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Evolutionary Applications

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Online ISSN: 1752-4571

Disciplines: Evolution

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Detection history of the North American A. glabripennis infestations and location of sampling areas for this study. (a) Date of detection and location of A. glabripennis infestations in North America. Infestations with (*) were included in the genomic analysis. MA, Massachusetts; OH, Ohio; IL, Illinois; NJ, New Jersey; NY, New York; SC, South Carolina. (b) Sampling map. The left panel shows geographic sampling in the invasive range, USA (purple) and Canada (red). Toronto (includes Toronto/Vaughan and Toronto/Mississauga), Amityville (south) (includes Massapequa, NY), Amityville (north) (includes Farmingdale, NY). The right panel shows sampling in the native range: China (green) and Korea (cyan). The different regions within China are illustrated by dashed ovals: North Plain region (N1, N2), Northwest (NW), Northeast (NE), South (S), as defined in Cui et al. (2022).
Population structure of native and North American invasive A. glabripennis. (a) Pairwise FST between populations (populations with < 4 individuals not shown), with a color ramp indicating degree of differentiation (blue = low, red = high) (see Table S4 for FST values). The native range includes YJ, Yanji; HRB, Harbin; CHC, Changchun; SHY, Shenyang; TOL, Tongliao; QI, Qingtongxia; YC, Yanchi; CHE, Chengde; BJ, Beijing; IMC, Huhhot; SHI, Shijiangzhuang; HS, Hengshui; JI, Jinan; TA, Taian; BB, Bengbu; CIX, Cixi. Invasive range includes Bos, Boston; Wor, Worcester; Beth, Bethel; Chi, Chicago; Lin, Linden; NYC, New York; Qu, Queen; Flush, Flushing; Massap, Massapequa; Far, Farmingdale; TOR, Toronto. See Figure 1 for locations. (b) Principal component analysis of all A. glabripennis populations, color‐coded by country. (c) Admixture bar plots showing the proportion of genetic membership ancestry for each individual, represented as vertical bars colored according to their estimated ancestry within each cluster. Optimal clustering is at K = 14 (see Figure S6 for K = 3 to K = 14). Image of an A. glabripennis adult was provided by Dr. Brent Sinclair.
Population assignment of invasive A. glabripennis individuals. (a) Scatterplot of two discriminant functions showing the clustering of invasive individuals (solid squares) with reference native populations (light circles). (b) Contingency table of individual assignments to a priori reference native populations based on DAPC discriminant functions. Square size indicates the number of invasive individuals (columns) assigned to each native population cluster (rows). MA, Massachusetts; OH, Ohio; IL, Illinois; NJ, New Jersey; NY, New York; TOR, Toronto; N1, North Plain region one; N2, North Plain region two; NW, Northwest; NE, Northeast; S, South. Single individuals from the NJ infestation were assigned to N2 and NE. Farmingdale (Far, NY) was treated separately from other NY samples based on the admixture results.
Maximum likelihood phylogenetic tree (unrooted) of the complete A. glabripennis dataset (n = 2768 SNPs). MA, Massachusetts; OH, Ohio; IL, Illinois; NJ, New Jersey; NY, New York; TOR, Toronto; N1, North Plain region one; N2, North Plain region two; NW, Northwest; NE, Northeast; S, South. Native lineages are colored in gray, while invasive populations are colored as in Figure 3. Branches marked with a “*” are collapsed clades containing multiple individuals. Branches with bootstrap values > 80% are labeled above the nodes.
Invasion history of North American A. glabripennis populations. MA, Massachusetts; OH, Ohio; Far, Farmingdale, New York; TOR: Toronto; N1, North Plain region one; N2, North Plain region two; NW, Northwest; NE, Northeast; S, South. Each native region is colored individually, while all invasive populations are in red. Invasive populations experienced a bottleneck event (dashed line) followed by population expansion (solid line). The unsampled ancestry population is shown in black. Confidence intervals (95% CI, in exact years) are indicated at the point of introduction date for each invasive population (time not to scale).

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Tracking the North American Asian Longhorned Beetle Invasion With Genomics

November 2024

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Evolutionary Applications is a fully open access journal, addressing evolutionary biology concepts to answer important biological questions. We delve into questions of health, social, and economic significance that relate to applied evolution. Our journal covers all taxonomic groups- from microbes to plants and animals. We have a large and interdisciplinary audience within industry, government, and health care. Our articles intersect across fields, bringing knowledge together.

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(A) Karyotype with overlapping ROH regions across all samples shows many ROH in Setophaga kirtlandii but nearly none in their close relatives. The darker shading indicates regions where ROH from different individuals overlap, and white areas represent non‐ROH regions. (B) Breeding range maps of the American Redstarts (Setophaga ruticilla, Nc = 42,000,000), Hooded Warblers (Setophaga citrina, Nc = 5,200,000), and the Kirtland's warblers (Setophaga kirtlandii, Nc = 4500‐5000) (Partners in Flight 2020).
Time to the most recent common ancestor (TMRCA) for ROH haplotypes, and genetic load dynamics shows recent inbreeding and elevated counts of putative deleterious mutations in S. kirtlandii. (A) The sum of all ROH lengths (SROH) and number of ROH (NROH) > 0.5 Mb plotted in each species (the x = y line is for orientation purposes) where each point represents an individual. (B) The number ROH (NROH) plotted for each ROH size category where each line represents an individual. In panels A and B, S. citrina and S. ruticilla show nearly identical distribution of ROH such that points and lines stack on each other at the axis. Panel (C) shows the total sum of ROH > 5 Mb for each sample where each point represents an individual. (D) Time to the most recent common ancestor (TMRCA) of haplotypes underlying ROH in S. kirtlandii samples was aged using estimated recombination rates (cM/Mb) from the Ficedula flycatchers and a generation time of 2 years. The secondary axis was scaled by subtracting TMRCA from sample years. (E) The number of genotypes with an alternate allele at synonymous, nonsynonymous, or loss‐of‐function site. In panel E, counts include both polymorphic and monomorphic sites; points jittered to minimize overlap between samples. *p‐value < 0.05, **p‐value < 0.01, ***p‐value < 0.001 by the Mann–Whitney U test.
(A) Proportion of alternate alleles at polymorphic sites predicted to be deleterious. (B) Proportion of heterozygotes at polymorphic sites that are predicted to be deleterious. (C) Proportion of alternate homozygotes at polymorphic sites predicted to be deleterious. NS, Not Significant, *p‐value < 0.05, **p‐value < 0.01, ***p‐value < 0.001 by the Mann–Whitney U test. Unfolded site frequency spectra for sites where private alternate alleles are predicted to be (D) deleterious and (E) loss of function. In both panels D and E, the frequency is calculated as the number of private alternate alleles deleterious or loss of function relative to the total number of private alternate alleles of each mutation type.
Temporal dynamics of effective population size using pairwise sequentially Markovian coalescent (PSMC). The x‐axis is thousands of years before present (Kya) and has been calibrated using a generation time (g) of 2 years and a per‐site mutation rate (μ) of 1.4e‐9.
Recently Delisted Songbird Harbors Extensive Genomic Evidence of Inbreeding, Potentially Complicating Future Recovery
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December 2024

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18 Reads

The Kirtland's warbler (Setophaga kirtlandii) is a rare migratory passerine species and habitat specialist of the North American Jack Pine Forests. Their near extinction in the 1970s classified them as endangered and protected under the Endangered Species Act of 1973. After decades of intense conservation management, their population size recovered, and they were delisted from federal protection in 2019. We explore the genomic consequences of this harsh bottleneck and recovery by comparing the genomic architecture of two closely related species whose population sizes have remained large and stable, Hooded Warblers (Setophaga citrina) and American Redstarts (Setophaga ruticilla). We used whole‐genome sequencing to characterize the distribution of runs of homozygosity and deleterious genetic variation. We find evidence that Kirtland's warblers exhibit genetic patterns consistent with recent inbreeding. Our results also show that Kirtland's warblers carry an excess proportion of deleterious variation, which could complicate management for this conservation‐reliant species. This analysis provides a genetically informed perspective that should be thoroughly considered when delisting other species from federal protections. Through the increasing accessibility of genome sequencing technology, it will be more feasible to monitor the genetic landscape of recovering populations to ensure their long‐term survival independent of conservation intervention.


