Jane Park, Charles Brown, Chelsea Hess, Madison Armstrong, David M. Rocke, Fernando Galvez, Andrew Whitehead
Persistence of wild species in human-altered environments is difficult, in part because challenges to fitness are complex when multiple environmental changes occur simultaneously, which is common in the Anthropocene. This complexity is difficult to conceptualize because the nature of environmental change is often highly context specific. A mechanism-guided approach may help to shape intuition and predictions about complexity; fitness challenges posed by co-occurring stressors with similar mechanisms of action may be less severe than for those with different mechanisms of action. We approach these considerations within the context of ecotoxicology because this field is built upon a rich mechanistic foundation. We hypothesized that evolved resistance to one class of common toxicants would afford resilience to the fitness impacts of another class of common toxicants that shares mechanisms of toxicity. Fundulus killifish populations in urban estuaries have repeatedly evolved resistance to persistent organic pollutants including PCBs. Since PCBs and some of the toxicants that constitute crude oil (e.g., high molecular weight PAHs) exert toxicity through perturbation of AHR signaling, we predicted that PCB-resistant populations would also be resilient to crude oil toxicity. Common garden comparative oil exposure experiments, including killifish populations with different exposure histories, showed that most killifish populations were sensitive to fitness impacts (reproduction and development) caused by oil exposure, but that fish from the PCB-resistant population were insensitive. Population differences in toxic outcomes were not compatible with random-neutral expectations. Transcriptomics revealed that the molecular mechanisms that contributed to population variation in PAH resilience were shared with those that contribute to evolved variation in PCB resilience. We conclude that the fitness challenge posed by environmental pollutants is effectively reduced when those chemicals share mechanisms that affect fitness. Mechanistic considerations may help to scale predictions regarding the fitness challenges posed by stressors that may co-occur in human-altered environments.
{"title":"Multiple Stressors in the Anthropocene: Urban Evolutionary History Modifies Sensitivity to the Toxic Effects of Crude Oil Exposure in Killifish","authors":"Jane Park, Charles Brown, Chelsea Hess, Madison Armstrong, David M. Rocke, Fernando Galvez, Andrew Whitehead","doi":"10.1111/eva.70112","DOIUrl":"https://doi.org/10.1111/eva.70112","url":null,"abstract":"<p>Persistence of wild species in human-altered environments is difficult, in part because challenges to fitness are complex when multiple environmental changes occur simultaneously, which is common in the Anthropocene. This complexity is difficult to conceptualize because the nature of environmental change is often highly context specific. A mechanism-guided approach may help to shape intuition and predictions about complexity; fitness challenges posed by co-occurring stressors with similar mechanisms of action may be less severe than for those with different mechanisms of action. We approach these considerations within the context of ecotoxicology because this field is built upon a rich mechanistic foundation. We hypothesized that evolved resistance to one class of common toxicants would afford resilience to the fitness impacts of another class of common toxicants that shares mechanisms of toxicity. <i>Fundulus</i> killifish populations in urban estuaries have repeatedly evolved resistance to persistent organic pollutants including PCBs. Since PCBs and some of the toxicants that constitute crude oil (e.g., high molecular weight PAHs) exert toxicity through perturbation of AHR signaling, we predicted that PCB-resistant populations would also be resilient to crude oil toxicity. Common garden comparative oil exposure experiments, including killifish populations with different exposure histories, showed that most killifish populations were sensitive to fitness impacts (reproduction and development) caused by oil exposure, but that fish from the PCB-resistant population were insensitive. Population differences in toxic outcomes were not compatible with random-neutral expectations. Transcriptomics revealed that the molecular mechanisms that contributed to population variation in PAH resilience were shared with those that contribute to evolved variation in PCB resilience. We conclude that the fitness challenge posed by environmental pollutants is effectively reduced when those chemicals share mechanisms that affect fitness. Mechanistic considerations may help to scale predictions regarding the fitness challenges posed by stressors that may co-occur in human-altered environments.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"18 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-05-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70112","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144074327","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Rapid climate change is affecting biodiversity and threatening locally adapted species. Relict species are often confined to relatively narrow, discontinuous geographic ranges and provide excellent opportunities to study local adaptation and extinction. Understanding the adaptive genetic variation and genetic vulnerability of relict species under climate change is essential for their conservation and management efforts. Here, we applied a landscape genomics approach to investigate the population genetic structure and predict adaptive capacity to climatic change for Taiwania cryptomerioides Hayata, a vulnerable Tertiary relict tree species in China. We used restriction site-associated DNA sequencing on 122 individuals across 10 sampling sites. We found three genetic groups across the Chinese range of T. cryptomerioides: the southwest, central-eastern, and Taiwanese groups. We detected significant signals of isolation by environment and isolation by distance, with environment playing a more important role than geography in shaping spatial genetic variation in T. cryptomerioides. Moreover, some outliers were related to defense and stress responses, which could reflect the genomic basis of adaptation. Gradient forest (GF) analysis revealed that precipitation-related variables were important in driving adaptive variation in T. cryptomerioides. Ecological niche modeling and GF analysis revealed that the central-eastern populations were more vulnerable to future climate change than other populations, with range contractions and high genetic offsets, suggesting these populations may be at higher risk of decline or local extinction. These findings deepen our understanding of local adaptation and vulnerability to climate change in relict tree species and will guide conservation and restoration programs for T. cryptomerioides in the future.
