Joel O. Odero, Tristan P. W. Dennis, Brian Polo, Joachim Nwezeobi, Marilou Boddé, Sanjay C. Nagi, Anastasia Hernandez-Koutoucheva, Ismail H. Nambunga, Hamis Bwanary, Gustav Mkandawile, Nicodem J. Govella, Emmanuel W. Kaindoa, Heather M. Ferguson, Eric Ochomo, Chris S. Clarkson, Alistair Miles, Mara K. N. Lawniczak, David Weetman, Francesco Baldini, Fredros O. Okumu
A major insecticide resistance mechanism in insect pests is knock-down resistance (kdr) caused by mutations in the voltage-gated sodium channel (Vgsc) gene. Despite being common in most malaria Anopheles vector species, kdr mutations have never been observed in Anopheles funestus, the principal malaria vector in Eastern and Southern Africa, with resistance mainly being conferred by detoxification enzymes. In a parallel study, we monitored 10 populations of An. funestus in Tanzania for insecticide resistance unexpectedly identified resistance to a banned insecticide, DDT, in the Morogoro region. Through whole-genome sequencing of 333 An. funestus samples from these populations, we found eight novel amino acid substitutions in the Vgsc gene, including the kdr variant, L976F (equivalent to L995F in An. gambiae), in tight linkage disequilibrium with another (P1842S). The mutants were found only at high frequency in one region and were accompanied by weak signatures of a selective sweep, with a significant decline between 2017 and 2023. Notably, kdr L976F was strongly associated with survivorship to exposure to DDT insecticide, while no clear association was noted with a pyrethroid insecticide (deltamethrin). The WHO prequalifies no DDT products for vector control, and the chemical is banned in Tanzania. Widespread DDT contamination and a legacy of extensive countrywide stockpiles may have selected for this mutation. Continued monitoring is necessary to understand the origin of kdr in An. funestus, and the threat posed to insecticide-based vector control in Africa.
{"title":"Discovery of Knock-Down Resistance in the Major African Malaria Vector Anopheles funestus","authors":"Joel O. Odero, Tristan P. W. Dennis, Brian Polo, Joachim Nwezeobi, Marilou Boddé, Sanjay C. Nagi, Anastasia Hernandez-Koutoucheva, Ismail H. Nambunga, Hamis Bwanary, Gustav Mkandawile, Nicodem J. Govella, Emmanuel W. Kaindoa, Heather M. Ferguson, Eric Ochomo, Chris S. Clarkson, Alistair Miles, Mara K. N. Lawniczak, David Weetman, Francesco Baldini, Fredros O. Okumu","doi":"10.1111/mec.17542","DOIUrl":"10.1111/mec.17542","url":null,"abstract":"<p>A major insecticide resistance mechanism in insect pests is knock-down resistance (<i>kdr</i>) caused by mutations in the voltage-gated sodium channel (<i>Vgsc</i>) gene. Despite being common in most malaria <i>Anopheles</i> vector species, <i>kdr</i> mutations have never been observed in <i>Anopheles funestus</i>, the principal malaria vector in Eastern and Southern Africa, with resistance mainly being conferred by detoxification enzymes. In a parallel study, we monitored 10 populations of <i>An</i>. <i>funestus</i> in Tanzania for insecticide resistance unexpectedly identified resistance to a banned insecticide, DDT, in the Morogoro region. Through whole-genome sequencing of 333 <i>An</i>. <i>funestus</i> samples from these populations, we found eight novel amino acid substitutions in the <i>Vgsc</i> gene, including the <i>kdr</i> variant, L976F (equivalent to L995F in <i>An</i>. <i>gambiae</i>), in tight linkage disequilibrium with another (P1842S). The mutants were found only at high frequency in one region and were accompanied by weak signatures of a selective sweep, with a significant decline between 2017 and 2023. Notably, <i>kdr</i> L976F was strongly associated with survivorship to exposure to DDT insecticide, while no clear association was noted with a pyrethroid insecticide (deltamethrin). The WHO prequalifies no DDT products for vector control, and the chemical is banned in Tanzania. Widespread DDT contamination and a legacy of extensive countrywide stockpiles may have selected for this mutation. Continued monitoring is necessary to understand the origin of <i>kdr</i> in <i>An</i>. <i>funestus</i>, and the threat posed to insecticide-based vector control in Africa.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":"33 22","pages":""},"PeriodicalIF":4.5,"publicationDate":"2024-10-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/mec.17542","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142386790","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Genís Garcia-Erill, Xi Wang, Malthe S. Rasmussen, Liam Quinn, Anubhab Khan, Laura D. Bertola, Cindy G. Santander, Renzo F. Balboa, Joseph O. Ogutu, Patrícia Pečnerová, Kristian Hanghøj, Josiah Kuja, Casia Nursyifa, Charles Masembe, Vincent Muwanika, Faysal Bibi, Ida Moltke, Hans R. Siegismund, Anders Albrechtsen, Rasmus Heller