Characterisation of stand dynamics in the four different silvicultural scenarios (colours): (a) stand density, Nha; (b) leaf area index, LAI. This figure illustrates the case without phenotypic variation (zeroVar) nor drought stress; see Appendix S3: Figure S1 for the other drought stress regimes and levels of phenotypic variation. In the unthinned scenario, the decline in Nha within each rotation is only driven by competition‐related mortality, with the exception of the seeding cut and final harvest. In contrast, the other scenarios exhibit Nha changes resulting from a combination of competition‐induced mortality and thinning interventions. The LAI increases within each rotation as stand develops and decreases at each thinning intervention: The intensive scenario consistently maintains a lower LAI compared to the trend scenario, while the juvenile stress scenario maintains an LAI identical to the unthinned scenario, followed by a slight elevation above the trend scenario. During Rotations 2 and 3, a higher initial density constraints growth and tree size, leading to a lower LAI. The prerecruitment period is intentionally omitted from the representation, as the model calibration for tree density and growth begins from the recruitment age. Furthermore, trees that have not yet reached recruitment age are not considered in the Nha and the LAI.
Dynamics of population genetic parameters in the unthinned scenario across three successive rotations according to the level of phenotypic variation (line type) and drought stress regime (colours): (a) Population genetic mean of vigour, μG.Vig; (b) population genetic mean of sensitivity, μG.Sensi; (c) additive genetic variance of vigour, VA(Vig); (d) additive genetic variance of sensitivity, VA(Sensi); and (e) genetic correlation between vigour and sensitivity, r (Vig, Sensi). In the absence of drought stress, sensitivity underwent no selective pressure; any minor changes were solely a result of genetic drift. The shaded areas represent the 95% intervals over 10 replicates for each genetic setup. The prerecruitment period is intentionally omitted from the representation, as the model does not account for any demo‐genetic changes during this phase.
Dynamics of tree size and demography in the unthinned scenario across three successive rotations according to the level of phenotypic variation (line type) and drought stress regime (colours): (a) Quadratic mean diameter, QMD; (b) competition‐induced mortality rate, CMR; (c) drought stress‐induced mortality rate, SMR; and (d) number of trees per hectare, Nha. The shaded areas represent the 95% intervals over 10 replicates for each genetic setup. The prerecruitment period is intentionally omitted from the representation, as the model does not account for any demographic changes during this phase. Additionally, trees that have not yet reached recruitment age are not considered in the Nha.
Dynamics of selective mortality and genetic changes across three successive rotations in four distinct silvicultural scenarios (colours): (a) Competition‐induced mortality rate, CMR; (b) drought stress‐induced mortality rate, SMR; (c) population genetic mean of vigour, μG.Vig; (d) population genetic mean of sensitivity, μG.Sensi; (e) additive genetic variance of vigour, VA(Vig); and (f) additive genetic variance of sensitivity, VA(Sensi). The thinning regimes for the different silvicultural scenarios are detailed in Table 2. This figure illustrates the baseline genetic variance (baseVA) under the severe drought stress regime; see Appendix S3: Figure S2 for the other drought stress regimes and levels of phenotypic variation. The shaded areas represent the 95% intervals over 10 replicates for each genetic setup. The prerecruitment period is intentionally omitted from the representation, as the model does not account for any demo‐genetic changes during this phase.
Quadratic mean diameter (QMD) at the end of three successive rotations (R1, R2 and R3) with phenotypic variation in four distinct silvicultural scenarios (colours). The thinning regimes for the different silvicultural scenarios are detailed in Table 2. The end‐of‐rotation quadratic mean diameter without phenotypic variation (zeroVar) is shown as an average across three rotations and is presented as a theoretical reference in the left panel. Tukey tests were performed independently for R1, R2, R3 and zeroVar, with letters indicating significance between silvicultural scenarios at the 0.05 threshold. In our simulations, the variability only arises from the stochastic components of the model. This figure illustrates the baseline genetic variance (baseVA) and the severe drought stress regime; see Appendix S3: Figure S3 for the other level of genetic variation (twiceVA) and other drought stress regimes. The boxplots show the distribution of values obtained from 10 replicates in each case.
Can Thinning Foster Forest Genetic Adaptation to Drought? A Demo‐Genetic Modelling Approach With Disturbance Regimes

December 2024

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14 Reads

In managed populations—whether for production or conservation—management practices can interfere with natural eco‐evolutionary processes, providing opportunities to mitigate immediate impacts of disturbances or enhance selection on tolerance traits. Here, we used a modelling approach to explore the interplay and feedback loops among drought regimes, natural selection and tree thinning in naturally regenerated monospecific forests. We conducted a simulation experiment spanning three nonoverlapping generations with the individual‐based demo‐genetic model Luberon2. Luberon2 integrates forest dynamics processes driving survival and mating success, including tree growth, competition, drought impacts and regeneration, with genetic variation in quantitative traits related to these processes. We focused on two variable traits: individual vigour, determining diameter growth potential without stress as the deviation from average stand growth, and individual sensitivity to drought stress as the slope of the relationship between diameter growth and drought stress level. We simulated simplified thinning scenarios, tailored to even‐aged stands. Considering plausible genetic variation and contrasting drought regimes, the predicted evolutionary rates for both traits aligned with documented rates in wild plant and animal populations. Thinning considerably reduced natural selective pressures caused by competition and drought compared to unthinned stands. However, the conventional thinning practice of retaining the larger trees resulted in indirect anthropogenic selection that enhanced genetic gain in vigour and lowered sensitivity by up to 30%. More intensive thinning aimed at reducing drought stress by reducing stand density hampered the selection against sensitivity to drought, potentially hindering long‐term adaptation. Conversely, avoiding the early, nonselective thinning step—thereby promoting both natural and anthropogenic selection—ultimately resulted in better stand performance while maintaining long‐term evolvability. This study emphasises the potential of evolution‐oriented forestry strategies to combine drought stress mitigation with genetic adaptation. It provides general insights into how population management, disturbance regimes and eco‐evolutionary responses interfere, aiding sustainable decision‐making amid environmental uncertainties.


Simulating Genetic Mixing in Strongly Structured Populations of the Threatened Southern Brown Bandicoot (Isoodon obesulus)

December 2024

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47 Reads

Genetic mixing aims to increase the genetic diversity of small or isolated populations, by mitigating genetic drift and inbreeding depression, either by maximally increasing genetic diversity, or minimising the prevalence of recessive, deleterious alleles. However, few studies investigate this beyond a single generation of mixing. Here, we model genetic mixing using captive, low‐diversity recipient population of the threatened Southern brown bandicoot (Isoodon obesulus) over 50 generations and compare wild populations across south‐eastern Australia as candidate source populations. We first assess genetic differentiation between 12 populations, including the first genomic assessment of three mainland Australian and three Tasmanian populations. We assess genetic diversity in the 12 populations using an individualised autosomal heterozygosity pipeline, using these results to identify a candidate recipient population for genetic mixing simulations. We found that populations fell into four major groups of genetic similarity: Adelaide Hills, western Victoria, eastern Victoria, and Tasmania, but populations within these groups were also distinct, and additional substructure was observed in some populations. Our autosomal heterozygosity pipeline indicated significant variability in mean heterozygosity between populations, identifying one extremely genetically degraded population on Inner Sister Island, Tasmania. Genetic mixing simulations of a low heterozygosity captive population in Victoria suggested the greatest increase in heterozygosity would be reached by using highly differentiated populations as mixing sources. However, when removing populations that may represent taxonomically discrete lineages, neither metrics of differentiation nor heterozygosity was strongly correlated with modelled heterozygosity increase, indicating the value of simulation‐based approaches when selecting source populations for population mixing.


Evolutionary Genomics Provides Insights Into Endangerment and Conservation of a Wild Apple Tree Species, Malus sieversii

December 2024

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18 Reads

Understanding the evolutionary history of a species is essential for effective conservation management. Malus sieversii, a relict broad‐leaf forest tree found in arid Central Asian mountains, has a narrow and fragmented distribution and is classified as an endangered species in China. This species is considered one of the ancestors of the domesticated apple trees. In the present study, we sampled five populations of M. sieversii and its wide‐ranging congener M. baccata from China. Through deep whole‐genome resequencing, we analyzed the population's genetic diversity, genetic structure, demographic history, fixation of deleterious mutations, and genomic divergence. Our results revealed that M. baccata exhibits a higher level of genetic diversity than M. sieversii. The effective population size of M. sieversii decreased, whereas that of M. baccata recovered after the bottleneck effect. In M. sieversii, the genetic structure of the Yili region was distinct from that of the Tacheng region. Populations at the rear edge of the Tacheng region showed a stronger fixation of deleterious mutations than those in the Yili region. Genomic divergence indicated that the positively selected genes were associated with physiological processes within the genomic islands between the Yili and Tacheng regions. Based on these findings, we recommend the establishment of two separate conservation units for the Yili and Tacheng lineages to preserve their genetic resources. Given the limited distribution range and high fixation rate of deleterious mutations, urgent protective measures are recommended for the Tacheng lineage.