{"title":"Local Adaptation and Climate Change Vulnerability of the Relict Tree Species Taiwania cryptomerioides Provide Insights Into Its Conservation and Restoration","authors":"Yang Lu, Hao Dong, Saibin Fan, Lu Yuan, Yuhui Wang, Zhuang Zhao, Yong Lai, Shixin Zhu, Jinyong Huang, Caipeng Yue, Yongpeng Ma, Ningning Zhang","doi":"10.1111/eva.70113","DOIUrl":"https://doi.org/10.1111/eva.70113","url":null,"abstract":"<p>Rapid climate change is affecting biodiversity and threatening locally adapted species. Relict species are often confined to relatively narrow, discontinuous geographic ranges and provide excellent opportunities to study local adaptation and extinction. Understanding the adaptive genetic variation and genetic vulnerability of relict species under climate change is essential for their conservation and management efforts. Here, we applied a landscape genomics approach to investigate the population genetic structure and predict adaptive capacity to climatic change for <i>Taiwania cryptomerioides</i> Hayata, a vulnerable Tertiary relict tree species in China. We used restriction site-associated DNA sequencing on 122 individuals across 10 sampling sites. We found three genetic groups across the Chinese range of <i>T. cryptomerioides</i>: the southwest, central-eastern, and Taiwanese groups. We detected significant signals of isolation by environment and isolation by distance, with environment playing a more important role than geography in shaping spatial genetic variation in <i>T. cryptomerioides</i>. Moreover, some outliers were related to defense and stress responses, which could reflect the genomic basis of adaptation. Gradient forest (GF) analysis revealed that precipitation-related variables were important in driving adaptive variation in <i>T. cryptomerioides</i>. Ecological niche modeling and GF analysis revealed that the central-eastern populations were more vulnerable to future climate change than other populations, with range contractions and high genetic offsets, suggesting these populations may be at higher risk of decline or local extinction. These findings deepen our understanding of local adaptation and vulnerability to climate change in relict tree species and will guide conservation and restoration programs for <i>T. cryptomerioides</i> in the future.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"18 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-05-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70113","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143950142","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Julian E. Beaman, Katie Gates, Frédérik Saltré, Carolyn J. Hogg, Katherine Belov, Kita Ashman, Karen Burke da Silva, Luciano B. Beheregaray, Corey J. A. Bradshaw
Genetic rescue is a conservation management strategy that reduces the negative effects of genetic drift and inbreeding in small and isolated populations. However, such populations might already be vulnerable to random fluctuations in growth rates (demographic stochasticity). Therefore, the success of genetic rescue depends not only on the genetic composition of the source and target populations but also on the emergent outcome of interacting demographic processes and other stochastic events. Developing predictive models that account for feedback between demographic and genetic processes (‘demo-genetic feedback’) is therefore necessary to guide the implementation of genetic rescue to minimize the risk of extinction of threatened populations. Here, we explain how the mutual reinforcement of genetic drift, inbreeding, and demographic stochasticity increases extinction risk in small populations. We then describe how these processes can be modelled by parameterizing underlying mechanisms, including deleterious mutations with partial dominance and demographic rates with variances that increase as abundance declines. We combine our suggestions of model parameterization with a comparison of the relevant capability and flexibility of five open-source programs designed for building genetically explicit, individual-based simulations. Using one of the programs, we provide a heuristic model to demonstrate that simulated genetic rescue can delay extinction of small virtual populations that would otherwise be exposed to greater extinction risk due to demo-genetic feedback. We then use a case study of threatened Australian marsupials to demonstrate that published genetic data can be used in one or all stages of model development and application, including parameterization, calibration, and validation. We highlight that genetic rescue can be simulated with either virtual or empirical sequence variation (or a hybrid approach) and suggest that model-based decision-making should be informed by ranking the sensitivity of predicted probability/time to extinction to variation in model parameters (e.g., translocation size, frequency, source populations) among different genetic-rescue scenarios.