Impalas are unusual among bovids because they have remained morphologically similar over millions of years—a phenomenon referred to as evolutionary stasis. Here, we sequenced 119 whole genomes from the two extant subspecies of impala, the common (Aepyceros melampus melampus) and black-faced (A. m. petersi) impala. We investigated the evolutionary forces working within the species to explore how they might be associated with its evolutionary stasis as a taxon. Despite being one of the most abundant bovid species, we found low genetic diversity overall, and a phylogeographic signal of spatial expansion from southern to eastern Africa. Contrary to expectations under a scenario of evolutionary stasis, we found pronounced genetic structure between and within the two subspecies with indications of ancient, but not recent, gene flow. Black-faced impala and eastern African common impala populations had more runs of homozygosity than common impala in southern Africa, and, using a proxy for genetic load, we found that natural selection is working less efficiently in these populations compared to the southern African populations. Together with the fossil record, our results are consistent with a fixed-optimum model of evolutionary stasis, in which impalas in the southern African core of the range are able to stay near their evolutionary fitness optimum as a generalist ecotone species, whereas eastern African impalas may struggle to do so due to the effects of genetic drift and reduced adaptation to the local habitat, leading to recurrent local extinction in eastern Africa and re-colonisation from the South.
黑斑羚在牛科动物中并不常见,因为它们在数百万年的时间里一直保持着形态上的相似--这种现象被称为进化停滞。在这里,我们对现存的两个黑斑羚亚种--普通黑斑羚(Aepyceros melampus melampus)和黑脸黑斑羚(A. m. petersi)--的119个全基因组进行了测序。我们研究了该物种内部的进化力量,以探讨这些力量如何可能与其作为一个类群的进化停滞有关。尽管黑斑羚是数量最多的牛科动物之一,但我们发现它的遗传多样性总体较低,而且存在从非洲南部向非洲东部扩展的系统地理学信号。与进化停滞的预期相反,我们在两个亚种之间和亚种内部发现了明显的遗传结构,表明存在古老的基因流动,而不是最近的基因流动。与南部非洲的普通黑斑羚相比,黑脸黑斑羚和东部非洲的普通黑斑羚种群有更多的同源染色体,而且利用遗传负荷的替代方法,我们发现与南部非洲的种群相比,自然选择在这些种群中的作用效率较低。结合化石记录,我们的研究结果与进化停滞的固定-最佳模型相一致,在该模型中,南部非洲核心区的黑斑羚能够作为一种通用生态区物种保持在其进化适应性最佳值附近,而东部非洲的黑斑羚则可能由于遗传漂变的影响和对当地栖息地适应性的降低而难以达到最佳值,从而导致东部非洲的黑斑羚在当地反复灭绝,并从南部重新拓殖。
{"title":"Extensive Population Structure Highlights an Apparent Paradox of Stasis in the Impala (Aepyceros melampus)","authors":"Genís Garcia-Erill, Xi Wang, Malthe S. Rasmussen, Liam Quinn, Anubhab Khan, Laura D. Bertola, Cindy G. Santander, Renzo F. Balboa, Joseph O. Ogutu, Patrícia Pečnerová, Kristian Hanghøj, Josiah Kuja, Casia Nursyifa, Charles Masembe, Vincent Muwanika, Faysal Bibi, Ida Moltke, Hans R. Siegismund, Anders Albrechtsen, Rasmus Heller","doi":"10.1111/mec.17539","DOIUrl":"10.1111/mec.17539","url":null,"abstract":"<p>Impalas are unusual among bovids because they have remained morphologically similar over millions of years—a phenomenon referred to as evolutionary stasis. Here, we sequenced 119 whole genomes from the two extant subspecies of impala, the common (<i>Aepyceros melampus melampus</i>) and black-faced (<i>A. m. petersi</i>) impala. We investigated the evolutionary forces working within the species to explore how they might be associated with its evolutionary stasis as a taxon. Despite being one of the most abundant bovid species, we found low genetic diversity overall, and a phylogeographic signal of spatial expansion from southern to eastern Africa. Contrary to expectations under a scenario of evolutionary stasis, we found pronounced genetic structure between and within the two subspecies with indications of ancient, but not recent, gene flow. Black-faced impala and eastern African common impala populations had more runs of homozygosity than common impala in southern Africa, and, using a proxy for genetic load, we found that natural selection is working less efficiently in these populations compared to the southern African populations. Together with the fossil record, our results are consistent with a fixed-optimum model of evolutionary stasis, in which impalas in the southern African core of the range are able to stay near their evolutionary fitness optimum as a generalist ecotone species, whereas eastern African impalas may struggle to do so due to the effects of genetic drift and reduced adaptation to the local habitat, leading to recurrent local extinction in eastern Africa and re-colonisation from the South.