Endangered Pinto/Northern Abalone (Haliotis kamtschatkana) are Panmictic Across Their 3700 km Range Along the Pacific Coast of North America

December 2024

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6 Reads

Connectivity is integral to the dynamics of metapopulations through dispersal and gene flow, and understanding these processes is essential for guiding conservation efforts. Abalone, broadcast‐spawning marine snails associated with shallow rocky habitats, have experienced widespread declines, and all seven North American species are threatened. We investigated the connectivity and population genomics of pinto/northern abalone (Haliotis kamtschatkana), the widest‐ranging of abalone species. We employed reduced representation sequencing (RADseq) to generate single nucleotide polymorphism (SNP) data, assessing population connectivity and potential adaptive variation at 12 locations across the full range from Alaska to Mexico. Despite depleted populations, our analysis of over 6000 SNPs across nearly 300 individuals revealed that pinto abalone maintains a high genetic diversity with no evidence of a genetic bottleneck. Neutral population structure and isolation by distance were extremely weak, indicating panmixia across the species' range (global FST = 0.0021). Phylogenetic analysis, principal components analysis, and unsupervised clustering methods all supported a single genetic population. However, slight population differentiation was noted in the Salish Sea and Inside Passage regions, with evidence for higher barriers to dispersal relative to outer coastal areas. This north‐central region may also represent the species' ancestral range based on relatively low population‐specific FST values; the northern and southern extremes of the range likely represent range expansions. Outlier analysis did not identify consensus loci implicated in adaptive variation, suggesting limited adaptive differentiation. Our study sheds light on the evolutionary history and contemporary gene flow of this threatened species, providing key insights for conservation strategies, particularly in sourcing broodstock for ongoing restoration efforts.


Genome‐Wide Diversity in Lowland and Highland Maize Landraces From Southern South America: Population Genetics Insights to Assist Conservation

December 2024

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32 Reads

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1 Citation

Maize (Zea mays ssp. mays L.) landraces are traditional American crops with high genetic variability that conform a source of original alleles for conventional maize breeding. Northern Argentina, one the southernmost regions of traditional maize cultivation in the Americas, harbours around 57 races traditionally grown in two regions with contrasting environmental conditions, namely, the Andean mountains in the Northwest and the tropical grasslands and Atlantic Forest in the Northeast. These races encounter diverse threats to their genetic diversity and persistence in their regions of origin, with climate change standing out as one of the major challenges. In this work, we use genome‐wide SNPs derived from ddRADseq to study the genetic diversity of individuals representing the five groups previously described for this area. This allowed us to distinguish two clearly differentiated gene pools, the highland northwestern maize (HNWA) and the floury northeastern maize (FNEA). Subsequently, we employed essential biodiversity variables at the genetic level, as proposed by the Group on Earth Observations Biodiversity Observation Network (GEO BON), to evaluate the conservation status of these two groups. This assessment encompassed genetic diversity (Pi), inbreeding coefficient (F) and effective population size (Ne). FNEA showed low Ne values and high F values, while HNWA showed low Ne values and low Pi values, indicating that further genetic erosion is imminent for these landraces. Outlier detection methods allowed identification of putative adaptive genomic regions, consistent with previously reported flowering‐time loci and chromosomal regions displaying introgression from the teosinte Zea mays ssp. mexicana. Finally, species distribution models were obtained for two future climate scenarios, showing a notable reduction in the potential planting area of HNWA and a shift in the cultivation areas of FNEA. These results suggest that maize landraces from Northern Argentina may be unable to cope with climate change. Therefore, active conservation policies are advisable.


Patterns of Gene Flow in Anopheles coluzzii Populations From Two African Oceanic Islands

November 2024

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20 Reads

The malaria vector Anopheles coluzzii is widespread across West Africa and is the sole vector species on the islands of São Tomé and Príncipe. Our interest in the population genetics of this species on these islands is part of an assessment of their suitability for a field trial involving the release of genetically engineered A. coluzzii. The engineered construct includes two genes that encode anti‐Plasmodium peptides, along with a Cas9‐based gene drive. We investigated gene flow among A. coluzzii subpopulations on each island to estimate dispersal rates between sites. Sampling covered the known range of A. coluzzii on both islands. Spatial autocorrelation suggests 7 km to be the likely extent of dispersal of this species, whereas estimates based on a convolutional neural network were roughly 3 km. This difference highlights the complexity of dispersal dynamics and the value of using multiple approaches. Our analysis also revealed weak heterogeneity among populations within each island but did identify areas weakly resistant or permissive of gene flow. Overall, A. coluzzii on each of the two islands exist as single Mendelian populations. We expect that a gene construct that includes a low‐threshold gene drive and has minimal fitness impact should, once introduced, spread relatively unimpeded across each island.


Tracking the North American Asian Longhorned Beetle Invasion With Genomics

November 2024

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131 Reads

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1 Citation

Biological invasions pose significant threats to ecological and economic stability, with invasive pests like the Asian longhorned beetle (Anoplophora glabripennis Motschulsky, ALB) causing substantial damage to forest ecosystems. Effective pest management relies on comprehensive knowledge of the insect's biology and invasion history. This study uses genomics to address these knowledge gaps and inform existing biosurveillance frameworks. We used 2768 genome‐wide single nucleotide polymorphisms to compare invasive A. glabripennis populations in North America, using genomic variation to trace their sources of invasion and spread patterns, thereby refining our understanding of this species' invasion history. We found that most North American A. glabripennis infestations were distinct, resulting from multiple independent introductions from the native range. Following their introduction, all invasive populations experienced a genetic bottleneck which was followed by a population expansion, with a few also showing secondary spread to satellite infestations. Our study provides a foundation for a genome‐based biosurveillance tool that can be used to clarify the origin of intercepted individuals, allowing regulatory agencies to strengthen biosecurity measures against this invasive beetle.


(a) Map depicting sampling sites. Areas where the Hyacinth Macaws is possibly extinct are shown as hollow circles within the distribution (light gray), with dark gray polygons indicating current main strongholds in the species' distribution (Birdlife International 2024). Distribution map kindly provided by BirdLife International (2023). Black lines denote state border lines, while dashed lines represent potential barriers to gene flow. (b) Pairwise relatedness estimates for all analyzed samples. (c) Inbreeding (Fis) estimates per genetically isolated grous. Colors refer to sampling sites. AQ = Aquidauana; MI = Miranda; MT = Barão de Melgaço; PA = Canaã dos Carajás; PE = Peixes, PI = São Gonçalo do Gurguéia.
Population structure of Hyacinth Macaws. (a) Admixture plot showing the estimated ancestry proportions using NGSadmix for K = 3 and K = 4. For each K‐value, 10 runs were performed, and CLUMPAK was used to estimate the major mode. Each partitioned vertical bar represents an individual's proportional membership to the inferred populations. (b) Principal component analysis (PCA) from PCAngsd. (c) Multidimensional scaling (MDS) analysis of pairwise FST values calculated with ANGSD. Colors refer to sampling sites from Figure 1a. The GO population was excluded from FST calculations as it has only one sample. AQ = Aquidauana; MI = Miranda; MT = Barão de Melgaço; PA = Canaã dos Carajás; PE = Peixes, PI = São Gonçalo do Gurguéia.
Past demographic history for each sampled population of Hyacinth Macaws. The GO population was excluded as it has only one sample. The stairway plot shows the historical effective population size (Ne, y axis) over the past generations (upper x‐axis) and years (lower x axis). Colors represent population structure from Figure 1.
Landscape genetics analysis. (a) Estimated migration rate surface produced by EEMS showing posterior mean migration rates (m) between sample sites in logarithmic scale. Blue shades indicate higher migration rates than expected, while red shades indicate reduced connectivity. The convergence plot is shown in Figure S2. (b) Posterior average genetic diversity (q) in logarithmic scale. Blue shades indicate higher diversity, while red shades indicate more homogenous areas than expected. (c) Popgraph network analysis for Anodorhynchus hyacinthinus populations. Circle sizes reflect the levels of genetic variation within populations (betweenness). Lines weight represents the genetic variation due to connecting node (weight), reflecting higher gene flow among sites. (d) Schematic representation of main connectivity from popgraph results. AQ = Aquidauana; MI = Miranda; MT = Barão de Melgaço; PA = Canaã dos Carajás; PE = Peixes; and PI = São Gonçalo do Gurguéia.
Prioritizing Conservation Areas for the Hyacinth Macaw (Anodorhynchus hyacinthinus) in Brazil From Low‐Coverage Genomic Data