{"title":"A Guide for Developing Demo-Genetic Models to Simulate Genetic Rescue","authors":"Julian E. Beaman, Katie Gates, Frédérik Saltré, Carolyn J. Hogg, Katherine Belov, Kita Ashman, Karen Burke da Silva, Luciano B. Beheregaray, Corey J. A. Bradshaw","doi":"10.1111/eva.70092","DOIUrl":"https://doi.org/10.1111/eva.70092","url":null,"abstract":"<p>Genetic rescue is a conservation management strategy that reduces the negative effects of genetic drift and inbreeding in small and isolated populations. However, such populations might already be vulnerable to random fluctuations in growth rates (demographic stochasticity). Therefore, the success of genetic rescue depends not only on the genetic composition of the source and target populations but also on the emergent outcome of interacting demographic processes and other stochastic events. Developing predictive models that account for feedback between demographic and genetic processes (‘demo-genetic feedback’) is therefore necessary to guide the implementation of genetic rescue to minimize the risk of extinction of threatened populations. Here, we explain how the mutual reinforcement of genetic drift, inbreeding, and demographic stochasticity increases extinction risk in small populations. We then describe how these processes can be modelled by parameterizing underlying mechanisms, including deleterious mutations with partial dominance and demographic rates with variances that increase as abundance declines. We combine our suggestions of model parameterization with a comparison of the relevant capability and flexibility of five open-source programs designed for building genetically explicit, individual-based simulations. Using one of the programs, we provide a heuristic model to demonstrate that simulated genetic rescue can delay extinction of small virtual populations that would otherwise be exposed to greater extinction risk due to demo-genetic feedback. We then use a case study of threatened Australian marsupials to demonstrate that published genetic data can be used in one or all stages of model development and application, including parameterization, calibration, and validation. We highlight that genetic rescue can be simulated with either virtual or empirical sequence variation (or a hybrid approach) and suggest that model-based decision-making should be informed by ranking the sensitivity of predicted probability/time to extinction to variation in model parameters (e.g., translocation size, frequency, source populations) among different genetic-rescue scenarios.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"18 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-05-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70092","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143944946","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Eric C. Anderson, Anthony J. Clemento, Matthew A. Campbell, Devon E. Pearse, Anne K. Beulke, Cassie Columbus, Ellen Campbell, Neil F. Thompson, John Carlos Garza
Genetic methods have become an essential component of ecological investigation and conservation planning for fish and wildlife. Among these methods is the use of genetic marker data to identify individuals to populations, or stocks, of origin. More recently, methods that involve genetic pedigree reconstruction to identify relationships between individuals within populations have also become common. We present here a novel set of multiallelic microhaplotype genetic markers for Chinook salmon, which provide excellent resolution for population discrimination and relationship identification from a rapidly and economically assayed panel of markers. We show how this set of genetic markers assayed by sequencing 204 amplicons, in tandem with a reference dataset of 1636 individual samples from 17 populations, provides definitive power to identify all known lineages of Chinook salmon in California. The inclusion of genetic loci that have known associations with phenotype and that were identified as outliers in examination of whole-genome sequence data allows resolution of stocks that are not highly genetically differentiated but are phenotypically distinct and managed as such. This same set of multiallelic genetic markers has ample variation to accurately identify parent-offspring and full-sibling pairs in all California populations, including the genetically depauperate winter-run lineage. Validation of this marker panel in coastal salmon populations not previously studied with modern genetic methods also reveals novel biological insights, including the presence of a single copy of a haplotype for a phenotype that has not been documented in that part of the species range, and a clear signal of mixed ancestry for a salmon population that is on the geographic margins of the primary evolutionary lineages present in California.