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":"33 22","pages":""},"PeriodicalIF":4.5,"publicationDate":"2024-10-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/mec.17539","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142379586","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Genetic mechanisms have been at the forefront of our exploration into the substrate of adaptive evolution and phenotypic diversification. However, genetic variation only accounts for a fraction of phenotypic variation. In the last decade, the significance of RNA modification mechanisms has become more apparent in the context of organismal adaptation to rapidly changing environments. RNA m6A methylation, the most abundant form of RNA modification, is emerging as a potentially significant player in various biological processes. Despite its fundamental function to regulate other major post-transcriptional mechanisms such as microRNA and alternative splicing, its role in ecology and evolution has been understudied. This review highlights the potential importance of m6A RNA methylation in ecological adaptation, emphasising the need for further research, especially in natural systems. We focus on how m6A not only affects mRNA fate but also influences miRNA-mediated gene regulation and alternative splicing, potentially contributing to organismal adaptation. The aim of this review is to synthesise key background information to enhance our understanding of m6A mechanisms driving species survival in dynamic environments and motivate future research into the dynamics of adaptive RNA methylation.
{"title":"Emerging Orchestrator of Ecological Adaptation: m<sup>6</sup>A Regulation of Post-Transcriptional Mechanisms.","authors":"Ehsan Pashay Ahi, Pooja Singh","doi":"10.1111/mec.17545","DOIUrl":"https://doi.org/10.1111/mec.17545","url":null,"abstract":"<p><p>Genetic mechanisms have been at the forefront of our exploration into the substrate of adaptive evolution and phenotypic diversification. However, genetic variation only accounts for a fraction of phenotypic variation. In the last decade, the significance of RNA modification mechanisms has become more apparent in the context of organismal adaptation to rapidly changing environments. RNA m<sup>6</sup>A methylation, the most abundant form of RNA modification, is emerging as a potentially significant player in various biological processes. Despite its fundamental function to regulate other major post-transcriptional mechanisms such as microRNA and alternative splicing, its role in ecology and evolution has been understudied. This review highlights the potential importance of m<sup>6</sup>A RNA methylation in ecological adaptation, emphasising the need for further research, especially in natural systems. We focus on how m<sup>6</sup>A not only affects mRNA fate but also influences miRNA-mediated gene regulation and alternative splicing, potentially contributing to organismal adaptation. The aim of this review is to synthesise key background information to enhance our understanding of m<sup>6</sup>A mechanisms driving species survival in dynamic environments and motivate future research into the dynamics of adaptive RNA methylation.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":" ","pages":"e17545"},"PeriodicalIF":4.5,"publicationDate":"2024-10-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142374766","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The role of epigenetics in regulating caste polyphenism in social insects has been debated. Here, we tested the importance of histone de/acetylation processes for the maintenance of queen hallmarks like a high fecundity and a long lifespan. To this end, we performed RNA interference experiments against histone deacetylase 3 (HDAC3) in the termite Cryptotermes secundus. Fat body transcriptomes and chemical communication profiles revealed that silencing of HDAC3 leads to signals indicative of queen hallmarks. This includes fostering of queen signalling, defence against ageing and a reduction of life-shortening IIS (insulin/insulin-like growth factor signalling) and endocrine JH (juvenile hormone) signalling via Kr-h1 (Krüppel-homologue 1). These observed patterns were similar to those of a protein-enriched diet, which might imply that histone acetylation conveys nutritional effects. Strikingly, in contrast to solitary insects, reduced endocrine JH signalling had no negative effect on fecundity-related vitellogenesis in the fat bodies. This suggests an uncoupling of longevity pathways from fecundity in fat bodies, which can help explain queens' extraordinary lifespans combined with high fecundity.