November 2024

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67 Reads

Estimates of current genetic diversity and population connectivity are especially important for endangered species that are subject to illegal harvesting and trafficking. Genetic monitoring can also ensure that management units are sustaining viable populations, while estimating genetic structure and population dynamics can influence genetic rescue efforts and reintroduction from captive breeding and confiscated animals. The Hyacinth Macaw (Anodorhynchus hyacinthinus) is a charismatic endangered species with a fragmented (allopatric) distribution. Using low coverage genomes, we aimed to investigate the dynamics across the remaining three large disjunct populations of Hyacinth Macaws in Brazil to inform conservation strategies. We obtained low coverage DNA data for 54 individuals from seven sampling sites. Our results showed that Hyacinth Macaws have four genetically structured clusters with relatively high levels of diversity. The Pantanal biome had two genetically distinct populations, with no obvious physical barriers that might explain this differentiation. We detected signs of gene flow between populations, with some geographical regions being more connected than others. Estimates of effective population size in the past million years of the species' evolutionary history showed a decline trend with the lowest Ne in all populations reached within the last few thousand years. Our findings suggest that populations from the Pantanal biome are key to connecting sites across its distribution, and maintaining the integrity of this habitat is important for protecting the species. Given the genetic structure found, we also highlight the need of conserving all wild populations to ensure the protection of the species' evolutionary potential.


Network of twelve major mtDNA haplotypes detected (a) and their spatial distribution in Polish Scots pine populations (b). Boundaries of the analyzed provenance regions are marked with white line based on the data from Polish Forest Seed Office https://www.bnl.gov.pl/. Population abbreviations are presented in Table 1.
Boxplots showing mean relatedness among individuals across 27 studied pine populations based on all SNPs.
Principal Component Analysis at nSSR loci (a) and all SNP loci (b) showing relationships between studied individuals. Most outlier individuals at SNPs loci were from population Md and Wi.
Heat map of FST values between analyzed populations of Scots pine for nSSR (a) SNPs (b) and outlier SNPs (c). Order of populations as in Table 1.
Genomic Data Support the Revision of Provenance Regions Delimitation for Scots Pine

November 2024

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70 Reads

Scots pine is a crucial component of ecosystems in Europe and Asia and a major utility species that comprises more than 60% of total forest production in Poland. Despite its importance, the genetic relationships between key conservation and the commercial value of Scots pine ecotypes in Poland remain unclear. To address this problem, we analyzed 27 populations (841 trees) of the most valuable Polish Scots pine ecotypes, including the oldest natural stands in all 24 regions of provenance established for the species in the country. By examining maternally inherited mitochondrial markers, nuclear microsatellite loci, and thousands of SNP markers from a genotyping array, we evaluated the genetic structure between and within them. These multilevel genomic data revealed high genetic similarity and a homogeneous structure in most populations, suggesting a common historical origin and admixture of populations after the postglacial recolonization of Central Europe. This research presents novel data on existing genomic resources among local ecotypes defined within strictly managed Polish regions of provenance, challenging their validity. Formal tests of the progeny of seed stands are needed to check whether the diversity in adaptation and quantitative traits still supports the delineation of provenance regions. In parallel, the health status of selected populations and the viability of seeds from these regions should be monitored to detect early‐stage symptoms of their environmental stress. It seems reasonable that periodic shortages of forest reproductive material (FRM) in a given region of provenance could be supplemented with the one from other regions that match their climatic envelope. Together, our results have important implications for the management of native Scots pine stands, particularly elite breeding populations, as they contribute to the discussion of the boundaries of provenance regions and the transfers of FRM that face increasing climate change.


Antagonistic effect of Drosophila melanogaster flies and synthetic sex pheromone Z4‐11Al on D. suzukii egg‐laying, in a dual choice oviposition assay. The oviposition index is the quotient, of the differential and the sum, of the eggs laid on the control and the treated blueberry. A positive oviposition index shows that more eggs were laid on the control berry (right‐hand side). (a, b) Blueberries were exposed to 3 and 10 D. melanogaster male or female flies. Compared with untreated berries, D. suzukii females laid significantly fewer eggs on berries pre‐exposed to 10 males or 10 females. (c) In a direct comparison, D. suzukii females laid fewer eggs on berries that were pre‐exposed to females rather than males. (d) Synthetic cVA, a D. melanogaster male pheromone, had no effect, (e) while 5 ng and 50 ng of the female pheromone Z4‐11Al decreased oviposition. (f) Ethanol had no effect on oviposition preference, and significantly more eggs were laid on berries treated with the unsaturated aldehyde E2‐11Al, compared to Z4‐11Al. Error bars show standard errors: asterisks show significance, according to GLMM fit by maximum likelihood (***p < 0.001).
Effect of Z4‐11Al on attraction of Drosophila suzukii females to volatiles of the yeast mutualist Hansenia uvarum. (a) In a wind tunnel, Z4‐11Al was released at 10 ng/min, into an airstream passing through a wash bottle containing a fermenting H. uvarum culture. (b) In a field trapping assay, Z4‐11Al dispensers added to traps baited with H. uvarum reduced captures of D. suzukii and D. simulans, not captures of D. melanogaster. Asterisks indicate a significant difference (p < 0.05) following GLMM fitted with binomial and Poisson distributions for landing and trap captures, respectively.
Sex Pheromone Mediates Resource Partitioning Between Drosophila melanogaster and D. suzukii

November 2024

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107 Reads

The spotted‐wing drosophila, Drosophila suzukii and the cosmopolitan vinegar fly D. melanogaster feed on soft fruit and berries and widely overlap in geographic range. The presence of D. melanogaster reduces egg‐laying in D. suzukii, possibly because D. melanogaster outcompetes D. suzukii larvae feeding in the same fruit substrate. Flies use pheromones to communicate for mating, but pheromones also serve a role in reproductive isolation between related species. We asked whether a D. melanogaster pheromone also modulates oviposition behaviour in D. suzukii. A dual‐choice oviposition assay confirms that D. suzukii lays fewer eggs on blueberries exposed to D. melanogaster flies and further shows that female flies have a stronger effect than male flies. This was corroborated by treating berries with synthetic pheromones. Avoidance of D. suzukii oviposition is mediated by the female D. melanogaster pheromone (Z)‐4‐undecenal (Z4‐11Al). Significantly fewer eggs were laid on berries treated with synthetic Z4‐11Al. In comparison, the male pheromone (Z)‐11‐octadecenyl acetate (cVA) had no effect on D. suzukii oviposition. Z4‐11Al is a highly volatile compound that is perceived via olfaction and it is accordingly behaviourally active at a distance from the source. D. suzukii is known to engage in mutual niche construction with the yeast Hanseniaspora uvarum, which strongly attracts flies. Adding Z4‐11Al to fermenting H. uvarum significantly decreased D. suzukii flight attraction in a laboratory wind tunnel and a field trapping assay. That a D. melanogaster pheromone regulates oviposition in D. suzukii demonstrates that heterospecific pheromone communication contributes to reproductive isolation and resource partitioning in cognate species. Stimulo‐deterrent diversion or push‐pull methods, building on combined use of attractant and deterrent compounds, have shown promise for control of D. suzukii. A pheromone that specifically reduces D. suzukii attraction and oviposition adds to the toolbox for D. suzukii integrated management.