{"title":"A Multipurpose Microhaplotype Panel for Genetic Analysis of California Chinook Salmon","authors":"Eric C. Anderson, Anthony J. Clemento, Matthew A. Campbell, Devon E. Pearse, Anne K. Beulke, Cassie Columbus, Ellen Campbell, Neil F. Thompson, John Carlos Garza","doi":"10.1111/eva.70110","DOIUrl":"https://doi.org/10.1111/eva.70110","url":null,"abstract":"<p>Genetic methods have become an essential component of ecological investigation and conservation planning for fish and wildlife. Among these methods is the use of genetic marker data to identify individuals to populations, or stocks, of origin. More recently, methods that involve genetic pedigree reconstruction to identify relationships between individuals within populations have also become common. We present here a novel set of multiallelic microhaplotype genetic markers for Chinook salmon, which provide excellent resolution for population discrimination and relationship identification from a rapidly and economically assayed panel of markers. We show how this set of genetic markers assayed by sequencing 204 amplicons, in tandem with a reference dataset of 1636 individual samples from 17 populations, provides definitive power to identify all known lineages of Chinook salmon in California. The inclusion of genetic loci that have known associations with phenotype and that were identified as outliers in examination of whole-genome sequence data allows resolution of stocks that are not highly genetically differentiated but are phenotypically distinct and managed as such. This same set of multiallelic genetic markers has ample variation to accurately identify parent-offspring and full-sibling pairs in all California populations, including the genetically depauperate winter-run lineage. Validation of this marker panel in coastal salmon populations not previously studied with modern genetic methods also reveals novel biological insights, including the presence of a single copy of a haplotype for a phenotype that has not been documented in that part of the species range, and a clear signal of mixed ancestry for a salmon population that is on the geographic margins of the primary evolutionary lineages present in California.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"18 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-05-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70110","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143938953","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Inés M. Sambade, João Estêvão, Marina Pampín, Andreia Cruz, Eric Guévélou, Andrés Blanco, Francisco Câmara, Jessica Gómez-Garrido, Fernando Cruz, Luca Bargelloni, Stefano Carboni, Tyler Alioto, Benjamin Costas, Sergio Fernández-Boo, Paulino Martínez
The grooved carpet shell clam (Ruditapes decussatus) is a bivalve of high commercial value distributed throughout the European coast. Its production has suffered a decline caused by different factors, especially by the parasite Perkinsus olsenii. Improving production of R. decussatus requires genomic resources to ascertain the genetic factors underlying resistance/tolerance to P. olsenii. In this study, the first reference genome of R. decussatus was assembled through long- and short-read sequencing (1677 contigs; 1.386 Mb) and further scaffolded at chromosome level with Hi-C (19 superscaffolds; 95.4% of assembly). Repetitive elements were identified (32%) and masked for annotation of 38,276 coding- and 13,056 non-coding genes. This genome was used as a reference to develop a 2bRAD-Seq 13,438 SNP panel for a genomic screening on six shellfish beds distributed across the Atlantic Ocean and Mediterranean Sea. Beds were selected by perkinsosis prevalence and the infection level was individually evaluated in all the samples. Genetic diversity was significantly higher in the Mediterranean than in the Atlantic region. The main genetic breakage was detected between those regions (FST = 0.224), being the Mediterranean more heterogeneous than the Atlantic. Several loci under divergent selection (394 outliers; 261 genomic windows) were detected across shellfish beds. Samples were also inspected to detect signals of selection for resistance/tolerance to P. olsenii by using infection-level and population-genomics approaches, and 90 common divergent outliers for resistance/tolerance to perkinsosis were identified and used for gene mining. Candidate genes and markers identified provide invaluable information for controlling perkinsosis and for improving production of the grooved carpet shell clam.
{"title":"Signatures of Selection for Resistance/Tolerance to Perkinsus olseni in Grooved Carpet Shell Clam (Ruditapes decussatus) Using a Population Genomics Approach","authors":"Inés M. Sambade, João Estêvão, Marina Pampín, Andreia Cruz, Eric Guévélou, Andrés Blanco, Francisco Câmara, Jessica Gómez-Garrido, Fernando Cruz, Luca Bargelloni, Stefano Carboni, Tyler Alioto, Benjamin Costas, Sergio Fernández-Boo, Paulino Martínez","doi":"10.1111/eva.70106","DOIUrl":"https://doi.org/10.1111/eva.70106","url":null,"abstract":"<p>The grooved carpet shell clam (<i>Ruditapes decussatus</i>) is a bivalve of high commercial value distributed throughout the European coast. Its production has suffered a decline caused by different factors, especially by the parasite <i>Perkinsus olsenii</i>. Improving production of <i>R</i>. <i>decussatus</i> requires genomic resources to ascertain the genetic factors underlying resistance/tolerance to <i>P. olsenii</i>. In this study, the first reference genome of <i>R</i>. <i>decussatus</i> was assembled through long- and short-read sequencing (1677 contigs; 1.386 Mb) and further scaffolded at chromosome level with Hi-C (19 superscaffolds; 95.4% of assembly). Repetitive elements were identified (32%) and masked for annotation of 38,276 coding- and 13,056 non-coding genes. This genome was used as a reference to develop a 2bRAD-Seq 13,438 SNP panel for a genomic screening on six shellfish beds distributed across the Atlantic Ocean and Mediterranean Sea. Beds were selected by perkinsosis prevalence and the infection level was individually evaluated in all the samples. Genetic diversity was significantly higher in the Mediterranean than in the Atlantic region. The main genetic breakage was detected between those regions (F<sub>ST</sub> = 0.224), being the Mediterranean more heterogeneous than the Atlantic. Several loci under divergent selection (394 outliers; 261 genomic windows) were detected across shellfish beds. Samples were also inspected to detect signals of selection for resistance/tolerance to <i>P. olsenii</i> by using infection-level and population-genomics approaches, and 90 common divergent outliers for resistance/tolerance to perkinsosis were identified and used for gene mining. Candidate genes and markers identified provide invaluable information for controlling perkinsosis and for improving production of the grooved carpet shell clam.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"18 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-05-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70106","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143939315","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Susanne Reier, Peter Trontelj, Luise Kruckenhauser, Martin Kapun, Alexandra Wanka, Anja Palandačić