{"title":"Histone Deacetylase 3 Is Involved in Maintaining Queen Hallmarks of a Termite","authors":"Louis Allan Okwaro, Judith Korb","doi":"10.1111/mec.17541","DOIUrl":"10.1111/mec.17541","url":null,"abstract":"<p>The role of epigenetics in regulating caste polyphenism in social insects has been debated. Here, we tested the importance of histone de/acetylation processes for the maintenance of queen hallmarks like a high fecundity and a long lifespan. To this end, we performed RNA interference experiments against <i>histone deacetylase 3</i> (<i>HDAC3</i>) in the termite <i>Cryptotermes secundus</i>. Fat body transcriptomes and chemical communication profiles revealed that silencing of <i>HDAC3</i> leads to signals indicative of queen hallmarks. This includes fostering of queen signalling, defence against ageing and a reduction of life-shortening IIS (insulin/insulin-like growth factor signalling) and endocrine JH (juvenile hormone) signalling via Kr-h1 (Krüppel-homologue 1). These observed patterns were similar to those of a protein-enriched diet, which might imply that histone acetylation conveys nutritional effects. Strikingly, in contrast to solitary insects, reduced endocrine JH signalling had no negative effect on fecundity-related vitellogenesis in the fat bodies. This suggests an uncoupling of longevity pathways from fecundity in fat bodies, which can help explain queens' extraordinary lifespans combined with high fecundity.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":"33 22","pages":""},"PeriodicalIF":4.5,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/mec.17541","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142374767","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Kai Wei, Saida Sharifova, Xiaoyun Zhao, Neelima Sinha, Hokuto Nakayama, Aurélien Tellier, Gustavo A. Silva-Arias
Drought stress is a key limitation for plant growth and colonization of arid habitats. We study the evolution of gene expression response to drought stress in a wild tomato, Solanum chilense, naturally occurring in dry habitats in South America. We conduct a transcriptome analysis under standard and drought experimental conditions to identify drought-responsive gene networks and estimate the age of the involved genes. We identify two main regulatory networks corresponding to two typical drought-responsive strategies: cell cycle and fundamental metabolic processes. The metabolic network exhibits a more recent evolutionary origin and a more variable transcriptome response than the cell cycle network (with ancestral origin and higher conservation of the transcriptional response). We also integrate population genomics analyses to reveal positive selection signals acting at the genes of both networks, revealing that genes exhibiting selective sweeps of older age also exhibit greater connectivity in the networks. These findings suggest that adaptive changes first occur at core genes of drought response networks, driving significant network re-wiring, which likely underpins species divergence and further spread into drier habitats. Combining transcriptomics and population genomics approaches, we decipher the timing of gene network evolution for drought stress response in arid habitats.
{"title":"Evolution of gene networks underlying adaptation to drought stress in the wild tomato Solanum chilense","authors":"Kai Wei, Saida Sharifova, Xiaoyun Zhao, Neelima Sinha, Hokuto Nakayama, Aurélien Tellier, Gustavo A. Silva-Arias","doi":"10.1111/mec.17536","DOIUrl":"10.1111/mec.17536","url":null,"abstract":"<p>Drought stress is a key limitation for plant growth and colonization of arid habitats. We study the evolution of gene expression response to drought stress in a wild tomato, <i>Solanum chilense,</i> naturally occurring in dry habitats in South America. We conduct a transcriptome analysis under standard and drought experimental conditions to identify drought-responsive gene networks and estimate the age of the involved genes. We identify two main regulatory networks corresponding to two typical drought-responsive strategies: cell cycle and fundamental metabolic processes. The metabolic network exhibits a more recent evolutionary origin and a more variable transcriptome response than the cell cycle network (with ancestral origin and higher conservation of the transcriptional response). We also integrate population genomics analyses to reveal positive selection signals acting at the genes of both networks, revealing that genes exhibiting selective sweeps of older age also exhibit greater connectivity in the networks. These findings suggest that adaptive changes first occur at core genes of drought response networks, driving significant network re-wiring, which likely underpins species divergence and further spread into drier habitats. Combining transcriptomics and population genomics approaches, we decipher the timing of gene network evolution for drought stress response in arid habitats.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":"33 21","pages":""},"PeriodicalIF":4.5,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/mec.17536","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142363631","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Yu Han, Li Liu, Mengyu Lei, Wei Liu, Huan Si, Yan Ji, Qiao Du, Mingjia Zhu, Wenjia Zhang, Yifei Dai, Jianquan Liu, Yanjun Zan
Understanding the genetic, and transcriptomic changes that drive the phenotypic plasticity of fitness traits is a central question in evolutionary biology. In this study, we utilised 152 natural Swedish Arabidopsis thaliana accessions with re-sequenced genomes, transcriptomes and methylomes and measured flowering times (FTs) under two temperature conditions (10°C and 16°C) to address this question. We revealed that the northern accessions exhibited advanced flowering in response to decreased temperature, whereas the southern accessions delayed their flowering, indicating a divergent flowering response. This contrast in flowering responses was associated with the isothermality of their native ranges, which potentially enables the northern accessions to complete their life cycle more rapidly in years with shorter growth seasons. At the transcriptome level, we observed extensive rewiring of gene co-expression networks, with the expression of 25 core genes being associated with the mean FT and its plastic variation. Notably, variations in FLC expression sensitivity between northern and southern accessions were found to be associated with the divergence FT response. Further analysis suggests that FLC expression sensitivity is associated with differences in CG, CHG and CHH methylation at the promoter region. Overall, our study revealed the association between transcriptome plasticity and flowering time plasticity among different accessions, providing evidence for its relevance in ecological adaptation. These findings offer deeper insights into the genetics of rapid responses to environmental changes and ecological adaptation.