Effects of demographic, genetic, and habitat rescue on the average number of reproductive individuals and seeds per plant post dispersal. Filled circles are mean values and the error bars represent associated standard errors. Colors represent the different values of the probability of new genetic variation (ps∈0.2,1.0$$ {p}_{\mathrm{s}}\in \left[0.2,1.0\right] $$) being added for genetic rescue. The first column of panels shows the effects of demographic rescue, the second column shows genetic rescue effects, and the third column of panels shows results for habitat rescue.
Temporal dynamics of S allele numbers (a), reproductive individuals (b) and inbreeding coefficient (FIS) (c). Each line represents the temporal trajectory of different variables for different scenarios of genetic (dashed lines, ps = 0.8) and demographic (solid lines, ps = 0) rescue. The control (i.e., no intervention) scenario is represented in dashed red lines.
Effects of the combination of demographic, genetic and habitat rescue on the number of reproductive individuals. Safe site increases represent fractions of suitable sites (φ∈0.25,0.5$$ \varphi \in \left[0.25,0.5\right] $$) for habitat rescue and the probability of new S alleles represents the probability of introducing new genetic variation (ps∈0.2,1.0$$ {p}_{\mathrm{s}}\in \left[0.2,1.0\right] $$) by genetic rescue. Each heatmap shows the effect of the number of individuals introduced (N∈10,50$$ N\in \left[10,50\right] $$). Colors represent values for the number of reproductive individuals.
Effects of the combination of genetic and habitat rescue on mate availability. Safe site increases represent fractions of suitable sites (φ∈0.25,0.5$$ \varphi \in \left[0.25,0.5\right] $$) for habitat rescue and probability of new S alleles represents the probability of introducing new genetic variation (ps∈0.2,1.0$$ {p}_{\mathrm{s}}\in \left[0.2,1.0\right] $$) by genetic rescue. The 3D surface represents average mate availability values for combinations of ps$$ {p}_s $$ and φ.$$ \varphi . $$ Colors represent average mate availability values going from low (dark purple) to high (yellow).
Genetic and Habitat Rescue Improve Population Viability in Self‐Incompatible Plants

November 2024

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22 Reads

Habitat fragmentation and the acceleration of environmental change threaten the survival of many plant species. The problem is especially pronounced for plant species with self‐incompatibility mating systems, which are obligate outcrossers, thus requiring high mate availability to persist. In such situations, plant populations suffering decreased fitness could be rescued by: (a) improving local habitat conditions (habitat rescue), (b) increasing the number of individuals (demographic rescue), or (c) introducing new genetic variation (genetic rescue). In this study, we used a spatially and genetically explicit individual‐based model to approximate the demography of a small (N = 250) isolated self‐incompatible population using a timescale of 500 years. Using this model, we quantified the effectiveness of the different types of rescues described above, singly and in combination. Our results show that individual genetic rescue is the most effective type of rescue with respect to improving fitness and population viability. However, we found that introducing a high number of individuals (N > 30) to a small population (N = 50) at the brink of extinction through demographic rescue can also have a positive effect on viability, improving average fitness by 55% compared to introducing a low number of individuals (N = 10) over a long timescale (> 500 years). By itself, habitat rescue showed the lowest effects on viability. However, combining genetic and habitat rescue provided the best results overall, increasing both persistence (> 30%) and mate availability (> 50%). Interestingly, we found that the addition of even a small number of new S alleles (20%) can be highly beneficial to increase mate availability and persistence. We conclude that genetic rescue through the introduction of new S alleles and an increase in habitat suitability is the best management strategy to improve mate availability and population viability of small isolated SI plant populations to overcome the effects of demographic stochasticity and positive density dependence.


Spring bearded seal harvest at Point Hope, Alaska. Seals are being prepared for use of the skin, meat, and oil. Photo credit Alaska Department of Fish and Game.
Locations of 13 coastal Alaskan villages spanning the range of bearded seals in the Bering, Chukchi, and Beaufort seas, where samples were collected. The spatial distribution of harvest locations for seals composing our 25 possible HSP‐GGPs and two POPs is also shown with filled stars (POPs red; HSP‐GGPs blue) next to the name of the village indicate the harvest location of both seals in a pair. The seals comprising both POPs were harvested at Point Hope. Curves connect the harvest locations for a pair harvested by different villages. If greater than 1, the number of occurrences of pairs between two villages is shown on the curve. See Table 1 for kin pair acronym definitions.
Age‐specific values of bearded seal female fecundity, male maturity, and survival values used as inputs to CKMR models. Fecundity and maturity schedules were fixed during estimation, while parameters of the survival function were estimated (the survival schedule shown is the expectation from the Bayesian prior).
Birth gap by HSP/UP PLOD values for HSP‐GGPs and third‐order kin. We performed mtDNA analysis on pairs with HSP/UP PLOD scores > 30 (i.e., potential HSP‐GGPs) to identify those that share mtDNA (maternally related, M) and those that do not (paternally related, P). Whether likely third‐order kin (i.e., pairs with PLOD scores < 30) are maternally or paternally related is unknown (U).
Prior and posterior estimates of survival‐at‐age, the later corresponding to the base model, which accounts for heterogeneity in the breeding success of adult males (Table 1; Model 2).
Estimating Demographic Parameters for Bearded Seals, Erignathus barbatus, in Alaska Using Close‐Kin Mark‐Recapture Methods

November 2024

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17 Reads

Reliable estimates of population abundance and demographics are essential for managing harvested species. Ice‐associated phocids, “ice seals,” are a vital resource for subsistence‐dependent coastal Native communities in western and northern Alaska, USA. In 2012, the Beringia distinct population segment of the bearded seal, Erignathus barbatus nauticus, was listed as “threatened” under the US Endangered Species Act requiring greater scrutiny for management assessments. We sought to estimate requisite population parameters from harvested seals by using close‐kin mark‐recapture (CKMR) methods, the first such application for marine mammals. Samples from 1758 bearded seals harvested by Bering, Chukchi, and Beaufort Sea communities during 1998–2020 were genotyped, genetically sexed, and aged by tooth annuli. After rigorous quality control, kin relationships were established for 1484 seals including two parent–offspring pairs (POPs) and 25 potential second‐order kin pairs. Most of the second‐order kin were half‐sibling pairs (HSPs), but four were potential grandparent‐grandchild pairs (GGPs). There were no full sibling pairs, suggesting a lack of mate fidelity. Mitochondrial DNA analysis identified 17 potential HSPs as paternally related, providing substantial evidence of persistent heterogeneity in reproductive success among adult males. The statistical CKMR model incorporates probabilities associated with POPs, HSPs, and GGPs and assumes known ages and a stable population. Our top model accommodates heterogeneity in adult male breeding success and yields an abundance estimate of ~409,000 with a coefficient of variation (CV) = 0.35, which is substantially greater than the “non‐heterogeneity” model estimate of ~232,000 (CV = 0.21), an important difference for managing a harvested species. Using CKMR methods with harvested species provides estimates of abundance with the added opportunity to acquire information about adult survival, fecundity, and breeding success that could be applied to other species of concern, marine and terrestrial.


Genetics in the Ocean's Twilight Zone: Population Structure of the Glacier Lanternfish Across Its Distribution Range

November 2024

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131 Reads

The mesopelagic zone represents one of the few habitats that remains relatively untouched from anthropogenic activities. Among the many species inhabiting the north Atlantic mesopelagic zone, glacier lanternfish (Benthosema glaciale) is the most abundant and widely distributed. This species has been regarded as a potential target for a dedicated fishery despite the scarce knowledge of its population genetic structure. Here, we investigated its genetic structure across the North Atlantic and into the Mediterranean Sea using 121 SNPs, which revealed strong differentiation among three main groups: the Mediterranean Sea, oceanic samples, and Norwegian fjords. The Mediterranean samples displayed less than half the genetic variation of the remaining ones. Very weak or nearly absent genetic structure was detected among geographically distinct oceanic samples across the North Atlantic, which contrasts with the low motility of the species. In contrast, a longitudinal gradient of differentiation was observed in the Mediterranean Sea, where genetic connectivity is known to be strongly shaped by oceanographic processes such as current patterns and oceanographic discontinuities. In addition, 12 of the SNPs, in linkage disequilibrium, drove a three clusters' pattern detectable through Principal Component Analysis biplot matching the genetic signatures generally associated with large chromosomal rearrangements, such as inversions. The arrangement of this putative inversion showed frequency differences between open‐ocean and more confined water bodies such as the fjords and the Mediterranean, as it was fixed in the latter for the second most common arrangement of the fjord's samples. However, whether genetic differentiation was driven by local adaptation, secondary contact, or a combination of both factors remains undetermined. The major finding of this study is that B. glaciale in the North Atlantic‐Mediterranean is divided into three major genetic units, information that should be combined with demographic properties to outline the management of this species prior to any eventual fishery attempt.


