Genomics of Adaptation to Human Contexts

Genomics of Adaptation to Human Contexts The pervasive and multifaceted effect of humans on other species is the prevalent story of biology in the 21st century. Human-driven selective pressures can have dramatic effects under remarkably short timescales (Hendry et al. 2017). In response, geneticists in traditionally disjunct fields from urban ecology to agriculture are using the same tools to ask related questions: How are species adapting to human contexts? What are the effects of human-imposed selection pressures? What sources of diversity fuel rapid evolution? Whether the system of interest is domesticated, invasive, or adapting to habitat alterations, genomic datasets hold the key for understanding rapid evolutionary shifts. These questions have spurred much recent scientific discussion (e.g., Molecular Ecology special issue April 2015: Invasion Genetics; Ecological Society of America conference 2016: Novel Ecosystems in the Anthropocene; PNAS special feature April 2014: The Modern View of Domestication, and more). To further this discussion, we hosted the “Genomics of Adaptation to Human Contexts” Symposium and Workshop (28–30 July 2016 at Colorado State University), supported by the American Genetics Association and the Genetics Society of America, to highlight exemplar research using large genomic datasets to investigate ecology and evolution in the Anthropocene. Early career researchers in many fields can benefit from understanding the parallel and potentially complementary approaches and tools used in other fields to answer very similar questions. Genetics researchers spend increasingly more time building and using software, but few have ever been taught how to do this efficiently. To meet this need, we hosted a Software Carpentry workshop (http://software-carpentry.org/workshops/) to train early career geneticists in the essential programmatic tools needed to analyze large genomic datasets. Software Carpentry is a nonprofit organization that organizes volunteer-taught workshops on basic computational skills and best practices. In the 2-day workshop, 23 participants from 8 institutions learned key computational skills including how to automate tasks using the Unix shell, how to track and share work using version control, and how to write software in R that is readable, reusable, and reliable. We provided supplementary travel funding to encourage the participation of early career researchers in this symposium, especially those from traditionally underrepresented groups. The following 1-day symposium consisted of 3 keynote talks by invited speakers, 10 contributed talks, and a poster session, showcasing research from a range of topic areas, including crop and animal breeding, invasive species, and adaptation to urban environments. Intriguingly similar themes ran through these disparate topics (e.g., accumulation of deleterious mutations as the result of rapid selection, intensity of anthropogenic disturbance, comparative approaches across urban-natural gradients, population divergence, and the effect of human-mediated migration). Keynote speakers included Dr John K. McKay (CSU) on Adaptation to climate, genotype by environment interaction, and crop breeding; Dr Regina Baucom (UMich) on Human-mediated selection in the agro-ecosystem: The evolution and genetics of herbicide resistance in an agricultural weed; and Dr Robert Wayne (UCLA) on Molecular adaptation of wild and domestic canids to anthropogenic landscapes. Other speakers included Justin Havird (CSU, Selection on the mitochondrial and nuclear genomes during domestication), Franz Lichtner (CSU, Sudden Oak Death: Human adaptation or evolution, a genomic inquisition), Amrutaa Varudakar (National Centre for Biological Sciences, India, Gut microflora of 2 rats: Commensal Rattus rattus, non-commensal Rattus satarae), Sierra Love Stowell (UC Boulder, Rescue genomics of greenback cutthroat trout), Brian Campbell (CSU, Genomic variation in industrial hemp and drug-type Cannabis sativa), and Stephen Pierce (CSU, Using genomics to decipher the impacts of historic selections in wheat breeding). To broaden the dissemination and conversation around these presentations, we developed a hashtag (#adapt2humans) and archived all tweets from the conference (http://bit.ly/2AtYD7X). We invited all participants to submit their work on the genomics of adaptation to human-influenced environments. The 6 papers in this collection represent a broad spectrum of questions and biological systems, but all focus on the use of genomic resources to understand how both intentional and unintentional artificial selection is driving evolution in other species. The potential magnitude of unintentional human selection should not be underestimated. Biologists have been considering the question of intended and unintended effects of artificial selection for more than 200 years (Wilner 2006). In The Variation of Plants and Animals under Domestication, Darwin describes the process of domestication as “an experiment on a gigantic scale” (1868). Over the last decade, we have begun to explore the effects of this experiment using genomic resources. Moyers et al. (this issue) review the evidence for a genetic “cost of domestication,” and find that with few exceptions, domesticated lineages show signs of increased deleterious genetic variation compared to their wild relatives. These signs include increased genome-wide linkage disequilibrium, reduced genetic diversity, increased numbers or substitutions of nonsynonymous relative to synonymous mutations, and more numerous or frequent mutations that annotate as deleterious in comparative analyses. The