了解基因组和转录组的变化如何驱动适性性状的表型可塑性是进化生物学的一个核心问题。在这项研究中,我们利用了152个瑞典拟南芥天然品种,并重新测序了基因组、转录组和甲基组,测量了两种温度条件(10°C和16°C)下的开花时间(FTs),以解决这一问题。我们发现,在温度降低的条件下,北方品种的开花时间提前,而南方品种的开花时间延迟,这表明开花反应存在差异。这种开花反应的差异与它们原产地的等温性有关,这可能使北方品种在生长季节较短的年份更快地完成其生命周期。在转录组水平上,我们观察到基因共表达网络的广泛重联,25个核心基因的表达与平均花期及其可塑性变化有关。值得注意的是,我们发现北方和南方品种对 FLC 表达敏感性的变化与 FT 反应的差异有关。进一步的分析表明,FLC表达敏感性与启动子区域的CG、CHG和CHH甲基化差异有关。总之,我们的研究揭示了不同品种间转录组可塑性与花期可塑性之间的关联,为其在生态适应中的相关性提供了证据。这些发现为快速响应环境变化和生态适应的遗传学提供了更深入的见解。
{"title":"Divergent Flowering Time Responses to Increasing Temperatures Are Associated With Transcriptome Plasticity and Epigenetic Modification Differences at FLC Promoter Region of Arabidopsis thaliana.","authors":"Yu Han, Li Liu, Mengyu Lei, Wei Liu, Huan Si, Yan Ji, Qiao Du, Mingjia Zhu, Wenjia Zhang, Yifei Dai, Jianquan Liu, Yanjun Zan","doi":"10.1111/mec.17544","DOIUrl":"https://doi.org/10.1111/mec.17544","url":null,"abstract":"<p><p>Understanding the genetic, and transcriptomic changes that drive the phenotypic plasticity of fitness traits is a central question in evolutionary biology. In this study, we utilised 152 natural Swedish Arabidopsis thaliana accessions with re-sequenced genomes, transcriptomes and methylomes and measured flowering times (FTs) under two temperature conditions (10°C and 16°C) to address this question. We revealed that the northern accessions exhibited advanced flowering in response to decreased temperature, whereas the southern accessions delayed their flowering, indicating a divergent flowering response. This contrast in flowering responses was associated with the isothermality of their native ranges, which potentially enables the northern accessions to complete their life cycle more rapidly in years with shorter growth seasons. At the transcriptome level, we observed extensive rewiring of gene co-expression networks, with the expression of 25 core genes being associated with the mean FT and its plastic variation. Notably, variations in FLC expression sensitivity between northern and southern accessions were found to be associated with the divergence FT response. Further analysis suggests that FLC expression sensitivity is associated with differences in CG, CHG and CHH methylation at the promoter region. Overall, our study revealed the association between transcriptome plasticity and flowering time plasticity among different accessions, providing evidence for its relevance in ecological adaptation. These findings offer deeper insights into the genetics of rapid responses to environmental changes and ecological adaptation.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":" ","pages":"e17544"},"PeriodicalIF":4.5,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142363630","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Kasha Strickland, Menna E. Jones, Andrew Storfer, Rodrigo K. Hamede, Paul A. Hohenlohe, Mark J. Margres, Hamish I. McCallum, Sebastien Comte, Shelly Lachish, Loeske E. B. Kruuk
Emerging infectious diseases (EIDs) not only cause catastrophic declines in wildlife populations but also generate selective pressures that may result in rapid evolutionary responses. One such EID is devil facial tumour disease (DFTD) in the Tasmanian devil. DFTD is almost always fatal and has reduced the average lifespan of individuals by around 2 years, likely causing strong selection for traits that reduce susceptibility to the disease, but population decline has also left Tasmanian devils vulnerable to inbreeding depression. We analysed 22 years of data from an ongoing study of a population of Tasmanian devils on Freycinet Peninsula, Tasmania, to (1) identify whether DFTD may be causing selection on body size, by estimating phenotypic and genetic correlations between DFTD and size traits, (2) estimate the additive genetic variance of susceptibility to DFTD, and (3) investigate whether size traits or susceptibility to DFTD were under inbreeding depression. We found a positive phenotypic relationship between head width and susceptibility to DFTD, but this was not underpinned by a genetic correlation. Conversely, we found a negative phenotypic relationship between body weight and susceptibility to DFTD, and there was evidence for a negative genetic correlation between susceptibility to DFTD and body weight. There was additive genetic variance in susceptibility to DFTD, head width and body weight, but there was no evidence for inbreeding depression in any of these traits. These results suggest that Tasmanian devils have the potential to respond adaptively to DFTD, although the realised evolutionary response will critically further depend on the evolution of DFTD itself.