Lineage Differentiation and Genomic Vulnerability in a Relict Tree From Subtropical Forests

November 2024

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152 Reads

The subtropical forests of East Asia are renowned for their high plant diversity, particularly the abundance of ancient relict species. However, both the evolutionary history of these relict species and their capacity for resilience in the face of impending climatic changes remain unclear. Using whole‐genome resequencing data, we investigated the lineage differentiation and demographic history of the relict and endangered tree, Bretschneidera sinensis (Akaniaceae). We employed a combination of population genomic and landscape genomic approaches to evaluate variation in mutation load and genomic offset, aiming to predict how different populations may respond to climate change. Our analysis revealed a profound genomic divergence between the East and West lineages, likely as the result of recurrent bottlenecks due to climatic fluctuations during the glacial period. Furthermore, we identified several genes potentially linked to growth characteristics and hypoxia response that had been subjected to positive selection during the lineage differentiation. Our assessment of genomic vulnerability uncovered a significantly higher mutation load and genomic offset in the edge populations of B. sinensis compared to their core counterparts. This implies that the edge populations are likely to experience the most significant impact from the predicted climate conditions. Overall, our research sheds light on the historical lineage differentiation and contemporary genomic vulnerability of B. sinensis. Broadening our understanding of the speciation history and future resilience of relict and endangered species such as B. sinensis, is crucial in developing effective conservation strategies in anticipation of future climatic changes.


Population structure and demographic history of annual and perennial rye. (A) and (B) Principal component analysis. Annual and perennial populations are surrounded by rounded rectangles. Ancestry proportions (K = 5) are shown by different coloured pie charts. (C) Genome‐wide mean nucleotide diversity. (D) Inbreeding coefficient (F). (E) Demographic model. Gene flow between annual and perennial rye is indicated by black arrows.
Genome‐wide correlation between genetic differentiation, sequence divergence, recombination rate and nucleotide diversity. (A) Pearson correlation (r) between absolute sequence divergence (dxy) and genetic differentiation (Z(FST)). (B) Pearson correlation (r) between genetic differentiation (Z(FST)) and average nucleotide diversity (πaverage). (C) Pearson correlation (r) between nucleotide diversity (πaverage) and absolute sequence divergence (dxy). (D) Pearson correlation (r) between genetic differentiation (Z(FST)) and population recombination rate (ρ, estimated in annual rye). (E) Pearson correlation (r) between population recombination rate (ρ, estimated in annual rye) and absolute sequence divergence (dxy).
Heterogeneous differentiation landscapes. Presence (A) and absence (B) of signatures of linked selection on chromosomes 3R and 1R, respectively. Dashed vertical lines delineate the low‐recombining region of each chromosome. Dashed horizontal lines correspond to FST‐outlier scans based on a genome‐wide threshold (black), low‐recombining regions (blue), intermediate‐recombining regions (orange) and high‐recombining regions (magenta).
Gene ontology enrichment in significantly differentiated regions. Gene ontology terms are separated into ‘Biological process’, ‘Cellular component’ and ‘Molecular function’. Within each class, we included the top 10 terms with the highest gene enrichment ratios, sorted by pFDR‐value in ascending order. A full list of all GO‐terms is available in Table S5.
Characterising the Genomic Landscape of Differentiation Between Annual and Perennial Rye

October 2024

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32 Reads

Annuality and perenniality represent two different life‐history strategies in plants, and an analysis of genomic differentiation between closely related species of different life histories bears the potential to identify the underlying targets of selection. Additionally, understanding the interactions between patterns of recombination and signatures of natural selection is a central aim in evolutionary biology, because patterns of recombination shape the evolution of genomes by affecting the efficacy of selection. Here, our aim was to characterise the landscape of genomic differentiation between weedy annual rye (Secale cereale L.) and wild perennial rye (Secale strictum C. Presl), and explore the extent to which signatures of selection are influenced by recombination rate variation. We used population‐level sequence data of annual and perennial rye to analyse population structure and their demographic history. Based on our analyses, annual and perennial rye diverged approximately 26,500 years ago (ya) from an ancestral population size of ~85,000 individuals. We analysed patterns of genetic diversity and genetic differentiation, and found highly differentiated regions located in low‐recombination regions, indicative of linked selection. Although all highly differentiated regions, as revealed by FST‐outlier scans, were located in low‐recombining regions, not all chromosomes showed this tendency. We therefore performed a gene ontology enrichment analysis, which showed that highly differentiated regions comprise genes involved in photosynthesis. This enrichment was confirmed when FST outlier scans were performed separately in low‐ and intermediate‐recombining regions, but not in high‐recombining regions, suggesting that local recombination rate variation in rye affects outlier scans. Cultivated rye is an annual crop, but the introduction of perenniality may be advantageous in regions with poor soil quality or under low‐input farming. Although the resolution of our analysis is limited to a broad‐scale, knowledge about the evolutionary divergence between annual and perennial rye might support breeding efforts towards perennial rye cultivation.


Map of the geographically defined management areas for the 11 stocks (management units in different colors) assessed by the International Council for the Exploration of the Sea (ICES) in the northeastern Atlantic. Stocks occurring in the Norwegian Sea and North Sea (study area) are the Norwegian spring‐spawning (NSS) herring stock, the North Sea autumn‐spawning (NSAS) herring stock, the Icelandic summer‐spawning herring (ISSH) stock, and the western Baltic spring‐spawning (WBSS) herring stock which are typically named after the putatively most abundant population (biological unit). Herring stocks in ICES subdivision 6a are genetically identified (Farrell et al. 2022). Overlapping management areas are indicated by cross hatched colors. The stippled line indicates the currently used management boundary between the exploited stocks at 62° N. The stippled box in the North Sea indicates the so‐called ‘transfer‐area’ where all herring catches (both from commercial catches and scientific surveys) are being split and allocated either to the NSAS or the WBSS herring stock for their assessments.
Map of sampling locations. Large points show baseline samples (see Table 1 for detailed information), and smaller points show mixed‐population samples from commercial catches and scientific surveys (HERAS, HERring Acoustic Survey; IESNS, International Ecosystem Survey in the Nordic Seas; IESSNS, International Ecosystem Summer Survey in the Nordic Seas) in 2019–2023. Inset, top right corner: Detailed map of the Sunnmøre area. The stippled lines are as in Figure 1.
Final baseline: Principal component analysis (PCA) biplot of the final baseline including 12 distinct herring populations: Baltic autumn‐spawning herring (BASH), central Baltic spring‐spawning herring (CBSS), Downs, local fjord populations, northeast Atlantic summer‐/autumn‐spawning herring (NASS), North Sea autumn‐spawning herring (NSAS), Norwegian spring‐spawning herring (NSS), spring‐spawning herring in ICES subdivision 6a (Sp‐6a), Trondheimsfjord herring (THF), western Baltic spring‐spawning herring (WBSS), western Baltic spring‐spawning herring in the Skagerrak (WBSS‐SK), and Pacific herring hybrids. Spawning time (autumn/winter negative, spring positive) represents the major driver of the differentiation displayed in the first axis. While the second axis seems to represent geographical/environmental distribution, and likely also multiple defining features e.g., differences in salinity.
Assignment results based on rubias for all mixed‐population samples combined for all years and ICES rectangles (1° longitude × 0.5° latitude). Note that the size of the pie charts does not reflect neither catch size nor sample size. Pie chart in the left corner represents the overall distribution of all samples combined, actual proportions of stocks per samples are provided in Figure 5. Population abbreviations are explained in the legend of Figure 3.
Violin plot showing the distribution of population proportions for all individual mixed‐population samples (N = 457, indicated by points) in the Norwegian Sea (north of 62° N) and the North Sea (south of 62° N). Assignment results based on rubias for all mixed‐population samples. Note that the absence (null observation) per populations is not included. Population abbreviations are explained in the legend of Figure 3.
Genetic Stock Identification Reveals Mismatches Between Management Areas and Population Genetic Structure in a Migratory Pelagic Fish

October 2024

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292 Reads

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1 Citation

Sustainable fisheries management is important for the continued harvest of the world's marine resources, especially as they are increasingly challenged by a range of climatic and anthropogenic factors. One of the pillars of sustainable fisheries management is the accurate identification of the biological units, i.e., populations. Here, we developed and implemented a genetic baseline for Atlantic herring harvested in the Norwegian offshore fisheries to investigate the validity of the current management boundaries. This was achieved by genotyping > 15,000 herring from the northern European seas, including samples of all the known populations in the region, with a panel of population‐informative SNPs mined from existing genomic resources. The final genetic baseline consisted of ~1000 herring from 12 genetically distinct populations. We thereafter used the baseline to investigate mixed catches from the North and Norwegian Seas, revealing that each management area consisted of multiple populations, as previously suspected. However, substantial numbers (up to 50% or more within a sample) of herring were found outside of their expected management areas, e.g., North Sea autumn‐spawning herring north of 62° N (average = 19.2%), Norwegian spring‐spawning herring south of 62° N (average = 13.5%), and western Baltic spring‐spawning herring outside their assumed distribution area in the North Sea (average = 20.0%). Based upon these extensive observations, we conclude that the assessment and management areas currently in place for herring in this region need adjustments to reflect the populations present. Furthermore, we suggest that for migratory species, such as herring, a paradigm shift from using static geographic stock boundaries towards spatial dynamic boundaries is needed to meet the requirements of future sustainable management regimes.