same pattern is found when comparing modern domesticated lineages subject to recent intense artificial selection (elite or improved varieties) against older domesticated lineages (landrace or noncommercial varieties). These patterns are likely driven by the combination of repeated genetic bottlenecks, strong artificial selection, and increased inbreeding that humans have intentionally and unintentionally applied during the process of domestication. Selective pressure from anthropogenic sources can also reveal the mechanisms underlying fundamental aspects of a species’ biology, such as mating system structure and function. Alvarado-Serrano et al. (this issue) demonstrate the predominant role that human actions, in the form of agricultural practices and herbicide usage, play in determining population-level mating system variation in the common morning glory (Ipomoea purpurea). Climate and human factors influence different floral traits demonstrating the flexibility that this species possesses to separately fine tune aspects of its mating system. However, the effect of human-induced selection is even stronger than climate, and consequently affects the evolutionary trajectory of this weedy species. Another unintended consequence of modern agricultural practices is reviewed by Patterson et al. (this issue): the evolution of increased EPSPS copy number in agricultural weeds, in response to the broad spectrum systemic herbicide glyphosate. Increased copy number at the EPSPS (enzyme 5-enolpyruvylshikimate-3-phosphate synthase) gene is thought to confer resistance to glyphosate by increasing the available pool of EPSPS enzyme, which is otherwise bound and inactivated by glyphosate, thus allowing the plant to maintain production of aromatic amino acids. To date, at least 4 species in the Amaranthaceae and 4 in the Poaceae have evolved glyphosate resistance through increased EPSPS copy number, even though glyphosate has been commercially available for less than 50 years, hinting that copy number variation may be a common mechanism for rapid adaptation, at least to glyphosate. Cities contain a wholly novel set of selective pressures not present in rural or natural environments. Consequently, urban landscapes can differentially affect allelic frequencies to the point in which urban populations become genetically distinct from their natural conspecifics. Measuring that distinction is now a current, and perhaps lucrative, research endeavor to explore. This idea is typified by Schell (this issue), who provides a review of previously completed molecular work in cities, then hypothesizes how a genomics approach may expand inferences into emerging questions in the field of urban ecology. In so doing, he provides a general rubric to address the zeitgeist question: are urban species merely plastic or are phenotypic correlations modulated by urban-adapted genotypes? Anthropogenic contexts represent novel challenges to population delineations by human-mediated increase in migration between populations, both intentional and unintentional. Turner et al. (this issue) investigate the impact of ornamental seed spreading on population structure in the state wildflower, Texas bluebonnet (Lupinus texensis). Their work demonstrates that across the core range of this endemic species, it is now nearly panmictic, likely the result of cultivation and the intense propagule pressure resulting from highway beautification efforts. This represents an unrecognized impact of beautification in the intermediate space between domestication and species introduction. The interplay between intentional and unintentional anthropogenic drivers in and outside novel landscapes is epitomized by work from Wilcox et al. (this issue), which seeks to resolve the debate as to whether invasive species of lionfish within and outside their native ranges exhibit signs of hybridization. This story is notable in that the invasive Atlantic range of lionfish (Pterois volitans), likely introduced via intentional discard of pet lionfish, are predominantly or exclusively hybrids of 2 species (Pterois miles and Pterois russelii) that natively co-occur along the geographically expansive oceanic overlap zone between the Indian and Pacific Oceans. The mtDNA COI break between these species (P. miles and P. russelii) is >5%, an astounding finding given that other documented cases of marine fish hybrids demonstrate nonviability beyond the 5% genetic break. This contribution consequently demonstrates how the combination of heterosis and human-associated introductions lead to potent invasive complexes. Though their systems and goals may be different, many geneticists are using similar tools to address similar questions about human-driven rapid evolution. By explicitly highlighting parallel effort across different fields, and by demonstrating the necessity of providing bioinformatic and programmatic training to graduate student and postdoctoral geneticists, we hope this symposium and themed collection will promote collaborative and interdisciplinary work on all fronts of the study of rapid adaptation in the Anthropocene. References Darwin C. 1868. The variation of animals and plants under domestication . London (UK): John Murray. Hendry AP, Gotanda KM, Svensson EI. 2017. Human influences on evolution, and the ecological and societal consequences. Phil Trans R Soc B . 372. doi: 10.1098/rstb.2016.0028 Wilner E. 2006. Darwin’s artificial selection as an experiment. Stud Hist Philos Biol Biomed Sci . 37: 26– 40. Google Scholar CrossRef Search ADS PubMed  © The American Genetic Association 2018. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Heredity Oxford University Press