{"title":"Adaptive potential in the face of a transmissible cancer in Tasmanian devils","authors":"Kasha Strickland, Menna E. Jones, Andrew Storfer, Rodrigo K. Hamede, Paul A. Hohenlohe, Mark J. Margres, Hamish I. McCallum, Sebastien Comte, Shelly Lachish, Loeske E. B. Kruuk","doi":"10.1111/mec.17531","DOIUrl":"10.1111/mec.17531","url":null,"abstract":"<p>Emerging infectious diseases (EIDs) not only cause catastrophic declines in wildlife populations but also generate selective pressures that may result in rapid evolutionary responses. One such EID is devil facial tumour disease (DFTD) in the Tasmanian devil. DFTD is almost always fatal and has reduced the average lifespan of individuals by around 2 years, likely causing strong selection for traits that reduce susceptibility to the disease, but population decline has also left Tasmanian devils vulnerable to inbreeding depression. We analysed 22 years of data from an ongoing study of a population of Tasmanian devils on Freycinet Peninsula, Tasmania, to (1) identify whether DFTD may be causing selection on body size, by estimating phenotypic and genetic correlations between DFTD and size traits, (2) estimate the additive genetic variance of susceptibility to DFTD, and (3) investigate whether size traits or susceptibility to DFTD were under inbreeding depression. We found a positive phenotypic relationship between head width and susceptibility to DFTD, but this was not underpinned by a genetic correlation. Conversely, we found a negative phenotypic relationship between body weight and susceptibility to DFTD, and there was evidence for a negative genetic correlation between susceptibility to DFTD and body weight. There was additive genetic variance in susceptibility to DFTD, head width and body weight, but there was no evidence for inbreeding depression in any of these traits. These results suggest that Tasmanian devils have the potential to respond adaptively to DFTD, although the realised evolutionary response will critically further depend on the evolution of DFTD itself.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":"33 21","pages":""},"PeriodicalIF":4.5,"publicationDate":"2024-09-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11521764/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142338003","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Joanna Różańska-Wróbel, Magdalena Migalska, Anna Urbanowicz, Maciej Grzybek, Ryan O. M. Rego, Anna Bajer, Dorota Dwuznik-Szarek, Mohammed Alsarraf, Jolanta Behnke-Borowczyk, Jerzy M. Behnke, Jacek Radwan
Coevolution of parasites with their hosts may lead to balancing selection on genes involved in determining the specificity of host–parasite interactions, but examples of such specific interactions in wild vertebrates are scarce. Here, we investigated whether the polymorphic outer surface protein C (OspC), used by the Lyme disease agent, Borrelia afzelii, to manipulate vertebrate host innate immunity, interacts with polymorphic major histocompatibility genes (MHC), while concurrently eliciting a strong antibody response, in one of its main hosts in Europe, the bank vole. We found signals of balancing selection acting on OspC, resulting in little differentiation in OspC variant frequencies between years. Neither MHC alleles nor their inferred functional groupings (supertypes) significantly predicted the specificity of infection with strains carrying different OspC variants. However, we found that MHC alleles, but not supertypes, significantly predicted the level of IgG antibodies against two common OspC variants among seropositive individuals. Our results thus indicate that MHC alleles differ in their ability to induce antibody responses against specific OspC variants, which may contribute to selection of OspC polymorphism by the vole immune system.