of life history traits used to calculate Ne/Nc. (a) generation interval (max. age), (b) total reproductive investment (offspring total) and (c) realised reproductive output (offspring survived) for wolves in Germany, per sex and both sexes combined, represented as box plots. Median values: Full line; average values: Dashed lines. Whiskers represent 1.5 × the interquartile range.
Estimating the Effective Size of European Wolf Populations

October 2024

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375 Reads

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1 Citation

Molecular methods are routinely used to estimate the effective size of populations (Ne). However, underlying model assumptions are frequently violated to an unknown extent. Although simulations can detect sources of bias and help to adjust sampling strategies and analyses methods, additional information from empirical data can also be used to calibrate methods and improve molecular Ne estimation methods. Here, we take advantage of long‐term genetic and ecological monitoring data of the grey wolf (Canis lupus) in Germany, and detailed population genetic studies in Poland, Spain and Portugal to improve Ne estimation strategies in this species, and species with similar life history traits. We first calculated Ne from average lifetime reproductive success and detailed census data from the German population, which served as a baseline to compare to molecular estimates based on linkage disequilibrium and sibship frequency. This yielded a robust Ne/Nc estimation that we used to calibrate molecular estimates of German, Polish and Iberian wolf populations. The linkage disequilibrium method was strongly influenced by spatial genetic structure, much more than the sibship frequency method. When Ne was estimated in local neighbourhoods, both methods yielded comparable results. Estimates of the metapopulation effective size seemed to correspond generally well with the sum of the estimates of local neighbourhoods. Overall, we found that the number of packs is a good proxy of the effective population size. Using this as a rule of thumb, we evaluated for all European wolf populations the Ne 500 indicator and concluded that half of the European wolf populations do not yet fulfil this criterion.


Evolutionary potential depends on richness. Imagine population 1 and population 4 from Table 1 being confronted with a new environment in which there is directional selection for one of the alleles. Assuming semi‐dominant fitness effects, the time to 90% fixation for allele A would be 32 time units in Pop1, and 60 time units in Pop4 (the number of generations depends on the absolute fitness difference, but expressed as relative time units the exact fitness difference is irrelevant). On average over all alleles, the average time to 90% fixation is in this case 1.45 times as long for population 4 (starting from p = 0.01 in four cases and p = 0.96 in one case) relative to population 1 (starting from p = 0.20 in five cases). The shape of the curve for an allele trajectory from 0.20 to 0.90 is identical to that from 0.01 to 0.90, except for the head start of 28 time units it has from 0.01 to 0.20. The evolutionary potential (the likelihood of reaching the end point), however, is identical as long as no alleles are lost by drift.
Population Size in Evolutionary Biology Is More Than the Effective Size

October 2024

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57 Reads

In population genetics idealized Wright‐Fisher (WF) populations are generally considered equivalent to real populations with regard to the major evolutionary processes that influence genotype and allele frequencies. As a result we often model the response of populations by focusing on the effective size Ne. The Diversity Partitioning Theorem (DPT) shows that you cannot model the behavior of a system solely on the basis of a diversity (accounting for unevenness among items) without taking richness into account. I show that the census population size (the number of adults, Nc) is equivalent to a richness, and that the effective size Ne is equivalent to a true diversity. It follows logically from the DPT that we require both Ne and Nc to understand how drift, selection, mutation, and gene flow interact to shape the course of evolution of populations. Here I review evidence that both Nc and Ne affect evolutionary trajectories of populations for neutral and adaptive processes. This also influences how we should consider evolutionary potential and genetic criteria for conservation of populations. The effective size of a population is of huge importance in evolutionary biology, but it should not be the sole focus when population size is concerned. Applied evolutionary studies need to integrate Nc in the equation more consistently when modeling the response to selection, mutation, migration, and drift.


Cross strategy used to generate diploid and triploid lines for this study. Detailed cross strategy and number of oysters used for each cross are described in Bodenstein, Casas, Tiersch and La Peyre (2023); Bodenstein et al. (2023).
Cumulative mortality of diploid and triploid oysters outplanted to (A) Grand Isle and (B) LUMCON sites, replotted from Bodenstein, Casas, Tiersch and La Peyre (2023), Bodenstein et al. (2023). The X‐axis indicates timepoints in months for which mortality data was collected, and the Y‐axis represents cumulative mortality. Oysters are grouped together based on their ploidy and cohorts. Purple line: Triploid oysters from LSU cohort; green dotted line: Triploid oysters from Auburn cohort; blue dotted line: Diploid oysters from LSU cohort; orange line: Diploid oysters from Auburn the cohort.
(A) PCA showing separation based on site, cohort, and ploidy; (B) transcriptomic shift measured as distance in multivariate space between diploid and triploid samples matched for their site, cohort, and dams.
(A) Eigengene expression plots for four modules showing significant correlation to site and cohort in WGCNA, with samples grouped together by their cohorts and ploidies; and GO terms with the highest p values in those corresponding modules. Orange: Diploids from the Auburn cohort; green: Diploids from the LSU cohort; blue: Triploids from the Auburn cohort; purple: Triploids from the LSU cohort. (B) Heatmap of WGCNA module‐trait relationship results. The X‐axis shows the experimental parameters of interest used for correlations. Red indicates positive correlations, and blue indicates negative correlations between a module and an experimental parameter.
Comparative Transcriptomic Analyses Reveal Differences in the Responses of Diploid and Triploid Eastern Oysters to Environmental Stress

October 2024

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50 Reads

Triploid oysters are commonly used as the basis for production in the aquaculture of eastern oysters along the USA East and Gulf of Mexico coasts. While they are valued for their rapid growth, incidents of triploid mortality during summer months have been well documented in eastern oysters, especially at low salinity sites. We compared global transcriptomic responses of diploid and triploid oysters bred from the same three maternal source populations at two different hatcheries and outplanted to a high (annual mean salinity = 19.4 ± 6.7) and low (annual mean salinity = 9.3 ± 5.0) salinity site. Oysters were sampled for gene expression at the onset of a mortality event in the summer of 2021 to identify triploid‐specific gene expression patterns associated with low salinity sites, which ultimately experienced greater triploid mortality. We also examined chromosome‐specific gene expression to test for instances of aneuploidy in experimental triploid oyster lines, another possible contributor to elevated mortality in triploids. We observed a strong effect of hatchery conditions (cohort) on triploid‐specific mortality (field data) and a strong interactive effect of hatchery, ploidy, and outplant site on gene expression. At the low salinity site where triploid oysters experienced high mortality, we observed downregulation of transcripts related to calcium signaling, ciliary activity, and cell cycle checkpoints in triploids relative to diploids. These transcripts suggest dampening of the salinity stress response and problems during cell division as key cellular processes associated with elevated mortality risk in triploid oysters. No instances of aneuploidy were detected in our triploid oyster lines. Our results suggest that triploid oysters may be fundamentally less tolerant of rapid decreases in salinity, indicating that oyster farmers may need to limit the use of triploid oysters to sites with more stable salinity conditions.


When Do Tumours Develop? Neoplastic Processes Across Different Timescales: Age, Season and Round the Circadian Clock

While it is recognised that most, if not all, multicellular organisms harbour neoplastic processes within their bodies, the timing of when these undesirable cell proliferations are most likely to occur and progress throughout the organism's lifetime remains only partially documented. Due to the different mechanisms implicated in tumourigenesis, it is highly unlikely that this probability remains constant at all times and stages of life. In this article, we summarise what is known about this variation, considering the roles of age, season and circadian rhythm. While most studies requiring that level of detail be done on humans, we also review available evidence in other animal species. For each of these timescales, we identify mechanisms or biological functions shaping the variation. When possible, we show that evolutionary processes likely played a role, either directly to regulate the cancer risk or indirectly through trade‐offs. We find that neoplastic risk varies with age in a more complex way than predicted by early epidemiological models: rather than resulting from mutations alone, tumour development is dictated by tissue‐ and age‐specific processes. Similarly, the seasonal cycle can be associated with risk variation in some species with life‐history events such as sexual competition or mating being timed according to the season. Lastly, we show that the circadian cycle influences tumourigenesis in physiological, pathological and therapeutic contexts. We also highlight two biological functions at the core of these variations across our three timescales: immunity and metabolism. Finally, we show that our understanding of the entanglement between tumourigenic processes and biological cycles is constrained by the limited number of species for which we have extensive data. Improving our knowledge of the periods of vulnerability to the onset and/or progression of (malignant) tumours is a key issue that deserves further investigation, as it is key to successful cancer prevention strategies.