The Dinaric Karst, a biodiversity hotspot, features complex surface and subterranean hydrological networks that influence aquatic species distribution. This study investigates how karst hydrology shapes the genetic structure of the surface-dwelling minnow Phoxinus lumaireul, examining both large-scale and small-scale population patterns. Using mitochondrial DNA and genome-wide single nucleotide polymorphism (SNP) data of 827 specimens of P. lumaireul, three hypotheses were tested: (1) karst underground water connections facilitate genetic connectivity within and across river systems, whereas non-karst rivers exhibit genetic connectivity mostly within the same system; (2) historical and occasional hydrological connections have shaped present-day population structure, leaving genetic signatures of relatedness where no contemporary hydrological links exist; and (3) genomic approaches provide additional insights into biologically relevant connections that may not be captured by classical tracing tests. The large-scale analyses confirmed three main genetic groups (1a–c), whose structure was likely shaped by Pleistocene glaciations and associated microrefugia rather than by karst hydrology. Small-scale structure analyses revealed that while karst hydrology facilitated gene flow within specific areas, connectivity was uneven and influenced by local hydrological dynamics and historical admixture events. Furthermore, some underground pathways identified by classical tracing tests lacked evidence of genetic connectivity, underscoring the limitations of traditional methods and the added value of genomic data in indirectly detecting biologically relevant hydrological connections. These findings highlight the influence of both historical processes and contemporary karst hydrology on P. lumaireul populations, emphasizing their vulnerability in karst ecosystems and the need for targeted conservation efforts.
{"title":"Factors Beyond Karstification Have Shaped the Population Structure of a Surface-Dwelling Minnow (Phoxinus lumaireul) Able to Disperse Underground","authors":"Susanne Reier, Peter Trontelj, Luise Kruckenhauser, Martin Kapun, Alexandra Wanka, Anja Palandačić","doi":"10.1111/eva.70104","DOIUrl":"https://doi.org/10.1111/eva.70104","url":null,"abstract":"<p>The Dinaric Karst, a biodiversity hotspot, features complex surface and subterranean hydrological networks that influence aquatic species distribution. This study investigates how karst hydrology shapes the genetic structure of the surface-dwelling minnow <i>Phoxinus lumaireul</i>, examining both large-scale and small-scale population patterns. Using mitochondrial DNA and genome-wide single nucleotide polymorphism (SNP) data of 827 specimens of <i>P. lumaireul</i>, three hypotheses were tested: (1) karst underground water connections facilitate genetic connectivity within and across river systems, whereas non-karst rivers exhibit genetic connectivity mostly within the same system; (2) historical and occasional hydrological connections have shaped present-day population structure, leaving genetic signatures of relatedness where no contemporary hydrological links exist; and (3) genomic approaches provide additional insights into biologically relevant connections that may not be captured by classical tracing tests. The large-scale analyses confirmed three main genetic groups (1a–c), whose structure was likely shaped by Pleistocene glaciations and associated microrefugia rather than by karst hydrology. Small-scale structure analyses revealed that while karst hydrology facilitated gene flow within specific areas, connectivity was uneven and influenced by local hydrological dynamics and historical admixture events. Furthermore, some underground pathways identified by classical tracing tests lacked evidence of genetic connectivity, underscoring the limitations of traditional methods and the added value of genomic data in indirectly detecting biologically relevant hydrological connections. These findings highlight the influence of both historical processes and contemporary karst hydrology on <i>P. lumaireul</i> populations, emphasizing their vulnerability in karst ecosystems and the need for targeted conservation efforts.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"18 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-05-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70104","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143938815","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Matthew W. Hopken, Clara P. Mankowski, Christine Thurber, Antoinette J. Piaggio, Kathleen M. Nelson, Richard B. Chipman, Zaid Abdo, Tore Buchanan, Ariane Massé, Amy T. Gilbert
Wide-ranging, generalist species provide both interesting and challenging opportunities for research questions focused on population structure. Their continuous distributions and ability to occupy diverse habitat types can obscure genetic signals of ancestry and geographic clustering. However, spatially informed population genetic approaches are notable for high-resolution identification of geographic clusters that often elude more classical clustering models. The northern raccoon (Procyon lotor) is a broadly distributed species in North America, with populations in diverse habitats ranging from dense urban to rural landscapes. Wildlife management agencies have an interest in understanding raccoon ecology, given their propensity for human-wildlife conflicts and zoonotic diseases. We combined samples from an extensive raccoon tissue repository with a RADcapture panel of 1000 microhaplotype loci to conduct spatial genetic analyses of raccoon populations in eastern North America. Our objective was to estimate patterns of genetic diversity on the landscape that may inform raccoon rabies management. Bayesian clustering analyses delineated multiple ancestry clusters that encompassed large areas across 22 US states and 2 Canadian provinces. We discovered a potential phylogeographic split between central and southern samples from those in the northeast region, which correlates with post-Pleistocene recolonization detected in a multitude of species from the region. A finer scale structure was identified using spatially explicit analyses and demonstrated variable dispersal/gene flow patterns within specific regions. The Appalachian Mountain region restricted local connectivity among raccoons, while raccoon populations in central New York, the Ohio River Valley, southern Québec, and southern Alabama demonstrated high genetic connectivity. The results from this study highlight how raccoon ecology and historical biogeography can help contextualize contrasting hypotheses about the influence of landscape on raccoon movement patterns, which can inform management of zoonotic disease risks at regional scales.