{"title":"Interplay between vertebrate adaptive immunity and bacterial infectivity genes: Bank vole MHC versus Borrelia afzelii OspC","authors":"Joanna Różańska-Wróbel, Magdalena Migalska, Anna Urbanowicz, Maciej Grzybek, Ryan O. M. Rego, Anna Bajer, Dorota Dwuznik-Szarek, Mohammed Alsarraf, Jolanta Behnke-Borowczyk, Jerzy M. Behnke, Jacek Radwan","doi":"10.1111/mec.17534","DOIUrl":"10.1111/mec.17534","url":null,"abstract":"<p>Coevolution of parasites with their hosts may lead to balancing selection on genes involved in determining the specificity of host–parasite interactions, but examples of such specific interactions in wild vertebrates are scarce. Here, we investigated whether the polymorphic outer surface protein C (OspC), used by the Lyme disease agent, <i>Borrelia afzelii</i>, to manipulate vertebrate host innate immunity, interacts with polymorphic major histocompatibility genes (MHC), while concurrently eliciting a strong antibody response, in one of its main hosts in Europe, the bank vole. We found signals of balancing selection acting on OspC, resulting in little differentiation in OspC variant frequencies between years. Neither MHC alleles nor their inferred functional groupings (supertypes) significantly predicted the specificity of infection with strains carrying different OspC variants. However, we found that MHC alleles, but not supertypes, significantly predicted the level of IgG antibodies against two common OspC variants among seropositive individuals. Our results thus indicate that MHC alleles differ in their ability to induce antibody responses against specific OspC variants, which may contribute to selection of OspC polymorphism by the vole immune system.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":"33 21","pages":""},"PeriodicalIF":4.5,"publicationDate":"2024-09-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142306804","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Eric H. Ignatz, Xi Xue, Jennifer R. Hall, Shahinur S. Islam, Matthew L. Rise, Ian A. Fleming
Escape of genetically distinct farmed Atlantic salmon (Salmo salar) raises concerns about their potential interactions with wild populations and the disruption of local adaptation through genetic admixture. It is often unknown whether genetic origin or common domestication effects will have a greater influence on consequences posed by escaped farmed fish. Previous work showed that domestication could have prevalent effects on the behaviour and growth of farmed salmon, independent of their genetic origin. Yet, less is known whether this extends more broadly to gene expression, particularly at critical early life stages. Thus, we compared the expression of 24 transcripts related to the immune response, structural maintenance, stress response and iron metabolism among distinct farmed (North American [NA] and European [EO]), wild (Newfoundland) and F1 hybrid salmon at hatching under controlled conditions using qPCR analyses. A slightly higher number of transcripts were differentially expressed between the wild population relative to EO (i.e. atf3a, atf3b, bnip3, trim37a, ftm, hp and gapdh) than NA-farmed salmon (i.e. epdl2, hba1a, hba1b, hbb4 and ftm). The most differences existed between the two farmed strains themselves (11 of 24 transcripts), with the fewest differentially expressed transcripts found between the F1 hybrids and the domesticated/wild maternal strains (4 of 24 transcripts). Interestingly, despite similarities in the overall extent of gene expression differences among cross types, the expression patterns differed relative to a past study that compared fry from the same cross types at the end of yolk sac absorption. Overall, our findings suggest that interbreeding of escaped farmed salmon with wild Newfoundland populations would alter transcript expression levels and that developmental stage influences these changes.