Genomics of Adaptation to Human Contexts

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Oxford University Press
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© The American Genetic Association 2018. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
ISSN
0022-1503
eISSN
1465-7333
D.O.I.
10.1093/jhered/esx113
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Abstract

The pervasive and multifaceted effect of humans on other species is the prevalent story of biology in the 21st century. Human-driven selective pressures can have dramatic effects under remarkably short timescales (Hendry et al. 2017). In response, geneticists in traditionally disjunct fields from urban ecology to agriculture are using the same tools to ask related questions: How are species adapting to human contexts? What are the effects of human-imposed selection pressures? What sources of diversity fuel rapid evolution? Whether the system of interest is domesticated, invasive, or adapting to habitat alterations, genomic datasets hold the key for understanding rapid evolutionary shifts. These questions have spurred much recent scientific discussion (e.g., Molecular Ecology special issue April 2015: Invasion Genetics; Ecological Society of America conference 2016: Novel Ecosystems in the Anthropocene; PNAS special feature April 2014: The Modern View of Domestication, and more). To further this discussion, we hosted the “Genomics of Adaptation to Human Contexts” Symposium and Workshop (28–30 July 2016 at Colorado State University), supported by the American Genetics Association and the Genetics Society of America, to highlight exemplar research using large genomic datasets to investigate ecology and evolution in the Anthropocene. Early career researchers in many fields can benefit from understanding the parallel and potentially complementary approaches and tools used in other fields to answer very similar questions. Genetics researchers spend increasingly more time building and using software, but few have ever been taught how to do this efficiently. To meet this need, we hosted a Software Carpentry workshop (http://software-carpentry.org/workshops/) to train early career geneticists in the essential programmatic tools needed to analyze large genomic datasets. Software Carpentry is a nonprofit organization that organizes volunteer-taught workshops on basic computational skills and best practices. In the 2-day workshop, 23 participants from 8 institutions learned key computational skills including how to automate tasks using the Unix shell, how to track and share work using version control, and how to write software in R that is readable, reusable, and reliable. We provided supplementary travel funding to encourage the participation of early career researchers in this symposium, especially those from traditionally underrepresented groups. The following 1-day symposium consisted of 3 keynote talks by invited speakers, 10 contributed talks, and a poster session, showcasing research from a range of topic areas, including crop and animal breeding, invasive species, and adaptation to urban environments. Intriguingly similar themes ran through these disparate topics (e.g., accumulation of deleterious mutations as the result of rapid selection, intensity of anthropogenic disturbance, comparative approaches across urban-natural gradients, population divergence, and the effect of human-mediated migration). Keynote speakers included Dr John K. McKay (CSU) on Adaptation to climate, genotype by environment interaction, and crop breeding; Dr Regina Baucom (UMich) on Human-mediated selection in the agro-ecosystem: The evolution and genetics of herbicide resistance in an agricultural weed; and Dr Robert Wayne (UCLA) on Molecular adaptation of wild and domestic canids to anthropogenic landscapes. Other speakers included Justin Havird (CSU, Selection on the mitochondrial and nuclear genomes during domestication), Franz Lichtner (CSU, Sudden Oak Death: Human adaptation or evolution, a genomic inquisition), Amrutaa Varudakar (National Centre for Biological Sciences, India, Gut microflora of 2 rats: Commensal Rattus rattus, non-commensal Rattus satarae), Sierra Love Stowell (UC Boulder, Rescue genomics of greenback cutthroat trout), Brian Campbell (CSU, Genomic variation in industrial hemp and drug-type Cannabis sativa), and Stephen Pierce (CSU, Using genomics to decipher the impacts of historic selections in wheat breeding). To broaden the dissemination and conversation around these presentations, we developed a hashtag (#adapt2humans) and archived all tweets from the conference (http://bit.ly/2AtYD7X). We invited all participants to submit their work on the genomics of adaptation to human-influenced environments. The 6 papers in this collection represent a broad spectrum of questions and biological systems, but all focus on the use of genomic resources to understand how both intentional and unintentional artificial selection is driving evolution in other species. The potential magnitude of unintentional human selection should not be underestimated. Biologists have been considering the question of intended and unintended effects of artificial selection for more than 200 years (Wilner 2006). In The Variation of Plants and Animals under Domestication, Darwin describes the process of domestication as “an experiment on a gigantic scale” (1868). Over the last decade, we have begun to explore the effects of this experiment using genomic resources. Moyers et al. (this issue) review the evidence for a genetic “cost of domestication,” and find that with few exceptions, domesticated lineages show signs of increased deleterious genetic variation compared to their wild relatives. These signs include increased genome-wide linkage disequilibrium, reduced genetic diversity, increased numbers or substitutions of nonsynonymous relative to synonymous mutations, and more numerous