{"title":"Contrasting Patterns of Raccoon (Procyon lotor) Spatial Population Genomics Throughout a Rabies Management Area in Eastern North America","authors":"Matthew W. Hopken, Clara P. Mankowski, Christine Thurber, Antoinette J. Piaggio, Kathleen M. Nelson, Richard B. Chipman, Zaid Abdo, Tore Buchanan, Ariane Massé, Amy T. Gilbert","doi":"10.1111/eva.70105","DOIUrl":"https://doi.org/10.1111/eva.70105","url":null,"abstract":"<p>Wide-ranging, generalist species provide both interesting and challenging opportunities for research questions focused on population structure. Their continuous distributions and ability to occupy diverse habitat types can obscure genetic signals of ancestry and geographic clustering. However, spatially informed population genetic approaches are notable for high-resolution identification of geographic clusters that often elude more classical clustering models. The northern raccoon (<i>Procyon lotor</i>) is a broadly distributed species in North America, with populations in diverse habitats ranging from dense urban to rural landscapes. Wildlife management agencies have an interest in understanding raccoon ecology, given their propensity for human-wildlife conflicts and zoonotic diseases. We combined samples from an extensive raccoon tissue repository with a RADcapture panel of 1000 microhaplotype loci to conduct spatial genetic analyses of raccoon populations in eastern North America. Our objective was to estimate patterns of genetic diversity on the landscape that may inform raccoon rabies management. Bayesian clustering analyses delineated multiple ancestry clusters that encompassed large areas across 22 US states and 2 Canadian provinces. We discovered a potential phylogeographic split between central and southern samples from those in the northeast region, which correlates with post-Pleistocene recolonization detected in a multitude of species from the region. A finer scale structure was identified using spatially explicit analyses and demonstrated variable dispersal/gene flow patterns within specific regions. The Appalachian Mountain region restricted local connectivity among raccoons, while raccoon populations in central New York, the Ohio River Valley, southern Québec, and southern Alabama demonstrated high genetic connectivity. The results from this study highlight how raccoon ecology and historical biogeography can help contextualize contrasting hypotheses about the influence of landscape on raccoon movement patterns, which can inform management of zoonotic disease risks at regional scales.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"18 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-05-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70105","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143938834","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
G. S. Silver, R. T. Lampman, N. Percival, N. Timoshevskaya, J. J. Smith, K. T. Bentley, J. Wade, S. R. Narum, J. E. Hess
Nonparasitic, nonmigratory Western Brook Lamprey (WBL; Lampetra ayresii), and parasitic, anadromous Western River Lamprey (WRL; L. ayresii) are sympatric lampreys that likely represent different life history variations of a single species. Novel genetic tools are critical for differentiating WBL and WRL, whose larvae preclude morphological identification (ID) and will enable comprehensive assessment of imperiled native lampreys of the Northeastern Pacific (including WBL, WRL, and Pacific Lamprey, Entosphenus tridentatus). We developed 47 candidate single nucleotide polymorphism (SNP) markers using whole genome resequencing of WBL (N = 24) and WRL (N = 15) from Ksi Ts'oohl Ts'ap Creek (Nass River, British Columbia, Canada) which are likely ecotypes distinguished by few divergent SNPs across multiple chromosomes. We used five novel candidate SNPs to perform genetic ID of WBL and WRL ecotypes in collections of mixed native lampreys from lower Columbia River tributaries (N = 1474), Ksi Ts'oohl Ts'ap Creek (N = 352), and ocean phase WRL from the Georgia Basin (Salish Sea, British Columbia, Canada; N = 91). Two previously published SNPs were used to ID genera, Entosphenus versus Lampetra. Morphological ID utilized photographs collected from a subset of genotyped lampreys, and high concordance was demonstrated between ID methods for genera (99%) and Lampetra ecotypes (> 98%). We characterized spatial and temporal composition of lamprey genera and ecotypes surveyed across NE Pacific tributaries under the expectation these compositions would be similar across nearby sites and across years at the same site. Proportions of lamprey genera were highly variable within regions and across years; however, Lampetra ecotypic proportions were spatially and temporally stable. WRL were rare in lower Columbia tributaries (~1% average rate among Lampetra) and common further north (> 40% of Lampetra). Genetic ID methods are powerful monitoring tools that create the novel ability to ascertain genera and ecotypes regardless of life stage, while increasing the efficiency of surveys by eliminating time-intensive morphological data collection.