{"title":"Defence-relevant gene expression differences in hatchlings among wild Newfoundland and farmed European and North American Atlantic salmon and their hybrids","authors":"Eric H. Ignatz, Xi Xue, Jennifer R. Hall, Shahinur S. Islam, Matthew L. Rise, Ian A. Fleming","doi":"10.1111/mec.17535","DOIUrl":"10.1111/mec.17535","url":null,"abstract":"<p>Escape of genetically distinct farmed Atlantic salmon (<i>Salmo salar</i>) raises concerns about their potential interactions with wild populations and the disruption of local adaptation through genetic admixture. It is often unknown whether genetic origin or common domestication effects will have a greater influence on consequences posed by escaped farmed fish. Previous work showed that domestication could have prevalent effects on the behaviour and growth of farmed salmon, independent of their genetic origin. Yet, less is known whether this extends more broadly to gene expression, particularly at critical early life stages. Thus, we compared the expression of 24 transcripts related to the immune response, structural maintenance, stress response and iron metabolism among distinct farmed (North American [NA] and European [EO]), wild (Newfoundland) and F<sub>1</sub> hybrid salmon at hatching under controlled conditions using qPCR analyses. A slightly higher number of transcripts were differentially expressed between the wild population relative to EO (i.e. <i>atf3a</i>, <i>atf3b</i>, <i>bnip3</i>, <i>trim37a</i>, <i>ftm</i>, <i>hp</i> and <i>gapdh</i>) than NA-farmed salmon (i.e. <i>epdl2</i>, <i>hba1a</i>, <i>hba1b</i>, <i>hbb4</i> and <i>ftm</i>). The most differences existed between the two farmed strains themselves (11 of 24 transcripts), with the fewest differentially expressed transcripts found between the F<sub>1</sub> hybrids and the domesticated/wild maternal strains (4 of 24 transcripts). Interestingly, despite similarities in the overall extent of gene expression differences among cross types, the expression patterns differed relative to a past study that compared fry from the same cross types at the end of yolk sac absorption. Overall, our findings suggest that interbreeding of escaped farmed salmon with wild Newfoundland populations would alter transcript expression levels and that developmental stage influences these changes.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":"33 21","pages":""},"PeriodicalIF":4.5,"publicationDate":"2024-09-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/mec.17535","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142306803","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ectomycorrhizal (ECM) fungi are important tree symbionts within forests. The biogeography of ECM fungi remains to be investigated because it is challenging to observe and identify species. Because most ECM plant taxa have a Holarctic distribution, it is difficult to evaluate the extent to which host preference restricts the global distribution of ECM fungi. To address this issue, we aimed to assess whether host preference enhances the endemism of ECM fungi that inhabit dipterocarp rainforests. Highly similar sequences of 175 operational taxonomic units (OTUs) for ECM fungi that were obtained from Lambir Hill's National Park, Sarawak, Malaysia, were searched for in a nucleotide sequence database. Using a two-step binomial model, the probability of presence for the query OTUs and the registration rate of barcode sequences in each country were simultaneously estimated. The results revealed that the probability of presence in the respective countries increased with increasing species richness of Dipterocarpaceae and decreasing geographical distance from the study site (i.e. Lambir). Furthermore, most of the ECM fungi were shown to be endemic to Malaysia and neighbouring countries. These findings suggest that not only dispersal limitation but also host preference are responsible for the high endemism of ECM fungi in dipterocarp rainforests. Moreover, host preference likely determines the areas where ECM fungi potentially expand and dispersal limitation creates distance–decay patterns within suitable habitats. Although host preference has received less attention than dispersal limitation, our findings support that host preference has a profound influence on the global distribution of ECM fungi.
{"title":"Host preference explains the high endemism of ectomycorrhizal fungi in a dipterocarp rainforest","authors":"Hirotoshi Sato, Ajuwin Lain, Takafumi Mizuno, Satoshi Yamashita, Jamilah Binti Hassan, Khairunnisa Binti Othman, Takao Itioka","doi":"10.1111/mec.17529","DOIUrl":"10.1111/mec.17529","url":null,"abstract":"<p>Ectomycorrhizal (ECM) fungi are important tree symbionts within forests. The biogeography of ECM fungi remains to be investigated because it is challenging to observe and identify species. Because most ECM plant taxa have a Holarctic distribution, it is difficult to evaluate the extent to which host preference restricts the global distribution of ECM fungi. To address this issue, we aimed to assess whether host preference enhances the endemism of ECM fungi that inhabit dipterocarp rainforests. Highly similar sequences of 175 operational taxonomic units (OTUs) for ECM fungi that were obtained from Lambir Hill's National Park, Sarawak, Malaysia, were searched for in a nucleotide sequence database. Using a two-step binomial model, the probability of presence for the query OTUs and the registration rate of barcode sequences in each country were simultaneously estimated. The results revealed that the probability of presence in the respective countries increased with increasing species richness of Dipterocarpaceae and decreasing geographical distance from the study site (i.e. Lambir). Furthermore, most of the ECM fungi were shown to be endemic to Malaysia and neighbouring countries. These findings suggest that not only dispersal limitation but also host preference are responsible for the high endemism of ECM fungi in dipterocarp rainforests. Moreover, host preference likely determines the areas where ECM fungi potentially expand and dispersal limitation creates distance–decay patterns within suitable habitats. Although host preference has received less attention than dispersal limitation, our findings support that host preference has a profound influence on the global distribution of ECM fungi.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":"33 21","pages":""},"PeriodicalIF":4.5,"publicationDate":"2024-09-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/mec.17529","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142255552","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}