structural variations based on a novel constructed dataset from 24 worldwide diverse populations

August 2022

·

96 Reads

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.

Genetic parallelism between European flat oyster populations at the edge of their natural range

August 2022

·

223 Reads

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.

A single genomic region involving a putative chromosome rearrangement in flat oyster (Ostrea edulis) is associated with differential host resilience to the parasite Bonamia ostreae

July 2022

·

207 Reads

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.

Cnidarian microRNA biogenesis pathways compared with bilaterians, green algae and plants. In cnidarians, pri‐miRNAs are proposed to be processed into pre‐miRNAs by the miRNA microprocessor complex composed of pasha and drosha. The loop structure is then removed by dicer, together with plant‐associated cofactors serrate and HYL1 to form the miRNA duplex. Hen1 methylates the 3′ end of the miRNA after miRNA loading and star strand ejection. 3′ ends methylation of miRNAs is common in both plants and cnidarians (Modepalli et al., 2018), whereas bilaterian miRNAs do not undergo this modification.
A phylogenetic relationship of metazoan Argonuate protein family. Multiple alignments were performed using MUSCLE and the rooted phylogenetic tree was constructed with the LG (G + I) model using the maximum likelihood method (with 1000 replicates). Bootstrap support values above 50% are indicated above branches.
(a) the phylogenetic tree of cnidarian species with small RNA sequencing; (b) list of species of cnidaria small RNA research. The green, yellow and orange grids indicate that the small RNAs in question have already been the subject of study, while the gray grids indicate that no studies have yet been conducted.
siRNA biogenesis. The ribonuclease III dicer dices dsRNA into short interfering RNAs (siRNA), which is often followed by signal amplification by RNA‐dependent RNA polymerases (RdRPs). When siRNAs are generated, they are bound by RISC, a multiprotein component complex (RNA‐induced silencing complex) and final silencing of foreign or invasive nucleic acids by Argonaute proteins.
piRNA biogenesis and TE targeting. Initiator piRNAs guide PIWI‐catalyzed cleavage of a target piRNA precursor (black triangles). The sliced target is then loaded into another PIWI protein (dark ellipses) to produce trailing piRNAs by the piRNA‐independent endonuclease and pre‐piRNA 3′‐to‐5′ trimming exonuclease (dark blue triangles) during the phasing mechanism. Simultaneously, cleavage by initiator piRNAs also generates responder piRNAs which bind to target RNAs to guide cleavage and then in turn act as initiator piRNAs after loading to another PIWI to silence the piRNA precursors. This mechanism of piRNA amplification is called the ping‐pong cycle and is conserved in cnidarians.
Small RNAs in Cnidaria: A review

July 2022

·

191 Reads

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.

Infographic of study design and scenarios investigating the spread of the invasive round goby (Neogobius melanostomus) across the steep salinity gradient of the Port of Gothenburg, Sweden. The three sites yielding genotypic data (green circles 1, 2 and 3), and the two of those sites yielding phenotypic data (1 and 2) are marked with grey info boxes. Numbered circles mark sites where initial sampling occurred in 2016: green shows sites where fish were caught for the study, yellow where one fish was caught and excluded, and red where no fish were caught after a minimum of 6 fishing hours with baited hook and line. Sites 7 and 10 were also fished with 3 baited cages overnight. An eleventh site (off the map 1 km up the river) was also sampled without catch. The purple circle marked X shows the site furthest upstream where N. melanostomus has been found during a fishing survey in 2018 (not part of the present study). Habitats are roughly categorized and separated with dotted lines according to salinity. Striped polygon shows the extent of the Gothenburg international shipping port, Scandinavia's largest port with over 5300 cargo vessels visiting in 2020
Neighbour‐joining tree based on pairwise FST estimates of round gobies (Neogobius melanostomus) sampled from 12 sites and genotyped at 12,937 SNPs. Colours represent the four larger geographic regions targeted
Individual ancestry of 305 round gobies (Neogobius melanostomus) based on 12,937 SNPs for (a) K = 3 and (b) K = 9 estimated using sNMF. Each vertical bar is one individual, and the colour is the proportion of that individual assigned to the different K clusters. Individuals are separated by sampling sites and grouped in the four Baltic Sea regions. Clusters 2–10 can be found in Figure S4
First (x‐axis) and second (y‐axis) component of a principal component analysis (PCA) on 305 round gobies (Neogobius melanostomus) genotyped at 12937 SNPs. The first component explains 10.56% of the total variation and the second 6.41%. Each point represents one individual, colours represent sampling sites, and shape is used for better distinction
Metabolic performance of round goby (Neogobius melanostomus) caught from two sites of different ambient salinities (Outer port or Inner port) and acclimated to salinities of first 15, then either 0 or 30 PSU at 10°C. Bars show mean values, boxes show median, and upper and lower quartile, and error bars show max and min with outliers denoted by dots. Jittered points show individual values. Letters indicate statistical differences outlined in the results. Panels show the following: (a) oxygen uptake (mg O2 kg⁻¹ h⁻¹) shown in top values as maximum metabolic rate (MMR) and shown in bottom values as resting metabolic rate (SMR) (lowest 20% of values measured every 15 min over 48 h). (b) Aerobic scope (MMR – SMR). (c) Factorial aerobic scope (MMR/SMR)
Invader at the edge — Genomic origins and physiological differences of round gobies across a steep urban salinity gradient

July 2022

·

109 Reads

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.