{"title":"Genetic Identification of Lamprey Genera and Anadromous Ecotypes in Watersheds of the Northeastern Pacific Ocean","authors":"G. S. Silver, R. T. Lampman, N. Percival, N. Timoshevskaya, J. J. Smith, K. T. Bentley, J. Wade, S. R. Narum, J. E. Hess","doi":"10.1111/eva.70108","DOIUrl":"https://doi.org/10.1111/eva.70108","url":null,"abstract":"<p>Nonparasitic, nonmigratory Western Brook Lamprey (WBL; <i>Lampetra ayresii</i>), and parasitic, anadromous Western River Lamprey (WRL; <i>L. ayresii</i>) are sympatric lampreys that likely represent different life history variations of a single species. Novel genetic tools are critical for differentiating WBL and WRL, whose larvae preclude morphological identification (ID) and will enable comprehensive assessment of imperiled native lampreys of the Northeastern Pacific (including WBL, WRL, and Pacific Lamprey, <i>Entosphenus tridentatus</i>). We developed 47 candidate single nucleotide polymorphism (SNP) markers using whole genome resequencing of WBL (<i>N</i> = 24) and WRL (<i>N</i> = 15) from Ksi Ts'oohl Ts'ap Creek (Nass River, British Columbia, Canada) which are likely ecotypes distinguished by few divergent SNPs across multiple chromosomes. We used five novel candidate SNPs to perform genetic ID of WBL and WRL ecotypes in collections of mixed native lampreys from lower Columbia River tributaries (<i>N</i> = 1474), Ksi Ts'oohl Ts'ap Creek (<i>N</i> = 352), and ocean phase WRL from the Georgia Basin (Salish Sea, British Columbia, Canada; <i>N</i> = 91). Two previously published SNPs were used to ID genera, <i>Entosphenus</i> versus <i>Lampetra</i>. Morphological ID utilized photographs collected from a subset of genotyped lampreys, and high concordance was demonstrated between ID methods for genera (99%) and <i>Lampetra</i> ecotypes (> 98%). We characterized spatial and temporal composition of lamprey genera and ecotypes surveyed across NE Pacific tributaries under the expectation these compositions would be similar across nearby sites and across years at the same site. Proportions of lamprey genera were highly variable within regions and across years; however, <i>Lampetra</i> ecotypic proportions were spatially and temporally stable. WRL were rare in lower Columbia tributaries (~1% average rate among <i>Lampetra</i>) and common further north (> 40% of <i>Lampetra</i>). Genetic ID methods are powerful monitoring tools that create the novel ability to ascertain genera and ecotypes regardless of life stage, while increasing the efficiency of surveys by eliminating time-intensive morphological data collection.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"18 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-05-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70108","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143930241","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
João Costa e Silva, Brad M. Potts, Peter A. Harrison
Native and restored forests are increasingly impacted by pests and diseases, including large herbivores. While community- and species-level impacts of these tree enemies are often well-documented, there is little understanding of their influence on finer-scale eco-evolutionary processes. We here study the influence of large-mammal herbivory on the survival and height growth of trees in a mixed species restoration planting of the Australian forest trees, Eucalyptus ovata and E. pauciflora, in Tasmania, Australia. Common-garden field trials mixing the two species were compared in adjacent unbrowsed (fenced) and browsed (unfenced) plantings. The browsed planting was exposed to mammal browsing by native marsupials, as well as feral introduced European fallow deer (Dama dama). Each tree species was represented by open-pollinated families from 22 paired geographic areas, allowing the assessment of the effects of browsing on the species and population differences, as well as on family variation within each species. In the browsed planting, a marked reduction in species and population differences, as well as in family variance, was observed for both height growth and survival. The pattern of height growth and survival of the populations of both species also differed between browsing regimes, with significant changes of climate relationships involving both focal tree attributes detected. Our results argue for a major disruption of the eco-evolutionary dynamics of restored forests in the presence of browsing by large mammalian herbivores, at the observed period of the tree life cycle. Importantly for forest restoration and conservation in the face of global change, our results challenge the choice of tree populations for translocation based solely on predicted or observed relationships of their home-site climate with current and predicted future climates of the restoration sites, while emphasising the need for genetic diversity to provide future resilience of restored forests to both biotic and abiotic stresses.