or frequent mutations that annotate as deleterious in comparative analyses. The same pattern is found when comparing modern domesticated lineages subject to recent intense artificial selection (elite or improved varieties) against older domesticated lineages (landrace or noncommercial varieties). These patterns are likely driven by the combination of repeated genetic bottlenecks, strong artificial selection, and increased inbreeding that humans have intentionally and unintentionally applied during the process of domestication. Selective pressure from anthropogenic sources can also reveal the mechanisms underlying fundamental aspects of a species’ biology, such as mating system structure and function. Alvarado-Serrano et al. (this issue) demonstrate the predominant role that human actions, in the form of agricultural practices and herbicide usage, play in determining population-level mating system variation in the common morning glory (Ipomoea purpurea). Climate and human factors influence different floral traits demonstrating the flexibility that this species possesses to separately fine tune aspects of its mating system. However, the effect of human-induced selection is even stronger than climate, and consequently affects the evolutionary trajectory of this weedy species. Another unintended consequence of modern agricultural practices is reviewed by Patterson et al. (this issue): the evolution of increased EPSPS copy number in agricultural weeds, in response to the broad spectrum systemic herbicide glyphosate. Increased copy number at the EPSPS (enzyme 5-enolpyruvylshikimate-3-phosphate synthase) gene is thought to confer resistance to glyphosate by increasing the available pool of EPSPS enzyme, which is otherwise bound and inactivated by glyphosate, thus allowing the plant to maintain production of aromatic amino acids. To date, at least 4 species in the Amaranthaceae and 4 in the Poaceae have evolved glyphosate resistance through increased EPSPS copy number, even though glyphosate has been commercially available for less than 50 years, hinting that copy number variation may be a common mechanism for rapid adaptation, at least to glyphosate. Cities contain a wholly novel set of selective pressures not present in rural or natural environments. Consequently, urban landscapes can differentially affect allelic frequencies to the point in which urban populations become genetically distinct from their natural conspecifics. Measuring that distinction is now a current, and perhaps lucrative, research endeavor to explore. This idea is typified by Schell (this issue), who provides a review of previously completed molecular work in cities, then hypothesizes how a genomics approach may expand inferences into emerging questions in the field of urban ecology. In so doing, he provides a general rubric to address the zeitgeist question: are urban species merely plastic or are phenotypic correlations modulated by urban-adapted genotypes? Anthropogenic contexts represent novel challenges to population delineations by human-mediated increase in migration between populations, both intentional and unintentional. Turner et al. (this issue) investigate the impact of ornamental seed spreading on population structure in the state wildflower, Texas bluebonnet (Lupinus texensis). Their work demonstrates that across the core range of this endemic species, it is now nearly panmictic, likely the result of cultivation and the intense propagule pressure resulting from highway beautification efforts. This represents an unrecognized impact of beautification in the intermediate space between domestication and species introduction. The interplay between intentional and unintentional anthropogenic drivers in and outside novel landscapes is epitomized by work from Wilcox et al. (this issue), which seeks to resolve the debate as to whether invasive species of lionfish within and outside their native ranges exhibit signs of hybridization. This story is notable in that the invasive Atlantic range of lionfish (Pterois volitans), likely introduced via intentional discard of pet lionfish, are predominantly or exclusively hybrids of 2 species (Pterois miles and Pterois russelii) that natively co-occur along the geographically expansive oceanic overlap zone between the Indian and Pacific Oceans. The mtDNA COI break between these species (P. miles and P. russelii) is >5%, an astounding finding given that other documented cases of marine fish hybrids demonstrate nonviability beyond the 5% genetic break. This contribution consequently demonstrates how the combination of heterosis and human-associated introductions lead to potent invasive complexes. Though their systems and goals may be different, many geneticists are using similar tools to address similar questions about human-driven rapid evolution. By explicitly highlighting parallel effort across different fields, and by demonstrating the necessity of providing bioinformatic and programmatic training to graduate student and postdoctoral geneticists, we hope this symposium and themed collection will promote collaborative and interdisciplinary work on all fronts of the study of rapid adaptation in the Anthropocene. References Darwin C. 1868. The variation of animals and plants under domestication . London (UK): John Murray. Hendry AP, Gotanda KM, Svensson EI. 2017. Human influences on evolution, and the ecological and societal consequences. Phil Trans R Soc B . 372. doi: 10.1098/rstb.2016.0028 Wilner E. 2006. Darwin’s artificial selection as an experiment. Stud Hist Philos Biol Biomed Sci . 37: 26– 40. Google Scholar CrossRef Search ADS PubMed  © The American Genetic Association 2018. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com

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Journal of HeredityOxford University Press

Published: Mar 1, 2018

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