Global distribution of collection sites and haplotype composition of populations of Liriomyza huidobrensis. Each circle represents pooled samples for each country. Sample sizes are shown within boxes; in addition, circles are approximately scaled for population size. Slices within each circle represent haplotypes present in that particular location and indicate relative abundance. All private haplotypes (those found only in a single country) are shown in grey. Haplotypes shared between two or more countries are indicated in color.
Regional distribution of private and invasive haplotypes in Ecuador and Peru. Details as in Figure 1. Non‐invasive haplotypes shared among locations are shown in a variety of patterns and colors.
Haplotype network for all haplotypes including invasive haplotypes, singletons from introduced populations, and those intercepted at US Ports of Entry. Invasive haplotypes Haps A–D found in the introduced location are shown in color as in Figures 1 and 2. Green circles are singleton haplotypes found in introduced populations. Black circles edged with red indicate haplotypes from individuals intercepted at US ports of entry.
Maximum likelihood analysis of global Liriomyza huidobrensis haplotypes. Invasive haplotypes Haps A–D found in the introduced location are shown in color as in previous figures. The number of individuals carrying each haplotype is shown in parentheses when more than one. Country names in red type indicate introduced populations. Black circles edged with red indicate haplotypes from individuals intercepted at US ports of entry. Bootstrap support values for Groups 1, 2, and 3 are presented at each node.
Peruvian origin and global invasions of five continents by the highly damaging agricultural pest Liriomyza huidobrensis (Diptera: Agromyzidae)

October 2024

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24 Reads

Identification of the geographic origin of invasive species can be critical to effective management and amelioration of negative impacts in the introduced range. Liriomyza huidobrensis is a polyphagous leafmining fly that is a devastating pest of many vegetable and floriculture crops around the world. Considered native to South and possibly Central America, L. huidobrensis became invasive in the 1980s and has since spread to at least 30 countries on five continents. We used phylogeographic analysis of over 2 kb of mitochondrial cytochrome oxidase I and II sequence data from 403 field‐collected specimens from both native and introduced populations to investigate the geographic origins of invasive L. huidobrensis worldwide. Within South America, there was substantial genetic variation, as well as the strong phylogeographic structure typical of a native range. In contrast, leafminers from the introduced range and Central America all contained little genetic variation and shared the same small set of haplotypes. These haplotypes trace to Peru as the ultimate geographic origin of invasive populations. Central America is rejected as part of the original geographic range of L. huidobrensis. Within Peru, the primary export region of Lima shared an extremely similar pattern of reduced haplotype variation to the invasive populations. An additional 18 specimens collected at US ports of entry did not share the same haplotype profile as contemporary invasive populations, raising perplexing questions on global pathways and establishment success in this species.


Landscape Heterogeneity and Environmental Dynamics Improve Predictions of Establishment Success of Colonising Small Founding Populations

October 2024

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82 Reads

In long‐distance dispersal events, colonising species typically begin with a small number of founding individuals. A growing body of research suggests that establishment success of small founding populations can be determined by the context of the colonisation event and the new environment. Here, we illuminate the importance of these sources of context dependence. Using a spatially explicit, temporally dynamic, mechanistic, individual‐based simulator of a model amphibian species, the cane toad (Rhinella marina), we simulated colonisation scenarios to investigate how (1) the number of founding individuals, (2) the number of dispersal events, (3) landscape's spatial composition and configuration of habitats (‘spatially heterogeneous landscapes’) and (4) the timing of arrival with regards to dynamic environmental conditions (‘dynamic environmental conditions’) influence the establishment success of small founding populations. We analysed the dynamic effects of these predictors on establishment success using running‐window logistic regression models. We showed establishment success increases with the number of founding individuals, whereas the number of dispersal events had a weak effect. At ≥ 20 founding individuals, propagule size swamps the effects of other factors, to whereby establishment success is near‐certain (≥ 90%). But below this level, confidence in establishment success dramatically decreases as number of founding individuals decreases. At low numbers of founding individuals, the prominent predictors are landscape spatial heterogeneity and dynamic environmental conditions. For instance, compared to the annual mean, founding populations with ≤ 5 individuals have up to 18% higher establishment success when they arrive in ‘packed’ landscapes with relatively limited and clustered essential habitats and right before the breeding season. Accounting for landscape spatial heterogeneity and dynamic environmental conditions is integral in understanding and predicting population establishment and species colonisation. This additional complexity is necessary for advancing biogeographical theory and its application, such as in guiding species reintroduction efforts and invasive alien species management.


Study site locations in the Upper St. Lawrence River system and results of the population structure. (A) The study sites are located near the island of Montreal, QC, Canada (right of the map). Sites are colored based on water calcium concentration (mg/L). Sites with low calcium and round gobies absent are HA‐LCGA, OKA‐LCGA, IB‐LCGA, PB‐LCGA, and IPE‐LCGA while sites with high calcium and round gobies present are PG‐HCGP, PST‐HCGP, PON‐HCGP, BEA‐HCGP, and GOY‐HCGP. The two exceptions are RAF‐LCGP (low calcium and round gobies present) and PDC‐HCGA (wetland, high calcium, and round gobies absent), which have inverted patterns. (B) Pairwise FST matrix between the 12 study populations based on non‐outliers SNPs. The gray bars correspond to the Ottawa River populations (LCGA) and the blue bars to the St. Lawrence populations (HCGP), except for PDC (HCGA, wetland refuge) and RAF (LCGP). (C) Phylogenetic relationships between populations are shown as an UPGMA tree, with numbers indicating support for each node based on 1000 bootstraps.
Experimental design of the laboratory reciprocal transplant experiment and results for the fecundity (total number of eggs produced) and survival of adult Amnicola limosus as a function of water treatment, origin water, and round goby cue treatment in the reciprocal transplant experiment. (A) Experimental design showing the two origin waters (Ottawa River Low Calcium/round Goby Absent LCGA in grey or St. Lawrence River High Calcium/round Goby Present HCGP in blue) with six replicate populations each, the water treatments (LCGA and HCGP) and the round goby cue treatment (+/–: With or without). (B) Top: Results of the converted coefficients of significant fixed effects (incident rate ratios and odds ratio) of the GLM and GLMM used to analyze fecundity and survival, respectively. Asterisks indicate threshold of p‐values: * for p < 0.05, ** for p < 0.01, *** for p < 0.001. Bottom: Raw data of the experiment, each dot represents a measurement for one population (origins in grey: LCGA, blue: HCGP), summarized by the mean for each treatment (black squares and triangles for treatments with or without round goby cues, respectively) and the 95% confidence interval around the mean (bootstrapping method).
Allele frequency of candidate SNPs associated with the calcium gradient or with the round goby presence/absence, and of the non‐outliers SNPs. Note that we removed SNPs that showed inconsistent allele frequency changes compared to the other candidate SNPs considered false positives. The color scale indicates the allele frequency in a given population, and the black line is the average allele frequency change. (A) Candidate SNPs positively associated with the low‐calcium concentration. (B) Candidate SNPs negatively associated with the low‐calcium concentration. (C) Random subset of 400 non‐outlier SNPs non‐associated with the calcium gradient. (D) Candidates SNPs positively associated with the round goby presence (a random subset of 400 SNPs). (E) Candidates SNPs negatively associated with the round goby presence (a random subset of 400 SNPs). (F) Random subset of 400 non‐outlier SNPs non‐associated with the round goby presence/absence.
Genome‐wide diversity indices. (A) Violin plots of nucleotide diversity pi, (B) Watterson's Theta, (C) and Tajima's D according to predation level (round goby absent/present), with median and interquartile ranges shown in the box plot insert. (D) Observed heterozygosity per population, comparing round goby‐impacted and refuge populations.
Limited Migration From Physiological Refugia Constrains the Rescue of Native Gastropods Facing an Invasive Predator

October 2024

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47 Reads

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


Epigenetic Diversity and the Evolutionary Potential of Wild Populations

October 2024

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61 Reads

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


Journal metrics


3.5 (2023)

Journal Impact Factor™


43%

Acceptance rate


8.5 (2023)

CiteScore™


55 days

Submission to first decision


$3,930 / £2,610 / €3,010

Article processing charge

Editors