{"title":"Mammalian Browsers Disrupt Eco-Evolutionary Dynamics in a Forest Tree Restoration Planting","authors":"João Costa e Silva, Brad M. Potts, Peter A. Harrison","doi":"10.1111/eva.70099","DOIUrl":"https://doi.org/10.1111/eva.70099","url":null,"abstract":"<p>Native and restored forests are increasingly impacted by pests and diseases, including large herbivores. While community- and species-level impacts of these tree enemies are often well-documented, there is little understanding of their influence on finer-scale eco-evolutionary processes. We here study the influence of large-mammal herbivory on the survival and height growth of trees in a mixed species restoration planting of the Australian forest trees, <i>Eucalyptus ovata</i> and <i>E. pauciflora</i>, in Tasmania, Australia. Common-garden field trials mixing the two species were compared in adjacent unbrowsed (fenced) and browsed (unfenced) plantings. The browsed planting was exposed to mammal browsing by native marsupials, as well as feral introduced European fallow deer (<i>Dama dama</i>). Each tree species was represented by open-pollinated families from 22 paired geographic areas, allowing the assessment of the effects of browsing on the species and population differences, as well as on family variation within each species. In the browsed planting, a marked reduction in species and population differences, as well as in family variance, was observed for both height growth and survival. The pattern of height growth and survival of the populations of both species also differed between browsing regimes, with significant changes of climate relationships involving both focal tree attributes detected. Our results argue for a major disruption of the eco-evolutionary dynamics of restored forests in the presence of browsing by large mammalian herbivores, at the observed period of the tree life cycle. Importantly for forest restoration and conservation in the face of global change, our results challenge the choice of tree populations for translocation based solely on predicted or observed relationships of their home-site climate with current and predicted future climates of the restoration sites, while emphasising the need for genetic diversity to provide future resilience of restored forests to both biotic and abiotic stresses.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"18 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-05-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70099","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143919369","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Justin J. S. Wilcox, James Ord, Dennis Kappei, Toni I. Gossmann
DNA methylation has fundamental implications for vertebrate genome evolution by influencing the mutational landscape, particularly at CpG dinucleotides. Methylation-induced mutations drive a genome-wide depletion of CpG sites, creating a dinucleotide composition bias across the genome. Examination of the standard genetic code reveals CpG to be the only facultative dinucleotide; it is however unclear what specific implications CpG bias has on protein coding DNA. Here, we use theoretical considerations of the genetic code combined with empirical genome-wide analyses in six vertebrate species—human, mouse, chicken, great tit, frog, and stickleback—to investigate how CpG content is shaped and maintained in protein-coding genes. We show that protein-coding sequences consistently exhibit significantly higher CpG content than noncoding regions and demonstrate that CpG sites are enriched in genes involved in regulatory functions and stress responses, suggesting selective maintenance of CpG content in specific loci. These findings have important implications for evolutionary applications in both natural and managed populations: CpG content could serve as a genetic marker for assessing adaptive potential, while the identification of CpG-free codons provides a framework for genome optimization in breeding and synthetic biology. Our results underscore the intricate interplay between mutational biases, selection, and epigenetic regulation, offering new insights into how vertebrate genomes evolve under varying ecological and selective pressures.
{"title":"The CpG Landscape of Protein Coding DNA in Vertebrates","authors":"Justin J. S. Wilcox, James Ord, Dennis Kappei, Toni I. Gossmann","doi":"10.1111/eva.70101","DOIUrl":"https://doi.org/10.1111/eva.70101","url":null,"abstract":"<p>DNA methylation has fundamental implications for vertebrate genome evolution by influencing the mutational landscape, particularly at CpG dinucleotides. Methylation-induced mutations drive a genome-wide depletion of CpG sites, creating a dinucleotide composition bias across the genome. Examination of the standard genetic code reveals CpG to be the only facultative dinucleotide; it is however unclear what specific implications CpG bias has on protein coding DNA. Here, we use theoretical considerations of the genetic code combined with empirical genome-wide analyses in six vertebrate species—human, mouse, chicken, great tit, frog, and stickleback—to investigate how CpG content is shaped and maintained in protein-coding genes. We show that protein-coding sequences consistently exhibit significantly higher CpG content than noncoding regions and demonstrate that CpG sites are enriched in genes involved in regulatory functions and stress responses, suggesting selective maintenance of CpG content in specific loci. These findings have important implications for evolutionary applications in both natural and managed populations: CpG content could serve as a genetic marker for assessing adaptive potential, while the identification of CpG-free codons provides a framework for genome optimization in breeding and synthetic biology. Our results underscore the intricate interplay between mutational biases, selection, and epigenetic regulation, offering new insights into how vertebrate genomes evolve under varying ecological and selective pressures.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"18 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-05-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70101","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143904955","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}